PerspectiveEvolution

Terrestrial Life--Fungal from the Start?

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Science  15 Sep 2000:
Vol. 289, Issue 5486, pp. 1884-1885
DOI: 10.1126/science.289.5486.1884

Early terrestrial environments were poor in nutrients and subject to desiccation; habitats were poorly shaded and thus fully exposed to the bright light of day. In 1975, Pirozynski and Malloch [HN1] (1) proposed that mutually beneficial (mutualistic) symbiosis [HN2] of fungi [HN3] and plants assisted in the original invasion of plants into these harsh terrestrial environments [HN4]. Others had previously suggested a mutualistic origin for land plants, but Pirozynski and Malloch's hypothesis was more fully developed than those of earlier workers. Advances in fungal systematics have outdated some of the evolutionary speculation in (1), but the basic premise that symbiotic relationships between so-called arbuscular mycorrhizal (AM) fungi [HN5] and the roots of higher plants were essential in the move of plants to land continues to be accepted. Mycorrhizae are symbiotic associations between many different types of fungi and plant roots [HN6]. The vast majority of plants are mycorrhizal, and they, including those associated with AM fungi, usually benefit from enhanced uptake of minerals and water.

The report by Redecker et al. [HN7] on page 1920 of this issue (2) comes close to confirming this 25-year-old premise. Before this report, the earliest record of an AM fungus, in association with vascular plants, came from the 400-million-year-old Rhynie Chert [HN8] (3). The 460-million-year-old Ordovician fungus reported in (2) (see the figure) was not discovered in association with plant remains, but its unique morphology strongly suggests that it was a member of the Glomales [HN9], a group in which all extant taxa are AM fungi.

Fungi everywhere.

Geologic time scale showing relative positions in time of fossils (A to F and ectomycorrhiza, black type) and estimates of phylogenetic splits (blue type) mentioned in Redecker et al. (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, 19). 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).

In addition to the unique morphology, there is circumstantial evidence that the fossil represents an AM fungus. Dispersed microfossil evidence indicates a contemporaneous presence of bryophyte-like plants at some Ordovician [HN10] sites. Bryophytes are a small group of plants comprising mosses, liverworts, and hornworts [HN11] and are believed to be among the earliest plants on Earth. Some extant bryophytes are associated with glomalean fungi (4). Furthermore, it has been shown that when certain bryophytes are infected experimentally with AM fungi, they form mycorrhiza-like associations. Using calibration points from the fossil record, estimated divergence times based on ribosomal DNA sequences are consistent with the existence of a lineage of Glomales in the Ordovician Period. The results reported by Redecker et al. indicate that the most derived fungal (Ascomycota-Basidiomycota [HN12]) lineage diverged at 600 million years ago (Ma), as suggested by Berbee and Taylor [HN13] (5). By comparison, the origin of plants has been conservatively placed at 600 Ma; the divergence of metazoans (animals) and fungi from a close common ancestor has been placed at 965 Ma, ±140 Ma, but a later date has also been proposed on the basis of protein data and revised calibration points (5).

Price (6, p. 375) has proposed that “in the broadest sense ecology recapitulates phylogeny,” so that in the progression from the earliest prokaryotic microorganisms to eukaryotic microorganisms, each group had a role in preparing Earth for successive groups of organisms. Moreover, Price helped popularize the ecological importance of microorganisms by pointing out that “Noah's ark ecologists” ignore organisms smaller than “bird food.” More recently, biologists have increasingly recognized the presence and function of microorganisms in communities and ecosystems (7). As a result, the apparent universality of plant and fungal associations is now well recognized.

In addition to AM fungi, other fungi form a variety of mycorrhizal associations that have been distinguished and named on the basis of morphology and plant host. The annual autumn fruitings of mushrooms in temperate forests throughout the world provide spectacular evidence of such mycorrhizal associations. However, the commonest mycorrhizal fungi usually do not produce aboveground evidence of their presence (8).

Endophytes [HN14] and lichens [HN15] 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 mycorrhizal fungi. One group, the Clavicipitaceae [HN16], produces 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 [HN17] comprise thousands of species of ascomycetes (10). The universality of mycorrhizal, endophytic, and lichen associations with plants belies the large number of independent origins that occurred as the phototrophs and fungi invaded Earth and filled its niches.

