Bringing a Trait‐Based Approach to Plant‐Associated Fungi
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Biol. Rev. (2020), 95, pp. 409–433. 409 doi: 10.1111/brv.12570 Fungal functional ecology: bringing a trait-based approach to plant-associated fungi Amy E. Zanne1,∗ , Kessy Abarenkov2, Michelle E. Afkhami3, Carlos A. Aguilar-Trigueros4, Scott Bates5, Jennifer M. Bhatnagar6, Posy E. Busby7, Natalie Christian8,9, William K. Cornwell10, Thomas W. Crowther11, Habacuc Flores-Moreno12, Dimitrios Floudas13, Romina Gazis14, David Hibbett15, Peter Kennedy16, Daniel L. Lindner17, Daniel S. Maynard11, Amy M. Milo1, Rolf Henrik Nilsson18, Jeff Powell19, Mark Schildhauer20, Jonathan Schilling16 and Kathleen K. Treseder21 1Department of Biological Sciences, George Washington University, Washington, DC 20052, U.S.A. 2Natural History Museum, University of Tartu, Vanemuise 46, Tartu 51014, Estonia 3Department of Biology, University of Miami, Coral Gables, FL 33146, U.S.A. 4Freie Universit¨at-Berlin, Berlin-Brandenburg Institute of Advanced Biodiversity Research, 14195 Berlin, Germany 5Department of Biological Sciences, Purdue University Northwest, Westville, IN 46391, U.S.A. 6Department of Biology, Boston University, Boston, MA 02215, U.S.A. 7Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97330, U.S.A. 8Department of Plant Biology, University of Illinois Urbana-Champaign, Urbana, IL 61801, U.S.A. 9Department of Biology, University of Louisville, Louisville, KY 40208, U.S.A. 10Evolution & Ecology Research Centre, School of Biological Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales 2052, Australia 11Department of Environmental Systems Science, Institute of Integrative Biology, ETH Z¨urich, 8092, Z¨urich, Switzerland 12Department of Ecology, Evolution, and Behavior, and Department of Forest Resources, University of Minnesota, St. Paul, MN 55108, U.S.A. 13Microbial Ecology Group, Department of Biology, Lund University, Lund, Sweden 14Department of Plant Pathology, Tropical Research & Education Center, University of Florida, Homestead, FL 33031, U.S.A. 15Biology Department, Clark University, Worcester, MA 01610, U.S.A. 16Plant & Microbial Biology, University of Minnesota, St. Paul, MN 55108, U.S.A. 17US Forest Service, Northern Research Station, Center for Forest Mycology Research, Madison, Wisconsin, WI 53726, U.S.A. 18University of Gothenburg, Department of Biological and Environmental Sciences, Gothenburg Global Biodiversity Centre, Box 461, 405 30 G¨oteborg, Sweden 19Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales 2751, Australia 20National Center for Ecological Analysis and Synthesis, 735 State Street, Suite 300, Santa Barbara, CA 93101, U.S.A. 21Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, CA 92697, U.S.A. ABSTRACT Fungi play many essential roles in ecosystems. They facilitate plant access to nutrients and water, serve as decay agents that cycle carbon and nutrients through the soil, water and atmosphere, and are major regulators of macro-organismal populations. Although technological advances are improving the detection and identification of fungi, there still exist key gaps in our ecological knowledge of this kingdom, especially related to function. Trait-based approaches have been instrumental in strengthening our understanding of plant functional ecology and, as such, provide excellent models for deepening our understanding of fungal functional ecology in ways that complement insights gained from traditional and -omics-based techniques. In this review, we synthesize current knowledge of fungal functional ecology, taxonomy and systematics and introduce a novel database of fungal functional traits (FunFun). FunFun is built to interface with other * Author for correspondence (Tel.: +202 994 8751; E-mail: [email protected]). Biological Reviews 95 (2020) 409–433 © 2019 Cambridge Philosophical Society 410 Amy E. Zanne and others databases to explore and predict how fungal functional diversity varies by taxonomy, guild, and other evolutionary or ecological grouping variables. To highlight how a quantitative trait-based approach can provide new insights, we describe multiple targeted examples and end by suggesting next steps in the rapidly growing field of fungal functional ecology. Key words: clades, ecology, endophytes, evolution, functional traits, fungi, guilds, mycorrhizae, pathogens, saprotrophs, taxonomy. CONTENTS I. Introduction .............................................................................................. 410 II. Trait-based perspectives on functional ecology ........................................................... 411 (1) Developing a fungal functional trait-based approach: lessons from plant ecology .................... 