SEARCH

SEARCH BY CITATION

Keywords:

  • endophytes;
  • evolution;
  • myco-heterotrophy;
  • mycorrhizal fungi;
  • symbiosis

Just as the processes that drive natural selection are now recognized to manifest at levels of biological organization above and below those of the individual – with trait variation, differential rates of birth and death, and heredity pervasive from nucleic acids to cells to populations (Williams, 1966; Dawkins, 1976; Sober, 1984;Keller, 1999; Okasha, 2008) – so too is co-evolution now viewed not just at the level of species, but also at phylogenetic scales ranging from genotypes to major clades (Thompson, 2005). Although strict-sense co-cladogenesis remains a holy grail among some biologists seeking to document reciprocal evolutionary change, researchers have begun to recognize that phylogenetic trees need not branch in parallel to indicate co-evolutionary history. A broader view encompassing ecology brings to light the ways in which co-evolutionary processes can be subtle – yet pervasive, rapid, and interlaced inexorably with geography, chance and the ecological community in which organisms are embedded.

Such a theme runs through the interface of mycology and botany, as showcased at the 2009 meetings of the Mycological Society of America and the Botanical Society of America in Snowbird, Utah. Speakers highlighted the ways in which the plant and fungal trees of life reflect co-evolutionary processes at multiple scales – from roots and leaves to grasslands and forests – often in ways more akin to interwoven branches than to parallel bifurcations. Not only were fungal associates of plants shown to respond to evolutionary change in their hosts, but responses of plants to fungi were a significant theme. (Presentation titles, author affiliations and related information can be found online at http://2009.botanyconference.org.)

Co-evolution of plants and fungi – ancient in nature and ongoing today – has shaped every plant, and by extension every terrestrial ecosystem, in ways we are only beginning to appreciate. By integrating from genotypes to the broadest phylogenetic scales, mycologists and botanists are examining recent and historical traces of important symbioses in ways that will inform a modern co-evolutionary synthesis.

Micro-evolutionary perspectives on plant–fungal co-evolution

  1. Top of page
  2. Micro-evolutionary perspectives on plant–fungal co-evolution
  3. Species-level co-evolution in plant–fungal interactions
  4. Co-evolution in the broad sense
  5. Synthesis
  6. References

Darwin argued that evolution by natural selection has three requisites: trait variation among individuals within a species, heritability of traits, and differential survival and reproduction in favor of individuals with the most beneficial traits (Darwin, 1859). Investigators are beginning to shed light on how these requisites, from the perspective of plants and fungi, influence an organism’s partners in symbiosis. For example, new evidence suggests that the composition of plant-associated fungal communities, including fungi as diverse as endophytes, ectomycorrhizal fungi and epiphytic lichens, can differ among genotypes of the trees with which they associate (e.g. Lamit, 2008; Sthultz et al., 2009a). Moreover, studies show considerable functional variation among genotypes of fungal symbionts, frequently with strong effects on host fitness (e.g. Koch et al., 2006; Ji, 2007). Unquestionably, genetically based trait variation has important ecological implications for plant–fungal interactions, consistent with Darwin’s first requisite for evolution by natural selection.

In testing Darwin’s second and third requisites, studies are moving beyond documenting genotype differences to investigate their heritability and evolutionary significance. Presentations by Jamie Lamit and Chris Sthultz, representing researchers at Northern Arizona University (NAU), showed that even long-lived trees such as pinyon pine (Pinus edulis) can be used to study co-evolution between plants and fungi. Strikingly, evidence is mounting that the propensity to harbor a certain composition of fungal symbionts can be passed from one generation to the next (Elamo et al., 1999; Sthultz, 2008). In northern Arizona, USA, P. edulis exhibits a genetically based polymorphism in resistance and susceptibility to chronic herbivory by a stem-boring moth (Whitham & Mopper, 1985; Mopper et al., 1991). Ectomycorrhizal communities differ dramatically between resistant and susceptible phenotypes, and long-term removal of moths from susceptible trees does not shift fungal composition to resemble resistant trees (Fig. 1a; Sthultz et al., 2009a). Ectomycorrhizal communities of seedlings grown in soil cores collected under resistant and susceptible trees group by the phenotypic class of their maternal parent, regardless of the source of their soil core, and contain fungal communities resembling those of adult trees of their phenotypic class (Sthultz, 2008).

image

Figure 1.  (a) Nonmetric multidimensional scaling ordination of ectomycorrhizal communities of adult Pinus edulis trees that are moth-resistant (diamond), moth-susceptible (square), or from which moths have been removed (triangle). Each symbol represents the mean plus ± 1 SE of ectomycorrhizal community ordination scores of trees for each group. (b) Trees with the moth-resistant phenotype have three times greater mortality than moth-susceptible phenotypes at four different sites and on average. Bar, ± 1 SE. Adapted from Sthultz et al. (2009a,b).

