Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis

Tisserant, Émilie; Malbreil, Mathilde; Kuo, Alan; Kohler, Annegret; Symeonidi, Aikaterini; Balestrini, Raffaella; Charron, Philippe; Duensing, Nina; Frey, Nicolas Frei dit; Gianinazzi‐Pearson, Vivienne; Gilbert, Luz B.; Handa, Yoshihiro; Herr, Joshua R.; Hijri, Mohamed; Koul, Raman; Kawaguchi, Masayoshi; Krajinski, Franziska; Lammers, Peter J.; Masclaux, Frédéric G.; Murat, Claude; Morin, Emmanuelle; Ndikumana, Steve; Pagni, Marco; Petitpierre, Denis; Requena, Natalia; Rosikiewicz, Pawel; Riley, Rohan; Saito, Katsuichi; Clemente, Hélène San; Shapiro, Harris; Tuinen, Diederik van; Bécard, Guillaume; Bonfante, Paola; Paszkowski, Uta; Shachar‐Hill, Yair; Tuskan, Gerald A.; Young, J. Peter W.; Sanders, Ian R.; Henrissat, Bernard; Rensing, Stefan A.; Grigoriev, Igor V.; Corradi, Nicolas; Roux, Christophe; Martin, Francis

doi:10.1073/pnas.1313452110

Cited by 709 publications

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“…This gene count is in line with the about 28 000 genes reported for R. irregularis, the closest relative of G. margarita so far sequenced (Tisserant et al, 2013;Lin et al, 2014). The G. margarita transcripts had an average GC content of 31.96%, a median contig length of 781 bp, and an average contig length of 1185.77 bp; the contig N50 based on all transcripts was 1683 bp.…”

Section: Resultssupporting

confidence: 86%

“…Pfam analysis identified 3838 domains (Supplementary Table S3). As observed in Rhizophagus (Tisserant et al, 2013), G. margarita showed an overrepresentation of proteins involved in signalling pathways and ubiquitin-related metabolism. Interestingly, for both fungi, the most abundant domains occurred in genes encoding tyrosine kinases and Sel1 (see Supplementary data).…”

Section: Resultsmentioning

confidence: 51%

“…These transcripts include phosphate transporters, saccharide transporters, chitinases, chitin synthases and HMG-box transcription factors putatively involved in mating-type recognition (see Supplementary Table S2 for a comprehensive list). AM fungi are considered to be asexual, but the huge number of mating type genes in R. irregularis (Tisserant et al, 2013) and in G. margarita opens the question of their biological meaning. Consistent with the analysis of the R. irregularis genome, the G. margarita transcriptome has cobalamin-dependent and cobalaminindependent methionine synthases, both sharing very high identity with the homologous genes in the R. irregularis genome.…”

Section: Resultsmentioning

confidence: 99%

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Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential

et al. 2015

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Arbuscular mycorrhizal fungi (AMF) occur in the rhizosphere and in plant tissues as obligate symbionts, having key roles in plant evolution and nutrition. AMF possess endobacteria, and genome sequencing of the endobacterium Candidatus Glomeribacter gigasporarum revealed a reduced genome and a dependence on the fungal host. To understand the effect of bacteria on fungal fitness, we used next-generation sequencing to analyse the transcriptional profile of Gigaspora margarita in the presence and in the absence of its endobacterium. Genomic data on AMF are limited; therefore, we first generated a gene catalogue for G. margarita. Transcriptome analysis revealed that the endobacterium has a stronger effect on the pre-symbiotic phase of the fungus. Coupling transcriptomics with cell biology and physiological approaches, we demonstrate that the bacterium increases the fungal sporulation success, raises the fungal bioenergetic capacity, increasing ATP production, and eliciting mechanisms to detoxify reactive oxygen species. By using TAT peptide to translocate the bioluminescent calcium reporter aequorin, we demonstrated that the line with endobacteria had a lower basal intracellular calcium concentration than the cured line. Lastly, the bacteria seem to enhance the fungal responsiveness to strigolactones, the plant molecules that AMF perceive as branching factors. Although the endobacterium exacts a nutritional cost on the AMF, endobacterial symbiosis improves the fungal ecological fitness by priming mitochondrial metabolic pathways and giving the AMF more tools to face environmental stresses. Thus, we hypothesise that, as described for the human microbiota, endobacteria may increase AMF innate immunity.