To overlook the ubiquitous mutualistic fungi, in association with plants, can have 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 opportunity to draw attention to yet more fungal mutualists. Symbiotic associations between fungi and animals [HN18], 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 participate 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 (16), and the scale insects that sacrifice individuals as fungal food in return for fungal protection (17). 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 plant associates. Investigations of fossil insects may reveal additional information on their symbionts (see the figure).

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.

HyperNotes Related Resources on the World Wide Web

General Hypernotes

The University of California Museum of Paleontology (UCMP) at Berkeley presents extensive Web exhibits about the phylogeny of living and fossil organisms, geology and geologic time, and evolutionary theory; the UCMP Subway offers links to other Internet resources. A presentation on fungi is included.

The Tree of Life, a project under the direction of D. Maddison, Department of Entomology, University of Arizona, presents information about the phylogenetic relationships and characteristics of organisms, as well as a selection of Internet links. An overview of the fungi is provided.

L. Moran, Department of Biochemistry, Faculty of Medicine, University of Toronto, provides a collection of Internet resources related to evolution.

Evolution on the Web for Biology Students is a presentation on evolution by R. Gendron, Biology Department, Indiana University of Pennsylvania; a page of other evolution links is also offered.

The Internet Resource Guide to Zoology from the Zoological Record includes a collection of links to evolution and phylogeny Web resources.

K. Holsinger, Department of Ecology and Evolutionary Biology, University of Connecticut, maintains an Internet directory of sites of interest to botanists, ecologists, and evolutionary biologists.

Links for Paleobotanists is maintained by K.-P. Kelber, Institute of Mineralogy, University of Würzburg, Germany.

Botany Online is a Web textbook by P. von Sengbusch, Department of Biology, University of Bielefeld, and Institute for General Botany, University of Hamburg, Germany. An Internet library on teaching botany and related topics is also offered.

The WWW Virtual Library: Mycology is maintained by K. Hodge, Department of Plant Biology, Cornell University.

The Mycological Society of America provides a slide collection online, a section of comments from mycologists about their careers, and a collection of Internet links.

The subject categories version of the Internet Directory for Botany includes a section of Internet resources on algae, bryophytes, and fungi.

Tom Volk's Fungi is a collection of resources on fungi maintained by T. Volk, Department of Biology, University of Wisconsin, La Crosse. He offers a slide presentation on fungi, as well as the Fungus of the Month collection.

Illustrations and other selections from the mycology textbook Fifth Kingdom by B. Kendrick are made available by Mycologue Publications. A glossary is provided.

J. Spatafora, Department of Botany and Plant Pathology, Oregon State University, provides lecture notes for a course on mycology.

G. Wong, Department of Botany, University of Hawaii at Manoa, Honolulu, provides lecture notes for a mycology course. Lecture notes on mycorrhiza and lichens are included.

D. Walters, Biological Sciences Department, California Polytechnic State University, San Luis Obispo, provides lecture notes for a course on evolution.

S. Leslie, Department of Earth Sciences, University of Arkansas, provides lecture notes for a paleobiology course.

P. Gore, Georgia Perimeter College, Clarkston, presents lecture notes and links to Internet resources for a historical geology course.

P. Ciesielski, Department of Geological Sciences, University of Florida, offers lecture notes for a course on the evolution of Earth and life.

D. Fitch, Department of Biology, New York University, makes available lecture notes and supplemental materials for a course on evolution. A presentation on systematics and phylogeny is included.

D. Rand, Program in Biology, Brown University, provides lecture notes for a course on evolutionary biology.

P. Strother, Department of Geology and Geophysics, Boston College, provides lecture notes for a course on the origin and evolution of life on Earth.

R. Gastaldo, Department of Geology, Colby College, Waterville, ME, offers lecture notes for a course on paleobotany and lecture notes for a historical geology course.

Numbered Hypernotes

1. According to the International Directory of Mycorrhizologists, K. Pirozynski is at the Earth Sciences Division of the Canadian Museum of Nature. D. Malloch (and research page) is in the Department of Botany, University of Toronto; his book Moulds: Isolation, Cultivation, Identification is available on the Web.

2. Compton's Encyclopedia Online has an article on symbiosis. Britannica.com offers brief Encyclopædia Britannica introductions to symbiosis and mutualism; the article on community ecology has a section on mutualism. G. Wong provides a slide lecture presentation on fungal symbiosis. Von Sengbusch's Botany Online includes a chapter titled “Interactions between plants and fungi: The evolution of their parasitic and symbiotic relations.”