Download figure to PowerPoint

A necessary consequence of the genetic basis to plant–fungal community interactions is that selection on one set of partners in symbiosis influences the other. In a recent drought, moth-resistant P. edulis suffered threefold higher mortality than moth-susceptible trees (Fig. 1b; Sthultz et al., 2009b). Given the tight connection between tree phenotypes and the fungal community, this suggests that selection on P. edulis will influence fungal communities associated with the two phenotypic classes of trees – or that selection is operating on the unique combinations of tree genotype and fungal community in concert. Both possibilities are tantalizing. Ongoing work will aim to uncover whether these patterns are simply the product of directional selection, or are true fingerprints of co-evolutionary phenomena.

At a larger scale, such strong selection may lead to local adaptation and speciation, as evidenced by Nancy Johnson and colleagues’ demonstration of local adaptation between the grass Andropogon gerardii and its arbuscular mycorrhizal fungi (AMF) (Johnson et al., 2010). In this case, the symbiosis is more efficient from the perspective of both plants and fungi when symbionts share an evolutionary history than when they do not. Complementing such findings was Suzanne Joneson’s study of gene regulation during the early stages of the establishment of lichen symbioses, and Tami MacDonald’s work on the acquisition of genes that influence the ability of mycobionts to lichenize. These studies brought a ‘real time’ ecological and genetic perspective to the meetings, linking genotypes to signatures of co-evolution at the species level and above.

Species-level co-evolution in plant–fungal interactions

  1. Top of page
  2. Micro-evolutionary perspectives on plant–fungal co-evolution
  3. Species-level co-evolution in plant–fungal interactions
  4. Co-evolution in the broad sense
  5. Synthesis
  6. References

Many foundational studies in co-evolution focus on highly specialized associations that display strong specificity (e.g. Darwin, 1862; Futuyma & Slatkin, 1983; Jordano, 1987). However, recognizing variation in specificity is fundamental to understanding how diversity is organized spatially, and maintained over ecological and evolutionary time (Thompson, 2005).

Mycologists have long been aware that fungal symbionts of plants range from facultative to obligate, and from cosmopolitan to highly specialized (e.g. Molina et al., 1992). Now, investigators are beginning to focus on the ecological and evolutionary consequences of such variation. Not only are some plant-associated fungal communities variable in their specificity across space – such as endophytes, which exhibit higher specificity at higher latitudes than in the tropics (Arnold & Lutzoni, 2007) – but they also differ in the outcomes of their functions over time and space. Particular species may be mutualists under some environmental conditions, but saprotrophs or parasites under others (e.g. Johnson et al., 1997), and over evolutionary time, changes among ecological states can be unexpectedly frequent (Arnold et al., 2009). The complex interplay that must occur when hosts and/or symbionts shift along the mutualism-to-parasitism continuum is an exciting but under-explored area of research.

To date, our best understanding of variation in such interactions comes from the illuminating case of mycoheterotrophy. Mycoheterotrophic plants, which receive some or all of their organic nutrition from fungal symbionts, have long been key pieces of the co-evolutionary puzzle. These ‘saprophytic plants’ gained recognition even in early botany textbooks (e.g. Skene, 1924):

‘It is not certain that any [saprophytic plants] really draw organic food directly from the soil. The fungus may in all cases act as an intermediary. …These plants would properly be regarded as the end of a series, exhibiting the extreme results of the mycorrhizal habit. … There are likely many cases of partial saprophytism which have not been recognized.’