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Section: Resultssupporting

confidence: 86%

Section: Resultsmentioning

confidence: 51%

Section: Resultsmentioning

confidence: 99%

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Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential

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“…Glomus intraradices (now known as Rhizophagus irregularis; Tisserant et al, 2013) promotes P acquisition in bean (Nielsen et al, 1998) and was used for this study. To facilitate the even distribution of spores, the inoculant (Premier Tech Biotechnologies), consisting of R. irregularis spores, was mixed thoroughly with 1.5 kg of sterilized sand before being mixed into the bulk growth medium prior to planting.…”

Section: Mycorrhizal Studymentioning

confidence: 99%

Reduction in Root Secondary Growth as a Strategy for Phosphorus Acquisition

2017

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We tested the hypothesis that reduced root secondary growth of dicotyledonous species improves phosphorus acquisition. Functional-structural modeling in SimRoot indicates that, in common bean (Phaseolus vulgaris), reduced root secondary growth reduces root metabolic costs, increases root length, improves phosphorus capture, and increases shoot biomass in lowphosphorus soil. Observations from the field and greenhouse confirm that, under phosphorus stress, resource allocation is shifted from secondary to primary root growth, genetic variation exists for this response, and reduced secondary growth improves phosphorus capture from low-phosphorus soil. Under low phosphorus in greenhouse mesocosms, genotypes with reduced secondary growth had 39% smaller root cross-sectional area, 60% less root respiration, 27% greater root length, 78% greater shoot phosphorus content, and 68% greater shoot mass than genotypes with advanced secondary growth. In the field under low phosphorus, these genotypes had 43% smaller root cross-sectional area, 32% greater root length, 58% greater shoot phosphorus content, and 80% greater shoot mass than genotypes with advanced secondary growth. Secondary growth eliminated arbuscular mycorrhizal associations as cortical tissue was destroyed. These results support the hypothesis that reduced root secondary growth is an adaptive response to low phosphorus availability and merits investigation as a potential breeding target.

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“…The first three sequenced mycorrhizal genomes, i.e., the ECM L. bicolor and T. melanosporum 4,5 and the arbuscular mycorrhizal fungus Rhizophagus irregularis 15 , demonstrated substantial losses in PCWDE genes. To assess the diversity of lignocellulose-decay capabilities of other mycorrhizal lineages, we cataloged 28 gene families and subfamilies encoding oxidoreductases and carbohydrateactive enzymes (CAZymes) associated with plant cell wall degradation (Fig.…”

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Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists

Kohler¹,

Kuo²,

Nagy³

et al. 2015

Nat Genet

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l e t t e r sTo elucidate the genetic bases of mycorrhizal lifestyle evolution, we sequenced new fungal genomes, including 13 ectomycorrhizal (ECM), orchid (ORM) and ericoid (ERM) species, and five saprotrophs, which we analyzed along with other fungal genomes. Ectomycorrhizal fungi have a reduced complement of genes encoding plant cell walldegrading enzymes (PCWDEs), as compared to their ancestral wood decayers. Nevertheless, they have retained a unique array of PCWDEs, thus suggesting that they possess diverse abilities to decompose lignocellulose. Similar functional categories of nonorthologous genes are induced in symbiosis. Of induced genes, 7-38% are orphan genes, including genes that encode secreted effector-like proteins. Convergent evolution of the mycorrhizal habit in fungi occurred via the repeated evolution of a 'symbiosis toolkit', with reduced numbers of PCWDEs and lineage-specific suites of mycorrhiza-induced genes.Fungi are often described as either saprotrophs, which degrade complex organic substrates, or biotrophs, which obtain carbon compounds from living hosts. Among the latter, ECM fungi provide crucial ecological services in interacting with forest trees. They are portrayed as mutualists trading host photoassimilates for nutrients and having limited capacity to decompose soil lignocellulose 1-3 , as a result of their reduced repertoire of PCWDEs 4-6 . However, recent studies are challenging this view [7][8][9][10] . An improved understanding of the ability of ECM fungi to decompose lignocellulose is needed to resolve mechanisms of nutrient cycling in forests. The ECM lifestyle in Laccaria bicolor is associated with the expression of new mycorrhizainduced small secreted proteins (MiSSPs) that are required for establishment of symbiosis 11,12 . Mycorrhizal symbioses have arisen repeatedly during fungal evolution and include not only ECM associations but also those with ERM and ORM mycorrhizae 13 . It is not known whether these symbioses share the genomic features found in L. bicolor 4 and Tuber melanosporum 5 . Here we assess whether there Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists

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Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis

Abstract: Blots were performed against DDR (p53 pSer15, histone 2AX pSer139), cell survival/ cell death (AKT pThr308, cleaved PARP), and cell signaling (ERK1/2 pThr202/Tyr204) markers and controls. Actin and GAPDH served as loading controls.

Cited by 709 publications

References 32 publications

Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential

Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential

Reduction in Root Secondary Growth as a Strategy for Phosphorus Acquisition

Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists

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