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Mycorrhizas across scales: a journey between genomics, global patterns of biodiversity and biogeochemistry

2016; Wiley; Volume: 209; Issue: 3 Linguagem: Inglês

10.1111/nph.13819

1469-8137

Pierre‐Luc Chagnon, François Rineau, Christina Kaiser,

Fungal Biology and Applications

Mycorrhizal fungi are found in almost all ecosystems of the planet. They interact with a majority of plant species, and it seems that every single aspect of the life history of a plant individual is affected by the presence of mycorrhizal fungal symbionts in its roots (van der Heijden et al., 2015). Mycorrhizal fungi are also known to affect plant population-level and community-level dynamics. Yet, classic 800-page plant ecology textbooks typically devote only one to two pages to mycorrhizal symbioses. Is it time to put mycorrhizal ecologists on the editorial boards of these textbooks? Meetings like the International Conference on Mycorrhizas (ICOM) tend to suggest that this might not be a bad idea. On August 3–7, 2015, mycorrhizal researchers from around the world shared their thoughts and empirical results on these globally widespread symbioses at a comfortable elevation of 2135 m in Flagstaff, Arizona, surrounded by beautiful landscapes, like widespread Ponderosa Pine forests, the San Francisco Peaks area, and the impressive Grand Canyon. New Phytologist was present as a sponsor, continuing its ongoing support of mycorrhizal research (Selosse & Martin, 2013; Dickie et al., 2015). Through talks and posters, mycorrhizal researchers literally took us on a journey across all scales of observation of this symbiosis: from the intracellular environment to global patterns of mycorrhizal fungal diversity and biogeochemical cycles (Fig. 1). Since the last ICOM (Martinez-Garcia et al., 2013), substantial advances have been made regarding our understanding of fungal evolution. This is largely attributable to efforts devoted to the sequencing of full fungal genomes. Comparative genomics helped, in particular, to identify groups of genes associated with the gain of physiological or ecological functions. For example, Jason Stajich (University of California, Riverside, CA, USA) described how the 1000 Fungal Genomes Project (http://1000.fungalgenomes.org/home/) helped to show that the transition from 'early' fungal species with a flagellated zoospore life stage to filamentous and yeast growth forms was accompanied by losses and gains of lineage-specific genes. Comparative genomics has also been applied to understand the evolution of the mycorrhizal lifestyle of fungi, that is, through the Mycorrhizal Genomics Initiative (MGI) project. The comparison of full genomes of ecologically diverse fungal taxa showed that the ectomycorrhizal (ECM), orchid- and ericoid-mycorrhizal symbioses evolved several times from white-rot, brown-rot and litter-degrader lifestyles (Kohler et al., 2015). Claude Murat (INRA, Nancy, France) explained how this was, on the one hand, linked with repeated loss of lineage-specific genes and genes coding for plant-cell wall degrading enzymes in ECM fungi (except for the canonical GH6 cellulase family in Ascomycetes). On the other hand, several gene sets were also associated with the gain of the mycorrhizal lifestyle; these were not orthologs but coding for similar functions between species. Kohler et al. (2015) (INRA, Nancy, France) showed that small secreted proteins (SSPs) were particularly represented among these genes. One of these SSPs was found to tune down the plant jasmonate induced defense pathway, reinforcing the hypothesis that some SSPs are fungal effector molecules involved in the manipulation of host immunity (Plett et al., 2014). Advances have been made as well on the understanding of the genome structure of arbuscular mycorrhizal (AM) fungi, through the Rhizophagus irregularis strain DAOM197198 sequencing projects. Because of its coenocytic nature, the genome of this fungus has been difficult to assemble, but a reliable release is now on its way, as presented by Christophe Roux (Toulouse University, Toulouse, France). Contrary to what was previously thought, the fungus was homokaryotic (that is, with same genetic content in all nuclei). The genome was also haploid, and very large (154 MB), partly because transposable elements accounted for one-third of the total genome size (Tisserant et al., 2013). He also showed that, as for ECM fungi, it seems that AM fungi rely on a specific 'mycorrhizal gene toolkit' to establish symbiosis with the plant. Indeed, the genes regulated in the symbiosis of this sequenced strain were very similar to the ones of Gigaspora rosea, as found by a transcriptome profiling approach. Fungal phylogenetics has been progressing very fast in the last two years, owing to comprehensive studies combining rDNA, proteomic, and taxonomic approaches. However, as pointed out by Dirk Redecker (Burgundy University, Dijon, France), this combination is often