411 (2) Utility of a trait-based perspective for fungal functional ecology ...................................... 411 (3) What can we learn from fungi? Unique contributions of fungal functional approaches ............... 413 (a) Small spaces, short times, big results .............................................................. 413 (b) It’s all in the partnership: understanding function by integrating plant and fungal traits .......... 414 (c) Broad-spectrum toolboxes ........................................................................ 414 (4) The FunFun database for fungal functional traits ..................................................... 414 (5) Targeted examples ................................................................................... 416 (a) Genotype–phenotype connections across fungal guilds ........................................... 416 (b) Colour as an understudied trait of fungi .......................................................... 419 III. Linking fungal diversity to taxonomic names within systematic hierarchies .............................. 419 (1) From molecules to species: assessing and describing fungal diversity ................................. 419 (2) Current state of the fungal tree of life ................................................................. 421 IV. Fungal guild assignments ................................................................................. 422 V. Fungal trait knowledge: guild overviews .................................................................. 422 (1) Endophytes ........................................................................................... 422 (2) Pathogens ............................................................................................ 423 (3) Saprotrophs .......................................................................................... 424 (4) Mycorrhizal fungi .................................................................................... 425 VI. Future directions for fungal functional ecology and evolution ............................................ 426 VII. Conclusions .............................................................................................. 427 VIII. Acknowledgments ........................................................................................ 427 IX. References ................................................................................................ 427 I. INTRODUCTION have been key to colonization of land by plants (Chisholm et al., 2006; Krings et al., 2007; Johnston-Monje & Raizada, In ecosystem functioning, diversity, and human use, fungi 2011; Lutzoni et al., 2018). are dominant but often hidden components of terrestrial Recent estimates suggest that the number of extant fungal ecosystems (Gadd, 2006; Stajich et al., 2009; Blackwell, 2011; species on Earth may be between 2–4 million (Hawksworth Kendrick, 2011; Hawksworth & L¨ucking, 2017; Steidinger &L¨ucking, 2017) and 165.6 million (Larsen et al., 2017), et al., 2019). They are perhaps best known as dead organic significantly outnumbering known plant species, which are matter decomposers, which makes them essential for cycling estimated at ∼350,000–400,000 species (Mora et al., 2011; of carbon and other nutrients through Earth’s ecosystems Larsen et al., 2017; https://stateoftheworldsplants.org/; and atmosphere (Rayner & Boddy, 1988; Floudas et al., 2012; http://www.theplantlist.org/). Most species, however, are van der Wal et al., 2013). Fungal biochemical pathways have too small or cryptic to be detected with the naked eye. We been harnessed for myriad processes, including production of have long distinguished various fungi from fruiting bodies or food, medicine, biofuels and other commodities. Conversely, cultures, but most fungi do not fruit regularly or grow in cul- fungal pathogens cause major losses in global food production ture. The advent of high-throughput sequencing (HTS) pro- (Strange & Scott, 2005; Schmaile & Munkvold, 2009; Fisher vided an important lens through which to view the taxonomic et al., 2012). Fungi have had a long and intimate association and functional diversity of these eukaryotes that would oth- with plants. As root- and leaf-associated symbionts, fungi erwise remain undetected or unidentified (Peay, Kennedy, & directly affect richness and productivity of present-day plant Talbot, 2016). Using HTS and other molecular tools, we can communities (van der Heijden et al., 1998; Bakker et al., 2012; now ascertain patterns of fungal diversity and community Mueller, Belnap, & Kuske, 2015), and these symbioses may assembly across space and time, as well as detect functional Biological Reviews 95 (2020) 409–433 © 2019 Cambridge Philosophical Society Fungal functional ecology 411 genes and gene products