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New Phytologist – an evolving host for mycorrhizal research

2007; Wiley; Volume: 174; Issue: 2 Linguagem: Inglês

10.1111/j.1469-8137.2007.02058.x

1469-8137

Francis Martin, Holly Slater,

Plant Parasitism and Resistance

'Sam Gamgee planted saplings in all the places where specially beautiful or beloved trees had been destroyed, and he put a grain of the precious dust from Galadriel in the soil at the root of each. The little silver nut he planted in the Party Field where the tree had once been; and he wondered what would come of it. All through the winter he remained as patient as he could, and tried to restrain himself from going round constantly to see if anything was happening. Spring surpassed his wildest hopes. His trees began to sprout and grow, as if time was in a hurry and wished to make one year do for twenty. In the Party Field a beautiful young sapling leaped up: it had silver bark and long leaves and burst into golden flowers in April. It was indeed a mallorn, and it was the wonder of the neighbourhood. In after years, as it grew in grace and beauty, it was known far and wide and people would come long journeys to see it: the only mallorn west of the Mountains and east of the Sea, and one of the finest in the world.' (J. R. R. Tolkien, The Return of the King, Book Six, Chapter IX, The Grey Havens) Next time you walk in the misty woods captivated by the sheer beauty and majesty of trees, thank the cast of a million species of soil organisms living in the endless foam of tiny niches of weathered rock, mineral particles and decomposing soil organic matter. As a tree forms, it interacts with guilds of beneficial microorganisms promoting its growth and development. The box of dust given by the Elven queen of Lothlorien, Galadriel, contained the needed mycorrhizal inoculum for promoting the growth of mallorn trees, but infortunately this ancestral knowledge was lost for millenia. It is now very strange to realize that before Professor Jack Harley began his research on the mycorrhiza of beech (Fagus sylvatica) in the middle of last century, botanists and foresters regarded mycorrhizas as being obscure and of little importance. Harley's series of outstanding, now classical, experiments on ectomycorrhizas elucidated the mechanisms by which tree mycorrhizas take up essential nutrients such as phosphate from the soil (Harley, 1953). He clarified the nature of what is undoubtedly the commonest and most important symbiosis in the world. Simply stated, nearly all families of plants form root symbiotic organs, termed mycorrhizas, with soil fungi belonging to all the main phyla; namely Glomeromycota, Ascomycotina and Basidiomycotina. Within days of their emergence in the upper soil profiles, up to 95% of short roots of trees are colonized by mycorrhizal fungi. The importance of this symbiosis in controlling plant nutrient status and growth is now well established (Read & Perez-Moreno, 2003). New Phytologist hosted Harley's seminal papers on ectomycorrhizal physiology, and from this a strong association between the journal and the mycorrhizal community has developed. Indeed, from ISI citation analysis, it is clear that mycorrhizal research still contributes greatly to the success of the journal; the most widely cited and influential article in recent years being the Tansley review by Read & Perez-Moreno (2003) discussing the key ecological role of the different types of mycorrhizal symbioses in plant nutrition. Today, with the advent of new tools and techniques, the possibility of integration across a wide range of disciplines from genomics to molecular ecology and field ecology is becoming a reality that is much encouraged by New Phytologist. In this Editorial we will highlight some of the recent innovative mycorrhizal research published in the journal and look to future challenges that lie ahead. This theme is continued throughout the Forum of this issue, including Commentaries on selected papers and a series of Letters stimulated by discussions and the ideas exchanged at the last International Conference on Mycorrhiza (ICOM5: July 2006, Granada, Spain). Primary research papers in the last few years have broken the ground for new lines of research from regulation of gene expression to the ecological relevance of mycorrhizal symbioses. To cite a few, these studies have provided a new perspective on how the mycorrhizal symbionts play a critical role in biogeochemical cycles. The main stumbling block has been that a large proportion of mycorrhizal fungi do not produce conspicuous fruit bodies or cannot be grown in laboratory cultures, but most importantly there were no techniques available to assess the extensive and highly active webs of extraradical hyphae permeating the soil. The techniques and approaches of above-ground ecology do not translate well to the soil environment. However, during the past decade, PCR-based molecular methods and DNA sequencing have been routinely used to identify mycorrhizal fungi, and the application of these molecular methods has provided detailed insights into the complexity of mycorrhizal fungal communities and populations, and offers exciting prospects for elucidation of the processes that structure ectomycorrhizal fungal communities (Horton & Bruns, 2001). These tools have managed to reveal the tremendous diversity of mycorrhizal fungi interacting with their host in space (Genney et al., 2006) and time (Koide et al., in press), but also how different environmental factors and forest land usage could alter the composition of these soil fungal communities (Richard et al., 2005; Toljander et al., 2006). These molecular ecology studies will spur work on dynamics and functions of mycorrhizal communities and populations, but also generate hypotheses about their role in the changing forest ecosystems. For example, it appears that the formidable webs of extramatrical hyphae of mycorrhizal fungi not only permeate the mineral soil horizons, but are also very abundant in litter and decaying wood debris (Rosling et al., 2003; Tedersoo et al., 2003). With improvements in molecular techniques and appropriate DNA databases (Kõljalg et al., 2005), identification of taxa in fungal ecology has expanded from fruit bodies to mycorrhizal roots to extraradical hyphae (Anderson & Cairney, 2004). Combined with isotopic tools, these techniques provide novel insights into soil fungal ecology. In an elegant study, Lindahl et al. (2007) reported on the spatial patterns of ectomycorrhizal and saprotrophic fungi from soil profiles in a Pinus sylvestris forest in Sweden, and compared those patterns with profiles of bulk carbon:nitrogen (C:N) ratios, and 15N and 14C contents (as a proxy for age). Saprotrophic fungi were found to primarily colonize relatively recently shed litter components on the surface of the forest floor, where organic C was mineralized while N was retained. Mycorrhizal fungi were prominent in the underlying, more decayed litter and humus, where they apparently mobilized N and made it available to their host plants. Mycorrhizas not only shape the plant communities, they also affect the functional diversity of rhizospheric bacteria (Frey-Klett et al., 2005). In their seminal paper, Schrey et al. (2005) have shown that a molecular cross-talk is taking place between the members of these multitrophic associations. But beyond a gross understanding of their demography, the specific spatiotemporal dynamics of mycorrhizal species and communities in the underground remain elusive. The physical, chemical and biological complexity of the soil makes this kind of investigation a daunting prospect. The current situation could be eased by the development of high-throughput molecular diagnostic tools, such as DNA oligoarrays, for cataloging soil microbes on the larger scale imposed by field studies of a very heterogeneous subterranean world. The use of molecular approaches to inform the ecology and evolution of mycorrhizal symbioses has been a hallmark of Marc-André Selosse's research programs, and we are pleased to announce his appointment to the Editorial Board. His group at the University of Montpellier (France) has contributed much to the understanding of the ecology and evolution of mycorrhizal symbioses (Richard et al., 2005; Selosse et al., 2006). In a fascinating example of how molecular tools have provided new cues to understand plant ecology, he showed that the endomycorrhizal symbionts of forest achlorophyllous orchids, such as Neottia nidus-avis, belong to the genus Sebacina, a common ectomycorrhizal taxon associated with temperate trees (Selosse et al., 2002). This study of myco-heterotrophic plants has profoundly modified our view of the specificity of mycorrhizal fungi toward their host plants and the carbon fluxes between the different inhabitants of forest soils (Bidartondo, 2004). Marc-André's interests and expertise in the ecology and evolution of symbioses mesh well with the mycorrhizal expertise of the journal board which includes Iver Jakobsen, Alastair Fitter, Francis Martin, and Ian Alexander, whose perspectives range from genomics to field ecology. The next challenge on the agenda is to identify the functions played by the assemblages of mycorrhizal fungi in situ (Read & Perez-Moreno, 2003). As a prerequisite of such large-scale functional ecology studies, we now need to discover genes controlling the functioning of the mycorrhizal symbioses. Critical in this endeavor will be the use of genomic information on the recently sequenced Populus trichocarpa (Tuskan et al., 2006) and its mycorrhizal mutualists. The completion or impending completion of the genome sequences of the ectomycorrhizal Laccaria bicolor and endomycorrhizal Glomus intraradices (Martin et al., 2004; http://genome.jgi-psf.org/Lacbi1/Lacbi1.home.html) provides an unprecedented opportunity to identify the key components of interspecific and organism–environment interactions (Whitham et al., 2006). By examining, modeling and manipulating patterns of gene expression, we can identify the genetic control points regulating the mycorrhizal response to changing host physiology, and better understand how these interactions control ecosystem function. Complex biological systems such as symbiosis are thought to be caused by the interaction of many genes and the environment, and the genetic components can be determined by association with genetic variation. Association mapping and ecotilling (Gilchrist et al., 2006) compare genomes in wide-ranging natural populations of individuals with different phenotypes to allow 'associations' between genetic markers and phenotypic traits, such as nutrient acquisition or symbiosis efficiency. This approach is sparking the development of higher density genotyping arrays with greater power to detect common genetic variations, such as single nucleotide polymorphisms (SNPs) and copy number variants (CNVs); the latter being likely involved in ectomycorrhiza development (Le Quéréet al., 2006). Mycorrhiza-regulated genes involved in N and phosphate absorption and organic matter decay have now been identified (Tuskan et al., 2006; Couturier et al., in press). Analysis of their sequence polymorphisms in wild populations will set the stage for understanding the adaptation of the subsurface symbiotic duet to changes in the environment. In addition, novel DNA sequencers based on massively parallel sequencing of millions of fragments will provide a cost-effective, efficient tool for conducting these candidate-gene based association genetic studies on a large scale in situ. The development of highly parallel genomic assays is still a relatively young field and has not yet been applied to soil microbial ecology. Sequencing of PCR-amplified ribosomal DNA will be substituted by genome sequencing of hundreds of environmental mycorrhizal samples and selected soil metagenomes in the near future. There is no doubt that massive sequencing of soil entities will be fertile ground for novel hypotheses about how mycorrhizal symbioses drive ecosystems. Future efforts in this area will advance our general perspective on mycorrhizal ecology and evolution and elucidate the biological dynamics that mediate the flux of matter and energy in terrestrial ecosystems. New Phytologist is pleased to continue to host and to support these innovative studies. FM would like to thank David and Nicolas Martin for sharing their in-depth expertise on Middle-Earth. Research conducted in Martin's laboratory on the molecular ecology and genomics of mycorrhizal symbioses is funded by INRA, the Région Lorraine and the European Network of Excellence EVOLTREE.