Chapter 10

Chapter 10 C4 Photosynthesis and Temperature Rowan F. Sage* Department of Ecology and Evolutionary Biology, The University of Toronto, 25 Willcocks Street, Toronto, ON M5S3B2, Canada

Ferit Kocacinar Faculty of Forestry, Kahramanmaras Sutcu Imam University, Merkez, 46100, Kahramanmaras, Turkey

David S. Kubien Department of Biology, University of New Brunswick, 10 Bailey Dr., Fredericton, NB, E3B 5A3, Canada

Summary .............................................................................................................................................................. I. Introduction .................................................................................................................................................. II. The Temperature Responses of C4 Photosynthesis and Growth ................................................................. A. Net CO2 Assimilation Rate .................................................................................................................... B. Interactions with CO2 and Light Intensity .............................................................................................. C. Growth .................................................................................................................................................. III. The Biogeography of C4 Photosynthesis....................................................................................................... A. Global Patterns ..................................................................................................................................... B. Cold-Adapted C4 Species ..................................................................................................................... C. Evolutionary and Ecological Perspectives ............................................................................................ D. Synopsis ............................................................................................................................................... IV. The Temperature Response of C4 Photosynthesis: Biochemical Controls .................................................... A. The Response of C4 Photosynthesis to Intercellular CO2 Partial Pressure ........................................... B. Photorespiration in C3 and C4 Plants ..................................................................................................... C. Quantum Yield ....................................................................................................................................... D. Rubisco Limitations ............................................................................................................................... E. Rubisco Activase Limitations ................................................................................................................ F. C4 Cycle Limitations .............................................................................................................................. 1. Pyruvate-Pi-Dikinase...................................................................................................................... 2. PEP Carboxylase ........................................................................................................................... 3. Other Enzymes .............................................................................................................................. G. Electron Transport Limitations .............................................................................................................. V. Fluorescence at Low Temperature ............................................................................................................... VI. Stomatal Limitations .................................................................................................................................... VII. Thermal Acclimation of C4 Photosynthesis ..................................................................................................

162 162 163 163 166 166 168 168 170 170 175 175 176 177 177 179 180 181 181 182 182 183 184 185 185

!UTHORFOR#ORRESPONDENCE E MAILRSAGE UTORONTOCA

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Rowan F. Sage et al.

VIII. Conclusion: Are C4 Plants Inherently More Sensitive to Low Temperature Than C3 Plants? ...................... 187 Acknowledgments ................................................................................................................................................ 187 References ........................................................................................................................................................... 188

Summary #PLANTSPERFORMPOORLYATLOWTEMPERATURE INCONTRASTTO#VEGETATION!SACONSEQUENCE LOWNUMBERS OF#SPECIESOCCURATHIGHLATITUDE HIGHELEVATION ANDDURINGCOOLERGROWINGSEASONS4HEMECHANISMS EXPLAININGTHEPOORPERFORMANCEOF#SPECIESINCOLDERCLIMATESHAVENOTBEENCLEARLYIDENTIFIED%ARLY PHYSIOLOGICALPERSPECTIVESINDICATETHAT#SPECIESFAILATLOWTEMPERATUREDUETOEITHERLOWQUANTUM YIELDOFTHE#RELATIVETOTHE#PATHWAY ORENZYMELABILITYINTHE#CYCLE MOSTNOTABLYAT0%0REGEN ERATIONBYPYRUVATE 0IDIKINASE00$+ !LTERNATIVELY RECENTPHYLOGENETICSURVEYSSHOWTHATALL#LINE AGESORIGINATEDFROM#ANCESTORSADAPTEDTOWARMCLIMATES INDICATINGTHEFAILUREOFMOST#SPECIESIN COLDERENVIRONMENTSCOULDREFLECTPRIORHEATADAPTATIONWITHINTHEIRRESPECTIVEEVOLUTIONARYLINEAGES .UMEROUS#SPECIESHAVEINDEPENDENTLYEVOLVEDCOLDTOLERANCETHESEPLANTSALLOWFOREXAMINATIONOF #PHOTOSYNTHESISATLOWTEMPERATUREWITHOUTCOMPLICATIONSFROMCHILLINGINJURY2ELATIVETOECOLOGI CALLY SIMILAR # SPECIES CHILLING ADAPTED # SPECIES HAVE SIMILAR OR SLIGHTLY REDUCED PHOTOSYNTHETIC CAPACITIESBELOWm#AND AFTERCOLDACCLIMATION SHOWNOCHILLINGLABILITYOF00$+ 0%0CARBOXYLASE OROTHERENZYMESOFTHE#CYCLE#OLD ADAPTED#SPECIESHAVEENHANCEDPHOTOPROTECTIVECAPACITYAT LOWTEMPERATUREASINDICATEDBYGREATERLEVELSOFANTIOXIDANTSANDCAROTENOIDPIGMENTS2UBISCOCAPAC ITYISSIMILARTOGROSS#/ASSIMILATIONRATEBELOWm#INCOLD ADAPTED#SPECIES INDICATINGITISAN IMPORTANTLIMITATIONON#PHOTOSYNTHESISATCOOLTEMPERATURE!CCLIMATIONANDADAPTATIONOF#SPECIES TOTHECOLDDOESNOTOVERCOMETHEAPPARENT2UBISCOLIMITATION)TISLIKELYTHATACEILINGONCARBONGAIN BYINSUFFICIENT2UBISCOCAPACITYATLOWTEMPERATUREMAYBEALEADINGTRAITTHATMALADAPTSTHE#PATHWAYTO COLDREGIONSOFTHEEARTH

I. Introduction #PHOTOSYNTHESISISACOMPLEXEVOLUTIONARYTRAIT THATHASEVOLVEDOVERTIMESINFAMILIESOF VASCULARPLANTS MAKINGITONEOFTHEMOSTCONVER GENT OF EVOLUTIONARY PHENOMENA 3AGE -UHAIDAT ET AL .EARLY ALL LINEAGES ARE ASSOCIATEDWITHSPECIESOFTROPICALORSUB TROPICAL ORIGIN ALTHOUGH SPECIES WITHIN SOME LINEAGES HAVERADIATEDINTOLOW TEMPERATUREENVIRONMENTS IN ALPINE HABITATS ALONG COOL MARITIME COASTS ANDINHIGHLATITUDEMARSHES,ONG 3AGE

!BBREVIATIONS!ǻ.ET#/ASSIMILATIONRATE#Iǻ)NTERCELLULAR PARTIALPRESSUREOF#/#Aǻ!MBIENTPARTIALPRESSUREOF#/ 0%0#ǻ0HOSPHOENOLPYRUVATECARBOXYLASE00$+ǻ0YRUVATE ORTHOPHOSPHATEDIKINASE2UBISCOǻ2IBULOSE BISPHOSPHATE CARBOXYLASEOXYGENASE

ETAL "ECAUSE#PLANTSARELARGELYABSENT INCOLDCLIMATES AND#PHOTOSYNTHESISISWIDELY REPORTEDTOBEINFERIORTO#PHOTOSYNTHESISINCOLD CLIMATES "ERRY AND "JORKMAN 3AGE AND 0EARCY APARADIGMHASARISENTHATTHE# PATHWAYISMALADAPTEDTOTHECOLD ANDCONFERSITS GREATEST ADVANTAGE IN WARM ENVIRONMENTS FOR EXAMPLE "LACKETAL "LACK $OLINER AND *OLLIFFE *ONES 2AVEN ET AL 4HIS VIEW HAS BEEN PERIODICALLY CHAL LENGED MOST RECENTLY BY AUTHORS WHO RAISE THE POSSIBILITY THAT THE TEMPERATURE REQUIREMENTS OF #PLANTSREFLECTTHEEVOLUTIONARYHISTORYOFTHEIR ANCESTORS RATHER THAN A SPECIFIC PHYSIOLOGICAL REQUIREMENTOFTHE#PATHWAYFORHEATORDROUGHT ,ONG %HLERINGER AND -ONSON %DWARDSAND3TILL 4HEREARE HOW EVER CLEARPHYSIOLOGICALMECHANISMSBEHINDTHE DIFFERENTTEMPERATURERESPONSESOF#AND#PHO TOSYNTHESIS AND THESE RESPONSES CORRELATE WELL

10

C4 Photosynthesis and Temperature

WITHTHEDISTRIBUTIONOF#SPECIESALONGTHERMAL GRADIENTS%HLERINGER %DWARDSAND7ALKER 0EARCY AND %HLERINGER %HLERINGER ETAL 3AGEETAL #LARIFYINGTHEDEGREETOWHICHTHETEMPERATURE RESPONSE OF # PHOTOSYNTHESIS AFFECTS THE DISTRI BUTION OF # PLANTS WILL HAVE MANY BENEFITS TO SOCIETY &OR ONE A BETTER UNDERSTANDING OF THE LIMITATIONS CONTROLLING THE TEMPERATURE RESPONSE OF # PHOTOSYNTHESIS COULD FACILITATE IMPROVED PRODUCTIVITY OF # CROPS AT A TIME WHEN GLOBAL FOODSTOCKSAREDECLINING ANDCOULDBECRITICALTO THE DEVELOPING BIOFUEL INDUSTRY # CROPS ARE EXPECTEDTOPROVIDEASIGNIFICANTCONTRIBUTIONTO THEFUTURESUPPLYOFBIOENERGYHOWEVER MUCHOF THEAVAILABLELANDANDMARKETSFORBIOFUELSAREIN HIGHERLATITUDES WHERELOWTEMPERATURESEVERELY LIMITS#CROPPRODUCTIVITY#LIFTON "ROWNETAL (EATON ET AL )N ADDITION CLIMATE WARMINGWILLDISRUPTCURRENTECOLOGICALRELATION SHIPS IN THE NEXT CENTURY # SPECIES ARE OFTEN THOUGHT TO RESPOND MORE TO RISING TEMPERATURES THAN # SPECIES HOWEVER THE SEASONALITY OF WARMING CONFOUNDS SUCH SIMPLE PREDICTIONS 3AGEAND+UBIEN 0REDICTINGRESPONSESOF EARTHȀSVEGETATIONTOCLIMATECHANGEWILLREQUIRE ATHOROUGHUNDERSTANDINGOFTHERESPONSEOFTHE # PATHWAY TO TEMPERATURE CHANGE 3AGE AND +UBIEN VON&ISCHERETAL 4HIS CHAPTER WILL RE EVALUATE THE RELATIONSHIP BETWEEN#PHOTOSYNTHESISANDTEMPERATURE BY INCORPORATING OLDER UNDERSTANDING WITH RECENT DEVELOPMENTSTHATHAVEBROADENEDOURPERSPEC TIVES AND IMPROVED OUR MECHANISTIC UNDER STANDING OF THE BIOCHEMICAL CONTROLS OVER THE TEMPERATURE RESPONSE OF # PHOTOSYNTHESIS 7E WILLFIRSTREVIEWTHETEMPERATURERESPONSESOF# AND#PHOTOSYNTHESISANDGROWTH ANDTHENDIS CUSSTHEBIOGEOGRAPHYOF#PHOTOSYNTHESIS WITH PARTICULAR FOCUS ON THE COLD TOLERANT OUTLIERS TO GENERAL PATTERN OF # PLANT DISTRIBUTION 4HE SECONDHALFOFTHECHAPTERDEVELOPSAMECHANISTIC FRAMEWORKTOINTERPRETTHETEMPERATURERESPONSE OF # PHOTOSYNTHESIS 4O LIMIT THE CHAPTER TO A MANAGEABLE SIZE WE SAY LITTLE ABOUT CHILLING INJURYTHATISNOTDIRECTLYLINKEDTOTHE#PATH WAY7ECONCLUDEWITHASYNTHESISOFBIOCHEMI CALANDECOLOGICALPERSPECTIVESTOARGUETHATTHE #PATHWAYCANBETOLERANTOFCOLDCLIMATES BUT IT INHERENTLY REQUIRES WARM CONDITIONS TO BE ECOLOGICALLYSUCCESSFUL

II. The Temperature Responses of C4 Photosynthesis and Growth A. Net CO2 Assimilation Rate 7ITHINADECADEOFTHEDISCOVERYOF#PHOTOSYN THESIS IN THE MID S IT WAS REALIZED THAT # SPECIES EXHIBITED HIGHER RATES OF PHOTOSYNTHESIS THAN # SPECIES AT WARMER CONDITIONS WHILE # SPECIES HAD HIGHER RATES OF PHOTOSYNTHESIS IN COOLER CONDITIONS "LACK ET AL "JORKMAN AND 0EARCY "LACK 7ILLIAMS ,ONG ET AL )SHII ET AL 6ONG AND -URATA ,ONG AND 7OOLHOUSE B +EMPAND7ILLIAMSREVIEWEDBY"ERRYAND "JORKMAN *ONES SEE ALSO 0EARCY ET AL -ONSON ET AL (ENNING AND "ROWN &LADUNGAND(ESSELBACH # SPECIESTYPICALLYEXHIBITAPRONOUNCEDRESPONSEOF PHOTOSYNTHESISTOINCREASINGTEMPERATUREUPTOA THERMALOPTIMUMBETWEENm#ANDm# WHILE #SPECIESHAVEABROADTHERMALOPTIMUMOFPHO TOSYNTHESIS BETWEEN m AND m# ,UDLOW AND 7ILSON "JORKMANAND0EARCY "JORK MANETAL 0EARCYAND(ARRISON ,ONGETAL 6ONGAND-URATA ,ONG AND 7OOLHOUSE B "ERRY AND "JORKMAN 0EARCY ET AL -ONSON ET AL ,OOMIS 4IESZENAND$ETLING "YTHE LATE S THESEPATTERNSHADBECOMEATEXTBOOK PARADIGM FOR EXAMPLE SEE 3ALISBURY AND 2OSS ! CONCERN REGARDING THIS EARLY PARADIGM WAS THAT MANY OF THESE PHOTOSYNTHETIC MEASURE MENTSDIDNOTCOMPARESPECIESOFSIMILARECOLOGI CAL HABITAT BUT INSTEAD EMPHASIZED COOL SEASON #CROPS WEEDSANDFORAGEGRASSESVERSUSWARM SEASON#SPECIES0EARCYAND%HLERINGER 0HOTOSYNTHETIC CAPACITY CAN VARY MARKEDLY IN PLANTSOFDIFFERENTGROWTHFORMANDHABITATSUCH THAT THESE FACTORS COULD INFLUENCE RESULTS MORE THANPHOTOSYNTHETICPATHWAY 4O AVOID SOME OF THESE CONFOUNDING EFFECTS WEMEASUREDTHETEMPERATURERESPONSEOFTHENET #/ASSIMILATIONRATE! FROM0ECTISMULTIFLOSC ULOSA # !STERACEAE AND TWO ECOTYPES OF THE PROSTRATE # HERB (ELIOTROPIUM CURRISAVICUM "ORAGINACEAE &IGA 0ECTISMULTIFLOSCULOSAIS APROSTRATEDUNESPECIESFROMTHE0ACIFICCOASTOF SUBTROPICAL -EXICO WHILE ( CURRISAVICUM IS A PROSTRATEHERBFROMCOASTALREGIONSOF.ORTHAND 3OUTH !MERICA /NE POPULATION WAS FROM THE


&IG 2EPRESENTATIVE TEMPERATURE RESPONSE CURVES OF NET #/ ASSIMILATION RATE IN # PLANTS AT THE PREVAILING ATMOSPHERIC #/ LEVEL DURING THE TIME OF MEASUREMENT A 0ECTIS MULTIFLOSCULOSA # AND A COOL AND WARM ECOTYPE OF (ELIOTROPIUM CURRISAVICUM # B -UHLENBERGIA RICHARDSONIS # +OELARIA MACRANTHA # AND #AREX HELLERI # C !TRIPLEX ROSEA # AND!TRIPLEXPATULASSPSPICATA# NOWCLASSIFIEDAS!DIOCA7ELSH FROMWARMmm#DAYNIGHT ANDCOOL mm#DAYNIGHT GROWTHCONDITIONSANDD &LAVERIATRINERVIA# &LAVERIAPRINGLEI# AND&LAVERIACRONQUISTII# 3PECIESINPANELA ANDB WEREGROWNDURINGSUMMERINAGREENHOUSEIN4ORONTO #ANADAANDTHENET#/ASSIMILATIONRATE MEASURED WITH A STEADY STATE GAS EXCHANGE SYSTEM 0ECTIS MULTIFLOSCULOSA WAS COLLECTED ON A BEACH DUNE NEAR -ANZANILO -EXICO4HEWARMECOTYPEOF(CURRISAVICUMWASCOLLECTEDALONGTHECOASTOF9UCATAN -EXICOTHECOOLECOTYPEAT0IGEON 0OINT #ALIFORNIA-UHLENBERGIARICHARDSONIS +MACRANTHAAND#AREXHELLERIWERECOLLECTEDAT MINANALPINEFELLFIELD INTHE7HITE-OUNTAINSOF#ALIFORNIA!TRIPLEXDATAFROMPANELC WASRECALCULATEDFROMRELATIVERATESGIVENBY"JORKMANAND 0EARCY FORPLANTSGROWNINAGROWTHCHAMBER&LAVERIADATAINPANELD AREFROM3CHUSTERAND-ONSON SQUARES AND/BERHUBERAND%DWARDS CIRCLES USINGGREENHOUSEGROWNPLANTS$ATAINPANELSA ANDB AREPUBLISHEDFORTHEFIRST TIME&LAVERIADATAAREREPRINTEDWITHPERMISSION

COOL COAST OF CENTRAL #ALIFORNIA WHILE THE OTHER WAS FROM THE HOT SUBTROPICS OF THE 9UCATAN 0ENISULA -EXICO)NBOTHOFTHESESITUATIONS THE CLASSICALPATTERNWASAPPARENTTHE#SPECIESOUT PERFORMED THE # ECOTYPES AT ELEVATED TEMPERA TURE WHILE BOTH THE WARM AND COOL CLIMATE ECOTYPESOFTHE#SPECIESHADAHIGHERPHOTOSYN THETIC CAPACITY THAN THE # PLANTS AT COOLER TEMPERATURES &IG A 3IMILAR RESPONSES HAVE BEEN MEASURED BETWEEN ECOLOGICALLY SIMILAR # AND # SPECIES FROM -OJAVE $ESERT SHRUBS

"JORKMANETAL OLDFIELDS0EARCYETAL AND GRAMINOIDS FROM SHORT GRASS PRAIRIES -ONSONETAL 4IESZENAND$ETLING 'ROWTHTEMPERATURECANCOMPLICATETHISGENERAL OBSERVATION HOWEVER WHEN GROWN AT COOL TEM PERATURES m# OR LESS # SPECIES CAN HAVE HIGHER!THAN#SPECIESACROSSAWIDERANGEOF TEMPERATURE WHILE THE REVERSE MAY BE TRUE IN WARMGROWTHCONDITIONSm#ORHIGHER"ERRY AND "JORKMAN "JORKMAN ET AL -ONSON ET AL %VEN IN THESE SITUATIONS

10


HOWEVER THE#SPECIESSTILLEXHIBITEDASTEEPER THERMAL RESPONSE OF ! BELOW THE TEMPERATURE OPTIMUM ANDAHIGHERTHERMALOPTIMUMTHANTHE #SPECIES "ECAUSE # SPECIES ARE REPUTED TO PERFORM POORLYINLOWTEMPERATURE WEEXAMINEDWHETHER THECLASSICTEMPERATURERESPONSEOFPHOTOSYNTHESIS WOULDALSOHOLDINTHECASEOFA#PLANTTHATHAS EVOLVEDTHEABILITYTOSURVIVEINCOLDCLIMATES4HE #GRASS-UHLENBERGIARICHARDSONISFROMTHEHIGH ALPINEZONEOFWESTERN.ORTH!MERICANEXHIBITED A MUCH HIGHER RATE OF PHOTOSYNTHESIS AT ELEVATED TEMPERATURETHANTHE#GRASS+OELERIAMACRANTHA AND#SEDGE#AREXHELLERIFROMTHESAMEHABITAT BELOWm# THETWO#SPECIESHADHIGHER!THAN THE#SPECIES&IGB "OTHSPECIESWEREGROWN INIDENTICALCONDITIONSINAGREENHOUSEUNDERMOD ERATE TEMPERATURES ABOUT ǻm# ! SIMILAR COMPARISON BETWEEN TWO ECOLOGICAL ASSOCIATES FROM HIGH LATITUDE FENS IN THE BOREAL FOREST ALSO DEMONSTRATED GREATER PHOTOSYNTHETIC CAPACITY OF THE#GRASS-UHLENBERGIAGLOMERATA THANTHE# GRASS#ALAMAGROSTISCANADENSIS ABOVEm#BUT NOTBELOWm#+UBIENAND3AGE A 4HESE RESULTSDEMONSTRATETHATEVENINPLANTSFROMCOLD CLIMATES THE TYPICAL # AND # PHOTOSYNTHETIC RESPONSESTOTEMPERATURESTILLPREVAIL ALTHOUGHTHE THERMALOPTIMUMOF!ANDTHE#VERSUS#CROSSO VER TEMPERATURES FOR ! ARE SHIFTED TO LOWER TEM PERATURES $IFFERENCES IN ENVIRONMENTAL RESPONSES MAY ALSOREFLECTPHYLOGENETICHISTORY!CKERLY %DWARDSETAL SUCHTHATRESULTSATTRIBUTED TO PHOTOSYNTHETIC PATHWAY COULD INSTEAD REFLECT ANCESTRALCONSTRAINTS&EWSTUDIES HOWEVER HAVE EXAMINED THE PHOTOSYNTHETIC TEMPERATURE RESPONSESOF#AND#SPECIESTHATAREPHYLOGE NETICALLY CLOSELY RELATED "JORKMAN AND 0EARCY STUDIEDTHETEMPERATURERESPONSESOFPHO TOSYNTHESIS IN !TRIPLEX ROSEA # AND !TRIPLEX PATULASSPSPICATA!TRIPLEXDIOCA #7ELSH FROMCENTRAL#ALIFORNIASEE/SMONDETAL FORADDITIONAL!TRIPLEXCOMPARISONS 4HESE CLOSELYRELATEDSPECIESARESIMILARINGROWTHFORM ANDMORPHOLOGY ANDBOTHGROWINDISTURBEDSOILS 7ELSH :ACHARIAS !TALOWGROWTH TEMPERATURE mm# DAYNIGHT TEMPERATURE THE#SPECIESHADSUPERIOR!BELOWm# WHEREAS ! IN THE # SPECIES WAS GREATER ABOVE m# &IGC"JORKMANAND0EARCY !TAWARM GROWTH TEMPERATURE mm# DAYNIGHT THE