Early in the molecular revolution, mycoheterotrophic associations were recognized as highly specific, propelling investigations of specificity in other plant–fungal systems. Presentations at Snowbird extended this momentum, documenting specificity among Basidiomycota and liverworts (Bidartondo & Duckett, 2009), AMF and nonphotosynthetic plants (Merckx et al., 2009), ectomycorrhizal fungi and heathland seedlings (Collier & Bidartondo, 2009), ectomycorrhizal fungi and nonphotosynthetic plants (Marc-André Selosse, presentation; Hynson & Bruns, 2009; see also Selosse, 2010), foliar endophytes and their hosts (A. Elizabeth Arnold, Mariana del Olmo, Romina Gazis, Jose Herrera, Demetra Kandalepas, Kali Lader, Michael Weiß, Jana U’Ren, presentations), Dikarya and orchids (Martin Bidartondo, presentation), and even fungi and their own endosymbionts (Michele Hoffman, presentation). Many of these talks provided examples in which fungal phylogenies did not reflect co-cladogenesis with hosts at the species level, yet still provided strong signals of co-evolution.

Notably, these presentations not only provided a perspective on how specificity shapes particular symbioses, but also addressed how specificity can translate to function. In particular, speakers showed that narrow plant receptivity implies low ecological redundancy in fungi, whereby a particular fungus can determine the establishment and survival of a plant, and thus – over the long term – the persistence and subsequent diversification of the lineage that plant represents. Although recognized for plant pathogens, as showcased in a new light at Snowbird by Michelle Hersh, this novel realization for nonpathogenic associations turns the tables on plant conservation by spotlighting conservation of species or groups of fungi, and highlights the sometimes overlooked reciprocity with which plants respond to their fungal inhabitants over evolutionary time. It also echoes our growing understanding of the crucial role of fungi in the colonization of land by plants (Heckman et al., 2001; François Lutzoni, presentation), a critical step in the diversification of the green tree of life.

Co-evolution in the broad sense

  1. Top of page
  2. Micro-evolutionary perspectives on plant–fungal co-evolution
  3. Species-level co-evolution in plant–fungal interactions
  4. Co-evolution in the broad sense
  5. Synthesis
  6. References

No plant in a natural setting exists in the absence of fungi. Spores and hyphae on exterior surfaces, endophytes within leaves and stems, and root-associated fungi ranging from mycorrhizal fungi to dark-septate endophytes comprise a living context for plant ecology in every terrestrial ecosystem (Blackwell, 2000; Rodriguez et al., 2009). Accordingly, most plants live in close association with members of multiple phyla of fungi, each distinctive in its evolutionary history and genomic architecture. Researchers studying broad-scale patterns in co-diversification must often peer through thousands of twigs of the fungal tree of life in the hope of finding a signal of the major branches that lie beneath.

Seeming at times a Quixotic task – and at other times a Herculean one – recent efforts are being informed by the rapid accumulation of fungal genome sequences (e.g. Martin et al., 2008; Eva Stukenbrock, presentation), advances in understanding evolutionary changes among major lineages (e.g. James et al., 2006), integration of phylogenetics with rules of community assembly (Jeri Parrent, presentation) and linking of survey data – including culture-based and environmental sampling – with large-scale phylogenetic inferences (e.g. Arnold et al., 2009). Talks at Snowbird described exciting new perspectives on the timing of major diversification events in fungal–plant associations (F. Lutzoni), the dominance of endophyte communities by different major clades of Ascomycota in plants representing different major lineages (U’Ren) and the insights at multiple levels emerging from studies of the ‘microbiomes’ of lichens and plants (Lutzoni).

Synthesis

  1. Top of page
  2. Micro-evolutionary perspectives on plant–fungal co-evolution
  3. Species-level co-evolution in plant–fungal interactions
  4. Co-evolution in the broad sense
  5. Synthesis
  6. References

Botanists and mycologists are entering a new decade with a shared perspective that plants co-evolve with the fungi on and in their tissues – even when strict-sense co-cladogenesis is not evident. Convincing data indicate that many plants depend on fungi, particularly in stressful environments, and that fungal symbionts range from mutualism to parasitism and from specificity to generalism, encompassing the ability to change over host ranges, short or long timescales, or as a function of environmental conditions (Rodriguez et al., 2009). Studies described at Snowbird provided evidence of plant–fungal co-evolution using approaches as diverse as micro-evolutionary experiments in the laboratory and field to measuring the congruence of fungal and plant phylogenies from the narrowest to the broadest levels.

