The recent joint meeting of the Botanical and Mycological Societies of America (July 25–29, 2009; Snowbird, Utah, USA) was an apt venue for a symposium examining the ecology and evolution of the symbiotic interactions that occur between plants and fungi. These highly diverse and cryptic symbioses, studied for many decades, are ancient and ubiquitous. Recently, the field has undergone rapid expansion, drawing from molecular systematics and ecological genomics to develop new DNA-based and RNA-based tools and associated bioinformatics. At a session on the phylogenetic and functional patterns of host plants and their associated fungi, speakers described research programs that combine cutting-edge and traditional methods to amass data about the nature and distribution of these interactions across scales, from local to global, in a co-evolutionary context. Several threads united the research programs presented, collectively pointing to an alignment of questions investigated at different scales to reveal a comprehensive picture of processes that shape symbiotic plant–fungal communities. This emergent view shows that the fields of botany and mycology are maturing in an understanding of plant–fungal interactions, founded on a rich collection of observations and burgeoning theories, now coupled with fresh perspectives garnered by using new tools. This Commentary captures these developments and provides an introductory overview to a cluster of Letters published in this issue of New Phytologist. Each letter focuses on one of three important areas within plant–fungal symbiosis that emerged from the meeting and will help to set the way forward: plant–fungal symbiotic co-evolution (Arnold et al., pp. 874–878); biogeography of these symbiotic partners (Peay et al., pp. 878–882); and phylogenetic community ecology of plants and their symbiotic partners (Parrent et al., pp. 882–886). Full details relating to presentation titles, author affiliations and related information about the 2009 Annual Botany & Mycology Conference can be found online at http://2009.botanyconference.org.
‘With symbiotic interactions between plants and fungi spanning a complex continuum from mutualism to parasitism …, an ongoing conversation between mycologists and botanists is critical.’
Innovative research that has steadily accrued in areas spanning micro-evolutionary processes, patterns of specificity, biogeography, and community phylogenetics of plants and fungi was highlighted at this year’s meeting showcasing this emergent multidimensional view of plant–fungal symbioses. As it becomes easier to characterize inter-specific and intra-specific genetic variation of both plants and fungi, we are poised to test theories about community assembly and co-evolution on landscape and global scales that previously were prohibitive. Speakers highlighted advancements in the understanding of interactions at the genotype level that affect the next generation, providing new evidence for local adaptation (presented by Louis J. Lamit), and how narrow receptivity of plant species leads to low ecological redundancy of mycorrhizal fungi, so that keystone fungal taxa can determine plant establishment, survival and diversification (presented by Martin Bidartondo). Such processes at local scales are critical for understanding the mechanisms of co-evolution with direct implications for macro co-evolution. Additionally, it is critical to identify ecologically relevant models of symbioses for the broad context of research from genomics to climate change. Symposium speakers Elizabeth Arnold and Kabir Peay, as well as the MSA Presidential Address by Roy Halling highlighted progress in understanding fungal biogeography and dispersal, previewing the value of such data for fueling ecologically relevant hypothesis-driven research about current and future distributions of fungi and their plant hosts. Additionally, Peay, among others, emphasized the exquisite sensitivity of symbiotic fungi to the spatio-temporal scale and ecological context of sampling, illustrated by his finding of a large difference in biodiversity patterns of plant hosts and fungal symbionts in different ecosystems. Extrapolations from Peay’s data suggest that tropical ecosystems rich in plant biodiversity can have 10–40 times the number of plant hosts to fungal symbionts of temperate ecosystems, which points to a potential disconnect between biodiversity patterns of host species and symbionts. The greater diversity of symbionts in temperate systems relative to host plants indicates that there may be a different pattern for symbiont diversity on a global basis, begging for follow-up studies and meta-analyses, and indicating the importance of examining biodiversity in areas previously thought to be low on biodiversity based solely on plant studies. Furthermore, Parrent presented data indicating that shifts in richness of constructed field communities of fungal symbionts were connected to their phylogenetic diversity. This finding suggests that competition among mycorrhizal fungi in the field, presumed to be stronger among closely related fungi, trumps plant–fungal interactions. Finally, Avis’s presentation of community shifts of fungal symbionts in woodlands experiencing elevated rates of nitrogen deposition illustrate the new quest to identify the tissue-level traits and their phylogenetic dispersal that may mediate community-level shifts occurring belowground, and recast traditional thinking about drivers of community assembly in changing environments.