SAMERELATIVEPATTERNPREVAILED ALTHOUGHBOTHTHE # AND # !TRIPLEX SPECIES EXHIBITED A HIGHER THERMALOPTIMUMANDREDUCED!ATEACHMEASURE MENT TEMPERATURE RELATIVE TO THE RESPONSES OBSERVED IN COOL GROWN PLANTS &IG C )N 0ANICUM GRASSES THE # SPECIES 0 MAXIMUM WHICH IS NOW -EGATHYRSUS MAXIMUS AND FOR MERLY5ROCHLOAMAXIMA "ARKWORTHETAL HADOVERTWICETHERATEOFPHOTOSYNTHESISABOVE m# BUTHALFTHERATEBELOWm# THANTHE# SPECIES0BISCULATUM ATTESTINGTOTHERAPIDDROP IN PHOTOSYNTHESIS BELOW m# IN THE # SPECIES &LADUNG AND (ESSELBACH )N A SEPARATE 0ANICUM STUDY (ENNING AND "ROWN 0PRIONTIS# HADHIGHER!FROMm#TOm# THANEITHERTHE#0LAXUM3TEINCHISMALAXA OR # 0 BOLIVIENSE 0 POLYGONATUM !T LOWER MEASUREMENTTEMPERATURESm#ANDm# THE #SPECIESHADASLIGHTLYHIGHER! BUTASTEMPERA TURE INCREASED ABOVE m# ! BECAME SUBSTAN TIALLY LARGER IN THE # THAN # SPECIES SUCH THAT THE # SPECIES HAD MORE THAN TWICE THE #/ ASSIMILATIONRATEATTHETHERMALOPTIMUMOFEACH SPECIES )N CLOSELY RELATED &LAVERIA SPECIES THE #&PRINGLEIAND&CRONQUISTIIHAVELOWER!THAN THE#SPECIES&TRINERVIAABOVEm#&IGD HOWEVER THEDIFFERENCESBETWEENTHE#AND# SPECIESDECLINEWITHFALLINGTEMPERATURE!Tm# #/ASSIMILATIONRATESARECOMPARABLEBETWEEN& TRINERVIA AND & PRINGLEI &IG D 3CHUSTER AND -ONSON /BERHUBERAND%DWARDS 4HE MOST CLOSELY RELATED # AND # PAIR IS PERHAPSTHE#AND#SUBSPECIESOF!LLOTEROPSIS SEMIALATA AGRASSFROMTHEMONSOONBELTOF3OUTH !FRICA SOUTH!SIAAND!USTRALIA)BRAHIMETAL /SBORNEETAL )N3OUTH!FRICA THETWOSUBSPECIESCO OCCUR ALTHOUGHTHE#SUB SPECIESTENDSTOBEDISPLACEDTOWARDSCOOLER DRIER UPLANDHABITATSRELATIVETOTHE#SUBSPECIES4HE #SUBSPECIESISNOTACTIVEINTHEWINTER DUETO FROST INTOLERANCE OF ITS CANOPY )BRAHIM ET AL 4HE # SUBSPECIES IS FROST TOLERANT AND THUSREMAINSWINTERACTIVE ALLOWINGITTOREDUCE THECOMPETITIVEPRESSUREFROMTHE#SUBSPECIES AND OTHER # SPECIES )N A COMPARISON OF THEIR RELATIVEPHOTOSYNTHETICRESPONSESTOTEMPERATURE /SBORNEETAL THEPATTERNWASSIMILARTO THATOBSERVEDIN&LAVERIA&IGD ANDBETWEEN 0PRIONTISAND0BOLIVIENSE(ENNINGAND"ROWN 4HEREWASNOPHOTOSYNTHETICADVANTAGEAT LOWTEMPERATUREFORTHE#!LLOTEROPSISSUBSPECIES


SINCETHE#/ASSIMILATIONRATESWERESIMILARBELOW m# HOWEVER THE # SUBSPECIES HAD A MUCH STRONGERRESPONSETORISINGTEMPERATURE SUCHTHATAT ǻm# ITHADDOUBLETHEPHOTOSYNTHETICCAPACITY OFTHE#SUBSPECIES/SBORNEETAL 4HE RESULTS AT SATURATING LIGHT INTENSITIES BETWEENCLOSELYRELATED#AND#GENOTYPESCON FORMTOTHEGENERALVIEWTHAT#PHOTOSYNTHESISIS MORERESPONSIVETORISINGTEMPERATUREANDHASA HIGHERTHERMALOPTIMUMTHANOBSERVEDINTHE# PLANTS#SPECIESEXHIBITEDHIGHER!ATTHETHER MAL OPTIMUM OFTEN BY A WIDE MARGIN 4HE # ADVANTAGE IS UNIVERSALLY LOST AT LOWER TEMPERA TURES ALTHOUGH # PLANTS DO NOT ALWAYS HAVE A LOWER #/ ASSIMILATION RATE AT LOW TEMPERATURE THANTHEIR#COUNTERPARTS

PPM THE#!4RESPONSEISLITTLECHANGED WITH ONLY A SMALL ENHANCEMENT OCCURRING NEAR THE THERMALOPTIMUM&IGC "YCONTRAST #SPE CIESSTILLSHOWASUBSTANTIALENHANCEMENTOF!BY RISING#/ABOVEm# ANDASARESULT CANEXHIBIT !4RESPONSESATHIGH#/THATMIMICTHOSEOF# SPECIES&IGSEEALSO"JORKMANETAL !TSUBSATURATINGLIGHTINTENSITIES !IN#PLANTS EXHIBITSLOWSENSITIVITYTOVARIATIONINTEMPERATURE ANDTHUSTHE!4CURVEBECOMESFLATTENEDWITHA BROAD THERMAL OPTIMUM &IG ,IGHT REQUIRE MENTSFOR!AREHIGHESTATTHETHERMALOPTIMUM SO THEFLATTENINGOFTHE!4RESPONSEWITHDECLINING LIGHTBEGINSATTHEOPTIMALTEMPERATURE ANDTHEN SPREADSTOLOWERTEMPERATURESASLIGHTLEVELSDROP FURTHER "ERRY AND "JORKMAN ,ONG AND 7OOLHOUSE A #ONSEQUENTLY THEGENERALIZA TIONTHAT#PLANTSAREMORERESPONSIVETOTEMPERA TUREANDHAVEAHIGHERTHERMALOPTIMUMTHAN# PLANTSONLYREFERSTOTHELIGHTSATURATEDCONDITION

B. Interactions with CO2 and Light Intensity

Net CO2 assimilation rate Mmol m 2 s 1

)N BOTH # AND # SPECIES THE TEMPERATURE RESPONSE OF ! THE !4 CURVE IS INFLUENCED BY ATMOSPHERIC #/ CONTENT AND LIGHT INTENSITY !T LOW #/ VALUES TYPICAL OF THE LATE 0LEISTOCENE ǻ PPM ABOUT ǻ YEARS AGO 7ARDETAL THE!4RESPONSEOF#PLANTS ISRELATIVELYSHALLOW WITHABROADTHERMAL OPTI MUM&IGA !S#/LEVELINCREASESTOTHECUR RENT #/ VALUE OF PPM THE RATE OF PHOTOSYNTHESISATTHETHERMALOPTIMUMINCREASES MARKEDLYINLEAVESOF#SPECIES CREATINGACURVE WITH A NARROWER THERMAL OPTIMUM AND GREATER RESPONSES TO CHANGING TEMPERATURE &IG B 7ITH FURTHER INCREASES IN #/ FROM TO

60

a

Ca =180

45

C. Growth 4HEREARENUMEROUSSTUDIESEXAMINING#AND# GROWTH AND COMPETITION RESPONSES TO TEMPERA TURE INCLUDINGMANYSPECIESOFSIMILARECOLOGICAL REQUIREMENTS#LEMENTSETAL "LACK "JORKMAN ET AL 6ONG AND -URATA 0EARCY ET AL #HRISTIE AND $ETLING ,OOMIS %VANS AND "USH *ONES 7ALL 'RISE .ORDETAL /SBORNE ET AL 7ARD ET AL 4HE MAJORITYOFTHESESTUDIESSHOWTHATWARMGROWTH TEMPERATURESABOVEǻm#FAVORTHE#SPECIES

b

60

c

Amaranthus retroflexus (C4)

45

30

30 Chenopodium album (C3)

15

15

Ca =380 0 10

20

30

40

10

20

30

40

Ca =700 10

20

0 30

40

Leaf temperature, qC

&IG4HETEMPERATURERESPONSEOF#PHOTOSYNTHESISIN!MARANTHUSRETROFLEXUSFILLEDSYMBOLS ANDOF#PHOTOSYNTHESISIN #HENOPODIUMALBUMOPENSYMBOLS MEASUREDATAMBIENT#/LEVELS#A OF ANDPPM!RROWSINDICATETEMPERA TURESWHEREPHOTOSYNTHESISRATESAREEQUIVALENT2EPRINTEDFROM3AGEAND0EARCY 0LANTSWEREGROWNATATMOSPHERIC#/ LEVELSOFPPM

10

C4 Photosynthesis and Temperature 30 2500

Net CO2 assimilation rate Mmolm 2 s 1

25 690 20 400 15

10

230

5

0

130

0

10

20 30 Leaf temperature, nC

40

&IG 4HE TEMPERATURE RESPONSE OF # PHOTOSYNTHESIS AT DIFFERENT LIGHT INTENSITIES IN 3PARTINA TOWNSENDII 3 ANGLICA GROWN IN A PLANT GROWTH CHAMBER AT PREVAILING ATMOSPHERIC #/ LEVELS ,IGHT INTENSITIES IN rMOL PHOTONS MȪ SȪ ARE GIVEN BESIDE EACH RESPECTIVE CURVE 2EDRAWN FROM,ONGAND7OOLHOUSE B7ITHPERMISSION

WHILETHE#SPECIESPREDOMINATEATTEMPERATURES BELOWm# ASMAYOCCUREARLYINTHEGROWING SEASON0EARCYETAL #HRISTIEAND$ETLING 7ALL REVIEWED IN ,OOMIS 4IESZENETAL *ONES !TMOSPHERIC #/ MODULATES THE CROSSOVER TEMPERATURE WHERE THE # AND # PERFORMANCES ARE EQUAL ,OWER GROWTH #/ REDUCES THE TEM PERATUREBELOWWHICH#SPECIESSHOWEQUIVALENT GROWTHASTHE#SPECIES WHILEHIGH#/RAISES THIS TEMPERATURE 'RISE %HLERINGER ET AL 7ARDETAL COMPAREDGROWTHOF# AND#ANNUALSATATMOSPHERIC#/LEVELSOFTHE LATE 0LEISTOCENE PPM OR 0A 4HE # ANNUAL!MARANTHUSRETROFLEXUSHADALARGEGROWTH ADVANTAGEOVERTHE#SPECIES!BUTILONTHEOPHRASTII INAWARMGROWTHTREATMENTmm#DAYNIGHT TEMPERATURE BUT THIS ADVANTAGE WAS MARKEDLY REDUCED IN A COOL TREATMENT mm# 5SING #HENOPODIUMALBUM# AND!RETROFLEXUS# 'RISE OBSERVEDTHATTHE#SPECIESLOSTITS GROWTH ADVANTAGE AT mm# WHEN ATMOS PHERIC#/WASINCREASEDTWOTOTHREETIMES)NA GROWTH REGIME AT mm# INCREASING #/ TO PPMREDUCEDBYHALFALARGEGROWTHADVAN TAGEOBSERVEDIN!RETROFLEXUSATCURRENT#/LEVELS !Tm#AND PPM#/ THE#SPECIESSTILL

GREWFASTERTHANTHE#SPECIES ALTHOUGHTHEGROWTH RATEDIFFERENCEWASABOUTOFTHATOBSERVEDAT CURRENT#/LEVELS 3PECIES AND GROWTH CONDITIONS SELECTED FOR #ǻ# COMPARISONS HAVE A LARGE INFLUENCE OVER THEOUTCOME4HEMAJORRICEWEEDSINTHE#GENUS %CHINOCHLOA FOREXAMPLE HAVESUPERIORGROWTH RELATIVE TO # RICE VARIETIES ABOVE m# IN PART BECAUSE OF THE HIGH CHILLING SENSITIVITY OF RICE HOWEVER WHEN COMPARED WITH WHEAT WHICH IS CHILLING TOLERANT DAYTIME CONDITIONS MUST BE WARMERTHANǻm#FORTHE%CHINOCHLOASPPTO EXHIBIT GREATER GROWTH %VANS AND "USH 4HISHIGHLIGHTSTHENEEDTOCOMPAREECOLOGICALLY SIMILAR SPECIES WITH SIMILAR GROWTH FORM IN ORDER TO ISOLATE CONSEQUENCES OF PHOTOSYNTHETIC PATHWAY !NUMBEROFSTUDIESHAVEEXAMINEDCOMPETITION BETWEENECOLOGICALLYSIMILARWEEDS"LACK 0EARCY ET AL &LINT AND 0ATTERSON !CKERLY ET AL 'RISE 7ARD ET AL OR PRAIRIE GRASSES #HRISTIE AND $ETLING GROWN IN CONTRASTING THERMAL REGIMES )NCREASING TEMPERATURE UNIVERSALLY ENHANCED # SPECIESRELATIVETOTHE#ASSOCIATESBYREVERSINGOR REDUCINGTHE#ADVANTAGEOBSERVEDATTHECOOLER GROWTH CONDITIONS &LINT AND 0ATTERSON OBSERVEDTHEWARM SEASONWEED8ANTHIUMPENN SYLVATICUM COCKLEBUR # HAD A LARGE INITIAL ADVANTAGEOVERTHE#!MARANTHUSHYBRIDUSDUE TOAMUCHLARGERSEEDSIZE4HEINITIALSIZEADVAN TAGEOFTHE#SPECIESREMAINEDINPLACEATADAY NIGHT TEMPERATURE OF mm# BUT WAS GREATLY REDUCEDATmm# 4WO SETS OF STUDIES HAVE EXAMINED GROWTH RESPONSES OF PHYLOGENETICALLY CLOSE # AND # SPECIES )N !TRIPLEX HABITAT OF ORIGIN PLAYED A MAJOR ROLE IN THE RELATIVE PERFORMANCE 7ARM CLIMATE#!TRIPLEXSPECIESRESPONDEDSTRONGLYTO TEMPERATURE WITHTHREE TOFIVEFOLDENHANCEMENTS INBIOMASSWHENGROWNATmmASCOMPARED TOmm#/SMONDETAL 4HE#SPECIES ALLFROMCOOLCOASTALCLIMATES SHOWEDAǻ REDUCTION IN YIELD IN THE WARM RELATIVE TO COOL TEMPERATUREREGIME.OTABLY A#SPECIESFROMA COOLCOASTALENVIRONMENT!TRIPLEXSABULOSA HAD ASIMILARGROWTHRESPONSETOVARYINGTEMPERATURE ASTHE#SPECIESITGREWASWELLASTHE#SPECIES IN COOL CONDITIONS AND ALSO SHOWED REDUCED GROWTH IN THE mm# REGIME /SMOND ET AL 4HE OTHER PHYLOGENETICALLY CONTROLLED

STUDYWASCONDUCTEDWITHTHE#AND#ECOTYPES OF!LLOTEROPSISSEMIALATA/SBORNEETAL !SOBSERVEDWITHPHOTOSYNTHESIS THE#ECOTYPE HAD SUBSTANTIALLY GREATER LEAF EXPANSION RATE ABOVE m# THAN THE # ECOTYPE WHILE BELOW m# THE TWO ECOTYPES HAD SIMILAR LEAF EXPAN SIONRATES III. The Biogeography of C4 Photosynthesis A. Global Patterns #SPECIESARECOMPLETELYABSENTFROMARCTICAND NEAR ARCTICLATITUDESmLATITUDE ANDARERARE IN THE HIGH LATITUDE BOREAL ZONE BETWEEN m. AND m. 4EERI AND 3TOWE 4AKEDA AND (AKOYAMA #OLLINS AND *ONES A 3CHWARZAND2EDMANN 3AGEETAL #OLLATZETAL 3TILLETAL 4HEYARE GENERALLY RARE AT HIGH ELEVATIONS ALTHOUGH THEY CANBELOCALLYCOMMONINTHETREELESSTUNDRAOF THEALPINEZONEINDRYMOUNTAINRANGES0YANKOV VON"2UTHSATZAND(OFFMANN 3AGE ETAL 3AGEAND3AGE 7ANG 7ANG ET AL )N THESE EXTREME CASES THE UPPERELEVATIONLIMITOFTHEALPINE#SPECIESIS LOWER THAN THE LOCAL ALPINE # VEGETATION 3AGE AND3AGE 4HESHIFTINDOMINANCEOF#TAXAFROMLOWTO HIGHLATITUDEHASBEENWELLDESCRIBEDINFLORISTIC ANALYSESFROMMOSTREGIONSOFTHEGLOBE!FRICAǻ %LLISETAL !KHANIETAL EASTERN!SIA AND *APAN ǻ 4AKEDA ET AL A 4AKEDA AND (AKOYAMA 5ENOAND4AKEDA !US TRALIA ǻ (ATTERSLEY 4AKEDA ET AL B %GYPTǻ"ATANOUNYETAL %UROPEǻ#OLLINS AND*ONES A)NDIAǻ4AKEDA -ONGOLIAǻ 0YANKOVETAL .ORTH!MERICAǻ4EERIAND 3TOWE 3TOWE AND 4EERI ,I ET AL 7ANAND3AGE 3OUTH!FRICAǻ6OGEL ETAL 3TOCKETAL REVIEWEDIN,ONG 3AGEETAL 3AGEETAL SUMMARIZEDMANYOFTHEPRIOREFFORTSINONEGLO BALMAPOF#GRASSDISTRIBUTIONS)NGRASSFLORIS TIC STUDIES THE PERCENT OF # GRASS SPECIES IN A LOCALGRASSFLORAAREESTIMATEDANDTHENPOSITIONED ONACONTINENTAL SCALEMAP#SPECIESDOMINATE LOWLAND GRASS FLORAS 'REATER THAN TWO THIRDS OF ALLGRASSSPECIESBELOWmLATITUDEARE# WHILE

Rowan F. Sage et al. # SPECIES DOMINATE ALL GRASS FLORAS ABOVE m 4HEZONEWHEREGRASSFLORASAREEQUALLY#AND# CORRESPONDS TO ABOUT ǻm LATITUDE 3EDGE FLORASSHOW#DOMINANCEATLOWERLATITUDESTHAN GRASS FLORAS 4AKEDA ET AL A B 5ENO AND 4AKEDA ,IETAL 3AGEETAL )NADDITIONTOTHEFLORISTICSTUDIES THECONTRIBU TIONOF#BIOMASSTOLOCALPRODUCTIVITYASAFUNCTION OF TEMPERATURE HAS BEEN ESTIMATED USING DIRECT BIOMASSMEASUREMENTSANDCARBONISOTOPERATIOS !USTRALIA ǻ "IRD AND 0OUSAI 7YNN AND "IRD -ONGOLIAǻ!UERSWALDETAL CENTRAL.ORTH!MERICAǻ0ARUELOAND,AUENROTH %PSTEIN ET AL 4IESZEN ET AL VON&ISCHERETAL 3OUTH!MERICAǻ 0ARUELOETAL -URPHYAND"OWMAN 4HESEDATAALSOSHOWADECLINEOF#CONTRIBUTION TOLOCALPRODUCTIVITYWITHINCREASINGLATITUDETHAT LARGELYMIRRORSTHECHANGEESTIMATEDWITHFLORIS TICDATA)N!USTRALIA THESHIFTFROM#TO#DOM INANCEOFGRASSLANDSOCCURSBELOWǻmLATITUDE AND # SPECIES DOMINATE GRASSLANDS ACROSS THE NORTHERN HALF OF THE COUNTRY )N CENTRAL .ORTH !MERICA THESHIFTOCCURSATm.ǻm. THELATITUDE OF THE STATE OF .EBRASKA 0RECIPITATION PATTERNS MODIFYTHESECROSSOVERPOINTS7HEREWINTERSARE WETANDSUMMERSDRY THECROSSOVERLATITUDESARE REDUCED%PSTEINETAL 3TILLETAL .UMEROUS STUDIES HAVE PLOTTED THE # GRASS REPRESENTATIONASAFUNCTIONOFALTITUDEUSINGFLO RISTIC BIOMASS AND CARBON ISOTOPE ASSESSMENTS !RGENTINA ǻ VON " 2UTHSATZ AND (OFFMANN #AVAGNARO #ABIDOETAL #EN TRAL !MERICA ǻ #HAZDON %AST !FRICA ǻ 4IESZENETAL ,IVINGSTONEAND#LAYTON %GYPT ǻ 3AYED AND -OHAMED (AWAII ǻ 2UNDEL *APANǻ.ISHIMURAETAL .EW 'UINEAǻ%ARNSHAWETAL "IRDETAL 7YOMING 53!ǻ"OUTTONETAL REVIEWED IN 3AGE ET AL !T TEMPERATE LATITUDES # GRASSESDROPOUTOFFLORASABOVEABOUT M WHILE IN TROPICAL LATITUDES THEY ARE ABSENT FROM FLORAS ABOVE ABOUT M WITH A FEW NOTABLE EXCEPTION THAT WILL BE DISCUSSED BELOW )N SUB TROPICAL(AWAII #BIOMASSPRODUCTIVITYISNEGLI GIBLEABOVE M WHILEINEQUATORIAL+ENYA #PRODUCTIONBECOMESINSIGNIFICANTABOVE M4IESZENETAL 2UNDEL (UMANCROPPINGSYSTEMSALSOREFLECTTHEGLOBAL PATTERNOF#GRASSDOMINANCE,OWLATITUDE LOW ELEVATION GRAIN CROPS ARE MAINLY # EXCEPT FOR