3. The Horticulture and Crop Science Department, Ohio State University, provides an introduction to fungi for a course on plant biology. The Online Biology Book, provided by M. Farabee, Estrella Mountain Community College, Avondale, AZ, includes an overview of fungi. Britannica.com makes available an Encyclopædia Britannica article on fungi. The University of Michigan Herbarium includes a presentation titled “Fun Facts about Fungi,” as well as a collection of Internet links on systematics. P. Bell, School of Natural Resources, Fleming College, Lindsay, ON, Canada, provides an introduction to fungi in lecture notes for a course on forest pathology. J. Sandridge, School of Biological Sciences, University of Nebraska, provides an introduction to fungi and lecture notes on fungal phyla for a biodiversity course. Fungal Web is a part of Microbial World, profiles of microorganisms presented by J. Deacon, Institute of Cell and Molecular Biology and Biology Teaching Organisation, University of Edinburgh. Ari Kornfeld's Natural Perspective Web site offers a presentation on fungi. G. Barron, professor emeritus, University of Guelph, presents a Web site of fungal images.

4. Britannica.com offers an Encyclopædia Britannica article on the evolution of land plants in the Ordovician through Middle Devonian periods. The UCMP's Virtual Paleobotany Laboratory includes a presentation on early land plants. P. Ciesielski provides lecture notes on the transition of plants to land for a course on the evolution of Earth and life. Hans Steur's Paleobotany Pages offer a presentation on how plants conquered the land. P. Strother provides lecture notes on the transition to terrestrial flora for a course on the origin and evolution of life on Earth. S. Carrington, Department of Biological and Chemical Sciences, University of the West Indies, Barbados, provides lecture notes on the conquest of the land by plants for a course on plant biodiversity. B. Dattilo, Department of Geosciences, Weber State University, Davis Campus, Layton, UT, provides lecture notes on the origin and early evolution of terrestrial communities for a course on the fossil record. R. Gastaldo offers lecture notes on early evidence for land inhabitation for a course on paleobotany.

5. The International Collection of Arbuscular and Vesicular-Arbuscular Mycorrhizal Fungi (INVAM) offers links to Internet resources and illustrated taxonomy resources for arbuscular mycorrhizal (AM) fungi, as well as a collection of articles and essays. The Green Gene Gazette Online, a publication of the Plant Biology Program at the University of Guelph, makes available an article by J. Klironomos titled “The ecology of arbuscular mycorrhizal fungi.” The Palaeobotanical Research Group, University of Münster, Germany, offers a presentation about vesicular arbuscular mycorrhizae. Y. Dalpé, Systematics Mycology/Botany Research Section, Agriculture and Agri-Food Canada, provides an introduction to arbuscular mycorrhizae; a report on the biodiversity of mycorrhizal fungi is also available.

6. Microbial World offers an introduction to mycorrhizae. The Mycorrhiza Research Group, University of the West Indies, provides an introduction to mycorrhizae. The Mycorrhiza Information Exchange, maintained by R. Augé, Department of Ornamental Horticulture and Landscape Design, University of Tennessee, makes available mycorrhizal essays, literature resources, and images, as well as links to Internet resources related to mycorrhiza. INVAM provides a draft of an article on mycorrhizae by J. Morton (which was published in the McGraw-Hill 1997 Yearbook of Science and Technology). D. Sylvia, Soil and Water Science Department, University of Florida, offers an overview of mycorrhizal symbioses. Von Sengbusch's Botany Online includes a presentation on mycorrhizae. Agripedia, an Internet instructional resource provided by the College of Agriculture, University of Kentucky, offers lecture notes by C. Schardl on mycorrhizae for a course on plant-microbe interactions. The Australian CSIRO Forestry and Forest Products Web site offers an illustrated presentation on mycorrhiza; an introduction to mycorrhizae and mycorrhizal associations and sections on arbuscular mycorrhizae and the roles of mycorrhizae are included.

7. D. Redecker is at the Bruns Laboratory, Department of Plant and Microbial Biology, University of California, Berkeley.R. Kodner and L. Graham are in the Department of Botany, University of Wisconsin.

