ArtiAddendum cleAddendum Article
Article Addendum
Plant Signaling & Behavior 8, e26964; November; © 2013 Landes Bioscience
On the persistence of memory Soft clocks and terrestrial biosphere-atmosphere interactions Víctor Resco de Dios* Hawkesbury Institute for the Environment; University of Western Sydney; Richmond, NSW Australia
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Keywords: biosphere-atmosphere interactions, circadian clock, diel cycles, gas exchange, endogenous regulation, evapotranspiration, gross ecosystem exchange, hysteresis, up-scaling Abbreviations: ET, evapotranspiration; GEE, gross ecosystem exchange; gs, stomatal conductance; VPD, leaf-to-air vapor pressure deficit *Correspondence to: Víctor Resco de Dios; Email:
[email protected] Submitted: 10/24/2013 Accepted: 10/25/2013 Citation: Resco de Dios V. On the persistence of memory: Soft clocks and terrestrial biosphereatmosphere interactions. Plant Signaling & Behavior 2013; 8:e26964; PMID: 24300129; http://dx.doi.org/10.4161/psb.26964 Addenda to: Resco de Dios V, Díaz-Sierra R, Goulden ML, Barton CVM, Boer MM, Gessler A, Ferrio JP, Pfautsch S, Tissue DT. Woody clockworks: circadian regulation of night-time water use in Eucalyptus globulus. New Phytol 2013; 200:743–52; PMID:23795820; http://dx.doi. org/10.1111/nph.12382
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he circadian clock is considered a central “orchestrator” of gene expression and metabolism. Concomitantly, the circadian clock is considered of negligible influence in the field and beyond leaf levels, where direct physiological responses to environmental cues are considered the main drivers of diel fluctuations. I propose to bridge the gap across scales by examining current evidence on whether circadian rhythmicity in gas exchange is relevant for field settings and at the ecosystem scale. Nocturnal stomatal conductance and water fluxes appear to be influenced by a “hard” clock that may override the direct physiological responses to the environment. Tests on potential clock controls over photosynthetic carbon assimilation and daytime transpiration are scant yet, if present, could have a large impact on our current understanding and modeling of the exchanges of carbon dioxide and water between terrestrial ecosystems and the atmosphere. “We propose that if we are to reliably scale measurements up from the leaf level, we must be able to explain the basic patterns of ecosystem CO2 exchange according to our present understanding of the biochemistry of leaf gas exchange.” -Hollinger et al. 1994,1 a proposition that has been extensively tested and validated over the past 19 y, and that also underpins current mathematical modeling of gas exchange.2 Similar analogous premises underlie the scaling and modeling of transpiration.3 Yet, there is a fundamental physiological process that regulates leaf level fluxes for which we do not
know whether or not it exerts a notable influence in the field and, by extension, whether or not it scales up to affect the exchanges of water and carbon between terrestrial ecosystems and the atmosphere: the circadian clock.4 Hennessey et al.5 observed a 20% oscillation in leaf photosynthesis in Phaseouls vulgaris in the free-running. If the same effect occurs at the ecosystem level, we could expect that the diel oscillation in Gross Ecosystem Exchange (GEE) under no variation in the physical environment (of light, temperature, etc.) would still be a fifth of that observed during a normally oscillating environment. This proportion would likely be higher for water loss because the relative oscillation in gs is usually higher than in leaf photosynthesis in the free-running.5 The key question to understand whether circadian rhythmicity is a significant driver of the daily pattern of GEE and ET (evapotranspiration) is whether it acts as a “soft” clock (its action is overridden by environmental cues) or as a “hard” clock (it remains a driver of importance similar to that of environmental cues). The circadian clock may impact ecosystem fluxes by at least 2 different ways. First, by setting a timedependent potential value. That is, GEE (or ET) at noon will necessarily be higher than in the afternoon, when “everything else” remains constant, if the clock is entrained to increase GEE (or ET) at noon.6 Suboptimal or limiting environmental conditions of temperature, vapor pressure deficit, and the like then reduce this time varying potential to its actual