RICE A#PLANTTYPICALLYGROWNONFLOODEDSOILS 3AGEAND0EARCY !THIGHLATITUDES ANDIN THETROPICALHIGHLANDS THECROPPINGSYSTEMS ARE EXCLUSIVELY # WITH TWO MAJOR EXCEPTIONS ǻ MAIZE ANDTHEPROSPECTIVEBIOFUELSPECIES -IS CANTHUS GIGANTEUS ,ONG #LIFTON "ROWN ETAL -AIZECULTIVATIONAT HIGHLATITUDE HOWEVER OCCURSTHROUGHTHEUSEOF EARLY YIELDINGVARIETIESWHERETHEPERIODOFACTIV ITY IS COMPRESSED INTO THE FEW WARM MONTHS OF SUMMER"YCONTRAST -ISCANTHUSAPPEARSTOHAVE SUBSTANTIALCOLDTOLERANCE DERIVEDFROMITSORIGIN INMONTANEHIGHLANDSOF4AIWAN *APANAND#HINA "EALEAND,ONG "EALEETAL #LIFTON "ROWNETAL )NADDITIONTOVARIATIONALONGLATITUDEANDELE VATION GRADIENTS THE OCCURRENCE OF # SPECIES REFLECTSASEASONALTREND)NTHETEMPERATEZONE #SPECIESARELARGELYACTIVEINTHELATESPRINGAND SUMMER # SPECIES BY CONTRAST CAN BE ACTIVE YEAR ROUND IN MILD TEMPERATE CLIMATES )N AREAS WITH HARSH WINTERS # SPECIES USUALLY BEGIN GROWTHWEEKSBEFORETHE#SPECIES)NTHE.ORTH !MERICANPLAINSGRASSLANDS THEMAJOR#GRASSES BEGIN GROWING -ARCH TO !PRIL WHILE THE # GRASSES BREAK BUD ǻ WEEKS LATER $ICKINSON AND$ODD +EMPAND7ILLIAMS/DE ETAL -ONSONAND7ILLIAMS -ON SONETAL 4IESZENAND$ETLING 3AGE ETAL )NTHESOUTHWESTERNDESERTSOF.ORTH !MERICA MOSTOFTHEHERBACEOUS#PRODUCTIVITY OCCURS IN WINTER TO SPRING WHILE THE # SPECIES ARE SUMMER ACTIVE WHERE MONSOON RAINS OCCUR 3AGEETAL )NTHESEDESERTS WINTERANNU ALSAREEXCLUSIVELY# WHILESUMMERANNUALSARE

% C4 Grass Species

100

a

Atlantic coast

80

MAINLY#-ULROYAND2UNDEL +EMP 'UO AND "ROWN )N MILD CLIMATES OF THE WARM TEMPERATE ZONE THE DIFFERENCES IN # AND #PERIODSOFACTIVITYCREATEDIFFICULTIESFORGAR DENERS AND LANDSCAPERS FOR EXAMPLE 2& 3AGE PERSONAL OBSERVATION WITH LAWNS IN !TH ENS 'EORGIA 53! ,AWNSTHATDOWELLINSUM MERCONSISTOF#GRASSESSUCHAS:OYSIAJAPONICA OR #YNODON DACTYLON "ERMUDA GRASS 4HESE GRASSESAREDORMANTINTHEMILDWINTERSWHEN# WEEDSCANINFESTTHELAWN EVENTUALLYRUININGTHE #TURF)FINSTEADTHEHOMEOWNERCHOSESA#TURF SUCHASAFESCUE THELAWNINITIALLYDOESWELLIN WINTER AND SPRING BUT BECOMES INFESTED WITH # WEEDSNOTABLYCRABGRASS $IGITARIASANGUINALIS DURINGTHESUMMER WHICHRUINTHE#TURF 4EMPERATURESTHRESHOLDSFOR#OCCURRENCEAND DOMINANCEHAVEBEENIDENTIFIEDBYREGRESSINGTHE PRESENCEOF#SPECIESVERSUSCLIMATEDATA4EERI AND3TOWE 0ARUELOAND,AUENROTH %PSTEINETAL "IRDAND0OUSAI 3AGEETAL 0YANKOVETAL 7ANAND 3AGE VON &ISCHER ET AL 4HESE TRENDS CONSISTENTLY SHOWED # GRASS SPECIES BECOMINGNEGLIGIBLEWITHINLOCALFLORASWHENTHE MINIMUM*ULYTEMPERATUREISBELOWǻm# AND THE MINIMUM MEAN DAYTIME HIGH IS BELOW ǻm#&IG3AGEETAL !SSHOWNIN &IG THESE TEMPERATURE TRENDS ARE PRESENT ON BOTH THE 0ACIFIC AND !TLANTIC COASTS OF .ORTH !MERICA 4HE 0ACIFIC COAST IS COOLER AND DRIER THAN THE !TLANTIC COAST IN THE SUMMER AND THIS DIFFERENCE SEPARATES THE TWO PLOTS OF # SPECIES REPRESENTATIONASAFUNCTIONOFLATITUDE&IGA HOWEVER WHEN PLOTTING THE TWO DISTRIBUTION b

100 80

60

60

40

40

20 0 10

Pacific coast

20

% C4 Grass Species

10

0 20 30 40 50 60 70 0 5 10 15 20 25 30 Northern Latitude, degrees Minimum July Temperature, nC

&IG4HEPERCENTAGEOF#SPECIESINLOCALGRASSFLORASFROMTHE0ACIFICOPENSYMBOLS AND!TLANTICFILLEDSYMBOLS COASTAL REGIONSOF.ORTH!MERICA ASAFUNCTIONOFLATITUDEPANELA ANDMINIMUM*ULYTEMPERATUREPANELB &ROM7ANAND3AGE 7ITHPERMISSION

CURVESASAFUNCTIONOFMID SUMMERTEMPERATURES BOTHCURVESSHOWTHESAMERELATIONSHIP&IGB 7HILE MINIMUM SUMMER TEMPERATURE IS FRE QUENTLYBESTCORRELATEDWITH#OCCURRENCEINA FLORA STRONGCORRELATIONSAREALSOSHOWNFORMEAN DAILY TEMPERATURE DEGREE DAYS NUMBER OF DAYS OVER m# AND FOR LOWER LATITUDE SITES MEAN ANNUALTEMPERATURE-EANANNUALTEMPERATUREIN TEMPERATELOCATIONSISOFTENPROBLEMATICBECAUSE CONTINENTAL INTERIORS CAN HAVE VERY COLD WINTERS THAT SKEW THE ANNUAL VALUE VON &ISCHER ET AL NOTED THAT # DOMINANCE OF SOIL CARBON ISOTOPERATIOSINCENTRAL.ORTH!MERICAOCCURRED WHENTHEFOLLOWINGINDICESEXCEEDEDm#nm#ǻ -AY HIGH TEMPERATURE *ULY AND !UGUST MEAN TEMPERATURE ANDHIGHTEMPERATURESFROM!PRILTO !UGUST)N!USTRALIA GRASSLANDSBECOME#DOM INATEDABOVEAMEANANNUALTEMPERATUREOFm# (ATTERSLEY )N THE HIGHLANDS OF (AWAII #OSTA 2ICA AND +ENYA # DOMINANCE OCCURS ABOVEAMEANDAILYMAXIMUMOFǻm# ANDA DAILY MEAN OF m# #HAZDON 4IESZEN ETAL 2UNDEL B. Cold-Adapted C4 Species 7HILE THE VAST MAJORITY OF # SPECIES OCCUR IN WARMCLIMATES MANY#PLANTSARECOLDTOLERANT (UNDREDS OF # PERENNIALS FROM TEMPERATE LATI TUDES SURVIVE WINTER TEMPERATURES OFTEN BELOW Ȫm#INTHEDORMANTSTATE2OWLEYETAL 2OWLEY 3CHWARZAND2EANEY 3AGE AND3AGE 7ALKERETAL $OZENSOF #SPECIESFROMDISTINCTEVOLUTIONARYLINEAGESARE ABLETOWITHSTANDCHILLINGANDFREEZINGCONDITIONS DURING THE GROWING SEASON 4ABLE -ARQUEZ ETAL ,IUAND/SBORNE &OREXAM PLE !NDEAN#GRASSESFROMTHE6ENEZUELANPAR AMOSURVIVETEMPERATURESASLOWASȪm#DURING THE GROWING SEASON -ARQUEZ ET AL # SPECIES ARE ALSO RECOGNIZED TO DO WELL IN COOL ENVIRONMENTS ALONG THE COAST OF SOUTHERN .EW :EALANDANDTHE0ACIFICNORTHWESTINTHE53! IN FOGGYCOASTALMARSHESALONGTHENORTH!TLANTICIN "RITAINAND#ANADA INBOREALFENS MEADOWSAND MARSHES ANDINEARLYSPRINGUNDERSTORIESOFFOR ESTSALONGTHECENTRAL-ISSISSIPPIRIVERVALLEYAND THE3IERRA.EVADAFOOTHILLSOF#ALIFORNIA,ONG #OLLINSAND*ONES A3MITHAND 7U 7AN AND 3AGE +AMLER +UBIENAND3AGE )NTHEWARMTEMPERATE ZONE NUMEROUS#SPECIESDEVELOPFROSTHARDINESS

Rowan F. Sage et al. AND REMAIN ACTIVE DURING MILD WINTER OR SPRING PERIODSTHATEXPERIENCESOMESUBZEROCOLD2OWLEY ET AL 2OWLEY ,IU AND /SBORNE #OLD ARID REGIONS ALSO CONTAIN # SHRUBS SUCH AS !TRIPLEX SPECIES THAT ARE ACTIVE DURING !PRIL WHEN SNOW AND SUBZERO TEMPERATURES CAN OCCUR#ALDWELLETAL A B -ANY#GRASSESANDDICOTSDOWELLINALPINE HABITATS WHERETHEYOFTENEXHIBITTHESAMESPE CIALIZEDGROWTHFORMSAS#SPECIES4ABLE # PLANTSWEREGENERALLYNOTTHOUGHTTOOCCURINTHE TRUE ALPINE ZONES UNTIL THE MID S WHEN 0YANKOV AND CO WORKERS 0YANKOV ET AL 0YANKOV 0YANKOV AND 6OSNESENSKAYA DESCRIBEDANUMBEROF#GRASSESANDDICOTS THATOCCURABOVE MINTHE0AMIRMOUNTAINS OF#ENTRAL!SIA4ABLE 4HESEDISCOVERIESCOM PLIMENTDESCRIPTIONSOFCOLD ADAPTEDGRASSESFROM THE HIGHLANDS OF .EW 'UINEA *APAN AND 4IBET SUCHASSPECIESINTHEGENUS-ISCANTHUS%ARNSHAW ETAL .ISHIMURAETAL 7ANG 4HE HIGHEST REPORTED ELEVATION FOR A # SPECIES WORLDWIDEIS M FORTHEGRASS/RINUSTHO ROLDIIFROM4IBET GROWINGONDRY GRAVELLYSTEPPE 7ANG )N THE !NDES NUMEROUS SPECIES EXTENDINTOTHEALPINEZONEUPTO MVON" 2UTHSATZAND(OFFMAN "OOMETAL 3AGEETAL ,ONG COMPILEDALISTOF SPECIESFROMTENGENERAOFGRASSESOCCURRING ABOVE MIN0ERUWHERETHEAVERAGEANNUAL TEMPERATURE IS LESS THAN m# EIGHT SPECIES IN THREEGENERAOCCURABOVE MWHERETHEAVER AGE ANNUAL TEMPERATURE IS BELOW ǻm# 4HE GENUS -UHLENBERGIA HAS EIGHT SPECIES COLLECTED ABOVE MIN0ERU WHILE0ASPALUMHASTEN SPECIES OCCURRING ABOVE M !BOVE M ALPINE # SPECIES SURVIVE SUBZERO GROWING SEASONTEMPERATURESTHATREGULARLYOCCURATNIGHT ANDOCCASIONALLYDURINGTHEDAY3AGEAND3AGE -ARQUEZETAL ANDARETOLERANTOF EPISODICSNOWFALLSDURINGMIDSUMMER C. Evolutionary and Ecological Perspectives 3INCETHEREALIZATIONTHAT#PLANTSAREPREDOMI NANTLYWARMCLIMATESSPECIES THEREHASBEENMUCH CONSIDERATIONOFTHECAUSATIVEMECHANISMS WITH SOMETHOUGHTGIVENTOWHETHERTHE#PATHWAYITSELF IS RESPONSIBLE FOR THE GLOBAL PATTERN %HLERINGER ,ONG %HLERINGERAND-ONSON %HLERINGER ET AL 3AGE 4HE

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10 C4 Photosynthesis and Temperature

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2EFERENCE 3CHWARZAND2EDMANN 7ANG


10


VARIOUS ARGUMENTS PUT FORWARD TO EXPLAIN THE TRENDSCANBEROUGHLYSEGREGATEDINTOTWOCATEGO RIES&IRST #SPECIESAREINTOLERANTOFCOLD AND SECOND #SPECIESREQUIREDAYTIMEWARMTH)NTOL ERANCEOFCOLDISINDICATEDBYCHILLINGANDFREEZ ING INJURY THAT OCCURS AT LOW TEMPERATURE "Y CONTRAST HEATREQUIRING#SPECIESCOULDBECOLD TOLERANT BUT WITHOUT WARM GROWING CONDITIONS THEYWOULDFAILTOESTABLISHORWOULDBEEXCLUDED BY ADJACENT # SPECIES "OTH COLD INJURY AND A HEATREQUIREMENTNEEDNOTREFLECTINHERENTPROB LEMSOFTHE#PATHWAY BUTCOULDINSTEADREFLECT NON PHOTOSYNTHETIC ADAPTATIONS TO WARM ENVIRON MENTS 7ITHTHEELUCIDATIONOFPHYLOGENIESINTHEGRASS FAMILYANDOTHERFAMILIESCONTAINING#LINEAGES #HRISTINETAL 6ICENTINIETAL ITISNOWAPPARENTTHATALL#TAXAAROSEFROM# ANCESTORSTHATCURRENTLYOCCURINWARMCLIMATES USUALLYINTHETROPICSANDSUBTROPICS3AGE %DWARDS AND 3TILL %DWARDS AND 3MITH )FALACKOFCOLDTOLERANCEDUETOANCESTRAL ADAPTATION EXPLAINED THE GENERAL ABSENCE OF # PLANTSINLOWTEMPERATURE THENINTIME #SPE CIES MIGHT GRADUALLY RADIATE INTO COLD CLIMATES ,ONG /LDER#LINEAGESSHOULDTHENHAVE MORECOLD ADAPTEDSPECIESTHANYOUNGERLINEAGES 4HISPATTERNGENERALLYAPPEARSTOBETHECASE/F THE COLD ADAPTED SPECIES LISTED IN 4ABLE MOST AREFROM#LINEAGESTHATAREESTIMATEDTOBEOVER MILLIONYEARSOLD WHILETHE#GRASSLINEAGES LESSTHANMILLIONYEARSOLDLACKHIGHELEVATION ANDHIGHLATITUDE#SPECIES WITHTHEEXCEPTIONOF THE 0ASPALUM CLADE #HRISTIN ET AL 4HE #HLORIDOIDEAELINEAGE FOREXAMPLE WHICHISESTI MATEDTOBETHEOLDEST#LINEAGE CONTAINSMANY COLD TOLERANT SPECIES AND GENERA INCLUDING THE HIGHEST ELEVATION AND LATITUDE # SPECIES IN THE WORLD4ABLE 7HILERECOGNIZINGTHEPOSSIBILITYTHATANCESTRAL COLDINTOLERANCECOULDEXPLAINTHEFAILUREOFMANY #SPECIESINCOLDCLIMATES THISARGUMENTDOESNOT ADDRESSWHETHERTHE#PATHWAYITSELFISINHERENTLY MALADAPTEDTOLOWTEMPERATURE EITHERBECAUSEOFA LESIONINTHEPATHWAYATLOWTEMPERATURE ORSIM PLYPOORPERFORMANCE!NUMBEROFLINESOFEVI DENCE INDICATE THAT THE # PATHWAY IS INHERENTLY PROBLEMATICINCOOLCLIMATESRELATIVETO#SPECIES ANDTHESEPROBLEMSWILLCONTRIBUTETOTHEBIOGEO GRAPHICPATTERNOF#DISTRIBUTION &IRST THEEVOLUTIONOFCOLDTOLERANCEHASREPEAT EDLYOCCURREDINTHEMANY#LINEAGES INDICATING

ITISNOTNECESSARILYADIFFICULTPROCESS7EESTIMATE THEREAREATLEASTINDEPENDENTORIGINSOFCOLD TOLERANCEIN#LINEAGES4ABLE ANDMOREWILL BE IDENTIFIED WHEN SPECIES LEVEL PHYLOGENIES BECOME AVAILABLE FOR ALL # LINEAGES 3ECOND MOSTOFTHE#TAXAWITHCOLDTOLERANCE SUCHAS THETEMPERATEZONEGRASSESOFTHE.ORTH!MERI CAN PRAIRIE AND HIGH LATITUDE MARSH SPECIES ARE LARGELYSUMMERACTIVE BREAKINGDORMANCYLATER THAN THEIR # ASSOCIATES !LTHOUGH THESE SPECIES HAVEEVOLVEDCOLDTOLERANCEANDWINTERSURVIVAL THEYSTILLARERESTRICTEDTOWARMPERIODSOFACTIV ITY 4HIRD IN THE SPECIES !LLOTEROPSIS SEMILATA THE#ECOTYPEISAREVERTANTFROMTHE#ECOTYPE )BRAHIM ET AL 4HE # ECOTYPE HAS ALSO EVOLVEDFREEZINGTOLERANCE ANDANABILITYTOACCLI MATETOTHECOLDTHATISNOTPRESENTINTHE#ECO TYPE/SBORNEETAL 4HE#ECOTYPELOSES ITSLEAFCANOPYFOLLOWINGWINTERFROSTS WHILETHE LEAVESOFTHE#ECOTYPEPERSISTANDPHOTOSYNTHE SIZEYEARROUND4HISTRAITAPPEARSTOHAVEALLOWED THE#ECOTYPETORADIATEINTOCOOLER UPLANDHABI TATSWHERETHE#ECOTYPEISNOTFOUND4HEFAILURE OFTHE#ECOTYPETOSHOWTHESAMEPATTERNOFCOLD ADAPTATIONASTHE#ECOTYPEINDICATESTHE#PATH WAY SOMEHOW LIMITS THE SUCCESS OF THE # ECO TYPEINCOOLERHABITATS &INALLY THEMICROSITEDISTRIBUTIONOFALPINEAND HIGHLATITUDE#PLANTSINDICATESTHEREISASTRONG CONSTRAINT ASSOCIATED WITH THE # PATHWAY THAT REFLECTSAPERFORMANCELIMITATIONATLOWTEMPERA TURES)NTHEALPINEZONE GROWINGSEASONTEMPER ATURESARELOW TYPICALLYLESSTHANm#DURINGTHE DAYANDFREQUENTLY BELOWm#ATNIGHT+³RNER 3AGEAND3AGE -ARQUEZETAL ,IGHTLEVELSAREVERYHIGHONCLOUD FREEDAYS BUT CLOUD FREENIGHTSEXPERIENCEREGULARFROSTEVENTS DUETORAPIDLOSSOFINFRAREDRADIATIONTOTHESKY 3AGEAND3AGE 4HEHIGHSOLARINSOLATION SUBSTANTIALLYWARMSALPINEMICROSITESDURINGTHE DAY WHERE WIND IS NOT GREAT AND CERTAIN ALPINE PLANT MORPHOLOGIES NOTABLY THE CUSHION PLANT ANDPROSTRATEMATMORPHOLOGYARENOTEDTOEFFEC TIVELY CAPTURE SOLAR HEAT AND WARM THE CANOPY WELL ABOVE AIR TEMPERATURE +³RNER # PLANTS OF THE ALPINE SUCH AS THE !NDEAN DICOT 'OMPHRENA MEYENIANA THAT GROWS TO M ANDANUMBEROFSPECIESFROMTHEVARIOUS#GRASS LINEAGESARENOTEDTOEXHIBITTHESEHEAT TRAPPING MORPHOLOGIES3AGEAND3AGE 3AGEETAL /THER ALPINE # SPECIES ARE RESTRICTED TO ARID SLOPES OR SALINIZED BASINS SUCH AS 3ALSOLA


SPECIES OF THE HIGH 0AMIRS OF CENTRAL !SIA 0YANKOV 9OUNGAND9OUNG 3AGE AND 3AGE DESCRIBE THE HABITAT OF -UHLENBERGIARICHARDSONISINTHE!LPINEREGION OFTHE7HITE-OUNTAINSOF#ALIFORNIA4HISSPE CIESOCCURSASHIGHAS M FEET AND IS ABLE TO FORM DOMINANT SWARDS AT M FT &IG -UHLENBERGIA RICHARDSONIS EXHIBITS A PROSTRATE GROWTH FORM THAT KEEPS THE PLANTS WITHIN THE SURFACE BOUNDARY LAYER WHERE INTENSESOLARHEATINGCANELEVATETHELEAFTEMPERA TURESǻm#ABOVEAIRTEMPERATURES SUCHTHAT WHEN THE SUN SHINES AND THE WIND IS LOW THE LEAVESGENERALLYOPERATEBETWEENm#ANDm# 4HESE CONDITIONS ARE COMMON ON MOST SUMMER DAYSINTHE7HITE-OUNTAINSALPINEZONEBETWEEN AMANDNOON!TTHEHIGHELEVATIONLIMITOFITS DISTRIBUTION -RICHARDSONISISRESTRICTEDTOLOCA TIONSWHERELEAVESCANBEWARMEDWELLABOVEAIR TEMPERATURES NOTABLYSOUTH EASTERNSLOPESWHICH FACETHEMID MORNINGSUN ANDAMONGROCKSTHAT BREAKTHEWIND7INDSPEEDUSUALLYISHIGHINTHE 12:00:00

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30 Temperature, nC

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AFTERNOON IN THE 7HITE -OUNTAINS AND CLOUDS MORECOMMON SUCHTHATHEATINGBYTHEAFTERNOON SUNONSOUTHWESTFACINGSLOPESISLESSSIGNIFICANT ,IFEINMICROSITESWHERESOLARHEATISTRAPPEDHAS ITSCOSTS HOWEVER!TNIGHT THESESAMESITESTEND TOBETHECOLDESTAREASONTHELANDSCAPE BECAUSE CONVECTION CANNOT COMPENSATE FOR THE HIGH RATE OF INFRARED HEAT LOSS TO THE SKY DUE TO A THICK BOUNDARYLAYERATTHEEARTHȀSSURFACE3URPRISINGLY -RICHARDSONISISMORELIKELYTOEXPERIENCEFROST THANOTHERALPINEVEGETATIONDUETOITSLOWLOCATION WITHIN THE BOUNDARY LAYER -UHLENBERGIA RICH ARDSONISISABLETOTOLERATETHESECOLDNIGHTSWITH NOAPPARENTINJURY LEADING3AGEAND3AGE TO CONCLUDE THAT THIS # PLANTS REQUIRES DAYTIME HEATTOREMAINCOMPETITIVE RATHERTHANAVOIDING NIGHTTIMECOLD7HERE-RICHARDSONISISUNABLE TO ACQUIRE SUFFICIENT SOLAR HEATING TO ROUTINELY EXPERIENCELEAFTEMPERATURESABOVEm# ITFAILS TOOCCURINTHECOMMUNITY!SELEVATIONINCREASES ABOVE M ITFIRSTDISAPPEARSFROMTHENORTH FACING SLOPES THEN EAST AND WEST FACES WITH

24 18 12 6

air

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Muhlenbergia richardsonis

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0 99/08/05 99/08/06 99/08/07 99/08/08 99/08/09 99/08/10 Date

