Terrestrial Life: Fungal from the Start? Meredith Blackwell Science, New Series, Vol. 289, No. 5486. (Sep. 15, 2000), pp. 1884-1885. Stable URL: http://links.jstor.org/sici?sici=0036-8075%2820000915%293%3A289%3A5486%3C1884%3ATLFFTS%3E2.0.CO%3B2-N Science is currently published by American Association for the Advancement of Science.
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PERSPECTIVES: EVOLUTION
Terrestrial LifeFungal from the Start? arly terrestrial environments were poor in nutrients and subject to desiccation; habitats were poorly shaded and thus fully exposedto the bright light of day. In 1975, Pi1~0zynsk.iand Malloch (I) proposed that mutually -cial (mutualistic) symbiosis of fungi and plants assisted in the ariginal invasion of plants into these harsh terrestrial environments. Others had previously suggested a mutualistic origin for land plants, but Pirozynski and Malloch's thesis was more fully developed than those of earlier workers. Advances in fungal systematics have outdated some of the evolutionary spedation in (I),but the basic premise that symbiotic relationships between so-called arbuscular mycorrW (AM) fungi and the foots of higher plants were essential in the move of plants to lamd continues to be accepted. Mycofihizae are symbiotic associations between many different types of fungi and plant roots. The vast majority of plants are mycorrhizal, and they, including those associated with AM usually-benefit &om enhanced uptake - of m i n d and water. The report by Redecker et al. on page 1920 of this issue (2) comes close to conf i g this 25-year-old premise. Before this report, the earliest record of an AM fungus,in~onwithvascnlarplants, came fiom the 400-million-yearr-oldRhynie Chert (3). The 460-million-year-old Ordovician fungus reported in (2) (seethe figure0nthenuxtpage)wasnot~in association with plant remains, but its unique morphology stmgly suggests that it was a member of the Glomales, a group in
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whichallextanttaxaareAM~.
In addition to the unique morphology, there is circumstantial evidence that the fogsilrepresentsanmfungus.Dispersed micmfogsil evidence indicates a contemporaneous presence of bryophyte-like plants at some Orduvician sites. Bqyophytes are a small group of plants c m @ i mosses, livacuwts, and hornworts and are believed to be among the earliest plants on Earth (see the figure above). Some extant bryophytes are associated with g l d e a n fungi (4). Furthemore, it has been shm
that when certain bryophytes are infected experimentally with AM fimgi, they form mycorrhiza-like associations. Using calibration points h m the fossil record, estimated diverpce times based on ribosomal DNA sequences are consistent with the existence of a lineage of Glomales in the Or-
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~ntsofearlyfungiand plants. (Top) Chytrids such as Chytridium confewae were the I fi& group of fungi to split from other fund after the fungus-anima1split ;bout 900 Ma. Ehy'trids are known from the Rhynie Chert 400 Ma.The fungus has a diameter of around 40 micrometers. (Right) Stalked starlike structureslift the female sex organs of the dloeciousliverwort Marchantia from the surface of the livemort thallus. liverwortsare nonvascular plants, and fossils of similar plants haw been found in Ordoviciandeposlts.The stalks are about 5 centimeters high.