Symposium participants agreed that future work will benefit from an interdisciplinary approach fusing traditional evolutionary studies with cutting-edge methods. Identifying traits that vary among plant or fungal genotypes, and how they lead to differences in community structure and function, is critical – and can be achieved through methods ranging from the identification of quantitative traits to detailed studies of gene expression. Speakers also agreed that the traditional approach of studying pairwise interactions is limiting: new research should consider not only diverse fungal symbionts of a given guild, but the simultaneous interactions of symbionts from roots and shoots, and their multipartite associations. This challenging prospect becomes ever more feasible through metagenomics and may be enhanced by ecological network analyses and structural equation modeling (Agrawal et al., 2007; Vacher et al., 2008; Mary Jane Epps, presentation). In part because most fungal communities remain largely understudied, investigators suggested that processes such as local adaptation need more attention: such processes appear frequently in the evolutionary history of plants and fungi, but rarely have studies encompassed sufficient scales – and precise enough tools – to diagnose them. Linking surveys of fungal communities to function (Parrent et al., this issue of New Phytologist, pp. 882–886) and geographic distributions (Peay et al., this issue of New Phytologist, pp. 878–882) represent key steps forward.

In this context, biologists from many backgrounds are connected by studying plant–fungal interactions. Together they are poised to provide new perspectives on co-evolution, and to move towards a science of ‘applied co-evolutionary biology’ (Thompson, 2005) to predict outcomes that may ensue as humans spread invasive plant and fungal species, eliminate native biodiversity and otherwise reshape the myriad species interactions that underpin terrestrial plant communities and the ecosystems they support. Understanding how plants and fungi are interwoven at multiple levels of biological organization promises to be key to both foundational and predictive science in the years to come.