&IGA ,EAFANDAIRTEMPERATUREPROFILESFOR-UHLENBERGIARICHARDSONISAT MINTHE7HITE-OUNTAINSOF#ALIFORNIA B 4HECORRESPONDINGNETRADIATIONFLUXABOVETHE-RICHARDSONISCANOPYDURING!UGUSTC -RICHARDSONISINTHE3IERRA .EVADAMOUNTAINSOF#ALIFORNIAAT MELEVATION

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FURTHERINCREASEINELEVATION ANDISLASTOBSERVED ONSOUTHEASTFACESATITSUPPERELEVATIONLIMIT .ORTHOFmINTHE#ANADIANBOREALZONE SIX SPECIES OF # PLANTS HAVE BEEN NOTED TO PREFER SPECIFICMICOSITES SUCHASSOUTH FACINGSLOPESOR OPEN SALINIZEDANDDROUGHT PRONESITES3CHWARZ AND2EDMANN -UHLENBERGIARICHARDSONIS ISTHENORTHERNMOST#SPECIESKNOWN OCCURRING ASFARNORTHASm#INTHE.ORTHWEST4ERRITORIES OF#ANADAONSOUTH FACINGSLOPES-UHLENBERGIA GLOMERATA IS COMMONLY FOUND ON RAISED HUM MOCKS IN FENS THESE LIKELY EXPERIENCE SEVERE EPISODIC DROUGHT +UBIEN AND 3AGE )N %UROPE THE NORTHERNMOST # SPECIES ARE EITHER 3PARTINA AND !TRIPLEX SPECIES IN COASTAL SALT MARSHES ORSUMMERAGRICULTURALWEEDS!MARAN THUS RETROFLEXUS #YPERUS LONGUS 3ALSOLA KALI AND3ETARIAVIRIDIS THATEXPLOITDISTURBEDMICRO SITESASFARNORTHASm,ONG *ONESETAL #OLLINSAND*ONES A B D. Synopsis #SPECIESCOMMONLYDOMINATEHERBACEOUSHABI TATSATLOWERLATITUDESANDALTITUDE BUTMANYHAVE EVOLVED COLD TOLERANCE AND OCCUR IN HIGHER LATI TUDEANDALTITUDELOCATIONS4HESECOLD ADAPTED# SPECIES HOWEVER ARESTILLRESTRICTEDTOSITUATIONS WHERE DAYTIME LEAF TEMPERATURES ARE ELEVATED UNLESS ENVIRONMENTAL STRESS MAINLY SALINITY OR DISTURBANCEOFFSETA#ADVANTAGEATLOWTEMPERA TURES !LPINE # SPECIES REPRESENT THE MOST EXTREMECASESOFCOLDADAPTATIONINTHE#FUNC TIONALTYPE YETTHEYSTILLREQUIREWARMMICROSITES OR EXHIBIT CANOPY MORPHOLOGIES THAT TRAP SOLAR RADIATION4HESEOBSERVATIONSSUPPORTTHEPERSPEC TIVETHATTHE#PATHWAYCANFUNCTIONINTHECOLD BUT IS SUPERIOR TO THE # PATHWAY ONLY IN WARM ENVIRONMENTS UNLESSENVIRONMENTALSTRESSALLOWS THE HIGHER 75% OF # PLANTS TO OFFSET THE COLD ADVANTAGEOFTHE#FLORA$AYTIMEHEATING DIS TURBANCEORSTRESSARETHUSKEYREQUIREMENTSFOR# SUCCESS IN THESE EXTREME ENVIRONMENTS /NLY WHERE SUFFICIENT DAYTIME HEATING CANNOT OCCUR SUCH AS IN THE !RCTIC ARE # SPECIES COMPLETELY ABSENT 7ITH THIS UNDERSTANDING WE NOW DISCUSS THE BIOCHEMICAL PROCESSES CONTROLLING THE RESPONSE OF#PHOTOSYNTHESISTOTEMPERATURE INORDERTO EVALUATE UNDERLYING MECHANISMS CONTROLLING THE GEOGRAPHICDISTRIBUTIONOF#SPECIES

IV. The Temperature Response of C4 Photosynthesis: Biochemical Controls 4HERESPONSEOF#PHOTOSYNTHESISTOTEMPERATURE HASBEENWELLSTUDIEDANDBIOCHEMICALMODELSOF THESE RESPONSES EXHIBIT GOOD PREDICTIVE POWER &ARQUHAR AND VON #AEMMERER VON #AEMMERER "ERNACCHI ET AL #ENAND3AGE 3AGEAND+UBIEN "Y CONTRAST THE ABILITY TO MODEL THE TEMPERATURE RESPONSE OF # PHOTOSYNTHESIS IS INCOMPLETE #OLLATZETAL VON#AEMMERERAND&URBANK VON#AEMMERER -ASSADETAL )N # SPECIES THE PRINCIPLE BIOCHEMICAL CONTROLS OVERPHOTOSYNTHESISARETHECAPACITYOF2UBISCOTO CONSUME 2U"0 WHICH REFLECTS 2UBISCO CONTENT ACTIVATIONSTATEAND#/SUPPLY ANDTHECAPACITY OF LIGHT HARVESTING ELECTRON TRANSPORT THE #ALVIN CYCLE AND STARCHSUCROSE SYNTHESIS TO REGENERATE 2U"0 VON #AEMMERER 3AGE AND +UBIEN !TLOWERLEVELSOFATMOSPHERIC#/ 2UBISCO CAPACITYTOCONSUME2U"0ISLIMITINGFOR#PHOTO SYNTHESISATTHETHERMALOPTIMUMANDMODERATELY SUB OPTIMALTOSUPRAOPTIMALTEMPERATURES!TTEM PERATURESFURTHERAWAYFROMTHETHERMALOPTIMUM 2U"0 REGENERATION CAPACITY CAN BECOME LIMITING THROUGH EITHER THE CAPACITY OF STARCH AND SUCROSE SYNTHESISTOREGENERATE0IATSUBOPTIMALTEMPERA TURES ORTHECAPACITYOFELECTRONTRANSPORTATBOTH HIGH OR LOW TEMPERATURE EXTREMES !S WELL THE CAPACITYOF2UBISCOACTIVASETOMAINTAIN2UBISCO INANACTIVECONFIGURATIONMAYBECOMELIMITINGAT HIGH TEMPERATURE m# PARTICULARLY IN PLANTS FROM COOLER CLIMATES !T ELEVATED #/ 2U"0 REGENERATION CAPACITY TENDS TO LIMIT # PHOTOSYN THESIS AT ALL TEMPERATURES WITH 0I REGENERATION BEINGTHEPREDOMINANTLIMITATIONATCOOLERTEMPERA TURES AND ELECTRON TRANSPORT THE PREDOMINANT LIMITATIONATELEVATEDTEMPERATURE!TEXTREMETEM PERATURES LESIONS IN THE PHOTOSYNTHETIC APPARATUS DEVELOP LEADINGTOPHOTOINHIBITIONANDPROLONGED LOSSOFCARBONGAIN EVENUPONRETURNTOMODERATE CONDITIONS%XTREMETEMPERATURELESIONSTENDTOBE ASSOCIATED WITH DAMAGE TO LIGHT HARVESTING AND ELECTRONTRANSPORTCOMPONENTS ORTHEDISSOCIATION OF 2UBISCO ACTIVASE "ERRY AND "JORKMAN 3ALVUCCI AND #RAFTS "RANDNER 3AGE AND +UBIEN )N#PLANTS 2UBISCOCAPACITY 2U"0REGENERA TIONCAPACITY ANDTHEABILITYOF2UBISCOACTIVASE

TO MAINTAIN 2UBISCO ACTIVATION HAVE ALSO BEEN PROPOSED TO BE LIMITING PHOTOSYNTHESIS ACROSS A RANGEOFTEMPERATURES0EARCY 3AGE +UBIENETAL #RAFTS "RANDNERAND3ALVUCCI $WYERETAL -ASSADETAL )N ADDITION THEBIOCHEMICALCAPACITYOFTHE#CYCLE TODELIVER#/TOTHEBUNDLESHEATHCANALSOCON TROL#PHOTOSYNTHESIS,ONG 0OTVINETAL -ATSUBA ET AL 3AGE AND +UBIEN 7ANGETALB 4WOLEADINGLIMITATIONS ASSOCIATEDWITHTHE#CYCLEARE0%0REGENERATION BY00$+ AND0%0CARBOXYLASEACTIVITY!THIRD POTENTIALLIMITATIONMAYARISEATTHEDECARBOXYLA TIONSTEPINTHE#CYCLE BUTTHISISNOTREGARDED ASAMAJORLIMITATIONINCURRENTMODELSOF#PHO TOSYNTHESIS)NADDITION THERATEOF#/LEAKAGE OUTOFTHEBUNDLESHEATHCANREDUCETHEEFFICIENCY OFNITROGENANDLIGHTUSEIN#PLANTS ANDCONTRIBUTE TOPHOTOSYNTHETICLIMITATION3IEBKEETAL +UBIEN ET AL +UBIEN AND 3AGE A "ELOW WEWILLEXAMINETHESIGNIFICANCEOFTHESE BIOCHEMICAL LIMITATIONS BY FIRST CONSIDERING GAS EXCHANGEAPPROACHESANDTHENBYADDRESSINGTHE ROLEOFTHEMAJORENZYMESHYPOTHESIZEDTOCONTROL THETEMPERATURERESPONSEOF#PHOTOSYNTHESIS A. The Response of C4 Photosynthesis to Intercellular CO2 Partial Pressure )NBOTH#AND#PLANTS THERESPONSEOFNET#/ ASSIMILATION TO INTERCELLULAR #/ THE !#I RESPONSE ISWIDELYUSEDTOEVALUATETHERESPONSE OFINDIVIDUALBIOCHEMICALPROCESSESTOTEMPERA TURE4HISISBECAUSETHESTOMATALEFFECTSAREFAC TOREDOUTINCALCULATINGINTERCELLULAR#/VALUES AND SPECIFIC BIOCHEMICAL LIMITATIONS CAN BE PARAMETERIZEDFROMTHEINITIALSLOPEAND#/SAT URATEDREGIONSOFTHE!#ICURVEUSINGTHEORETICAL MODELSVON#AEMMERERAND&ARQUHAR VON #AEMMERER )N#SPECIES THEINITIALSLOPE OF THE !#I RESPONSE SHOWS A WEAK THERMAL DEPENDENCE WHILE THE #/ SATURATED PLATEAU SHOWSAPRONOUNCEDRESPONSETORISINGTEMPERA TUREUPTOTHETHERMALOPTIMUMOFPHOTOSYNTHESIS &IG SEEALSO)SHIIETAL ,ONGAND7OOL HOUSE A ,AISK AND %DWARDS 3AGE 0ITTERMANN AND 3AGE !S A CONSEQUENCE THE#/SATURATIONPOINTRISESWITH TEMPERATURE)FTHEINTERCELLULAR#/LEVELINAIR THEOPERATING#I ISNOTAFFECTEDBYTEMPERATURE


&IG 4HE #/ RESPONSE OF # PHOTOSYNTHESIS AT THREE TEMPERATURES IN &LAVERIA BIDENTIS PLANTS GROWN IN A PLANT GROWTH CHAMBER AT m# -EASUREMENT TEMPERATURES ARE BESIDE EACH CURVE !RROWS INDICATE THE OPERATIONAL #I THE INTERCELLULAR#/PARTIALPRESSUREATPREVAILINGATMOSPHERIC #/LEVELS &ROM+UBIEN

THENTHERISEINTHE#/ SATURATEDPLATEAURELATIVE TOTHEINITIALSLOPEOFTHE!#IRESPONSEWILLCAUSE #/ SATURATEDPHOTOSYNTHESISATLOWTEMPERATURE TOSHIFTTO#/ LIMITEDPHOTOSYNTHESISATELEVATED TEMPERATURE WHICH WILL HAVE CONSEQUENCES FOR THE!4RESPONSE&IG !TLOW#/LEVELSWHERE THEOPERATING#IFALLSONTHEINITIALSLOPE !WILLBE RELATIVELY INSENSITIVE TO THE RISE IN TEMPERATURE AND THE !4 RESPONSE WILL HAVE A BROAD THERMAL OPTIMUM&IGA )FSTOMATALCONDUCTANCEWERE LOWENOUGHTHATTHEOPERATING#ISHOULDFALLBELOW THE #/ SATURATION POINT THEN # PHOTOSYNTHESIS COULD LOSE THERMAL SENSITIVITY AND EXHIBIT A BROADERTHERMALOPTIMUMTHANITWOULDIF!WERE #/ SATURATED )N THE CASE OF THE RESPONSES IN &IG THESTIMULATIONOF!ATTHETHERMALOPTIMUM BYINCREASING#/ISEXPLAINEDBYINCREASINGTHE OPERATING #I FROM THE INITIAL SLOPE REGION TO THE #/ SATURATED PLATEAU 7HEN THE OPERATING #I IS ABOVETHE#/SATURATIONPOINT THE!4RESPONSE ISPRONOUNCED REFLECTINGTHETEMPERATURESTIMULA TIONOFTHE#/ SATURATEDPLATEAU&IGC 5NLIKE # PHOTOSYNTHESIS WHERE THE INITIAL SLOPEOFTHE#/RESPONSECURVEATLIGHTSATURA TION GENERALLY REFLECTS 2UBISCO CAPACITY THE !# I INITIAL SLOPE OF # PHOTOSYNTHESIS IS MODELED TO LARGELY REFLECT THE ACTIVITY OF 0%0#

10


VON #AEMMERER AND &URBANK VON #AEMMERER !T LOW #/ 0%0# OPERATES BELOWITS+MFOR#/ ANDTHUSHASAWEAKRES PONSETOTEMPERATURE,AISKAND%DWARDS HENCE THEINITIALSLOPEISALSOINSENSITIVETOTEM PERATURE4HE#/SATURATEDPLATEAUISMODELEDTO REFLECT THE MINIMUM OF EITHER 2UBISCO CAPACITY 2U"0REGENERATIONCAPACITY OR0%0REGENERATION INMOSTSITUATIONSVON#AEMMERERAND&URBANK VON#AEMMERER 3AGE !TCOOLER TEMPERATURES THE REDUCTION IN THE #/ SATURATED PLATEAUCANLOWERTHE#/SATURATIONPOINTBELOW THE OPERATIONAL #I SO PHOTOSYNTHESIS BECOMES LIMITEDBYONEOFTHETEMPERATURE SENSITIVEPROC ESSESTHATDETERMINETHE#/ SATURATEDRATEOF! /NCETHISOCCURS PHOTOSYNTHESISEXHIBITSASTEEP DECLINEWITHFURTHERREDUCTIONSINTEMPERATURE 2ECENTEXAMINATIONSOFTHETHERMALRESPONSEOF #/ SATURATED!INCOLD TOLERANT#PLANTSINDICATE 2UBISCOCAPACITYISANIMPORTANTLIMITATIONONTHE #/ SATURATED PLATEAU AT COOLER TEMPERATURE m# BUT NOT AT WARM TEMPERATURES NEAR THE THERMAL OPTIMUM 3AGE AND +UBIEN )NSTEAD 2U"0REGENERATION 0%0REGENERATIONOR 0%0 CARBOXYLASE CAPACITY APPEARS TO LIMIT ! AT WARMER TEMPERATURES IN # PLANTS ALTHOUGH IT IS NOTCLEARWHICHISTHEMOSTIMPORTANT!CHALLENGE FOR THE FUTURE WILL BE DEVELOPING A CAPABILITY TO DISTINGUISH BETWEEN THESE POSSIBLE LIMITATIONS OVER#PHOTOSYNTHESISATELEVATEDTEMPERATURE B. Photorespiration in C3 and C4 Plants 0HOTORESPIRATION OCCURS BECAUSE 2UBISCO CAN BOTHOXYGENATEANDCARBOXYLATE2U"04HEOXY GENATION OF 2U"0 PRODUCES PHOSPHOGLYCOLATE WHICHMUSTBECONVERTEDBACKTO0'!THROUGH THEEXPENDITUREOFPHOTOSYNTHETICENERGYANDTHE LOSSOFPREVIOUSLYFIXED#/4HUS THEOXYGENA TIONOF2U"0ANDTHEASSOCIATEDPHOTORESPIRATORY METABOLISMSIGNIFICANTLYINHIBIT#PHOTOSYNTHE SIS IN WARM LOW #/ CONDITIONS FAVORING PHO TORESPIRATION3HARKEY )NHOTENVIRONMENTS WHERE # PHOTOSYNTHESIS IS MOST PRODUCTIVE I NHIBITIONDUETOPHOTORESPIRATIONIN#SPECIESIS ǻ %HLERINGER ET AL 3AGE AND 0EARCY 0HOTORESPIRATION EXPLAINS MUCH OF THE D IFFERENCE IN THE RESPONSES OF # AND # PHOTOSYNTHESIS TO TEMPERATURE 5NDER NON PHO TORESPIRATORY CONDITIONS OXYGEN OR HIGH

#/ THE !4 RESPONSES OF ECOLOGICAL SIMILAR # AND # SPECIES BECOME SIMILAR 0EARCY AND %HLERINGER &OR EXAMPLE THE THERMAL OPTIMUMOF#PHOTOSYNTHESISINCREASESTOWARDS THE#VALUEWHENPHOTORESPIRATIONISREDUCEDBY / REDUCTION OR #/ ENRICHMENT 0EARCY AND %HLERINGER 3AGEAND+UBIEN #PLANTSALSOEXPERIENCEPHOTORESPIRATION BUT ITISGENERALLYSMALL ESTIMATEDTOBEǻOF! UNDERPHYSIOLOGICALCONDITIONSIN.!$0 -%AND .!$ -%SUBTYPES6OLKAND*ACKSON +U AND%DWARDS &URBANKAND"ADGER DE 6EAU AND "URRIS ,AISK AND %DWARDS VON#AEMMERER 9OSHIMURA ETAL 5ENOETAL OROFTHE# VALUE$AIETAL #SPECIESEXPRESS A FULL COMPLIMENT OF PHOTORESPIRATORY ENZYMES BUTATLEVELSMUCHLOWERTHANOBSERVEDIN#SPE CIES +U AND %DWARDS 9OSHIMURA ET AL 5ENOETAL 0HOTORESPIRATIONISDIF FICULTTOOBSERVEIN#SPECIES BECAUSEPHOTORES PIRATORY#/RELEASEOCCURSINTHEBUNDLESHEATH CELLS4HIS#/ISEITHERQUICKLYRE ASSIMILATEDBY BUNDLE SHEATH 2UBISCO OR SHOULD IT ESCAPE THE BUNDLE SHEATH IS CAPTURED BY 0%0 CARBOXYLASE AND SENT BACK TO THE BUNDLE SHEATH 6OLK AND *ACKSON +UAND%DWARDS $AIETAL (ENCE THEREISLITTLEOBSERVEDPHOTORESPI RATION RESPONSE TO TEMPERATURE UNLESS THE #/ LEVELINTHEBUNDLESHEATHISREDUCED FOREXAMPLE BYDROUGHTSTRESS OR/LEVELISINCREASED+UAND %DWARDS $AIETAL )NMAIZELEAVES AT/ THEQUANTUMYIELDOFPHOTOSYNTHESIS DECLINESABOUTFROMm#TOm# INDICAT INGAPROGRESSIVERISEINPHOTORESPIRATIONWITHRIS INGTEMPERATURE$AIETAL !T/ BY CONTRAST THE QUANTUM YIELD OF #/ UPTAKE IN MAIZEISUNAFFECTEDBYTEMPERATUREABOVEm# INDICATINGTHATPHOTORESPIRATIONRATESREMAINLOW IN#PLANTSINCURRENTATMOSPHERICCONDITIONS C. Quantum Yield 4HEMAXIMUMQUANTUMYIELDOFPHOTOSYNTHESIS ISEQUALTOTHEINITIAL LINEARSLOPEOFTHERESPONSE OF!TOABSORBEDLIGHTINTENSITY-AXIMUMQUAN TUMYIELDISCLOSELYASSOCIATEDWITHTHEBIOGEO GRAPHICDISTRIBUTIONOF#VERSUS#GRASSES AND APPROXIMATES THE RELATIVE PHOTOSYNTHETIC AND GROWTHPERFORMANCEOF#AND#SPECIESACROSSA RANGE OF TEMPERATURES %HLERINGER

0.12

Quantum Yield mol CO 2 mol 1 photon

%HLERINGERETAL 4HEMAXIMUMQUANTUM YIELD OF # PHOTOSYNTHESIS IS TYPICALLY GREATER THAN#PHOTOSYNTHESISABOVEm# ANDLESSTHAN # PHOTOSYNTHESIS BELOW m# %HLERINGER AND "JORKMAN %HLERINGER AND 0EARCY "ETWEEN m# AND m# A CROSSOVER TYPICALLY OCCURSBETWEENTHE#AND#QUANTUMYIELDSTHAT DEPENDS UPON #/ LEVEL AND THE SUB TYPE OF # PHOTOSYNTHESIS%HLERINGERAND"JORKMAN %HLERINGER %HLERINGER AND 0EARCY %HLERINGER ET AL .!$0 -% SUB TYPES HAVE A HIGHER QUANTUM YIELD THAN .!$ -% # SPECIES ANDTHUSALOWERCROSS OVERTEMPERATURE OF # VERSUS # QUANTUM YIELD %HLERINGER AND 0EARCY 1UANTUMYIELD BASEDMODELSHAVE BEENFREQUENTLYUSEDTOPREDICTBOTHTHEDISTRIBU TIONOF#SPECIESACROSSTHEGLOBE ANDTHECHANGE INDISTRIBUTIONWITHPASTANDFUTURECLIMATECHANGE %HLERINGER %HLERINGERETAL #OLLATZETAL 3TILLETAL &OREXAM PLE THETRANSITIONTEMPERATUREBETWEEN#AND# DOMINANCE OF THE .ORTH !MERICAN GRASS FLORA CORRESPONDSTOTHECROSSOVERTEMPERATUREFOR# AND#QUANTUMYIELDS%HLERINGER 4HECLOSEASSOCIATIONBETWEENMAXIMUMQUAN TUM YIELD AND PERFORMANCE PARAMETERS SUCH AS NET #/ ASSIMILATION RATE GROWTH OR ECOLOGICAL DOMINANCE HAVELEDTOTHEHYPOTHESISTHATQUAN TUMYIELDDIFFERENCESARECAUSALMECHANISMSTHAT EXPLAINTHERELATIVEPERFORMANCEOF#VERSUS# VEGETATION %HLERINGER AND "JORKMAN %HLERINGER #OLLATZETAL 3TILLETAL 4HIS HYPOTHESIS HAS BEEN QUESTIONED BECAUSE MAXIMUM QUANTUM YIELD DIFFERENCES WOULD HAVE PHYSIOLOGICAL SIGNIFICANCE ONLY AT VERYLOWLIGHTLEVELS3AGEAND+UBIEN )N MOST # PLANTS THE VAST MAJORITY OF CARBON IS ABSORBED AT LIGHT INTENSITIES ABOVE THE RANGE WHERE QUANTUM YIELD DIFFERENCES WOULD BE SIG NIFICANT INDICATINGMAXIMUMQUANTUMYIELDISA SMALL CONTRIBUTOR TO DIFFERENCES IN # PERFORM ANCE,ONG 3AGEETAL +UBIENAND 3AGE B (OWEVER AS DEMONSTRATED BY &IG MAXIMUM QUANTUM YIELD IS INVERSELY RELATED TO THE PHOTORESPIRATION RATE IN # PLANTS ANDTHUSISAROBUSTINDEXOFTHERELATIVEDRAGON #PHOTOSYNTHESISCAUSEDBYPHOTORESPIRATION -AXIMUMQUANTUMYIELDISJUSTONEMEASURE OFQUANTUMYIELDTHATHASSIGNIFICANCEFORUNDER STANDING RELATIONSHIP BETWEEN TEMPERATURE AND THEPERFORMANCEOF#RELATIVETO#PLANTS!S