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value. Second, the circadian clock may affect the sensitivity of gas exchange to environmental drivers in time. That is, the amplitude in the response to a change in light or temperature, to name a couple of environmental cues, could be different at mid-morning than at noon if the clock affects the responsiveness of gas exchange with time. Field studies have traditionally assumed that the control of the clock over leaf-to-ecosystem scales is soft, and of negligible importance relative to that of environmental cues. Recent evidence suggests otherwise. Nocturnal water loss often contributes around 10% of the total transpired water (although it can exceed 25% of the total water loss in some desert plants7). The temporal pattern of nocturnal stomatal conductance (gs) under non-limiting water supply is often characterized by an initial decline during the first hours after dusk, and a posterior increase that peaks around dawn. This nocturnal increase in gs may be attributed to the circadian clock when variation in the environmental drivers of gs is negligible (a “constant environment”).8 However, with the exception of some overcast nights, temperature tends to decrease while relative humidity tends to increase during the night, which leads to a decrease in vapor pressure deficit (VPD). In those species where nocturnal gs shows a negative response to VPD,9 the nocturnal increase in gs may be attributed to a combination of endogenous controls and of direct physiological responses References 1. Hollinger DY, Kelliher FM, Byers JN, Hunt JE, McSeveny TM, Weir PL. Carbon dioxide exchange between an undisturbed old-growth temperate forest and the atmosphere. Ecol 1994; 75:134-50; http://dx.doi.org/10.2307/1939390 2. Dietze MC. Gaps in knowledge and data driving uncertainty in models of photosynthesis. Photosynth Res 2013:1-12; http://dx.doi.org/10.1007/s11120013-9836-z; PMID:23645396 3. Bond-Lamberty B, Peckham SD, Gower ST, Ewers BE. Effects of fire on regional evapotranspiration in the central Canadian boreal forest. Glob Change Biol 2009; 15:1242-54; http://dx.doi. org/10.1111/j.1365-2486.2008.01776.x 4. Resco V, Hartwell J, Hall A. Ecological implications of plants ability to tell the time. Ecol Lett 2009; 12:583-92; http://dx.doi.org/10.1111/j.14610248.2009.01295.x; PMID:19504722 5. Hennessey TL, Freeden AL, Field CB. Environmental effects on circadian rhythms in photosynthesis and stomatal opening. Planta 1993; 189:369-76; http:// dx.doi.org/10.1007/BF00194433; PMID:24178493
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to the environment. However, nocturnal gs in many species has been found to respond positively to VPD under a changing environment.10-12 A nocturnal increase in gs in species that respond positively to VPD can only be explained by the action of a hard clock, that overrides the effect of environmental variation. Unraveling the effect of the clock on daytime processes is more complicated than on nocturnal processes, because of the larger number of environmental cues present. However, current evidence points toward the circadian clock being also a general driver of daytime carbon and water fluxes. The diurnal pattern in GEE or ET is often asymmetrical and, “everything else” being equal, significant differences in fluxes arise depending on time of day. This hysteresis has traditionally been attributed to a combination of hydraulic feedbacks after decreased leaf water availability as the day advances, decreased source demand, and increased photorespiration, among others.13-15 Although scarce, current evidence points toward circadian regulation of gs as an additional driver of the diurnal hysteresis on water and carbon fluxes.16 For instance, Mencuccini et al.17 observed that stomatal opening after root pressurization was lower in the afternoon than in the morning, which could not be attributed to changes in abscisic acid. Indeed, after employing a series of filters to remove environmental variation, Resco de Dios et al.6 observed a diel pattern in Net Ecosystem Exchange resembling that under a changing environment. 6.