challenging, because proteomic-based and hybrid rDNA-proteomic-based phylogenies sometimes give very different outcomes, emphasizing the need for large multilocus databases. This issue and others are being addressed, and a new, comprehensive fungal tree of life is on its way to be generated, as presented by Romina Gazis (Clark University, Worcester, MA, USA). While the influence of mycorrhizal fungi on plant phosphorus (P) and nitrogen (N) nutrition has been recognized for a long time (e.g. Mosse, 1973), many studies presented at the Eighth ICOM (ICOM8) provide evidence that mycorrhizal fungi must be recognized as far more than nutritional symbionts, given their important role, for example, in the regulation of plant hormone signaling and defenses (e.g. Plett et al., 2014; Pozo et al., 2015), or in the transfer of plant allelopathic compounds through common mycelial networks (Johnson & Gilbert, 2015). This should bring us to further re-evaluate the stabilization of mycorrhizal symbioses at evolutionary timescales. Most research focusing on this topic has up to now focused on the reciprocity of the nutritional rewards provided by plants and fungi to each other (e.g. Bever et al., 2009; Kiers et al., 2011; Werner et al., 2014). Yet, some researchers at ICOM8 presented results that cannot easily be explained by this balanced biological market framework (e.g. Walder et al., 2012; Niles Hasselquist, Swedish University of Agricultural Science, Umeå, Sweden; Josh Smith, UBC Okanagan, Kelowna, Canada). This may highlight the need to take a broader perspective on the evolutionary stability of mycorrhizal symbioses. Smith (1972) coined the term evolutionary stable strategy (ESS) to designate an individual's behavior that should persist through natural selection as long as it maximizes lifetime fitness. This became a key aspect of animal foraging theories, where it was predicted that animals should evolve ESSs by behaving/foraging in a way that maximizes energetic intakes and minimizes costs associated to such foraging activities. It is now well recognized in this literature that factors other than energetic values of prey and traveling time to catch them (i.e. energy expenditure) should be considered to identify ESSs: for example, the risk that an active forager takes by exposing itself to its own predators, or the cost that a predator accepts by rejecting a prey of suboptimal quality (e.g. Pyke et al., 1977). Likewise, from the discussion earlier on mycorrhizal mutualists, while it seems convenient to see those symbionts as simply trading N or P against plant-derived carbon (C), if we are to ask why remaining mycorrhizal is an ESS for a plant, we must take into account all potential costs and benefits that significantly affect lifetime fitness. The broad impacts that mycorrhizal fungi seem to have on plant multitrophic interactions or ecosystem processes may feed back on plant fitness. Those indirect effects are, however, difficult to quantify. Regarding this issue, the long standing debate about whether measuring plant performance with vegetative biomass only is an adequate proxy for fitness remains, as many examples suggest that it is not (e.g. Philip et al., 2001). Ever since the development of next-generation sequencing technologies, the characterization of mycorrhizal fungal communities has kept going on at an unprecedented pace. This now allows large-scale, synthetic project gathering information about biogeographical patterns of mycorrhizal fungal diversity (e.g. Bahram et al., 2015). But this increased capacity to characterize mycorrhizal fungal communities also comes with a need for trait-based studies to understand what shifts in fungal community composition tell us about (1) community assembly rules and (2) ecosystem physiology and biogeochemistry (e.g. Chagnon et al., 2013; Aguilar-Trigueros et al., 2014; Rillig et al., 2015). In this regard, researchers presented their empirical efforts to characterize traits of different mycorrhizal fungal taxa (e.g. in orchid mycorrhizal fungi, Marc-André Selosse, Muséum National d'Histoire Naturelle, Paris, France), and to provide databases to promote the use of such functional information (FUNGuild, by Nguyen et al., 2015). Evidence was mounting at the conference that mycorrhizal fungal traits have a significant impact on terrestrial C, N and P cycling. Several talks showed that both amount and decomposability of C deposited into the soil by mycorrhizal fungi strongly depends on mycorrhizal guilds/taxa. For example, ECM-dominated sites exhibited three-times more fungal standing biomass and 1.5-times more hyphal production than AM-dominated sites in temperate hardwood forests (Tanya E. Cheeke, Indiana University, Bloomington, IN, USA). Fernandez et al. (2015) (University of Minnesota, St Paul, MN, USA) showed that necromass of melanin-rich Cenococcum geophilum persisted in the soil many times longer than necromass of other ECM fungal species. At the ecosystem level, Clemmensen