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0.06

0.04 0.0

0.1 0.2 0.3 0.4 Photorespiration / photosynthesis

&IG 4HE RELATIONSHIP BETWEEN THE MAXIMUM QUAN TUM YIELD OF PHOTOSYNTHESIS AND THE RATIO OF PHOTORES PIRATION TO PHOTOSYNTHESIS FOR A # PLANT -ODELED ACCORDING TO 3AGE AND +UBIEN USING THE EQUATION dA g dI a

0.125 0.0625Vo / Vc WHERE D! D) IS THE INITIAL G A 1 Vo / Vc

SLOPE OF THE LIGHT RESPONSE OF ! VERSUS ABSORBED PHOTONS )A AND 6O6C IS THE OXYGENATION TO CARBOXYLATION RATE OF 2UBISCO

LIGHT INTENSITY INCREASES ABOVE ǻ rMOL MȪ SȪ PHOTOPROTECTION MECHANISMS ARE ACTI VATEDTHATREDUCETHEQUANTUMEFFICIENCYOFPHO TOSYNTHESIS CAUSING THE INSTANTANEOUS QUAN TUM YIELD TO DECLINE BELOW THE MAXIMUM QUANTUMYIELDOBSERVEDATLOWLIGHT4EMPERATURE AFFECTSTHEENGAGEMENTOFPHOTOPROTECTIONMECH ANISMSANDTHUSTHEINSTANTANEOUSQUANTUMYIELD AT ANY GIVEN LIGHT INTENSITY +UBIEN AND 3AGE B&ARAGEETAL !TCOOLTEMPERATURES PHOTOPROTECTIONISGREATERINBOTH#AND#SPE CIES BECAUSETHETEMPERATURELOWERSTHECAPACITY OFTHECARBONFIXATIONREACTIONSTOUSEABSORBED LIGHT ENERGY ,ABATE ET AL (ALDIMANN +UBIEN AND 3AGE B 3AVITCH ET AL # PLANTS AT LOW TEMPERATURE APPEAR TO MAINTAINGREATERLEVELSOFPHOTOPROTECTION DUETO AGREATERRESTRICTIONINDEMANDFORENERGY,ABATE ET AL +UBIEN AND 3AGE B )N TWO BOREAL GRASS SPECIES +UBIEN AND 3AGE B OBSERVED THAT RELAXATION OF PHOTOPROTECTIVE QUENCHING FOLLOWING SHADING WAS FASTER IN A # GRASS #ALAMAGROSTIS CANADENSIS THAN A CO OCCURRING # GRASS -UHLENBERGIA GLOMERATA BELOWm#+UBIENAND3AGE B 4HISLAG IN RECOVERY OF THE INSTANTANEOUS QUANTUM YIELD

10


FURTHERREDUCESTHEOVERALLLIGHTUSEEFFICIENCYOF #PHOTOSYNTHESISINADYNAMICLIGHTENVIRONMENT ONACOOLDAY$UETOPHOTOPROTECTION THEACTUAL QUANTUM YIELD DIFFERENCES BETWEEN # AND # SPECIES IN THE FIELD MAY NOT REFLECT MAXIMUM QUANTUMYIELDDIFFERENCESMEASUREDINTHELAB D. Rubisco Limitations )N#PLANTS THETEMPERATURERESPONSEOFTHEFULLY ACTIVATED CAPACITY OF 2UBISCO IN VITRO IS NEARLY IDENTICAL TO THE TEMPERATURE RESPONSE OF GROSS PHOTOSYNTHESIS BELOW ǻm# &IG "ELOW ABOUT m# SIMILAR VALUES OF 2UBISCO ACTIVITY INVITROAND#/ASSIMILATIONRATEHAVEBEENDEM ONSTRATEDFORTHE#DICOTWEED!MARANTHUSRET ROFLEXUSORIGINATINGFROMNORTHERN%UROPE3AGE ALPINEGRASSESFROMTHE2OCKY-OUNTAINS OF .ORTH !MERICA 0ITTERMANN AND 3AGE THE # DICOT &LAVERIA BIDENTIS AND THE BOREAL#GRASS-UHLENBERGIAGLOMERATA"JORK MAN AND 0EARCY AND 0EARCY ALSO NOTED SIMILAR CHANGES IN 2UBISCO ACTIVITY AND PHOTOSYNTHETICCAPACITYIN!TRIPLEXSHRUBSBELOW m# LEADINGTHEMTOSUGGESTTHAT2UBISCOMAY LIMIT # PHOTOSYNTHESIS AT LOW TEMPERATURE "ECAUSE 2UBISCO OPERATES NEAR #/ SATURATION IN THE # BUNDLE SHEATH AT COOLER TEMPERATURES 3AGE THEIDENTICALTEMPERATURERESPONSE

Gross Photosynthesis or V cmax Mmol m 2 s 1

70

F. bidentis Ag F. bidentis Vcmax

60

Flaveria

M. giomerata Ag M. glomerata Vcmax

50 40 30 20

Muhlenbergia

10 0

0

10

20 30 Leaf Temperature, °C

40

&IG 4HE TEMPERATURE RESPONSE OF GROSS PHOTOSYNTHESIS !G AND THE MAXIMUM 2UBISCO ACTIVITY IN VITRO 6CMAX IN THE # PLANTS &LAVERIA BIDENTIS AND -UHLENBERGIA GLOMER ATA2UBISCOSAMPLESWERECOLLECTEDFROMTHESAMEPLANTSIN WHICH!WASMEASURED&ROM+UBIEN

OF 2UBISCO AND CARBON ASSIMILATION IS STRONG EVIDENCE THAT 2UBISCO CAPACITY IS AN IMPORTANT LIMITATION FOR PHOTOSYNTHESIS AT COOLER TEMPERA TURESIN#PLANTS!BOVEm# 2UBISCOCAPACITY INVITROEXCEEDSTHEOBSERVEDRATEOFPHOTOSYNTHE SIS INDICATING2UBISCOISNOTAMAJORLIMITATION UNLESSTHEBUNDLESHEATH#/LEVELSBECOMELOW ENOUGHTOGREATLYLIMIT2U"0CARBOXYLATION4HIS POSSIBILITYAPPEARSUNLIKELYGIVENTHELOWLEVELOF PHOTORESPIRATION ESTIMATED FOR # LEAVES $AI ETAL 4OFURTHEREXAMINETHEPOSSIBILITYTHAT2UBISCO CONTROLS#PHOTOSYNTHESISATCOOLERTEMPERATURE +UBIEN ET AL EXAMINED THE RELATIONSHIP BETWEENGROSSPHOTOSYNTHESISAND2UBISCOCAPAC ITYIN&LAVERIABIDENTISPLANTSTRANSFORMEDWITHAN ANTISENSE CONSTRUCT AGAINST THE SMALL SUBUNIT OF 2UBISCO!NTISENSE&BIDENTISHADANYWHEREFROM TO LESS 2UBISCO THAN WILD TYPE LINES &URBANKETAL )F2UBISCOWASLIMITINGAT LOW TEMPERATURE IN THE WILD TYPE THEN REDUCING 2UBISCOVIAANANTISENSECONSTRUCTWOULDINCREASE THE TEMPERATURE AT WHICH THE IN VIVO KCAT GROSS #/ UPTAKE NUMBER OF 2UBISCO ACTIVE SITES WOULDDIVERGEFROMTHEINVITROKCATRUBISCOACTIV ITYNUMBER OF ACTIVE SITES #ONSISTENTLY THE INVIVOKCATOFTHEWILDTYPEDIVERGEDFROMTHEIN VITRORESPONSEATABOUTm# WHILETHEANTISENSE LINESDIDNOTSTATISTICALLYDIVERGEUNTILABOVEm# +UBIEN ET AL &URTHERMORE THE RATIO OF GROSS #/ ASSIMILATION IN THE WILD TYPE TO ANTI SENSELINEWASEQUALTOTHERATIOOFRUBISCOCONTENT INTHETWOLINESBELOWm# WHICHSHOULDBETHE CASEIF2UBISCOISLIMITING!BOVEm# THERATIO OFGROSS#/ASSIMILATIONINTHEWILD TYPEVERSUS ANTISENSE LINES DECLINED BELOW THE CONTENT RATIO REFLECTINGTHEAPPEARANCEOFANON 2UBISCOLIMITA TIONONPHOTOSYNTHESISINTHEWILDTYPELINE )N#PLANTS THEREISGENERALLYLITTLEORNOCHANGE INTHERATIOOFTHEQUANTUMYIELDOFPHOTOSYSTEM)) TO THE QUANTUM YIELD OF GROSS #/ FIXATION Ʒ03))Ʒ#/ FROM MODERATE TO HIGH TEMPERATURE /BERHUBER AND %DWARDS %DWARDS AND "AKER HOWEVER THERATIOINCREASESASLEAF TEMPERATURE DECLINES BELOW ǻm# 4HIS INCREASEINƷ03))Ʒ#/BEGINSATAHIGHERTEMPERA TUREINTHEANTISENSE&BIDENTISLINESWITHREDUCED 2UBISCO CONTENT AND REACHES A GREATER VALUE AT COOLER TEMPERATURES +UBIEN ET AL )N # PLANTS Ʒ03))Ʒ#/ IS AFFECTED BY THE RATE OF #/LEAKAGEOUTOFTHEBUNDLESHEATHCELL BECAUSE

LEAKAGE REDUCES Ʒ#/ BUT DOES NOT AFFECT Ʒ03)) 3IEBKE ET AL +UBIEN ET AL INTER PRETEDTHERISEINƷ03))Ʒ#/ATLOWTEMPERATUREAS EVIDENCE FOR INCREASED #/ LEAKAGE )F 2UBISCO CAPACITYISREDUCEDBYDECLININGTEMPERATURETOA GREATERDEGREETHANTHE#CYCLEACTIVITY THEBUN DLE SHEATH #/ LEVEL SHOULD INCREASE CREATING A GREATER#/GRADIENTBETWEENTHEMESOPHYLLAND BUNDLESHEATHCELLS ANDTHUSDRIVINGAFASTERLEAK RATE)NCREASEDPHOTORESPIRATIONCANALSOINCREASE Ʒ03))Ʒ#/ BUTTHISSHOULDNOTBEACONCERNATLOW TEMPERATURE DUE TO AN INCREASE IN THE SPECIFICITY OF 2UBISCO FOR #/ RELATIVE TO / *ORDAN AND /GREN 7HYDOES2UBISCOBECOMELIMITINGIN#SPE CIES AT COOLER TEMPERATURES 4HE ABILITY OF # PLANTSTOCONCENTRATE#/AROUND2UBISCOTONEAR THE#/SATURATIONPOINT ANDTHEHIGHERKCATOF# 2UBISCO ALLOWS # SPECIES TO UTILIZE THE 2U"0 GENERATEDBYTHELIGHTREACTIONSWITHATHIRDTOA QUARTEROFTHE2UBISCOAS#SPECIES3CHMITTAND %DWARDS /SMONDETAL 3AGEETAL 3AGE !TELEVATEDTEMPERATURE THE CATALYTICCAPACITYOF2UBISCOISMORETHANSUFFI CIENTTOMEETTHE#/AND2U"0SUPPLYPROVIDED BYTHE#CYCLEANDLIGHTREACTIONS RESPECTIVELY (OWEVER 2UBISCOHASA1NEAR SOITSTURNO VER CAPACITY DECLINES RAPIDLY WITH TEMPERATURE !T COOLER TEMPERATURES THE 2UBISCO CAPACITY DECLINESBELOWTHECAPACITYOFTHE#CYCLEAND 2U"0 REGENERATION SIMPLY BECAUSE OF THE LOW AMOUNTOF2UBISCOINTHE#RELATIVETOA#LEAF # PLANTS COULD CONCEIVABLY COMPENSATE FOR COOLER TEMPERATURES BY PRODUCING MORE 2UBISCO RELATIVE TO OTHER LEAF PHOTOSYNTHETIC ENZYMES 4HEREISLITTLEEVIDENCETOSUPPORTTHISHYPOTHESIS IN#SPECIESADAPTEDTOCOOLCLIMATESHOWEVER FEW STUDIES HAVE DIRECTLY ASSESSED 2UBISCO CON TENTINCOOL ANDWARM ADAPTED#SPECIESUNDER SIMILAR GROWTH CONDITIONS )N ONE SUCH COMPARI SON 0ITTERMANN AND 3AGE EXAMINED HIGH ANDLOWELEVATIONECOTYPESOF"OUTELOUAGRACILIS AND OBSERVED NO CLEAR DIFFERENCE IN 2UBISCO CONTENT $URING ACCLIMATION TO COLD INCREASED 2UBISCO CONTENT COULD BE EXPECTED TO RELIEVE A 2UBISCO LIMITATION HOWEVER THERE IS NO EVI DENCETOSUPPORTSUCHAPOSSIBILITY)NTHECHILLING TOLERANT#SPECIES-ISCANTHUSGIGANTEUS -UH LENBERGIA MONTANA AND - GLOMERATA 2UBISCO CONTENT WAS SIMILAR IN PLANTS GROWN IN CHILLING CONDITIONSǻm# COMPAREDTOWARMCONDITIONS

Rowan F. Sage et al. 0ITTERMANN AND 3AGE +UBIEN AND 3AGE A.AIDUETAL .AIDUAND,ONG 7ANG ET AL A )N CONTRAST TO RESPONSES IN CHILLINGTOLERANTPLANTS CHILLING SENSITIVE#PLANTS SUCHASMAIZESHOWAPROLONGEDDECLINEIN2UBISCO CONTENT FOLLOWING GROWTH IN CHILLING CONDITIONS .AIDUETAL !LSO GROWTHATTEMPERATURES ABOVEm#REDUCED2UBISCOCONTENTIN!TRIPLEX LENTIFORMIS AND THREE WARM ADAPTED # SPECIES RELATIVE TO 2UBISCO LEVEL IN LEAVES GROWN BELOW m#0EARCY $WYERETAL !TLOW TEMPERATUREWHERE2UBISCOISPOTENTIALLYLIMITING HOWEVER THERE ARE FEW STUDIES DESCRIBING THIS PHENOMENON 4HELACKOFANOBVIOUSABILITYOFCOOL TOLERANT # SPECIES TO INCREASE 2UBISCO FOLLOWING COLD ACCLIMATION OR ADAPTATION INDICATES THAT THE AMOUNT OF 2UBISCO # PLANTS MAY CONTAIN IS EVOLUTIONARILY CONSTRAINED 3AGE /NE POSSIBLECONSTRAINTMAYBETHESTRUCTURALPROP ERTIES OF THE # LEAF )N # LEAVES 2UBISCO IS COMPARTMENTALIZEDINTOAFRACTIONOFTHEBUNDLE SHEATHVOLUME EITHERATTHEPERIPHERYINCLASSI CAL.!$0 -%GRASSES ORALONGTHEINNERHALF OF THE BUNDLE SHEATH CELLS IN MOST OF OTHER # TYPES $ENGLER AND .ELSON 3AGE AND -C+OWN 4HISLOCALIZATIONPLACESAVOL UMELIMITONHOWMUCH2UBISCOCOULDBEPACK AGED INTO A # LEAF 4HERE ARE ALSO ECOLOGICAL CONSTRAINTS TO CONSIDER )NVESTING IN A LARGE AMOUNT OF 2UBISCO AT LOW TEMPERATURE WOULD REDUCETHENITROGENUSEEFFICIENCYADVANTAGEOF # PLANTS DURING WARMER TEMPERATURES LATER IN THE GROWING SEASON WHEN THE # PATHWAY IS MOSTADAPTIVE E. Rubisco Activase Limitations !SOBSERVEDIN#PLANTS THEACTIVATIONSTATEOF 2UBISCODECLINESABOVETHETHERMALOPTIMUMOF PHOTOSYNTHESIS IN MAIZE IN CLOSE PROPORTION TO THE DECLINE IN PHOTOSYNTHESIS #RAFTS "RANDNER AND 3ALVUCCI #RAFTS "RANDNER AND 3AL VUCCIARGUEDTHAT2UBISCODEACTIVATIONISDUETO HEATLABILITYOF2UBISCOACTIVASE ANDTHELOSSOF 2UBISCOACTIVATIONISRESPONSIBLEFORTHEDECLINE IN ! ABOVE THE THERMAL OPTIMUM (ENDRICKSON ETAL FOUNDNOEVIDENCEFORALIMITATIONBY 2UBISCO ACTIVASE AT ELEVATED TEMPERATURE IN THE # SPECIES &LAVERIA BIDENTIS WITH GENETICALLY REDUCEDLEVELSOF2UBISCOACTIVASE4HEYOBSERVED

10


NO RELATIONSHIP BETWEEN ACTIVASE CONTENT AND ! NOR BETWEEN ACTIVASE CONTENT AND 2UBISCO CAR BAMYLATION STATE BETWEEN AND OF WILD TYPEACTIVASELEVELS4HECARBAMYLATIONSTATE OF 2UBISCO WAS REDUCED AT m# COMPARED TO m# BUT THIS CHANGE WAS NOT CORRELATED WITH ACTIVASECONTENT4HESERESULTSSUPPORTTHEPOSSI BILITY THAT DEACTIVATION OF 2UBISCO AT ELEVATED TEMPERATURES DOES NOT REFLECT A HEAT LABILITY OF ACTIVASE BUTINSTEADMAYBEARESPONSETOOTHER LIMITATIONSINTHEPHOTOSYNTHETICAPPARATUS F. C4 Cycle Limitations 1. Pyruvate-Pi-Dikinase

0YRUVATE 0I DIKINASE00$+ REGENERATES0%0IN THE # CYCLE USING THE EQUIVALENT OF TWO !40 MOLECULES +ANAI AND %DWARDS )N TEM PERATURESTUDIES ATTENTIONHASFOCUSEDON00$+ IN#PLANTSBECAUSEITCANSHOWSUBSTANTIALCOLD LABILITY ANDTHEACTIVITYINVIVOISREPORTEDTOBE CLOSE TO OR BELOW OBSERVED PHOTOSYNTHETIC RATES 4AYLORETAL 3UGIYAMAAND"OKU 3UGIYAMAETAL,ONG 5SUDAETAL 0OTVIN ET AL 3IMON AND (ATCH -ATSUBAETAL $UETAL A 4HE COLD LABILITY IS TWOFOLD THE ACTIVE ENZYME IS A TETRAMERTHATDISSOCIATESINTOINACTIVEMONOMERS INVITROBETWEENm#ANDm#INMOST#SPE CIESEXAMINED ANDTHERATEOFACTIVATIONSLOWS WHILE DEACTIVATION ACCELERATES AT COOL TEMPERA TURES PARTICULARLY IN # PLANTS FROM WARM CLI MATES (ATCH 7ANG ET AL B #IRCUMSTANTIALEVIDENCEFOR00$+HAVINGAMAJOR LIMITINGROLEOVER!IN#PLANTSATLOWTEMPERA TURE HAS BEEN THE CLOSE ASSOCIATION BETWEEN THE TEMPERATURE FOR COLD LABILITY OF 00$+ AND THE MEAN MINIMUM GROWING SEASON TEMPERATURE WHERE # SPECIES DROP OUT OF REGIONAL FLORAS ,ONG 7HILETHEREISSOMEEVIDENCEFORA 00$+LIMITATIONINCERTAINSPECIES FOREXAMPLE INWARMECOTYPESOFBARNYARDGRASS0OTVINETAL MAIZE 7ANG ET AL B SUGARCANE $U ET AL A AND SORGHUM 4AYLOR ET AL PARTICULARLYAFTERASUDDENCHILL THEREISLIT TLEEVIDENCETHATCOLD TOLERANT#PLANTSARE00$+ LIMITEDWHENACCLIMATEDTOTHECOLD3IMONAND (ATCH $UETAL A B0ITTERMANNAND 3AGE +UBIENAND3AGE A7ANG ETAL B )NTHECOLD TOLERANTBIOENERGYCROP

-ISCANTHUS GIGANTEUS PLANTS ACCLIMATE TO THE COLD BY INCREASING 00$+ CONTENT TO A GREATER DEGREETHANOTHERENZYMES POTENTIALLYOVERCOM INGA00$+LIMITATIONWHICHMAYINITIALLYOCCUR UPON CHILLING .AIDU ET AL 7ANG ET AL B )NTHECOLDTOLERANT#GRASS-UHLENBER GIA MONTANUM TRANSFER OF PLANTS TO m# NIGHTS LEDTOADROPINPHOTOSYNTHESISATALLMEASUREMENT LEVELSOF#/ATBOTHm#ANDm# INDICATING ENZYMESINTHE#CYCLEHADBEENIMPAIRED!FTER WEEKSOFACCLIMATIONTOm#NIGHTS PHOTOSYN THESISHADFULLYRECOVEREDTOTHEPRE CHILLINGVAL UES0ITTERMANNAND3AGE 4HE LABILITY AND ACTIVATION CHARACTERISTICS OF 00$+ATLOWTEMPERATUREDEPENDUPONTOTALPROTEIN ANDSOLUTECONCENTRATIONS)NCREASED00$+ AND HIGHERPOLYOLANDDIVALENTCATIONCONCENTRATIONS STABILIZETHE00$+TETRAMERINCOLDENVIRONMENTS IN VITRO (ATCH 3HIRAHASHI ET AL 9AMAZAKIAND3UGIYAMA +RALLETAL )NMANYSPECIES COLDADAPTATIONOF00$+ACTIV ITYISNOTASSOCIATEDWITHCHANGESTO00$+ITSELF BUT INSTEAD REFLECT AN ALTERED CELLULAR ENVIRON MENT3IMON NOTEDTHAT00$+FROMACOLD AND WARM ECOTYPE OF %CHINOCHLOA CRUS GALLI EXHIBITED IDENTICAL KINETIC PROPERTIES 3UGARCANE VARIETIES DIFFERING IN COLD TOLERANCE ALSO EXPRESS 00$+ FORMS WITH SIMILAR THERMAL RESPONSES INVITRO$UETAL B 3OMEFORMSOF00$+HAVEGREATERCOLDSTABIL ITY &LAVERIA BROWNII EXPRESSES A 00$+ THAT EXHIBITSGREATERCOLDSTABILITYTHANTHE00$+FROM ITS CLOSE RELATIVE THE # PLANT &LAVERIA BIDENTIS "URNELL 5SAMI ET AL /HTA ET AL 4HISDIFFERENCEISATTRIBUTEDTOVARIATIONIN ASFEWASTHREEAMINOACIDRESIDUESNEARTHECAR BOXY TERMINUS/HTAETAL 2ECENTLY COLD TOLERANT SEGMENTS OF 00$+ GENES HAVE BEEN TRANSFORMED INTO PARTS OF THE MAIZE GENE FOR # 00$+ LEADINGTOAHYBRIDGENETHATCODEDFORA COLDTOLERANTFORMOF00$+INMAIZE/HTAETAL 4HERESULTINGIMPACTONPHOTOSYN THESISWASSMALL HOWEVER4HEAUTHORSCLAIMED TOHAVEDETECTEDASLIGHTENHANCEMENTOFPHOTO SYNTHESIS BY THE CHIMERIC PROTEIN AT m# BUT INCONSISTENTLY THEREWASNOENHANCEMENTATANY OTHERTEMPERATURE INCLUDINGm# WHICHISCLOSE TOTEMPERATURESCOMMONLYUSEDASCHILLINGTREAT MENTSINMANYSTUDIES/HTAETAL !NIMPORTANTTOOLINEVALUATINGTHECONTROLAN ENZYME HAS OVER PHOTOSYNTHESIS IS TO DEVELOP