With symbiotic interactions between plants and fungi spanning a complex continuum from mutualism to parasitism that is influenced by both plant and fungal partners (Jones & Smith, 2004; Karst et al., 2008; Rodriguez & Redman, 2008), an ongoing conversation between mycologists and botanists is critical. Scientists in both disciplines are poised to profit from new theory in co-evolution that is rapidly being generated and tested by investigators examining other interacting organisms, both symbiotic and free-living, including plant-pollinator systems and even symbioses in the sea (Bascompte et al., 2006; Ollerton et al., 2007), and take into consideration that species (and genotypes) interact within a geographic mosaic (Thompson, 2005). Coupling micro-perspectives and macro-perspectives on symbiotic interactions between plants and fungi with the latest genomic tools is likely to take us in exciting new directions (see Arnold et al., 2010; Peay et al., 2010– both in this issue). Such tools provide new ways to characterize diversity from local to global scales, and place that diversity into an evolutionary framework spanning from events that have occurred quite recently to more ancient diversification events (Arnold et al., 2009). Moreover, by placing phylogenetically informed interactions in a geographic framework, these tools can help to address broad questions about the ecological processes shaping biogeographical patterns.
As we gain increasingly detailed information about fungal communities, a specific goal mentioned by several speakers is to use phylogenetic analyses to address the conservatism of functional traits and their ecological implications (Cavender-Bares et al., 2009). This potentially powerful approach can proceed by relying on the use of phylogenetic dispersal of a community as a proxy for functional diversity, as highlighted in symposium presentations by Arnold and by Parrent and in the accompanying Letter by Parrent et al. This approach also allows broad questions about ecosystem function to be complemented with narrower, more detailed, studies that address function in taxon-specific organismal terms. As discussed by many speakers, and during a discussion following the symposium, additional progress will require remedying the current scarcity of information about plant and fungal functional traits related to these symbioses. Given that fungi, belowground plant organs and mycorrhizal symbioses are diverse and cryptic, this is a vast challenge, but headway has been made with further progress forthcoming. In some instances, it may be possible to mine functional trait data from the literature. For example, it may be possible to infer fungal dispersal syndromes from measures of spore size, spore longevity, or fruiting body height (presented by Kabir Peay). While it has proven relatively straightforward to gather data for aboveground functional traits of diverse plant species (e.g. Grime, 2001; Reich et al., 2003), a few studies have shown that it is possible to gain comparable functional trait data from belowground tissues such as fine roots (e.g. Guo et al., 2008; Comas & Eissenstat, 2009) and fungal hyphae (presented by Jeri Parrent). Moving forward, it will be useful to identify key functional differences among symbionts, such as hyphal exploration types (e.g. Agerer, 2001) and extend them to arbuscular mycorrhizal fungi (AMF) (presented by Jeri Parrent). Finally, there is an ongoing hunt for relevant and reliable biochemical and molecular traits that can be easily scored using high-throughput methods (Bidartondo & Gardes, 2005).
Overall, as detailed in the accompanying Letters, speakers presenting research in Utah synthesized our current understanding of plant–fungal symbioses and indicated future directions that would be fruitful in advancing this field. These presentations illustrated how research on plant–fungal interactions can profit from new theoretical frameworks such as co-evolutionary theory (Thompson, 2005), conservation-oriented biogeography (Cadotte et al., 2006; Lockwood et al., 2007) and the merger of phylogenetic community ecology with functional trait approaches (Cavender-Bares et al., 2009). In the face of global change – waves of species extinctions and invasions, anthropogenic changes to Earth’s soils and atmosphere, damage to ecosystem services – it is critical to advance a comprehensive understanding of the symbiotic interactions between plants and fungi occurring at multiple scales.