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ddcian Period. The resultsreportsdby Redecker et al. indicate that the most derived fungal (Asoomycota-Basidiomycota)lineage diverged at 600 million years ago @la), as suggested by Berbee and Taylor (5). By comparison,the origin of plants has been commvatively placed at 600 Ma, the dkrgence of metazoans (animals) and andgi h m a close common amestor has been placed at 965 Ma, *I40 Ma, but a later date has also been proposed on the basis of proThe author Is in the Department of Biological ki- tein data and revised catibraton points (5). Price (6, p. 375) has proposed that ''in ences, Louisiana State University. Baton Rouge, U 70803, USA E-mail: ~ n i x l s n c d s u . ~ the broadest sense ecology recapitulates -
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phylogeny," so that in the progression from the earliest prokaryotic m i c r o o to~ euksryotic m-i each group had a role in preparing Earth for successive groups of organisms. Moreover, Price h e 1 4 &the ecological importance of microorganisms by pointing out that "Noah's ark ecologists" ignore organisms smaller than '?bird food" More m t l y , biologists have increasingly recognized the m c e and andction of m i c 1 0 0 in ~ communities and ecosystems (7). As a result, the apparent universality of plant and fimgalasmiati~~l~isnowwellrecognized. In addition toAM fimgi,other ftmgi hm a variety of mycorrhizal associations that have been dhhgukhed and named on the bask of morphology and plant hod The annual autumn hitings of mushroams in temperate fares*, thm@out the world provide spectacvlarevi~ofsrachmyconhizalassociatiom. However, the cammonest mycorrhizalfungiusuallydonotproduoeaboveground evideme of their presence (8). Endophytes and lichens are two more examples of fungus-plant mutualisms. With very few exceptions, terrestrial plants all have endophytic fungi in their aboveground parts, but they too can be overlooked because they are microscopic and cause no outward signs of their presence. The role of endophytic fungi is less well known than that of mycmrhizal fungi. One group, the Clavicipitmeae, produces
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alkaloids in endophytic associations, primarily with grasses. Other plants have endophytic associations with a diverse assemblage of fungi (9). Lichen-forming fungi associated with green algae and cyanobacteria comprise thousands of species of ascomycetes (10). The universality of mycorrhizal, endophytic, and lichen associations with plants belies the $ 6 large number of independent origins that occurred as the photolrophs and fungi invaded Earth and fded its niches. To overlook the ubiquitous mutualistic fimgi, in association with plants, can have
15 SEPTEMBER 2000 VOL 289 SCIENCE www.sciencernag.org
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S C I E N C E ' S COMPASS
unfortunate consequences. For example, if one were unaware of endophytes, one would expect DNA extracted from the leaves of plants to be plant DNA, and a symbiotic fungus has tricked more than one systematist (11, 12). Worse yet, fungi can contaminate other fungi growing with them, an even more difficult situation to detect. Sequence alignment tools and specific primers are now commonly used to prevent mistakes. It is equally important to consider the physiological effects of plant mutualists to a plant, and the consequences of mutualism are now more frequently taken into account in experimental studies (13). Redecker et al.'s discovery of an Ordovician AM fungus affords an opportuni-
ty to draw attention to yet more fungal mutualists. Symbiotic associations between fungi and animals, although usually of more recent origin, may be as pervasive as those between fungi and plants, despite their discontinuous taxonomic distributions. There are several well-known fungal mutualists of animals, such as gilled mushrooms cultivated by ants and Old World termites, fungi carried by bark beetles and wood wasps in their ectoskeleton "pockets" to feed their young, and fungal fermenters in the gut of many mammalian herbivores. Less generally known are the vitamin-supplying fungal symbionts in the gut of aquatic insect larvae and adult marine crustaceans (14), yeasts that partici-
Ages from Dl' -
Fungal fossils
Animals few
Ruminate fungal flagellates (40 h,=, Cicada fungus pathogen-deer t ~ f f l pathogen e spli (43 Ma)
Ectomycorrhiza (50 Ma) Lichen (50 Ma)
E Gllled mushroom from amber (90 Ma)
Moet modem l.n$ectalndudlng moths, beenel o-homrs tennnekr (Jumdc)
Dung beetle8 (200 Ma) Dlpfera (225 Ma)