ANTISENSECONSTRUCTSAGAINSTTHEENZYMEOFINTEREST WHICH THEN ALLOWS FOR SELECTIVE REDUCTION OF THAT ENZYME 5SING AN ANTISENSE APPROACH &URBANK ETAL ESTIMATEDCONTROLCOEFFICIENTSFOR00$+ IN &LAVERIA BIDENTIS ATm#WEREǻ WHILE THECONTROLCOEFFICIENTFOR2UBISCOWASESTIMATED WITH 2UBISCO ANTISENSE LINES TO BE 5NFOR TUNATELY THERE HAS BEEN NO FOLLOW UP WORK WITH THESE00$+ANTISENSELINESATLOWERTEMPERATURE ANDTHEYARENOLONGERVIABLE24&URBANK PERSONAL COMMUNICATION &OLLOW UP WORK WITH THEANTI 2UBISCOLINEOF&BIDENTISATLOWERTEM PERATURE SHOWS THE 2UBISCO CONTROL COEFFICIENT APPROACHESUNITYBELOWm# AND#/LEAKINESS INCREASES WHICH REFLECTS A GREATER #/ GRADIENT BETWEENMESOPHYLLANDBUNDLESHEATHCELLS+UB IENETAL )FRELATIVE00$+LIMITATIONSHAD INCREASED LEAKINESSSHOULDHAVEDECLINEDSINCETHE #/DELIVERYTOTHEBUNDLESHEATHWOULDSLOW )NSUMMARY THEREISLITTLEDIRECTEVIDENCETHAT 00$+ISAMAJORLIMITATIONINCOLD TOLERANTPLANTS THATHAVEACCLIMATEDTOCOOLERTEMPERATURES00$+ LIMITATIONS MAY BE IMPORTANT IN COLD SENSITIVE GENOTYPES IN BARNYARD GRASS MAIZE SUGARCANE ANDSORGHUMHOWEVER INSOMEOFTHESESPECIES 00$+SHOWSINCREASEDCOLDSTABILITYINVARIETIES FROMCOOLERCLIMATES3IMONAND(ATCH $U ET AL B 4HUS EVOLUTIONARY ADAPTATION TO COOLERCONDITIONSINCLUDESSTABILIZATIONOF00$+ 4HERE IS NO CLEAR EVIDENCE THAT COLD LABILITY OF 00$+ISTHEPROBLEMTHATEXPLAINSTHERARITYOF# SPECIESINCOLDCLIMATES 2. PEP Carboxylase

0%0 CARBOXYLASE 0%0# LIKE 00$+ EXHIBITS COLD LABILITY IN # PLANTS FROM WARM CLIMATES WHILE#PLANTSFROMCOOLCLIMATESEXHIBITAFORM OF 0%0 CARBOXYLASE THAT REMAINS STABLE AT LOW TEMPERATURE +RALL AND %DWARDS FOR TWO SPECIES OF 0ANICUM -ATSUBA ET AL FOR 3PARTINA AND :OYSIA GRASSES )N :OYSIA 0%0# ACTIVITYDECLINEDBYTWO THIRDSUPONEXPOSURETO mm#DAYNIGHTCONDITIONS LEADINGTOTHECON CLUSIONITCOULDBEANIMPORTANTLIMITATIONINTHIS COLD INTOLERANT PLANT AFTER PROLONGED COLD EXPO SURE -ATSUBA ET AL )N THE COLD TOLERANT SPECIES 3PARTINA ANGLICA 0%0# LEVELS FELL INTHEFIRSTWEEKOFCOLDEXPOSUREBUTTHENSTABI LIZED-ATSUBAETAL )NSUGARCANEFOLLOW ING COLD EXPOSURE 0%0# ACTIVITY IS RELATIVELY

Rowan F. Sage et al. STABLE AT LOW TEMPERATURE $U ET AL A B #OLD ADAPTEDECOTYPESOF%CHINOCHLOACRUS GALLI DIFFEREDFROMWARMECOTYPESBYHAVINGALOWER KCAT ACROSS A RANGE OF ASSAY TEMPERATURES OTHER WISETHEENZYMESWERESIMILARANDDIDNOTACCOUNT FOR DIFFERENCES IN LOW TEMPERATURE PERFORMANCE OFTHEECOTYPES(AMELAND3IMON 0%0#THUSSEEMSTOHAVELITTLECONTROLOVER! AT COOLER TEMPERATURES IN COLD TOLERANT SPECIES EXCEPT PERHAPS SHORTLY AFTER FOLLOWING TRANSFER FROM WARM TO COOL CONDITIONS !NALYSES OF THE !#I RESPONSE IN A RANGE OF CHILLING TOLERANT # SPECIESSHOWTHEINITIALSLOPETOBEINSENSITIVETO DIFFERENCES IN MEASUREMENT TEMPERATURE EXCEPT SHORTLYAFTERCHILLING ANDTHEPHOTOSYNTHESISRATE INAIRTYPICALLYFALLSONTHE#/SATURATEDREGION OFTHECURVEWHERE2UBISCO 00$+ORLIGHTHAR VESTINGARETHOUGHTTOBELIMITING0ITTERMANNAND 3AGE 3AGE +UBIENAND3AGE A 4HUSWHILESOMEWARM ADAPTED#SPE CIES CAN SHOW A DECLINE IN 0%0# ACTIVITY THAT COULDLIMITPHOTOSYNTHESISINCOLDGROWTHCONDI TIONS ITAPPEARSTHAT0%0#ISALSONOTANENZYME THATWOULDEXCLUDE#PHOTOSYNTHESISFROMCOLD CLIMATES 3. Other Enzymes

.!$0 -$(CATALYZESTHECONVERSIONOF/!!TO MALATEINTHE#CYCLE+ANAIAND%DWARDS ANDHASBEENNOTEDTOHAVENOCONTROLOVER#PHO TOSYNTHESIS IN ANTISENSE &LAVERIA BIDENTIS PLANTS UNLESSTHECONTENTISREDUCEDBYABOUT&UR BANKETAL 4REVANIONETAL (ENCE THIS ENZYME WOULD NOT BE EXPECTED TO BECOME A MAJORLIMITATIONUNLESSITHADAMUCHHIGHERTHER MALDEPENDENCYTHAN2UBISCOAND00$+ WHICH MAYOCCURIFITWASEXTREMELYCOLDSENSITIVE$U ETALA B OBSERVEDALARGEREDUCTIONININI TIAL .!$0 -$( ACTIVITY WITH LOW TEMPERATURE EXPOSUREINACOLDSENSITIVELINESOFSUGARCANE BUT NOTACOLDTOLERANTLINETOTAL.!$0 -$(ACTIVITY INBOTHLINESWASLITTLEAFFECTED4HESERESULTSINDI CATEREGULATIONOFTHISENZYMEISSENSITIVETOCHILL INGINMALADAPTEDPLANTS "ECAUSETHEYLACK00$+ ITHASBEENSUGGESTED THAT0%0CARBOXYKINASE0#+ TYPEOF#PLANTS MAYBEINHERENTLYMORETOLERANTOFTHECOLDTHAN .!$0 -%AND.!$ -%TYPESOF#PLANTSTHAT RELY ON 00$+ FOR 0%0 REGENERATION -ATSUBA ETAL )NACOMPARISONOFTWO0#+ TYPEOF

10


# SPECIES THE COLD TOLERANT VARIETY 3PARTINA ANGLICA MAINTAINEDSTEADYLEVELSOF0#+FOLLOW INGTRANSFERTOm#GROWTHCONDITIONS WHEREAS 0#+ACTIVITIESDECLINEDBYOVERINTHECOLD SENSITIVE:OYSIAJAPONICA)N:OYSIA 0%0#LEVELS DECLINEDBYTWO THIRDS WHILE2UBISCOLEVELSFELL ABOUTCOMPAREDTOTHEINITIALCONTROLCONDI TIONATm#4HESERESULTSSUPPORTTHEVIEWTHAT LABILITY OF 0#+ AND 0%0# ARE NOT PROBLEMS IN COLD ADAPTED#SPECIES BUTCANLIMIT!INCOLD SENSITIVESPECIESEXPOSEDTOLOWTEMPERATURE /THERENZYMESOFPHOTOSYNTHESISAPPEARTOBE STABLEINCOLDTOLERANT#PLANTSFOLLOWINGCHILL ING ALTHOUGHTHEYMAYDECLINEINCOLDINTOLERANT PLANTS ,EEGOOD AND %DWARDS -ATSUBA ETAL $UETAL A.AIDUETAL )N :EA MAYS FOR EXAMPLE THERE IS A PROLONGED DECLINE IN A WIDE RANGE OF PROTEINS FOLLOWING EXPOSURE TO LOW TEMPERATURE INDICATING MANY PROBLEMS ARISE IN CHILLED MAIZE AS A RESULT OF A GENERALCOLDINTOLERANCE RATHERTHANALESIONSPE CIFICTOTHE#PATHWAY.AIDUETAL 7ANG ETAL B G. Electron Transport Limitations )N#PLANTS LIMITATIONSINELECTRONTRANSPORTARE DIFFICULT TO DISCERN BECAUSE THE MESOPHYLL AND BUNDLESHEATHCHLOROPLASTSCANDIFFERINTHEIRELEC TRON TRANSPORT CAPACITY AND THE ENERGY REQUIRE MENTSOFTHE#AND#CYCLESDIFFER!SARESULT FEWSTUDIESREPORTELECTRONTRANSPORTASAFUNCTION OFTEMPERATUREIN#PLANTS&ROMWHATISREPORTED ITISKNOWNTHATELECTRONTRANSPORTCAPACITYDECAYS ABOVETHETHERMALOPTIMUMINAMANNERTHATINDI CATESITCOULDBECOMEANIMPORTANTLIMITATIONAT HIGH TEMPERATURE "JORKMAN ET AL "ERRY AND "JORKMAN #ONSISTENTLY INCREASING TEMPERATUREABOVETHETHERMALOPTIMUMREDUCES THE#/SATURATEDRATEOFPHOTOSYNTHESISINMAIZE BUT HAS LITTLE EFFECT ON THE !#I INITIAL SLOPE AT LEASTTOm#-ASSADETAL )NMAIZE CHANGESINLEVELSOFMETABOLITESFROM THE#AND#CYCLESINDICATETHERECOULDBEALIM ITATION IN ENERGY SUPPLY AT m# ,ABATE ET AL &ROMm#TOm# THE0'!TOTRIOSEǻ0 RATIO DECLINED WHICH IS CONSISTENT WITH A REDUC TIONINENERGYUTILIZATION ASMAYOCCURIF2UBISCO OR00$+WERELIMITING(OWEVER ATm# 0'! 40 RATIOS INCREASED SHARPLY INDICATING ENERGY U TILIZATIONISNOLONGERLIMITING BUTENERGYSUPPLY

MAYBE,ABATEETAL ,OWENERGYSUPPLY INMAIZECOULDRESULTFROMEXTENSIVEPHOTOINHIBI TION THIS SPECIES EXPERIENCES AT LOW TEMPERATURE (ALDIMANN $ETAILEDMETABOLITEASSAYSON OTHER # SPECIES ACROSS A RANGE OF TEMPERATURES ARELACKING SOFURTHEREVIDENCEISNOTAVAILABLE)N !TRIPLEX SPECIES GROWN AT m# #ALDWELL ET AL B NOTED THAT MALATE AND ASPARTATE POOLS INCREASE RELATIVE TO THE RESPECTIVE POOL SIZES IN PLANTS AT WARM TEMPERATURES 4HIS RESULT IS CON SISTENT WITH A LIMITATION IN 2UBISCO AT LOW TEM PERATURE BUT COULD ALSO INDICATE A PROBLEM WITH DECARBOXYLATIONORELECTRONTRANSPORTCAPACITY )NCONTRASTTOTHEMETABOLITELITERATURE THEFLU ORESCENCE LITERATURE EXAMINING # RESPONSES TO LOW TEMPERATURE IS COMPARATIVELY RICH PARTICU LARLY WITH STUDIES OF MAIZE A CHILLING SENSITIVE SPECIESPRONETOPHOTOINHIBITIONINLOWTEMPERA TURES,ABATEETAL &RYERETAL ,ORETO ET AL -ASSACCI ET AL (ALDI MANN +INGSTON 3MITH ET AL +UBIEN ETAL +UBIENAND3AGE A B.AIDUAND ,ONG &ARAGEETAL 3AVITCHETAL -UCH OF THIS LITERATURE DESCRIBES THE RESPONSES OF PHOTOCHEMICAL AND NON PHOTOCHEMICAL FLUORES CENCEQUENCHINGATLOWTEMPERATURE4HESESTUD IES GENERALLY CONFIRM THAT PHOTOCHEMICAL QUENCHING DECLINES WITH TEMPERATURE AND NON PHOTOCHEMICAL QUENCHING MARKEDLY RISES MAINLYREFLECTINGAPHOTOPROTECTIVERESPONSEBYTHE XANTHOPHYLL CYCLE &RYER ET AL -ASSACCI ET AL (ALDIMANN ,EIPNER ET AL +UBIEN AND 3AGE B &ARAGE ET AL !DDITIONAL PHOTOPROTECTIVE MECHANISMS COMPLEMENTZEAXANTHINDEPENDENTQUENCHINGOF FLUORESCENCE IN MAIZE AT LOW TEMPERATURE ALTHOUGH THESE REMAIN TO BE IDENTIFIED 3AVITCH ETAL 4HEFLUORESCENCERESULTSAREGENER ALLYCONSISTENTWITHALIMITATIONINCARBONMETAB OLISMRATHERTHANTHELIGHTREACTIONSATSUBOPTIMAL TEMPERATURE +UBIEN ET AL +UBIEN AND 3AGE B 5SING WHOLE LEAF FLUORESCENCE TO ESTIMATEELECTRONTRANSPORTCAPACITYINVIVOINTHE COLD TOLERANT # GRASS -UHLENBERGIA GLOMERATA +UBIENAND3AGEA ESTIMATEDTHATELECTRON TRANSPORT CAPACITY WAS NON LIMITING BELOW THE THERMAL OPTIMUM BUT IT COULD BE LIMITING FOR PHOTOSYNTHESIS ABOVE THE THERMAL OPTIMUM IN BOTHWARMANDCOOLGROWNPLANTS&IG %LEC TRON TRANSPORT CAPACITY SHARED THE SAME THERMAL OPTIMUM AS #/ ASSIMILATION IN - GLOMERATA

Rowan F. Sage et al. Cool grown Warm grown

a

125

8n-10°C

34n-40°C

0.5 Flaveria bidentis

100

0.4

required: warm-grown

50

&PSII

75 required: cool-grown

0.3 0.2

25 0

anti-rbcS

0.1 0

10 20 30 Leaf temperature nC

Wildtype Theoretical Spring maize

40

&IG 4HE RESPONSE OF ELECTRON TRANSPORT TO TEMPERATURE IN THE # GRASS -UHLENBERGIA GLOMERATA GROWN IN A COOL mm# DAYNIGHT AND WARM mm# GROWTH CHAM BER 3YMBOLS ARE FROM MEASUREMENTS USING CHLOROPHYLL A FLUORESCENCE AT A 00&$ OF rMOL MȪ SȪ AND PPM#/4HESOLIDANDDASHEDLINESINDICATETHETHEORETICAL RATE OF ELECTRON TRANSPORT REQUIRED TO SUPPORT THE OBSERVED 2U"0 CARBOXYLATION CAPACITY IN COOL AND WARM GROWN PLANTS RESPECTIVELY 7HERE MEASURED ELECTRON TRANSPORT RATESEXCEEDTHETHEORETICALREQUIREMENTS ELECTRONTRANSPORT CAPACITY IS NON LIMITING 7HERE OBSERVED RATES ARE BELOW THEORETICALREQUIREMENTS ANELECTRONTRANSPORTLIMITATIONIS POSSIBLE&ROM+UBIENAND3AGE A

b

0.0 Muhlenbergia glomerata

0.4

&PSII

Electron transport rate Mmol m 2 s 1

150

0.3 0.2 Warm-grown (26/22nC) Cool-grown (14/10nC) Theoretical Cold grown Cyperus

0.1 0.0 0.00

0.01

0.02

0.03

0.04

&CO2 (molco2 molhv 1)

ANDTHEREDUCTIONINTHEESTIMATEDELECTRONTRANS PORTRATEABOVETHETHERMALOPTIMUMWASSIMILAR TO THE REDUCTION IN PHOTOSYNTHESIS +UBIEN AND 3AGE A V. Fluorescence at Low Temperature /NE OF THE COMMON RESPONSES OBSERVED IN # PLANTSATLOWTEMPERATUREISARISEINTHERATIOOF Ʒ03))Ʒ#/ WHICHREFLECTSTHEELECTRONREQUIREMENT FOR #/ FIXATION )N WARM CONDITIONS INCLUDING SUPRAOPTIMALTEMPERATURES Ʒ03))Ʒ#/ISNEARTHE THEORETICAL VALUE OF HOWEVER BELOW m# Ʒ03))Ʒ#/INCREASESTOǻ%DWARDSAND"AKER /BERHUBERAND%DWARDS &RYERETAL +UBIEN ET AL +UBIEN AND 3AGE A&ARAGEETAL "AKER 4HISRISE IN Ʒ03))Ʒ#/ IS ALSO OBSERVED AS A SHIFT OF THE RESPONSEOFƷ03))VERSUSƷ#/FROMTHEIRTHEORETI CAL RELATIONSHIP PARTICULARLY IN WARM ADAPTED SPECIESEXPOSEDTOCHILLING&IG 7HILEPLANTS GROWNINWARMCONDITIONSTENDTOTRACKTHETHEO RETICAL RESPONSE # PLANTS GROWN IN COOL CONDI TIONS OFTEN SHOW AN ENHANCED Ʒ03)) VERSUS Ʒ#/

&IG 4HE RELATIONSHIP BETWEEN THE INSTANTANEOUS QUAN TUM YIELD OF PHOTOSYTEM )) Ʒ03)) AND THE INSTANTANEOUS QUANTUM YIELD OF #/ ASSIMILATION Ʒ#/ IN THE # PLANTS &LAVERIA BIDENTIS PANEL A AND -UHLENBERGIA GLOMERATA PANELB &OR&BIDENTISAND-GLOMERATA THERESPONSES WEREGENERATEDBYVARYINGLEAFTEMPERATURE+UBIEN ANDTHECORRESPONDINGTEMPERATURERANGESARESHOWNABOVE THEGRAPH&LAVERIABIDENTISPLANTSWEREFROMA2UBISCOANTI SENSELINEOPENSQUARES ORWILD TYPELINEFILLEDSQUARES 0LANTS OF - GLOMERATA WERE GROWN IN A WARM mm# DAYNIGHT ǻ FILLED SYMBOLS OR COOL mm# DAYNIGHT ǻ OPENSYMBOLS REGIMEINPLANTGROWTHCHAMBERS4HESOLID LINES SHOW THEORETICAL RESPONSES BETWEEN Ʒ03)) AND Ʒ#/ ASSUMINGPHOTONSAREREQUIREDPER#/FIXED4HEDASHED LINESSHOWTHERESPONSESLOPEFORMEASUREDRESPONSESFROM SPRING GROWNMAIZEPANELA FROM&RYERETAL AND COOL GROWN#YPERUSLONGUSATm#PANELB FROM&ARAGE ETAL 3UMMERTREATMENTSOFMAIZEANDm#GROWN # LONGUS PRODUCED RELATIONSHIPS SIMILAR TO THE THEORETICAL RESPONSESSHOWN

RESPONSE RELATIVE TO THE THEORETICAL RESPONSE &IG&RYERETAL &ARAGEETAL ! RISE IN Ʒ03))Ʒ#/ ABOVE THE THEORETICAL VALUE INDICATESTHATANINCREASEDFRACTIONOFELECTRONSMOV ING THROUGH 03)) ARE NOT BEING UTILIZED BY CARBON FIXATION +UBIEN ET AL &ARAGE ET AL

