Exploring the Genome of glomeromycotan fungi

Chapitre 1International audienceAll fungi forming a mutualistic symbiosis with plant roots called arbuscular mycorrhiza were formerly grouped together in one order, the Glomales, placed in the Zygomycota (Morton 1993). Based on molecular analyses suggestingthat arbuscular mycorrhizal fungi should be separated from other fungal taxa, they were transferred a decade ago to the Glomeromy-cota , a new phylum created specifically for them (Schu¨ ssler et al. 2001). Whilst members of this monophyletic group originated from the same common ancestor as the Ascomycota and Basidiomycota, they have no obvious affinity to other major extant phylogenetic groups in the kingdom Fungi (James et al. 2006) and they probably diverged from the other fungal lineages several hundred million years before plants colonized terrestrial habitats 400–500 million years ago (mya) (Heckman et al. 20 01). Glomeromycotan fungi are complex but extremely successful organisms. They establish a compatible interaction with plants by either avoiding or suppressing plant defence reactions whilst redirecting host metabolic flow to their benefit without being detrimental to their host. The mechanisms by which this bio-trophy is achieved are largely unknown but the Glomeromycota have accompanied land plants through evolution and survived across periods of important environmental change to become ecologically and agriculturally impor-tant symbionts which improve the overall fit-ness of very different plant taxa in terrestrial ecosystems world-wide (Smith and Read 2008 ). Substantial evidence has accumulated about how a rational use of the microsymbiont proper-ties should significantly contribute to decreasing fertilizer and pesticide use in agriculture (Gianinazzi et al. 20 10). Although the Glomeromycota show consid-erable diversity between or within morphologi-cally recognizable species (Rosendahl 2008), they share some singular biological traits which limit experimental approaches that can be exploited to characterize their complexity. One particularity is their reproduction through large asexual spores , each of which is a single cell harbouring several hundreds or thousands of nuclei. The main mechanism for filling a spore with so many nuclei appears to be a massive influx of nuclei from subtending myce-lium into the developing spore (Jany and Pawlowska 2010). No sexual stage is known for these fungi but, although they are assumed to only reproduce asexually, recent transcrip-tome analyses indicate that they do possess genetic information essential for sexual repro-duction and meiosis (Tisserant et al. 2012 ). Absence of a sexual cycle raises questions about how Glomeromycota deal with deleteri-ous mutations usually eliminated through meiosis and how they have adapted to new hosts or habitats during evolution. High poly-ploidy, with multiple gene copies in the same genome, has been speculated as a possible mechanism to buffer against mutational events (Pawlowska and Taylor 2004 ), whilst nuclear exchange through hyphal anastomosis between different individuals of a same species (Casana and Bonfante 1988; Giovannetti et al. 2001 ) provides the possibility for genetic flux and recombination events (Croll et al. 2009 ; Angelard and Sanders 2011). However, basic information concerning ploidy, karyosis, num-ber of chromosomes or whether meiosis does occur in the Glomeromycota is still lacking, and evidence for genetic exchange, recombination or segregation is very limited. Another particularity is that all glomeromy-cotan fungi are obligate symbionts which have so far proved to be incalcitrant to pure culture in the absence of a host root on which they depend as a carbon source. This introduces inherent limitations in the application of standard tech-niques like genetic transformation or mutant generation/characterization, and it greatly hin-ders advances in the knowledge about gene function in these organisms. As previously pointed out (Gianinazzi-Pearson et al. 2001), there is converging evidence that the Glomero-mycota are an unusual group of fungi, and information about their genome structure, com-plexity and function is essential to understand-ing the processes regulating their symbiotic attributes, their reproductive biology and their apparent stability during coevolution in symbi-osis with many different plant taxa. Despite the fact that the biology of glomeromycotan fungi makes them extremely difficult to manipulate experimentally, the advent of powerful molecu-lar techniques has considerably furthered research during the past decade. The present chapter updates on the state of the art on Glo-meromycota genomics within the past decade (Gianinazzi-Pearson et al. 20 01), as well as on progress made through targeted and high-throughput sequencing programmes into an understanding of their basic biology