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

ABSTRACT: The mutualistic symbiosis involving Glomeromycota, a distinctive phylum of early diverging Fungi, is widely hypothesized to have promoted the evolution of land plants during the middle Paleozoic. These arbuscular mycorrhizal fungi (AMF) perform vital functions in the phosphorus cycle that are fundamental to sustainable crop plant productivity. The unusual biological features of AMF have long fascinated evolutionary biologists. The coenocytic hyphae host a community of hundreds of nuclei and reproduce clonally through large multinucleated spores. It has been suggested that the AMF maintain a stable assemblage of several different genomes during the life cycle, but this genomic organization has been questioned. Here we introduce the 153-Mb haploid genome of Rhizophagus irregularis and its repertoire of 28,232 genes. The observed low level of genome polymorphism (0.43 SNP per kb) is not consistent with the occurrence of multiple, highly diverged genomes. The expansion of mating-related genes suggests the existence of cryptic sex-related processes. A comparison of gene categories confirms that R. irregularis is close to the Mucoromycotina. The AMF obligate biotrophy is not explained by genome erosion or any related loss of metabolic complexity in central metabolism, but is marked by a lack of genes encoding plant cell wall-degrading enzymes and of genes involved in toxin and thiamine synthesis. A battery of mycorrhiza-induced secreted proteins is expressed in symbiotic tissues. The present comprehensive repertoire of R. irregularis genes provides a basis for future research on symbiosis-related mechanisms in Glomeromycota.

SUBMITTER: Tisserant E

PROVIDER: S-EPMC3864322 | biostudies-literature | 2013 Dec

REPOSITORIES: biostudies-literature

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

Tisserant Emilie E Malbreil Mathilde M Kuo Alan A Kohler Annegret A Symeonidi Aikaterini A Balestrini Raffaella R Charron Philippe P Duensing Nina N Frei dit Frey Nicolas N Gianinazzi-Pearson Vivienne V Gilbert Luz B LB Handa Yoshihiro Y Herr Joshua R JR Hijri Mohamed M Koul Raman R Kawaguchi Masayoshi M Krajinski Franziska F Lammers Peter J PJ Masclaux Frederic G FG Murat Claude C Morin Emmanuelle E Ndikumana Steve S Pagni Marco M Petitpierre Denis D Requena Natalia N Rosikiewicz Pawel P Riley Rohan R Saito Katsuharu K San Clemente Hélène H Shapiro Harris H van Tuinen Diederik D Bécard Guillaume G Bonfante Paola P Paszkowski Uta U Shachar-Hill Yair Y YY Tuskan Gerald A GA Young J Peter W JP Sanders Ian R IR Henrissat Bernard B Rensing Stefan A SA Grigoriev Igor V IV Corradi Nicolas N Roux Christophe C Martin Francis F

Proceedings of the National Academy of Sciences of the United States of America 20131125 50

The mutualistic symbiosis involving Glomeromycota, a distinctive phylum of early diverging Fungi, is widely hypothesized to have promoted the evolution of land plants during the middle Paleozoic. These arbuscular mycorrhizal fungi (AMF) perform vital functions in the phosphorus cycle that are fundamental to sustainable crop plant productivity. The unusual biological features of AMF have long fascinated evolutionary biologists. The coenocytic hyphae host a community of hundreds of nuclei and repr ...[more]