10


4HISCOULDOCCURIF! PHOTORESPIRATIONINCREASES ATLOWTEMPERATURE DUETOLOW#/INTHEBUNDLE SHEATHASWOULDOCCURIF00$+WASTHELIMITING STEP " LOWTEMPERATUREINDUCESANALTERNATIVE ELECTRONSINK SUCHASOXYGENTHROUGHTHE-EHLER REACTION OR # #/ LEAKAGE FROM THE BUNDLE SHEATH INCREASES )NCREASED PHOTORESPIRATION IS UNLIKELYTOBETHECAUSEOFINCREASEDƷ03))Ʒ#/AT LOWTEMPERATURE BECAUSETHE2UBISCOSPECIFICITY FOR#//RISESSUBSTANTIALLYATCOOLERTEMPERA TURES ANDTHEREISLITTLEDETECTABLESIGNOFINCREASED OXYGENSENSITIVITYOFPHOTOSYNTHESISIN#PLANTS ATNORMAL/LEVELS*ORDANAND/GREN +U AND %DWARDS $AI ET AL !LSO THE OPERATING #I IS GREATER THAN THE #/ SATURATION POINT AND THERE IS LITTLE REDUCTION IN THE INITIAL SLOPE OF PHOTOSYNTHESIS WHICH SHOULD OCCUR IF #/ SUPPLY TO THE BUNDLE SHEATH IS IMPAIRED 3AGE )N#PLANTS CYCLICORPSEUDOCY CLIC ELECTRON FLOW THROUGH 03) IS AN IMPORTANT MEANSTOPRODUCEEXTRA!40REQUIREDBYTHE# CYCLE%DWARDSAND7ALKER&URBANKETAL -AROCOETAL !TLOWTEMPERATURES INCREASED FLOW OF ELECTRONS TO / VIA 03) CAN GENERATE ADDITIONAL REACTIVE OXIDATIVE SPECIES WHICHINTURNCONSUME.!$0( THEREBYREDUC INGTHEFLOWOFELECTRONSTO#/REDUCTION4HIS WOULD REDUCE Ʒ#/ RESULTING IN A RISE IN Ʒ03)) Ʒ#/ &RYER ET AL &ARAGE ET AL )NCREASED#/LEAKAGEFROMTHEBUNDLESHEATHIS A LIKELY POSSIBILITY BECAUSE AN INCREASE IN THE DEGREE TO WHICH 2UBISCO LIMITS PHOTOSYNTHESIS AT LOW TEMPERATURE WOULD ALLOW #/ LEVELS TO ACCUMULATE IN THE BUNDLE SHEATH THEREBY DRIV ING INCREASED DIFFUSIVE EFFLUX OF #/ +UBIEN ETAL

VAPOR PRESSURE DIFFERENCE 60$ BETWEEN LEAF ANDAIRISREDUCEDINLOWTEMPERATUREBECAUSETHE SATURATIONVAPORPRESSUREOFTHEAIRDECLINES(IGH 60$INDUCESSTOMATALCLOSUREINMOSTSITUATIONS BUT BELOW m# THE HIGHEST 60$ POSSIBLE IS ABOUTK0A WHICHISGENERALLYTOOLOWTOSUB STANTIALLY REDUCE STOMATAL CONDUCTANCE IN NON DROUGHTED PLANTS ,ONG AND 7OOLHOUSE A 0OSTLAND"OLHAR .ORDENKAMPF !TTHETHERMALOPTIMUMANDABOVE HIGH60$ CAN OCCUR PARTICULARLY FOR THOSE # SPECIES IN SEMI ARID AND ARID HABITATS 7ITH THE RISE IN THE #/SATURATIONPOINTWITHINCREASINGTEMPERATURE THEOPERATING#ICOULDFALLBELOWTHE#/SATURA TIONPOINTONTHE!#ICURVE"ECAUSETHEINITIAL SLOPEOFTHE!#ICURVEIN#SPECIESISTYPICALLY VERYSTEEP THESTOMATALLIMITATIONCOULDBELARGE IFTHEOPERATING#IFALLSONTHEINITIALSLOPE4HIS PHENOMENONHASBEENINFREQUENTLYSTUDIED HOW EVER SO THERE ARE FEW CASE STUDIES OF STOMATAL LIMITATIONTOHIGHLIGHTFOR#SPECIES)NHIGHELE VATION # GRASSES 0ITTERMANN AND 3AGE OBSERVED NO STOMATAL LIMITATION IN WELL WATEREDPLANTSATMODERATE60$LEVELSATMEAS UREMENT TEMPERATURES OF m# m# AND m# "UNCE NOTED LITTLE CHANGE IN ! IN !MARANTHUS HYPOCHONDRIACUS AND 0ORTULACA OLERACEA WITH INCREASING 60$ AT A RANGE OF AIR TEMPERATURES BETWEEN m AND m# DESPITE A HIGH 60$ INDUCED DECLINE IN STOMATAL CONDUCT ANCE )N MAIZE THE REDUCTION IN ! WITH RISING 60$FROMTOMBARWASABOUTHALFASGREAT AS OBSERVED IN THE # SPECIES CASTOR BEAN AND TOBACCO$AIETAL 4HESERESULTSSUPPORT THEHYPOTHESISTHATINGENERAL #SPECIESARELESS LIKELYTOEXPERIENCESTOMATALLIMITATIONSINWELL WATEREDCONDITIONSTHAN#SPECIES

VI. Stomatal Limitations )N # PLANTS LOW STOMATAL CONDUCTANCE LIMITS PHOTOSYNTHESISONLYWHENITREDUCESTHE#IBELOW THE #/ SATURATION POINT 5NLESS THE STOMATAL CONDUCTANCE IS SUBSTANTIALLY REDUCED BY LOW HUMIDITY OR ABIOTIC STRESS STOMATAL LIMITATIONS ARE UNLIKELY TO OCCUR BELOW m# BECAUSE THE OPERATING#IISABOVETHE#/SATURATIONPOINTIN MOST # PLANTS AT THESE TEMPERATURES ,ONG AND 7OOLHOUSE A 0ITTERMANN AND 3AGE 3AGE )N ADDITION THE MAXIMUM

VII. Thermal Acclimation of C4 Photosynthesis !CCLIMATION REFERS TO A SERIES OF ADJUSTMENTS IN THE LEAF THAT COMPENSATE FOR THE CHANGE IN ENVI RONMENTALCONDITIONSANDALLOWFORPERFORMANCE INTHENEWENVIRONMENTTHATISGREATERTHANWOULD OCCUR HAD THERE BEEN NO COMPENSATORY ADJUST MENTS4HISCONTRASTSWITHINJURYRESPONSES WHERE THENEWENVIRONMENTREDUCESCARBONGAINPOTEN TIALBYDAMAGINGONEORMORECOMPONENTSOFTHE

PHOTOSYNTHETIC APPARATUS -ANY STUDIES DESCRIBE THE THERMAL ACCLIMATION OF #/ FIXATION IN # PLANTS&IGC"JORKMANAND0EARCY #ALD WELL ET AL B 0EARCY AND (ARRISON 0EARCY "JORKMAN ET AL +EMP AND 7ILLIAMS0EARCYETAL "OWMANAND 4URNER $U ET AL B 0ITTERMANN AND 3AGE .AIDUETAL .AIDUAND,ONG +UBIEN AND 3AGE A B $WYER ET AL %XCEPT FOR A CHANGE IN THE THERMAL OPTI MUM OF PHOTOSYNTHESIS NO GENERAL PATTERN OF ACCLIMATION CAN BE SUMMARIZED AS THE ACCLIMA TIONRESPONSEDEPENDSUPONTHETHERMALENVIRON MENTTOWHICHTHEPLANTSAREADAPTED/NEPATTERN OFACCLIMATIONISOBSERVEDIN#PLANTSADAPTEDTO ANDGROWNINWARMENVIRONMENTS)NTHISGROUP PLANTSGROWNABOVEm#SHOWASTRONGENHANCE MENTOFPHOTOSYNTHESISATHIGHTEMPERATUREANDA PRONOUNCEDDECLINEINPHOTOSYNTHESISATLOWTEM PERATURERELATIVETOSPECIESGROWNATCOOLTEMPER ATURE)N!TRIPLEXLENTIFORMISAND!HYMENALYTRA GROWTHINHIGHTEMPERATURESHIFTSTHETHERMALOPTI MUMTOWARMERTEMPERATURES BUTDOESNOTCHANGE THESHAPEOFTHE!4CURVE0EARCYAND(ARRISON 0EARCY "JORKMANETAL 4HE SHIFTTOHIGHERTEMPERATURESOFTHEINITIALSLOPEOF THE!4RESPONSEIN!LENTIFORMISWITHANINCREASE IN GROWTH TEMPERATURE IS ASSOCIATED WITH A REDUCTIONIN2UBISCOACTIVITYINVITRO ANDONLYA SLIGHTDECLINEIN0%0CARBOXYLASEACTIVITY0EARCY )N 4IDESTROMIA OBLONGIFOLIA WHICH IS ADAPTED TO HOT SUMMERS IN THE -OJAVE DESERT GROWTHATLOWTEMPERATUREm# CAUSESAGREAT REDUCTION IN PHOTOSYNTHESIS AT ALL MEASUREMENT TEMPERATURES "ERRY AND "JORKMAN "JORKMANETAL SIMILARTOWHATISOBSERVED INCHILLINGSENSITIVE#SPECIESSUCHASMAIZETHAT AREGROWNATǻm# ! SECOND PATTERN OF ACCLIMATION COMMONLY OBSERVEDISFORGROWTHATWARMERTEMPERATURESTO INCREASE ! AT THE THERMAL OPTIMUM AND WARM MEASUREMENT TEMPERATURES WHILE AT COOL MEAS UREMENTTEMPERATURES !ISLITTLECHANGEDBETWEEN WARM AND COOL GROWN PLANTS #ALDWELL ET AL BFOR!TRIPLEXCONFERTIFOLIAAND!VESICARIA "OWMANAND4URNER FOR"OUTELOUASPECIES 0ITTERMANN AND 3AGE FOR -UHLENBERGIA MONTANUM.AIDUETAL FOR-ISCANTHUS GIGANTEA +UBIEN AND 3AGE A FOR -UHLEN BERGIAGLOMERATA )NTHE#SHRUB!TRIPLEXCON FERTIFOLIA FOR EXAMPLE GROWTH AT m# CAUSED A

Rowan F. Sage et al. DROPINPHOTOSYNTHESISATALLBUTTHECOOLESTMEAS UREMENTTEMPERATURESRELATIVETOTHERATESMEAS URED IN PLANTS GROWN AT m# #ALDWELL ET AL A 4HELACKOFACCLIMATIONINTHEPHOTOSYN THESIS RATE AT LOWER TEMPERATURE IN -ISCANTHUS AND-UHLENBERGIAISASSOCIATEDWITHALACKOFANY CHANGE IN 2UBISCO CONTENT WHICH IS CONSISTENT WITHA2UBISCOLIMITATIONON#/UPTAKEATLOW TEMPERATURES IN THESE # SPECIES 4HIS APPARENT INABILITY TO ADJUST PHOTOSYNTHESIS AND 2UBISCO CONTENTATLOWGROWTHTEMPERATURELED3AGEAND -C+OWN TOSUGGESTTHATCOLD ADAPTED# SPECIESSUCHAS"OUTELOUA -ISCANTHUSAND-UH LENBERGIAMAYHAVEALOWCAPACITYFORPHOTOSYN THETICACCLIMATIONTOCOOLERCONDITIONS !THIRDPATTERNOFACCLIMATIONWASOBSERVEDBY $WYERETAL INTHREEWARM CLIMATE#SPE CIESTHEGRASSES#ENCHRUSCILIARISAND0ENNISETUM COLORATUM ANDTHEDICOT&LAVERIABIDENTIS GROWN ATmm#ANDm#DAYNIGHTTEMPERATURES )NEACHSPECIES THEWARMGROWNPLANTSEXHIBITED LOWER ! AT THE COOLER MEASUREMENT TEMPERATURES THANTHECOOL GROWNPLANTSHOWEVER THEREWASLIT TLECHANGEIN!ABOVETHETHERMALOPTIMUMBETWEEN THETREATMENTS)NALLTHREESPECIES THESECHANGES IN#/ASSIMILATIONRATEINWARMCOMPAREDTOCOOL GROWTHCONDITIONSWEREASSOCIATEDWITHADROPIN THEAMOUNTOF2UBISCO CARBONICANHYDRASE CYTO CHROME F AND LEAF NITROGEN 0%0# LEVELS DID NOT CHANGE !TRIPLEX ROSEA ALSO EXHIBITS THIS TYPE OF ACCLIMATIONRESPONSE&IGC )N SUMMARY # SPECIES CAN SHOW SUBSTANTIAL ADJUSTMENTS IN THE PHOTOSYNTHETIC RESPONSE TO TEMPERATUREFOLLOWINGGROWTHINDIFFERENTTHERMAL ENVIRONMENTS HOWEVER THESE CHANGES APPEAR TO BE MOST PRONOUNCED IN WARMER CONDITIONS PARTICULARLY IN PLANTS FROM WARM ENVIRONMENTS # PLANTS FROM COOL ENVIRONMENTS APPEAR TO BE LIMITED IN THEIR ABILITY TO ACCLIMATE TO VARYING THERMAL CONDITIONS BELOW THE THERMAL OPTIMUM -OSTSTUDIESOFGROWTHATLOWTEMPERATUREHAVE FOCUSEDONSTRESSFULCHILLINGRESPONSESNOTABLYIN MAIZE WHERE PROLONGED EXPOSURE TO LOW TEM PERATUREISACCOMPANIEDBYPHOTOINHIBITION ALOSS OF LEAF PROTEIN CONTENT AND EVENTUAL LEAF DEATH (OWEVER MOSTOFTHESESPECIESAREOFTROPICALOR SUBTROPICALORIGIN ANDTHECHILLINGRESPONSESARE NOTNECESSARILYINDICATIVEOFPROBLEMSWITHTHE# PATHWAY ASSIMILARRESPONSESAREOBSERVEDIN# SPECIES FROM LOW LATITUDES FOLLOWING CHILLING #HILLING TOLERANT#SPECIESSHOWAGOODABILITYTO

10


OVERCOME SHORT TERM LIMITATIONS IN THE # CYCLE AND PHOTOSYSTEMS FOLLOWING GROWTH AT CHILLING TEMPERATURES ANDAPPEARTOMAINTAINASTABLEPHO TOSYNTHETIC CAPACITY AFTER AN ACCLIMATION PERIOD 7HERE EXAMINED 2UBISCO CAPACITY APPEARS TO CONTROL!INTHESESPECIESATLOWTEMPERATURE VIII. Conclusion: Are C4 Plants Inherently More Sensitive to Low Temperature Than C3 Plants? 4HE LACK OF # PLANTS IN POLAR BOREAL AND MOST COOL TEMPERATE HABITATS DEMONSTRATES THAT # PLANTS ARE LESS ECOLOGICALLY SUCCESSFUL IN COLDER CLIMATES(OWEVER THEOCCURRENCEOFDOZENSOF# SPECIESINCOLDCLIMATESATHIGHELEVATIONANDIN SPECIALIZEDMICROSITESOFTHEBOREALANDCOOLTEM PERATEREGIONSDEMONSTRATESTHATTHE#PATHWAY CAN BE TOLERANT OF LOW TEMPERATURE INCLUDING FREEZINGCONDITIONSDURINGTHEGROWINGSEASON# SPECIES HAVE EVOLVED FROM # LINEAGES OF WARM CLIMATES LEADING TO THE HYPOTHESIS THAT THEY ARE EXCLUDEDFROMCOLDAREASDUETOPRIORADAPTATIONS TOHIGHERTEMPERATURE#ERTAINLY FAILUREOFMANY #SPECIESINCOLDCLIMATESISDUETOAGENERALCOLD INTOLERANCE JUSTASFAILUREOFLOW LATITUDE#TAXA INTHECOLDREFLECTSCHILLINGSENSITIVITY(OWEVER THEREPEATEDEVOLUTIONOFCOLDTOLERANCEINNUMER OUS # GRASS SEDGE AND DICOT LINEAGES INDICATES THATACQUISITIONOFCOLDTOLERANCEISNOTANOVER WHELMINGBARRIERTOTHERADIATIONOF#PLANTSINTO COLDENVIRONMENTS!SWELL THERAPIDACQUISITION OFFREEZINGTOLERANCEINTHE#ECOTYPEOF!LLOTEROP SISSEMIALATAINDICATESCOLDTOLERANCECANEVOLVE QUICKLYINEVOLUTIONARYTIME /FPARTICULARNOTEISTHELOCALDISTRIBUTIONOF# SPECIESADAPTEDTOCOLDREGIONS!LPINE#SPECIES ARERESTRICTEDTOMICROSITESTHATAREWARMDURING THEDAYORHAVEGROWTHFORMSTHATEFFICIENTLYTRAP SOLARHEAT!THIGHLATITUDESINTHENORTHERNBOREAL REGION MANYSPECIESOCCURONSOUTHFACINGSLOPES WHERESOLARHEATINGISHIGH)NCASESWHERETHEREIS NOIDENTIFIABLERESTRICTIONTOWARMMICROSITES THE # SPECIES FROM HIGH LATITUDE ARE RESTRICTED TO DROUGHT OR SALINE MICROSITES WHERE THE HIGHER WATERUSEEFFICIENCYOFTHE#PATHWAYMAYCOM PENSATEFORTHEABIOTICSTRESS)NTHESESITUATIONS THEVEGETATIONAWAYFROMTHESTRESSEDHABITATSIS COMPLETELY# INDICATINGTHATTHESTRESSOFFSETSAN ADVANTAGE THE # SPECIES MAY HAVE IN THE COLD

%COLOGICALDISTURBANCEMAYALSOCREATETEMPORARY NICHESFOR#SPECIESINCOLDREGIONSBYCHECKING COMPETITIVEPRESSUREFROM#PLANTS 4HECONCLUSIONFROMTHESPECIESDISTRIBUTIONIS THAT#PLANTSCANEVOLVETOLERANCEOFCOLDCONDI TIONS BUT STILL REQUIRE WARM MICROSITES DISTUR BANCE OR ABIOTIC STRESS TO REALIZE ECOLOGICAL SUCCESS4HISVIEWISCONSISTENTWITHOURPHYSIO LOGICAL UNDERSTANDING 7HILE # PHOTOSYNTHESIS CANPERFORMASWELLAS#SPECIESATLOWTEMPERA TURE THEUNIVERSALPATTERNISFOR#SPECIESTOPER FORMBETTERATHIGHTEMPERATURESTHAN#SPECIES OFSIMILARGROWTHFORMANDECOLOGICALHABIT4HIS DIFFERENCEINPERFORMANCEISDUEINLARGEPARTTO THEABILITYOF#PLANTSTORAISE#/LEVELSAROUND 2UBISCOHIGHENOUGHTOSUPPRESSMOSTPHOTORES PIRATION ANDTOALLOW2UBISCOTOOPERATEATHIGH EFFICIENCY!TLOWTEMPERATURE THEPHYSIOLOGICAL EXPLANATIONS ARE LESS CLEAR ALTHOUGH RECENT PROGRESS SUGGESTS WHY THE # PATHWAY MAY DO LESS WELL IN THE COLD 4HE IDEA THAT SUPERIOR # QUANTUMYIELDSEXPLAIN#SUCCESSATLOWTEMPER ATUREISINADEQUATEINADIRECTSENSE BECAUSEMAX IMUMQUANTUMYIELDDIFFERENCESDONOTRELATETO CONDITIONSUNDERWHICHTHEVASTMAJORITYOFDAILY CARBON IS ASSIMILATED ,IMITATIONS IN # CYCLE ENZYMES SUCH AS 0%0# OR 00$+ ARE NOT LIKELY EXCEPT SHORTLY AFTER EXPOSURE TO CHILLING COLD ADAPTED#SPECIESHAVECOLD STABLEFORMSOFTHESE ENZYMES AND SYNTHESIZE SUFFICIENT QUANTITY TO OVERCOME ANY SHORT TERM LIMITATION )NSTEAD THE COMMONPATTERNOFLIMITATIONAPPEARSTOBEALOW CAPACITYOF2UBISCO!TLOWTEMPERATURE THELOW AMOUNTOF2UBISCOIN#PLANTSIMPOSESACEILING ONPHOTOSYNTHESISTHATADAPTATIONANDACCLIMATION APPEARUNABLETOOVERCOME4HISLOWCEILINGMAY INTURNRESTRICTTHEABILITYOF#SPECIESTOCOMPETE AGAINSTTHEIR#ASSOCIATESINPERENNIALLYCOLDCLI MATES ANDTODEALWITHOTHERECOLOGICALCHALLENGES THATMAYBEPRESENT!NINFLEXIBLECEILINGONCAR BONGAINIMPOSEDBYALOW2UBISCOCAPACITYMAY THUSBETHEKEYTRAITTHATMALADAPTSTHE#PATHWAY TOLOWTEMPERATUREENVIRONMENTS Acknowledgments 4HE AUTHORS ARE GRATEFUL FOR SUPPORT FROM THEIR NATIONAL FUNDING AGENCIES THE #ANADIAN .ATURAL 3CIENCEAND%NGINEERING#OUNCIL.3%2# WHICH FUNDED2&3AGEAND$3+UBIEN AND4HE3CIENTIFIC

AND 4ECHNOLOGICAL 2ESEARCH #OUNCIL OF 4URKEY 4"í4!+ GRANT NO / TO & +OCACINAR 7EALSOTHANK-S$EBBIE4AMFORTECHNICALASSIST ANCEWITHTHETHEWORKTHATWASORIGINALLYGENER ATEDBYTHEAUTHORS References !CKERLY$$ #OLEMAN*3 -ORSE32AND"AZZAZ&! #/ AND TEMPERATURE EFFECTS ON LEAF AREA PRODUCTION IN TWOANNUALPLANT SPECIES%COLOGYǻ !CKERLY$$ #OMPARATIVEPLANTECOLOGYANDTHEROLE OF PHYLOGENETIC INFORMATION )N 0RESS -# 3CHOLES *$ AND "ARKER -' EDS 0HYSIOLOGICAL 0LANT %COLOGY PPǻ"LACKWELL /XFORD !KHANI( 4RIMBORN0AND:IEGLER( 0HOTOSYNTHETIC PATHWAYS IN #HENOPODIACEAE FROM !FRICA !SIA AND %UROPEWITHTHEIRECOLOGICAL PHYTOGEOGRAPHICALANDTAX ONOMICALIMPORTANCE0LANT3YST%VOLǻ !UERSWALD+ 7ITTMER- -ANNEL44 "AI9& 3CHAUFELE2 AND3CHNYDER( ,ARGEREGIONAL SCALEVARIATIONIN ## DISTRIBUTION PATTERN OF )NNER -ONGOLIA STEPPE IS REVEALED BY GRAZER WOOL CARBON ISOTOPE COMPOSITION "IOGEOSCIENCESǻ "AKER .2 #HLOROPHYLL FLUORESCENCE A PROBE OF PHOTOSYNTHESISINVIVO!NNU2EV0LANT"IOLǻ "ARKWORTH-% !NDERSON,+ #APELS+- ,ONG3AND"IEP -"EDS -ANUALOF'RASSESFOR.ORTH!MERICA 5TAH3TATE5NIVERSITY0RESS ,OGAN 5TAH "ATANOUNY+( 3TICHLER7AND:IEGLER( 0HOTOSYN THETICPATHWAYS DISTRIBUTION ANDECOLOGICALCHARACTERIS TICSOFGRASSSPECIESIN%GYPT/ECOLOGIAǻ "EALE #6 AND ,ONG 30 #AN PERENNIAL # GRASSES ATTAIN HIGH EFFICIENCIES OF RADIANT ENERGY CONVERSION IN COOLCLIMATES0LANT#ELL%NVIRONǻ "EALE#6 "INT$!AND,ONG30 ,EAFPHOTOSYNTHESIS IN THE # GRASS -ISCANTHUS X GIGANTEUS GROWING IN THE COOLTEMPERATECLIMATEOFSOUTHERN%NGLAND*%XP"OT ǻ "ERNACCHI #* 3INGSAAS %, 0IMENTEL # 0ORTIS !2 AND ,ONG30 )MPROVEDTEMPERATURERESPONSEFUNCTIONS FORMODELSOF2UBISCO LIMITEDPHOTOSYNTHESIS0LANT#ELL %NVIRONǻ "ERNACCHI #* 0IMENTEL # AND ,ONG 30 )N VIVO TEMPERATURERESPONSEFUNCTIONSOFPARAMETERSREQUIREDTO MODEL 2U"0 LIMITED PHOTOSYNTHESIS 0LANT #ELL %NVIRON ǻ "ERRY*AND"JORKMAN/ 0HOTOSYNTHETICRESPONSEAND ADAPTATION TO TEMPERATURE IN HIGHER PLANTS !NNU 2EV 0LANT0HYSIOLǻ "ESNARD' -UASYA!- 2USSIER& 2OALSON%( 3ALAMIN. AND#HRISTIN0 ! 0HYLOGENOMICSOF#PHOTOSYNTHESIS IN THE SEDGES #YPERACEAE -ULTIPLE APPEARANCES AND GENETICCONVERGENCE-OL"IOL%VOLǻ