8. The Palaeobotanical Research Group, University of Münster, Germany, offers a presentation on the Rhynie Chert and its flora; a presentation by H. Kerp on the history of palaeozoic forests is also available. The presentation on early land plants from UCMP's Virtual Paleobotany Laboratory includes a section on the Rhynie flora; a photo of the Rhynie Chert is provided. UCMP provides information about the fungi fossil record. The UCMP presentation on the Devonian has a section on the Rhynie Chert. H. Steur's Paleobotany Pages provides an introduction to the Rhynie Chert with photos of fungi fossils and other Rhynie Chert images. The Rhynie Chert Research Group, University of Aberdeen, Scotland, presents a history of the study of the Rhynie Cherts.

9. INVAM offers an overview of Glomales, as well as a book chapter by J. Morton titled “Evolution of fungi in Glomales,” which has a section on the origin of the arbuscular mycorrhizal symbiosis. A student Web project by J. Jonely on Glomales was prepared for a course on fungi taught by A. Gargas, Department of Botany, University of Wisconsin. J. Spatafora offers lecture notes on Endogonales and Glomales.

10. UCMP offers a presentation on the Ordovician. An Encyclopædia Britannica article on the Ordovician is available from Britannica.com. P. Gore presents lecture notes on the Ordovician for a historical geology course. A Web exhibit of Ordovician fossils from Wisconsin is presented by the University of Wisconsin, Fox Valley campus.

11. The American Bryological and Lichenological Society offers a collection of Internet resources. UCMP provides introductions to the Anthocerotophyta (hornworts) and the Bryophyta (mosses). Land Plants Online, a presentation by D. Nickrent and K. Renzaglia, Department of Plant Biology, Southern Illinois University, Carbondale, includes information about liverworts, hornworts, and mosses. S. Carrington provides lecture notes on bryophytes for a course on plant biodiversity. R. Stotler and B. Crandall-Stotler, Department of Plant Biology, Southern Illinois University, Carbondale, provide information resources on bryophytes.

12. The section on fungi of the Tree of Life offers presentations on the Basidiomycota and the Ascomycota. Microbial World offers a presentation on Basidiomycota. J. Spatafora offers lecture notes on Basidiomycota and Ascomycota for a mycology course. The Münster Palaeobotanical Research Group provides information about the oldest fossil ascomycetes.

13. M. Berbee (and also) is in the Department of Botany, University of British Columbia. J. Taylor is in the Department of Plant and Microbial Biology, University of California, Berkeley.

14. The November 1998 newsletter of the Tree Pathology Cooperative Programme of the Forestry and Agricultural Biotechnology Institute, South Africa, had an article on endophytes by D. Wilson. The Ontario Ministry of Agriculture, Food and Rural Affairs makes available an article by P. Charbonneau about endophytes on turfgrass plants.

15. Microbial World offers a presentation on lichens. UCMP provides an introduction to lichens. The North American Lichen Project provides an introduction to the biology of lichens and a selection of lichen images. Fun with Lichens is an educational presentation by the Department of Botany and Plant Pathology, Oregon State University. D. Jones, Environmental Science Research Group, University of Bangor, Wales, provides lecture notes on lichens for a course on plant-soil-microbial interactions. The Münster Palaeobotanical Research Group provides information about the oldest fossil lichen.

16. J. Spatafora provides information about the Clavicipitaceae. Agripedia from the University of Kentucky offers lecture notes by C. Schardl on Epichloe/Neotyphodium (family Clavicipitaceae) symbiosis with grass for a course on plant-microbe interactions.

17. UCMP presents information on cyanobacteria and green algae. The Department of Botany of the Smithsonian National Museum of Natural History offers an introduction to algae and links to phycological Internet resources. D. Krempels, Department of Biology, University of Miami, provides an introduction to the cyanobacteria.

18. J. Sandridge discusses fungal associations with animals in lecture notes on fungal mutualism for a biodiversity course. G. Wong offers lecture notes on fungi and animals for a mycology course. R. Lichtwardt, emeritus professor of botany, University of Kansas, offers an illustrated presentation on the taxonomy and co-evolution of Trichomycetes (gut-inhabiting fungi) and their hosts. M. Blackwell offers a presentation on Laboulbeniales, ascomycetous fungi that are associates of arthropods.

19. M. Blackwell is in the Department of Biological Sciences, Louisiana State University, Baton Rouge.

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