et al. (2015) (SLU, Uppsala, Sweden) demonstrated that ericoid mycorrhizal systems facilitated a much larger belowground C sequestration (despite lower litter inputs) than ECM systems because of lower decomposability and less efficient nutrient turnover of ericoid compared with ECM fungal species. The latter shows that not only decomposability, but also decomposing ability of mycorrhizal fungi influence the net C exchange between terrestrial systems and the atmosphere (Fernandez & Kennedy, 2015). In particular ericoid and ECM fungal species are known to be able to decompose soil organic matter (SOM); their specific roles, however, have remained controversial. Francois Rineau (Hasselt University, Hasselt, Belgium) showed that ECM species degrade organic matter using a brown-rot-like mechanism, but lacked – contrary to their saprotrophic counterparts – the genes to convert the degraded carbohydrates into energy (Shah et al., 2015). ECM degradation of SOM was thus dependent on the presence of a simple sugar source (Rineau et al., 2013), indicating that ECM fungi may degrade SOM for nutrient foraging, fueled by energy from their host plants. This may assign ECM fungi a distinguished role within the concerted, multispecies effort of terrestrial organic matter decomposition (Lindahl & Tunlid, 2015). Apart from their own decomposing activities, mycorrhizal fungi may also 'prime' free-living microbial decomposers by releasing energy-rich labile C compounds into the soil (similar to root exudation in the 'rhizosphere priming effect'). While the significant effect of rhizosphere priming on terrestrial C cycling is widely acknowledged (Kuzyakov, 2010), much less is known about a possible 'hyphosphere priming effect' (Jansa et al., 2013). Hyphosphere priming may be a valuable mechanism especially for AM, which lack decomposing capacities themselves, but depend on the uptake of mineral nutrients. Several presentations (e.g. by Mary Firestone, University of California, Berkeley, CA, USA) at ICOM8 reported that AM fungi accelerated SOM decomposition. Gu Feng (China Agricultural University, Beijing, P. R. China) and Kaiser et al. (2015) (University of Vienna, Vienna, Austria) showed the rapid transfer of recent photosynthates into AM hyphae-associated soil bacteria. Mycorrhizal fungi may also contribute to soil C sequestration by depositing plant-derived C into physically protected microsites in the soil, as demonstrated by Mary Firestone and Edith Hammer (Lund University, Lund, Sweden). The potential significance of microscale interactions between mycorrhiza and soil bacteria for SOM decomposition urges the need for more interactions between soil microbial ecologists and mycorrhizal researchers. Despite the striking evidence for the role of mycorrhizal fungi for cycling of C, N and P in terrestrial ecosystems, they are still not integrated into most large ecosystem scale models (as pointed out by Kathleen Treseder, University of California, Irvine, CA, USA). New findings presented at ICOM8 strongly suggest that doing so may substantially improve our ability to predict the response of terrestrial biogeochemical cycles to climate change. The extensive use of new biotechnological tools to study mycorrhizal symbioses was a dominant trend in many of the findings at the ICOM8: using SIMS and NanoSIMS to visualize the flow of recent photosynthates across the plant–fungus interface (Nuccio et al., 2013; Kuga et al., 2014; Kaiser et al., 2015); transcriptome profiling to detect the genes potentially involved in the symbiosis, in the nutrient uptake, or in the interaction with soil organisms; comparative genomics to decipher the evolution of the symbiosis; characterize with unprecedented depth whole mycorrhizal fungal communities using high-throughput sequencing technologies; and new databases (e.g. FUNGuild, Mycodb) to integrate all these collected data. However, in spite of all the promises that those new tools offer to mycorrhizal researchers, we need to keep in mind that the best way to optimize their potential is to ground empirical questions in clear theoretical frameworks. This is also true for theoretical developments in the mycorrhizal field, such as the use of network-based statistical approaches to look at mycorrhizal communities (e.g. Chagnon et al., 2014). Nevertheless, it seems that with all those novel tools available, mycorrhizal researchers will continue to rapidly increase our understanding of the significance of mycorrhizal symbioses for terrestrial plants. After ICOM8, it seems obvious that plant ecophysiology, population and community level ecology, as well as terrestrial biogeochemical cycles can no longer be considered outside the context of the mycorrhizal symbiosis – in tomorrow's research as well as in textbooks. The authors would like to thank all the conference participants, who were live twittering during the conference, your tweets (#ICOM8) were a valuable additional resource for writing the report.