Rowan F. Sage et al. "IRD-) (ABERLE3'AND#HIVAS!2 %FFECTOFALTITUDE ONTHECARBON ISOTOPECOMPOSITIONOFFORESTANDGRASSLAND SOILSFROM0APUA .EW 'UINEA'LOB"IOGEOCHEM#YCLES ǻ "IRD-)AND0OUSAI0 6ARIATIONSOFDELTA#INTHE SURFACE SOIL ORGANIC CARBON POOL 'LOB "IOGEOCHEM #YCLESǻ "IXING3AND0HILLIPS3- !RUNDINELLA)N:HENGYI 7 2AVEN 0( AND $EYUAN ( %DS &LORA OF #HINA ǻ 0OACEAE 6OL PPǻ-ISSOURI"OTANICAL'ARDEN 0RESS 3T,OUIS -/ "JORKMAN / 0EARCY 27 AND .OBS -7 0HOTOSYN THETICCHARACTERISTICS#ARNEGIE)NST9EARBOOKǻ "JORKMAN / AND 0EARCY 27 %FFECT OF GROWTH TEMPERATUREONTHETEMPERATUREDEPENDENCEOFPHOTOSYNTHE SISINVIVOANDON#/FIXATIONBYCARBOXYDISMUTASEINVITRO IN#AND#SPECIES#ARNEGIE)NST9EAROOKǻ "JORKMAN/ 0EARCY27 -OONEY(AND(ARRISON!4 0HOTOSYNTHETIC ADAPTATION TO HIGH TEMPERATURES ǻ FIELD STUDYIN$EATH6ALLEY #ALIFORNIA3CIENCEǻ "JORKMAN/ -AHALL" .OBS- 7ARD7 .ICHOLSON& AND -OONEY( !NANALYSISOFTHETEMPERATUREDEPEND ENCEOFGROWTHUNDERCONTROLLEDCONDITIONS#ARNEGIE)NST 9EARBOOKǻ "JORKMAN/ "OYNTON*AND"ERRY* #OMPARISONOF HEAT STABILITY OF PHOTOSYNTHESIS CHLOROPLAST MEMBRANE REACTIONS PHOTOSYNTHETICENZYMES ANDSOLUBLEPROTEININ LEAVES OF HEAT ADAPTED AND COLD ADAPTED # SPECIES #ARNEGIE)NST9EARBOOKǻ "JORKMAN/ "ADGER-2AND!RMOND0! 2ESPONSES ANDADAPTATIONTOHIGHTEMPERATURES)N4URNER.#AND +RAMER0*EDS !DAPTATIONOFPLANTSTOWATERANDHIGH TEMPERATURESTRESS PPǻ7ILEY .EW9ORK "LACK ## #HEN 4- AND "ROWN 2( "IOCHEMICAL BASISFORPLANTCOMPETITION7EED3CIǻ "LACK## %COLOGICALIMPLICATIONSOFDIVIDINGPLANTS INTO GROUPS WITH DISTINCT PHOTOSYNTHETIC PRODUCTIONS CAPACITIES!DV%COL2ESǻ "OOM! -ORA' #LEEF!-AND(OOGHIEMSTRA( (IGH ALTITUDE # GRASSLANDS IN THE NORTHERN !NDES RELICTS FROM GLACIALCONDITIONS2EV0ALAEOBOT0ALYNOLǻ "OUTTON47 (ARRISON!4AND3MITH". $ISTRIBUTION OFBIOMASSOFSPECIESDIFFERINGINPHOTOSYNTHETICPATHWAY ALONG AN ALTITUDINAL TRANSECT IN SOUTHEASTERN 7YOMING GRASSLAND/ECOLOGIAǻ "OWMAN7$AND4URNER, 0HOTOSYNTHETICSENSITIVITY TOTEMPERATUREINPOPULATIONSOFTWO#"OUTELOUA0OACEAE SPECIESNATIVETODIFFERENTALTITUDES!M*"OTǻ "RAKO,AND:ARUCCHI*, #ATALOGUEOFTHE&LOWERING 0LANTS AND 'YMOSPERMS OF 0ERU -ISSOURI "OTANICAL 'ARDEN0RESS 3T,OUIS -/ "UNCE*! ,OWHUMIDITYEFFECTSONPHOTOSYNTHESISIN SINGLELEAVESOF#PLANTS/ECOLOGIAǻ "UNCE*! $IFFERENTIALSENSITIVITYTOHUMIDITYOFDAILY PHOTOSYNTHESISINTHEFIELDIN# SPECIESAND# SPECIES /ECOLOGIAǻ

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"URNELL *. ! COMPARATIVE STUDY OF THE COLD SENSI TIVITYOFPYRUVATE 0IDIKINASEIN&LAVERIASPECIES0LANT #ELL0HYSIOLǻ #ABIDO- !TECA. !STEGIANO-%AND!NTON!- $ISTRIBUTION OF # AND # GRASSES ALONG AN ALTITUDINAL GRADIENTINCENTRAL!RGENTINA*"IOGEOGǻ #ALDWELL-- 7HITE23 -OORE24AND#AMP,"A #ARBON BALANCE PRODUCTIVITY AND WATER USE OF COLD WINTERDESERTSHRUBCOMMUNITIESDOMINATEDBY#AND# SPECIES/ECOLOGIAǻ #ALDWELL-- /SMOND#"AND.OTT$,B #PATH WAY PHOTOSYNTHESIS AT LOW TEMPERATURE IN COLD TOLERANT !TRIPLEXSPECIES0LANT0HYSIOLǻ #AVAGNARO *" $ISTRIBUTION OF # AND # GRASSES AT DIFFERENTALTITUDESINATEMPERATEARIDREGIONOF!RGENTINA /ECOLOGIAǻ #EN90AND3AGE2& 4HEREGULATIONOFRUBISCOACTIVITY INRESPONSETOVARIATIONINTEMPERATUREANDATMOSPHERIC#/ PARTIALPRESSUREINSWEETPOTATO0LANT0HYSIOLǻ #HAZDON2, %COLOGICALASPECTSOFTHEDISTRIBUTIONOF #GRASSESINSELECTEDHABITATSOF#OSTA 2ICA"IOTROPICA ǻ #HRISTIE%+AND$ETLING*+ !NALYSISOFINTERFERENCE BETWEEN#AND#GRASSESINRELATIONTOTEMPERATUREAND SOIL NITROGENSUPPLY%COLOGYǻ #HRISTIN0! "ESNARD' 3AMARITANI% $UVALL-2 (ODKIN SON42 3AVOLAINEN6AND3ALAMIN. /LIGOCENE #/DECLINEPROMOTED#PHOTOSYNTHESISINGRASSES#URR "IOLǻ #HRISTIN 0! 3ALAMIN . +ELLOGG %! 6ICENTINI ! AND "ESNARD ' )NTEGRATING PHYLOGENY INTO STUDIES OF #VARIATIONINTHERASSES0LANT0HYSIOLǻ #LEMENTS &% 7EAVER *% AND (ANSON (# 0LANT #OMPETITION#ARNEGIE)NSTITUTION 7ASHINGTON #LIFTON "ROWN *# ,ONG 30 *ORGENSEN 5 (UMPHRIES 3! 3CHWARZ+5AND3CHWARZ( -ISCANTHUSPRODUC TIVITY )N *ONES -" AND 7ALSH - EDS -ISCANTHUS FOR %NERGYAND&IBER PPǻ*AMES*AMES ,ONDON #OLLATZ '* 2IBAS #ARBO - AND "ERRY *! #OUPLED PHOTOSYNTHESIS STOMATALCONDUCTANCEMODELFORLEAVESOF #PLANTS!UST*0LANT0HYSIOLǻ #OLLATZ'* "ERRY*!AND#LARK*3 %FFECTSOFCLIMATE AND ATMOSPHERIC #/ PARTIAL PRESSURE ON THE GLOBAL DISTRIBUTION OF # GRASSES PRESENT PAST AND FUTURE /ECOLOGIAǻ #OLLINS20AND*ONES-"A 4HEINFLUENCEOFCLIMATIC FACTORSONTHEDISTRIBUTIONOF#SPECIESIN%UROPE6EGETATIO ǻ #OLLINS20AND*ONES-"B 4HESEASONALPATTERNOF GROWTHANDPRODUCTIONOFATEMPERATE#SPECIES #YPERUS LONGUS*%XP"OTǻ #RAFTS "RANDNER3*AND3ALVUCCI-% 3ENSITIVITYOF PHOTOSYNTHESISINA#PLANT MAIZE TOHEATSTRESS0LANT 0HYSIOLǻ $AI: %DWARDS'EAND+U-3" #ONTROLOFPHOTOSYN THESIS AND STOMATAL CONDUCTANCE IN 2ICINUS COMMUNIS ,

CASTOR BEAN BY LEAF TO AIR VAPOR PRESSURE DEFICIT 0LANT 0HYSIOLǻ $AI:9 +U-3"AND%DWARDS'% #PHOTOSYNTHESIS

THE#/ CONCENTRATINGMECHANISMANDPHOTORESPIRATION 0LANT0HYSIOLǻ $AI: +U-3"AND%DWARDS'% /XYGENSENSITIVITY OFPHOTOSYNTHESISANDPHOTORESPIRATIONINDIFFERENTPHOTO SYNTHETICTYPESINTHEGENUS&LAVERIA0LANTAǻ $ENGLER.'AND.ELSON4 ,EAFSTRUCTUREANDDEVEL OPMENTIN#PLANTS)N3AGE2&AND-ONSON2+EDS # 0LANT"IOLOGY PPǻ!CADEMIC 3AN$IEGO #! $E6EAU%*AND"URRIS*% 0HOTORESPIRATORYRATESIN WHEAT AND MAIZE AS DETERMINED BY / LABELING 0LANT 0HYSIOLǻ $ICKINSON#%AND$ODD*, 0HENOLOGICALPATTERNSIN THESHORTGRASSPRAIRIE!M-IDL.ATǻ $OLINER,(AND*OLLIFFE0! %COLOGICALEVIDENCECON CERNINGTHEADAPTIVESIGNIFICANCEOFTHE#DICARBOXYLIC ACIDPATHWAYOFPHOTOSYNTHESIS/ECOLOGIAǻ $U9# .OSE!AND7ASANO+A %FFECTSOFCHILLING TEMPERATURE ON PHOTOSYNTHETIC RATES PHOTOSYNTHETIC ENZYMEACTIVITIESANDMETABOLITELEVELSINLEAVESOFTHREE SUGARCANESPECIES0LANT#ELL%NVIRONǻ $U9# .OSE!AND7ASANO+B 4HERMALCHARACTER ISTICSOF#PHOTOSYNTHETICENZYMESFROMLEAVESOFTHREE SUGARCANESPECIESDIFFERINGINCOLDSENSITIVITY0LANT#ELL 0HYSIOLǻ $WYER3! 'HANNOUM/ .ICOTRA!AND6ON#AEMMERER3 (IGHTEMPERATUREACCLIMATIONOF#PHOTOSYNTHE SIS IS LINKED TO CHANGES IN PHOTOSYNTHETIC BIOCHEMISTRY 0LANT#ELL%NVIRONǻ %ARNSHAW-* #ARVER+! 'UNN4# +ERENGA+ (ARVEY6 'RIFFITHS(AND"ROADMEADOW-3* 0HOTOSYNTHETIC PATHWAY CHILLINGTOLERANCEANDCELLSAPOSMOTICPOTENTIAL VALUES OF GRASSES ALONG AN ALTITUDINAL GRADIENT IN 0APUA .EW'UINEA/ECOLOGIAǻ %DWARDS %* AND 3MITH 3! 0HYLOGENETIC ANALYSES REVEALTHESHADYHISTORYOF#GRASSES0ROC.AT!CAD3CI 53! ǻ %DWARDS%* 3TILL#*AND$ONOGHUE-* 4HERELEVANCE OF PHYLOGENY TO STUDIES OF GLOBAL CHANGE 4RENDS %COL %VOLǻ %DWARDS%*AND3TILL#* #LIMATE PHYLOGENYANDTHE ECOLOGICALDISTRIBUTIONOF#GRASSES%COL,ETTǻ %DWARDS'%AND"AKER.2 #AN#/ASSIMILATIONIN MAIZE LEAVES BE PREDICTED ACCURATELY FROM CHLOROPHYLL FLUORESCENCEANALYSIS0HOTOSYNTH2ESǻ %DWARDS '% AND 7ALKER $! # # -ECHANISMS AND#ELLULARAND%NVIRONMENTAL2EGULATION OF0HOTOSYN THESIS"LACKWELL3CIENTIFIC /XFORD %HLERINGER * AND "JORKMAN / 1UANTUM YIELDS FOR #/UPTAKEIN#AND#PLANTS DEPENDENCEONTEMPERA TURE #/AND/CONCENTRATION0LANT0HYSIOLǻ %HLERINGER*2 )MPLICATIONSOFQUANTUMYIELDDIFFER ENCESONDISTRIBUTIONSOF#AND#GRASSES/ECOLOGIA ǻ

%HLERINGER * AND 0EARCY 27 6ARIATION IN QUANTUM YIELDFOR#/UPTAKEAMONG#AND#0LANTS0LANT0HYSIOL ǻ %HLERINGER*2 3AGE2& &LANAGAN,"AND0EARCY27 #LIMATE CHANGE AND THE EVOLUTION OF # PHOTOSYNTHESIS 4RENDS%COL%VOLǻ %HLERINGER *2 AND -ONSON 2+ %VOLUTIONARY AND ECOLOGICAL ASPECTS OF PHOTOSYNTHETIC PATHWAY VARIATION !NNU2EV%COL3YSTǻ %HLERINGER*2 #ERLING4%AND(ELLIKER"2 #PHOTO SYNTHESIS ATMOSPHERIC#/ANDCLIMATE/ECOLOGIA ǻ %HLERINGER*2 4HEINFLUENCEOFATMOSPHERIC#/ TEM PERATURE AND WATER ON THE ABUNDANCE OF ## TAXA )N %HLERINGER*2 #ERLING4%AND$EARING-$EDS !(ISTORY OF!TMOSPHERIC#/ANDITS%FFECTSON0LANTS !NIMALSAND %COSYSTEMS PPǻ3PRINGER "ERLIN %LLIS20 6OGEL*#AND&ULS! 0HOTOSYNTHETICPATH WAYS AND THE GEOGRAPHICAL DISTRIBUTION OF GRASSES IN 3OUTHWEST!FRICA .AMIBIA3!FR*3CIǻ %PSTEIN(% ,AUENROTH7+ "URKE)#AND#OFFIN$0 %COLOGICALRESPONSESOFDOMINANTGRASSESALONGTWOCLI MATIC GRADIENTS IN THE GREAT PLAINS OF THE 5NITED 3TATES *6EG3CIǻ %PSTEIN(% ,AUENROTH7+ "URKE)#AND#OFFIN$0 0RODUCTIVITYPATTERNSOF#AND#FUNCTIONALTYPESINTHE 53'REAT0LAINS%COLOGYǻ %VANS ,4 AND "USH -' 'ROWTH AND DEVELOPMENT OFCHANNELMILLET%CHINOCHLOATURNERIANA INRELATIONTOITS POTENTIALASACROPPLANTANDCOMPAREDWITHOTHER%CHINOCHLOA MILLETS RICEANDWHEAT&IELD#ROPS2ESǻ &ARAGE0+ "LOWERS$ ,ONG30AND"AKER.2 ,OW GROWTHTEMPERATURESMODIFYTHEEFFICIENCYOFLIGHTUSEBY PHOTOSYSTEM))FOR#/ASSIMILATIONINLEAVESOFTWOCHILL ING TOLERANT#SPECIES #YPERUSLONGUS,AND-ISCANTHUS XGIGANTEUS0LANT#ELL%NVIRONǻ &ARQUHAR '$ AND VON #AEMMERER 3 -ODELING OF PHOTOSYNTHETICRESPONSETOENVIRONMENTALCONDITIONS)N ,ANGE /, .OBEL 03 /SMOND #" AND :IEGLER ( EDS 0HYSIOLOGICAL 0LANT %COLOGY )) 7ATER 2ELATIONS AND #ARBON !SSIMLATION %NCYCLOPEDIA OF 0LANT 0HYSIOLOGY .EW3ERIES 6OL" PPǻ3PRINGER 6ERLAG "ERLIN &LADUNG-AND(ESSELBACH* %FFECTOFVARYINGENVI RONMENTSONPHOTOSYNTHETICPARAMETERSOF# # #AND #SPECIESOF0ANICUM/ECOLOGIAǻ &LINT%0AND0ATTERSON$4 )NTERFERENCEANDTEMPERA TUREEFFECTSONGROWTHINSOYBEAN'LYCINEMAX ANDASSO CIATED#AND#WEEDS7EED3CIǻ &RYER-* /XBOROUGH+ -ARTIN" /RT$2AND"AKER.2 &ACTORS ASSOCIATED WITH DEPRESSION OF PHOTOSYN THETIC QUANTUM EFFICIENCY IN MAIZE AT LOW GROWTH TEM PERATURE0LANT0HYSIOLǻ &RYER-* !NDREWS*2 /XBOROUGH+ "LOWERS$!AND"AKER .2 2ELATIONSHIPBETWEEN#/ASSIMILATION PHOTO SYNTHETIC ELECTRON TRANSPORT AND ACTIVE / METABOLISM IN

Rowan F. Sage et al. LEAVESOFMAIZEINTHEFIELDDURINGPERIODSOFLOWTEMPERA TURE0LANT0HYSIOLǻ &URBANK24AND"ADGER-2 0HOTOSYNTHETICOXYGEN EXCHANGEINATTACHEDLEAVESOF#MONOCOTYLEDONS!UST* 0LANT0HYSIOLǻ &URBANK24AND"ADGER-2 0HOTORESPIRATORYCHAR ACTERISTICSOFISOLATEDBUNDLESHEATHSTRANDSOF#MONO COTYLEDONS!UST*0LANT0HYSIOLǻ &URBANK24 #HITTY*! *ENKINS#,$ 4AYLOR7# 4REVANION 3* VON #AEMMERER 3 AND !SHTON !2 'ENETIC MANIPULATION OF KEY PHOTOSYNTHETIC ENZYMES IN THE # PLANT&LAVERIABIDENTIS!UST*0LANT0HYSIOLǻ &URBANK24 *ENKINS#,$AND(ATCH-$ #0HOTO SYNTHESIS QUANTUMREQUIREMENT #ACIDOVERCYCLINGAND 1 CYCLEINVOLVEMENT!UST*0LANT0HYSIOLǻ 'RISE$* %FFECTSOF%LEVATED#/AND(IGH4EMPERA TUREONTHE2ELATIVE'ROWTH2ATESAND#OMPETITIVE)NTER ACTIONS "ETWEEN A # #HENOPODIUM ALBUM AND A # !MARANTHUSHYBRIDUS !NNUAL0H$THESIS5NIVERSITYOF 'EORGIA !THENS '! 'UO 1& AND "ROWN *( 4EMPORAL FLUCTUATIONS AND EXPERIMENTALEFFECTSINDESERTPLANTCOMMUNITIES/ECOLO GIAǻ (ALDIMANN0 %FFECTSOFCHANGESINGROWTHTEMPERA TUREONPHOTOSYNTHESISANDCAROTENOIDCOMPOSITIONIN:EA MAYSLEAVES0HYSIOL0LANTARUMǻ (ALDIMANN 0 ,OW GROWTH TEMPERATURE INDUCED CHANGES TO PIGMENT COMPOSITION AND PHOTOSYNTHESIS IN :EAMAYSGENOTYPESDIFFERINGINCHILLINGSENSITIVITY0LANT #ELL%NVIRONǻ (AMEL.AND3IMON*0 -OLECULARFORMSANDKINETIC PROPERTIESOFPHOSPHOENOLPYRUVATECARBOXYLASEFROMBARN YARDGRASS%CHINOCHLOACRUS GALLI, "EAUV0OACEAE #AN*"OTǻ (ATCH-$ 2EGULATIONOF#PHOTOSYNTHESIS FACTORS AFFECTING COLD MEDIATED INACTIVATION AND REACTIVATION OF PYRUVATE PI DIKINASE!UST*0LANT0HYSIOLǻ (ATTERSLEY07 4HEDISTRIBUTIONOF#GRASSESAND# GRASSESIN!USTRALIAINRELATIONTOCLIMATE/ECOLOGIA ǻ (EATON%! $OHLEMAN&'AND,ONG30 -EETING53 BIOFUELGOALSWITHLESSLANDTHEPOTENTIALOF-ISCANTHUS 'LOB#HANGE"IOLǻ (ENDRICKSON , 3HARWOOD 2 ,UDWIG - 7HITNEY 3- "ADGER-2ANDVON#AEMMERER3 4HEEFFECTSOF 2UBISCOACTIVASEON#PHOTOSYNTHESISANDMETABOLISMAT HIGHTEMPERATURE*%XP"OTǻ (ENNING*#AND"ROWN2( %FFECTSOFIRRADIANCEAND TEMPERATURE ON PHOTOSYNTHESIS IN # # AND ## 0ANICUMSPECIES0HOTOSYNTH2ESǻ (ULTEN%AND&RIES- !TLASOF.ORTH%UROPEAN6AS CULAR 0LANTS .ORTH OF THE 4ROPIC OF #ANCER VOLUME ) +OELTZ3CIENTIFIC +³NISGSTEIN 'ERMANY )BRAHIM$' 'ILBERT-% 2IPLEY"3AND/SBORNE#0 3EASONAL DIFFERENCES IN PHOTOSYNTHESIS BETWEEN THE #

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10


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