References

  1. Top of page
  2. Micro-evolutionary perspectives on plant–fungal co-evolution
  3. Species-level co-evolution in plant–fungal interactions
  4. Co-evolution in the broad sense
  5. Synthesis
  6. References
  • Agrawal AA, Ackerly DD, Adler F, Arnold AE, Cáceres C, Doak DF, Post E, Hudson PJ, Maron J, Mooney KA et al. 2007. Filling key gaps in population and community ecology. Frontiers in Ecology and the Environment 5: 145152.
  • Arnold AE, Lutzoni F. 2007. Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88: 541549.
  • Arnold AE, Miadlikowska J, Higgins KL, Sarvate SD, Gugger P, Way A, Hofstetter V, Kauff F, Lutzoni F. 2009. A phylogenetic estimation of trophic transition networks for ascomycetors fungi: are lichens cradles of symbiotic fungal diversification? Systematic Biology 58: 283297.
  • Bidartondo MI, Duckett JG. 2009. Conservative ecological and evolutionary patterns in liverwort–fungal symbioses. Proceedings of the Royal Society B, doi: 10.1098/rspb.2009.1458
  • Blackwell M. 2000. Terrestrial life – fungal from the start? Science 289: 18841885.
  • Collier FA, Bidartondo MI. 2009. Waiting for fungi: the ectomycorrhizal invasion of lowland heathlands. Journal of Ecology 97: 950963.
  • Darwin C. 1859. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. London, UK: John Murray.
  • Darwin C. 1862. On the various contrivances by which British and foreign orchids are fertilized by insects. London, UK: John Murray.
  • Dawkins R. 1976. The selfish gene. Oxford, UK: Oxford University Press.
  • Elamo P, Helander MJ, Saloniemi I, Neuvonen S. 1999. Birch family and environmental conditions affect endophytic fungi in leaves. Oecologia 118: 151156.
  • Futuyma DJ, Slatkin M 1983. Coevolution. Sunderland, MA, USA: Sinauer Associates.
  • Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB. 2001. Molecular evidence for the early colonization of land by fungi and plants. Science 293: 11291133.
  • Hynson NA, Bruns TD. 2009. Evidence of a myco-heterotroph in the plant family Ericaceae that lacks mycorrhizal specificity. Proceedings of the Royal Society London Series B, doi:10.1098/rspb.2009.1190.
  • James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J et al. 2006. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443: 818822.
  • Ji B. 2007. Taxonomic and functional diversity of AM fungi in serpentine and prairie grasslands. PhD thesis, University of Pennsylvania, Philadelphia, PA, USA.
  • Johnson NC, Graham JH, Smith FA. 1997. Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytologist 135: 575585.
  • Johnson NC, Wilson GWT, Bowker MA, Wilson J, Miller RM. 2010. Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proceedings of the National Academy of Sciences, USA, doi: 10.1073/phas.0906710107.
  • Jordano P. 1987. Patterns of mutualistic interactions in pollination and seed dispersal: connectance, dependence asymmetries, and coevolution. The American Naturalist 129: 657677.
  • Keller L. 1999. Levels of selection in evolution. Princeton, NJ, USA: Princeton University Press.
  • Koch AM, Croll D, Sanders IR. 2006. Genetic variability in a population of arbuscular mycorrhizal fungi causes variation in plant growth. Ecology Letters 9: 103110.
  • Lamit LJ. 2008. Genetic variation in a foundation species influences associated primary producers: Populus and lichens. MS Thesis, Northern Arizona University, USA.
  • Martin F, Aerts A, Ahren D, Brun A, Danchin EGJ, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V et al. 2008. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452: 8892.
  • Merckx V, Bidartondo MI, Hynson NA. 2009. Myco-heterotrophy: when fungi host plants. Annals of Botany, doi:10.1093/aob/mcp235.
  • Molina R, Massicotte H, Trappe JM. 1992. Specificity phenomena in mycorrhizal symbiosis: community-ecological consequences and practical implications. In: AllenMF, ed. Mycorrhizal functioning. London, UK: Chapman & Hall, 357423.
  • Mopper S, Mitton J, Whitham TG, Cobb NS, Christensen KM. 1991. Genetic differentiation and heterozygosity in pinyon pine associated with herbivory and environmental stress. Evolution 45: 989999.
  • Okasha S. 2008. Evolution and the levels of selection. Oxford, UK: Oxford University Press.
  • Parrent JL, Peay K, Arnold AE, Comas LH, Avis P, Tuininga A. 2010. Moving from pattern to process in fungal symbioses: linking functional traits, community ecology, and phylogenetics. New Phytologist 185: 882886.
  • Peay KG, Bidartondo MI, Arnold AE. 2010. Not every fungus is everywhere: scaling to the biogeography of fungal–plant interactions across roots, shoots and ecosystems. New Phytologist 185: 878882.
  • Rodriguez R, White JF Jr, Arnold AE, Redman RS. 2009. Fungal endophytes: diversity and functional roles. New Phytologist 182: 314330.
  • Selosse M-A. 2010. Introduction to a Virtual Special Issue on mycoheterotrophy: New Phytologist sheds light on non-green plants. New Phytologist 185: 591593.
  • Skene M. 1924. The biology of flowering plants. London, UK: Sidgwick & Jackson.
  • Sober E. 1984. The nature of selection: evolutionary theory in philosophical focus. Chicago, IL, USA: University of Chicago Press.
  • Sthultz CM. 2008. Influence of genes, herbivores and drought on the mortality and ectomycorrhizal fungal community of a foundation tree. PhD thesis, Northern Arizona University, Northern Arizona, AZ, USA.
  • Sthultz CM, Gehring CA, Whitham TG. 2009a. Deadly combination of genes and drought: increased mortality of herbivore-resistant trees in a foundation species. Global Change Biology 15: 19491961.
  • Sthultz CM, Whitham TG, Kennedy K, Deckert R, Gehring CA. 2009b. Genetically-based susceptibility to herbivory influences the ectomycorrhizal fungal communities of a foundation tree species. New Phytologist 184: 657667.
  • Thompson JN. 2005. The geographic mosaic of coevolution. Chicago, IL, USA: University of Chicago Press.
  • Vacher C, Piou D, Desprez-Loustau M-L. 2008. Architecture of an antagonistic tree/fungus network: the asymmetric influence of past evolutionary history. PLoS ONE 3: e1740.
  • Whitham TG, Mopper S. 1985. Chronic herbivory: impacts on tree architecture and sex expression of pinyon pine. Science 227: 10891091.
  • Williams GC. 1966. Adaptation and natural selection. Princeton, NJ, USA: Princeton University Press.