PMID: 24277808

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Project description:How cells control the proper delivery of vesicles and their associated cargo to specific plasma membrane (PM) domains upon internal or external cues is a major question in plant cell biology. A widely held hypothesis is that expansion of plant exocytotic machinery components, such as SNARE proteins, has led to a diversification of exocytotic membrane trafficking pathways to function in specific biological processes. A key biological process that involves the creation of a specialized PM domain is the formation of a host-microbe interface (the peri-arbuscular membrane) in the symbiosis with arbuscular mycorrhizal fungi. We have previously shown that the ability to intracellularly host AM fungi correlates with the evolutionary expansion of both v- (VAMP721d/e) and t-SNARE (SYP132α) proteins, that are essential for arbuscule formation in Medicago truncatula. Here we studied to what extent the symbiotic SNAREs are different from their non-symbiotic family members and whether symbiotic SNAREs define a distinct symbiotic membrane trafficking pathway. We show that all tested SYP1 family proteins, and most of the non-symbiotic VAMP72 members, are able to complement the defect in arbuscule formation upon knock-down/-out of their symbiotic counterparts when expressed at sufficient levels. This functional redundancy is in line with the ability of all tested v- and t-SNARE combinations to form SNARE complexes. Interestingly, the symbiotic t-SNARE SYP132α appeared to occur less in complex with v-SNAREs compared to the non-symbiotic syntaxins in arbuscule-containing cells. This correlated with a preferential localization of SYP132α to functional branches of partially collapsing arbuscules, while non-symbiotic syntaxins accumulate at the degrading parts. Overexpression of VAMP721e caused a shift in SYP132α localization toward the degrading parts, suggesting an influence on its endocytic turn-over. These data indicate that the symbiotic SNAREs do not selectively interact to define a symbiotic vesicle trafficking pathway, but that symbiotic SNARE complexes are more rapidly disassembled resulting in a preferential localization of SYP132α at functional arbuscule branches.

Project description:BackgroundSmall RNAs (sRNAs) are short non-coding RNA molecules (20-30 nt) that regulate gene expression at transcriptional or post-transcriptional levels in many eukaryotic organisms, through a mechanism known as RNA interference (RNAi). Recent studies have highlighted that they are also involved in cross-kingdom communication: sRNAs can move across the contact surfaces from "donor" to "receiver" organisms and, once in the host cells of the receiver, they can target specific mRNAs, leading to a modulation of host metabolic pathways and defense responses. Very little is known about RNAi mechanism and sRNAs occurrence in Arbuscular Mycorrhizal Fungi (AMF), an important component of the plant root microbiota that provide several benefits to host plants, such as improved mineral uptake and tolerance to biotic and abiotic stress.ResultsTaking advantage of the available genomic resources for the AMF Rhizophagus irregularis we described its putative RNAi machinery, which is characterized by a single Dicer-like (DCL) gene and an unusual expansion of Argonaute-like (AGO-like) and RNA-dependent RNA polymerase (RdRp) gene families. In silico investigations of previously published transcriptomic data and experimental assays carried out in this work provided evidence of gene expression for most of the identified sequences. Focusing on the symbiosis between R. irregularis and the model plant Medicago truncatula, we characterized the fungal sRNA population, highlighting the occurrence of an active sRNA-generating pathway and the presence of microRNA-like sequences. In silico analyses, supported by host plant degradome data, revealed that several fungal sRNAs have the potential to target M. truncatula transcripts, including some specific mRNA already shown to be modulated in roots upon AMF colonization.ConclusionsThe identification of RNAi-related genes, together with the characterization of the sRNAs population, suggest that R. irregularis is equipped with a functional sRNA-generating pathway. Moreover, the in silico analysis predicted 237 plant transcripts as putative targets of specific fungal sRNAs suggesting that cross-kingdom post-transcriptional gene silencing may occur during AMF colonization.