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pate in sterol utilization and nitrogen recycling in gut pockets of insects such as plant hoppers (15), mildly parasitic ascomycetes that associate with arthropods for nutrition and dispersal (I@, and the scale insects that sacrifice individuals as fungal food in return for fungal protection (1 7). The list can go on, and intriguing new animal-fungus associations continue to be discovered, such as the many new species of yeasts that lay unsuspected in the gut of mushroom-feeding beetles (18). When the animal-symbiotic fungi are better known, their distributions may seem as continuous as those of ~ l a nassociates. t Investigations of fossil insects may reveal additional information on their svmbionts (see the figure, this page). Renewed interest in fungal evolutionary biology has come not only from phylogenetic studies but is enhanced by the discovery of fossils such as the one discussed here. Evolutionary studies that integrate the fossil record, divergence based on DNA, and knowledge of symbiotic associations will continue to be important and will be extended to a broader range of organisms. Awareness of the symbiotic relationships is essential if we are to learn more about the fungi themselves. Perhaps a next report may include an Ordovician AM fungal fossil associated with a plant. References and Notes
AM fungus (240 iia) C Basldlomyceteclamp connections (290 Ma)
B Glomales (Rhynie, 400 Ma) D Ascomycetes (Rhynle, 400 Ascomycetes (Silurian)
A Glomales (480-455 Ma)
1. K. A. Pirozynski and D. W. Malloch, Biosystems 6, 153 (1975). 2. D. Redecker, R. Kodner, L E. Graham, Science 289,1920 (2000). 3. T. N.Taylor etaL M w o g i a 87, &11 (1995). In additionto AM fungi, the studies of Taylor and his colleagues have provided information on other Rhynie fungi, including chytrids, algal parasites, axomycetes, and a cyanolichen. 4. D. J. Read et aL Philos. Trans Bid Sd.355,815 (2000); C. H. Wellman and J.Gray, Philos Trans B i d Scl355.717 (2000). 5. M. L. Berbee and J. W. Taylor. The Mycota. D. J. McLaughlin, E. C . McLaughlin, P. A. Lemke, Eds. (Springer-Verlag, New York, 2000), vol. VII, pp. 229-246: M. S.Y. Lee, j. Mol. Evol. 49,385 (1999). 6. P.W. Price,Agrc Ecoyst Environ. 24,369 (1988). 7. M. A. Selosse and F. Le Tacon, Trends Ecol. EvoL 13, 15 (1998). 8. M. Cardes and T. D. Bruns, Canj.Bot 74,1572 (1996). 9. E.Arnold et aL Ecol Lett 3,267 (2000). 10. D. L Hawksworth et aL, Dictionaryo f the Fungi(CAB Intemational,WaUingford, UK, 1996). 11. F. J. Camacho et al, M d Em16,983 (1997). 12. W. P. Zhang et al, M d Phylogenet E d 8,205 (1997). 13. M. F. Allen et aL, Can. j. Bot 58,371 (1980); K. K. Newsham et al, Em183,991 (1995). 1 4 J. K. Misra and R W. Lichtwardt, lIIudratedGenera of Trichomycetes: Fungal Symbionts o f Insects and Other Arthropods (Science Publishen. Enfield, NH, 2000); C. L Van Dover and R. W. Lichtwardt, Biol. Bull. 171, 461 (1986). 15. J. M.Wetze1 etal, j. Chem E d 18,2083 (1992);T.Sasaki et a1.j. lnsectphysid42.125 (1996). 16. A. Weir and P. M. Hammond. Biodiver. Consew. 6, 701 (1997). 17. R C. Conner, BioL Rev. 70,427 (1995). 18. 5-0. Suh and M. Blackwell unpublishedresults. 19. C. J. Alexopoulos et aL, Introductory Mycology (Wiley, NewYok 19%). 20. D. J. Cantrell and J. C. Douglas. Austr. j. Bot 36, 257 (1988). 21. Iwould like to thank BerbeeandTaylor for allowing me to cite their paper prior to publication [see (S)].
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Fungi everywhere. Geologic time scale showing relative positions in time of fossils (A to F and edomycorrhiza, black type) and estimates of phylogenetic splits (blue type) mentioned in Redecker etal. (2) and Berbee and Taylor (5). Animal fossils (red type) are known associates of several groups of symbiotic fungi, and could help in the discovery of fungal symbiont fossils (5, 79). See also Selosse and Le Tacon (7). Information on endophytes might be obtained by investigating grasses and other plant groups.The first definite Lichen fossil (50 Ma) is relatively recent.A few much earlier reports of Rhynie and even Precambrian lichens exist but are not fully accepted (6). www.sciencemag.org
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References and Notes 2
Glomalean Fungi from the Ordovician Dirk Redecker; Robin Kodner; Linda E. Graham Science, New Series, Vol. 289, No. 5486. (Sep. 15, 2000), pp. 1920-1921. Stable URL: http://links.jstor.org/sici?sici=0036-8075%2820000915%293%3A289%3A5486%3C1920%3AGFFTO%3E2.0.CO%3B2-G 13
Arbuscular Mycorrhiza Protect an Annual Grass from Root Pathogenic Fungi in the Field K. K. Newsham; A. H. Fitter; A. R. Watkinson The Journal of Ecology, Vol. 83, No. 6. (Dec., 1995), pp. 991-1000. Stable URL: http://links.jstor.org/sici?sici=0022-0477%28199512%2983%3A6%3C991%3AAMPAAG%3E2.0.CO%3B2-4
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