Resco de Dios V, Goulden ML, Ogle K, Richardson AD, Hollinger DY, Davidson EA, Alday JG, Barron-Gafford GA, Carrara A, Kowalski AS, et al. Endogenous circadian regulation of carbon dioxide exchange in terrestrial ecosystems. Glob Change Biol 2012; 18:1956-70; http://dx.doi. org/10.1111/j.1365-2486.2012.02664.x 7. Ogle K, Lucas RW, Bentley LP, Cable JM, BarronGafford GA, Griffith A, Ignace D, Jenerette GD, Tyler A, Huxman TE, et al. Differential daytime and night-time stomatal behavior in plants from North American deserts. New Phytol 2012; 194:464-76; http://dx.doi.org/10.1111/j.14698137.2012.04068.x; PMID:22348404 8. Resco de Dios V, Díaz-Sierra R, Goulden ML, Barton CVM, Boer MM, Gessler A, Ferrio JP, Pfautsch S, Tissue DT. Woody clockworks: circadian regulation of night-time water use in Eucalyptus globulus. New Phytol 2013; 200:743-52; http:// dx.doi.org/10.1111/nph.12382; PMID:23795820
Plant Signaling & Behavior
Even if current evidence may be pointing toward a hard clock action, lack of data still impedes any generalization. In fact, we do not even know how widespread circadian regulation of gas exchange may be across species. However, the potential risk of ignoring whether such a “memory” of the recent past is persistent and leaves an imprint on GEE and ET seems too high under current efforts toward quantifying and predicting the responses of the carbon and water cycles to environmental changes. Because response curves are logistically complex at the ecosystem scale, models are parameterized from the relationship between GEE or ET and the parameter of interest (light, temperature, etc.). These relationships will necessarily be confounded by the clock, because of the uneven distribution of light and temperature over a day. Low temperature and light levels are common early and late in the day, and vice versa, high temperature and light levels only occur around midday. Thus, we could be attributing the temporal variation in fluxes to variation in environmental cues, when they could be driven by a combination of direct responses to environmental cues and endogenous circadian processes. Like Don Quixote, we could be fighting windmills, thinking that they are giants. Disclosure of Potential Conflicts of Interest
No potential conflicts of interest were disclosed.
9.
Barbour MM, Buckley TN. The stomatal response to evaporative demand persists at night in Ricinus communis plants with high nocturnal conductance. Plant Cell Environ 2007; 30:711-21; http:// d x.doi.org /10.1111/j.1365-3040.2007.01658.x; PMID:17470147 10. Resco de Dios V, Turnbull MH, Barbour MM, Ontedhu J, Ghannoum O, Tissue D. Soil phosphorous and endogenous rhythms exert a larger impact than CO2 or temperature on nocturnal stomatal conductance in Eucalyptus tereticornis. Tree Physiol 2013; 33:1206-1215; http://dx.doi.org/10.1093/ treephys/tp091 11. Zeppel MJB, Lewis JD, Chaszar B, Smith R A, Medlyn BE, Huxman TE, Tissue DT. Nocturnal stomatal conductance responses to rising [CO2], temperature and drought. New Phytol 2012; 193:929-38; http://dx.doi.org/10.1111/j.14698137.2011.03993.x; PMID:22150067 12. Caird MA, Richards JH, Donovan LA. Nighttime stomatal conductance and transpiration in C3 and C4 plants. Plant Physiol 2007; 143:410; http://dx.doi.org/10.1104/pp.106.092940; PMID:17210908
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13. Lüttge U, Hertel B. Diurnal and annual rhythms in trees. Trees (Berl) 2009; 23:683-700; http://dx.doi. org/10.1007/s00468-009-0324-1 14. Jones H. Stomatal control of photosynthesis and transpiration. J Exp Bot 1998; 49:387-98; http:// dx.doi.org/10.1093/jxb/49.Special_Issue.387
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15. Azcón-Bieto J. Inhibition of photosynthesis by carbohydrates in wheat leaves. Plant Physiol 1983; 73:681-6; http://dx.doi.org/10.1104/pp.73.3.681; PMID:16663282 16. Sanchez A, Shin J, Davis SJ. Abiotic stress and the plant circadian clock. Plant Signal Behav 2011; 6:223-31; http://dx.doi.org/10.4161/psb.6.2.14893; PMID:21325898
17. Mencuccini M, Mambelli S, Comstock J. Stomatal responsiveness to leaf water status in common bean (Phaseolus vulgaris L.) is a function of time of day. Plant Cell Environ 2000; 23:1109-18; http://dx.doi. org/10.1046/j.1365-3040.2000.00617.x
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