Project description:IntroductionAdventitious root (AR) development, affected by various biotic and abiotic factors, is the most important procedure in tea plant (Camellia sinensis L.) cutting propagation. Establishing symbiotic relationships with most terrestrial plants, AMF (Arbuscular mycorrhizal fungus) can mediate the AR formation of several herbaceous and woody plants in previous studies.MethodsIn this paper, effects of combined application of AMF and exogenous auxin on AR formation of cuttings from different tea plant varieties ('Pingyangtezao', 'Longjing 43' and 'Longjingchangye') were studied. Then we also performed RNA-Seq analysis with 'Pingyangtezao' cuttings aiming to find the possible auxin-related pathway of AM fungal regulation on AR formation. To accurately uncover the regulatory mechanism of AMF on AR formation of tea cuttings, rooting process were separated into four stages (S0, non-rooting; S1, AR protrusion; S2, AR formation and S3, AR elongation) at the same sampling time.Results and discussionResults showed that IBA treatment increased the mycorrhizal colonization rate, especially in 'Pingyangtezao' variety (from 37.58% to 46.29%). Both inoculating AMF and addition of IBA promoted the AR formation, and rooting of different tea plant varieties showed different dependence on auxin. AMF could alleviate the effect of auxin-related inhibitors (2,3,5-triiodobenzoic acid, L-α-(Aminooxy)-β-phenylpropionic acid and α-(phenylethyl-2-oxo)-IAA) on rooting of tea cuttings, even though the colonization of AMF was hindered at various degrees. Transcriptomic analysis showed that different numbers of differentially expressed genes (DEGs) at various rooting stages of tea cuttings with the most at S2 stage (1360 DEGs), indicating the increasing regulation by AMF with the development of AR. Similar trend was found in auxin-related DEGs, and family genes of YUC, GH, PIN, LAX, SAUR, AUX, and ABP involved in the AM fungal regulation on AR formation of tea cuttings. Additionally, AMF strongly mediated auxin transport and signal transduction pathways in tea cuttings as showed by the results of correlation analysis. Overall, interaction of AMF and exogenous auxin in promoting rooting and the preliminary mechanism of AMF regulating AR formation of tea cuttings was deciphered in this paper, which may provide a basis for further deep mechanistic research and cutting propagation of tea production.

Project description:Arbuscular mycorrhizal (AM) play an important role in improving plant growth and development. The interaction between phytohormones and AM symbiosis is gradually revealed. Here we examined the effect of Brassinosteroids (BR) on AM symbiosis and discussed the synergistic promotion of plant growth by BR and AM symbiosis. The xylophyta Eucalyptus grandis Hill (E. grandis) was inoculated with AM fungi Rhizoglomus irregularis R197198 (R. irregularis) and treated with different concentrations (0, 1, 10, and 100 nM) of 24-epibrassinolide (24-epiBL) for 6 weeks. With the increase of 24-epiBL concentration, E. grandis growth was firstly promoted and then inhibited, but inoculation with AM fungi alleviated this inhibition. 24-epiBL and R. irregularis colonization significantly improved E. grandis growth and antioxidant system response, and the synergistic effect was the best. Compared with the control group, 24-epiBL treatment significantly increased the mycorrhizal colonization and arbuscular abundance of AM fungi R. irregular in E. grandis roots. The expression of AM symbiosis maker genes was significantly increased by 24-epiBL treatment. Both 24-epiBL treatment and AM colonization upregulated gibberellins (GA) synthesis genes, but no inhibition caused by GA levels was found. 24-epiBL is a kind of synthetic highly active BR. Based on the results of 24-epiBL treatment, we hypothesized that BR actively regulates AM symbiosis regulates AM symbiosis without affecting GA-INSENSITIVE DWARF1 (GID1)-DELLA expression. The synergistic treatment of BR and AM symbiosis can significantly promote the growth and development of plants. IMPORTANCE Brassinosteroids (BR) and Arbuscular mycorrhizas (AM) symbiosis play an important role in improving plant growth and development. Previous studies have shown that there is a complex regulatory network between phytohormones and AM symbiosis. However, the interactions of BR-signaling and AM symbiosis are still poorly understood. Our results suggest that BR actively regulates the colonization and development of AM fungi, and AM fungal colonization can alleviate the inhibition of plant growth caused by excessive BR. In addition, BR actively regulates AM symbiosis, but does not primarily mediate gibberellins-DELLA interaction. The synergistic treatment of BR and AM symbiosis can significantly promote the growth and development of plants. The conclusions of this study provide a reference for phytohormones-AM symbiosis interaction.

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

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

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