Dataset Information

Dual RNA-seq reveals large-scale non-conserved genotype?×?genotype-specific genetic reprograming and molecular crosstalk in the mycorrhizal symbiosis.

ABSTRACT: Arbuscular mycorrhizal fungi (AMF) impact plant growth and are a major driver of plant diversity and productivity. We quantified the contribution of intra-specific genetic variability in cassava (Manihot esculenta) and Rhizophagus irregularis to gene reprogramming in symbioses using dual RNA-sequencing. A large number of cassava genes exhibited altered transcriptional responses to the fungus but transcription of most of these plant genes (72%) responded in a different direction or magnitude depending on the plant genotype. Two AMF isolates displayed large differences in their transcription, but the direction and magnitude of the transcriptional responses for a large number of these genes was also strongly influenced by the genotype of the plant host. This indicates that unlike the highly conserved plant genes necessary for the symbiosis establishment, most of the plant and fungal gene transcriptional responses are not conserved and are greatly influenced by plant and fungal genetic differences, even at the within-species level. The transcriptional variability detected allowed us to identify an extensive gene network showing the interplay in plant-fungal reprogramming in the symbiosis. Key genes illustrated that the two organisms jointly program their cytoskeleton organization during growth of the fungus inside roots. Our study reveals that plant and fungal genetic variation has a strong role in shaping the genetic reprograming in response to symbiosis, indicating considerable genotype?×?genotype interactions in the mycorrhizal symbiosis. Such variation needs to be considered in order to understand the molecular mechanisms between AMF and their plant hosts in natural communities.

SUBMITTER: Mateus ID

PROVIDER: S-EPMC6474227 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Dual RNA-seq reveals large-scale non-conserved genotype × genotype-specific genetic reprograming and molecular crosstalk in the mycorrhizal symbiosis.

Mateus Ivan D ID Masclaux Frédéric G FG Aletti Consolée C Rojas Edward C EC Savary Romain R Dupuis Cindy C Sanders Ian R IR

The ISME journal 20190115 5

Arbuscular mycorrhizal fungi (AMF) impact plant growth and are a major driver of plant diversity and productivity. We quantified the contribution of intra-specific genetic variability in cassava (Manihot esculenta) and Rhizophagus irregularis to gene reprogramming in symbioses using dual RNA-sequencing. A large number of cassava genes exhibited altered transcriptional responses to the fungus but transcription of most of these plant genes (72%) responded in a different direction or magnitude depe ...[more]

PMID: 30647457

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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:BackgroundTomato (Solanum lycopersicum) establishes a beneficial symbiosis with arbuscular mycorrhizal (AM) fungi. The formation of the mycorrhizal association in the roots leads to plant-wide modulation of gene expression. To understand the systemic effect of the fungal symbiosis on the tomato fruit, we used RNA-Seq to perform global transcriptome profiling on Moneymaker tomato fruits at the turning ripening stage.ResultsFruits were collected at 55 days after flowering, from plants colonized with Funneliformis mosseae and from control plants, which were fertilized to avoid responses related to nutrient deficiency. Transcriptome analysis identified 712 genes that are differentially expressed in fruits from mycorrhizal and control plants. Gene Ontology (GO) enrichment analysis of these genes showed 81 overrepresented functional GO classes. Up-regulated GO classes include photosynthesis, stress response, transport, amino acid synthesis and carbohydrate metabolism functions, suggesting a general impact of fungal symbiosis on primary metabolisms and, particularly, on mineral nutrition. Down-regulated GO classes include cell wall, metabolism and ethylene response pathways. Quantitative RT-PCR validated the RNA-Seq results for 12 genes out of 14 when tested at three fruit ripening stages, mature green, breaker and turning. Quantification of fruit nutraceutical and mineral contents produced values consistent with the expression changes observed by RNA-Seq analysis.ConclusionsThis RNA-Seq profiling produced a novel data set that explores the intersection of mycorrhization and fruit development. We found that the fruits of mycorrhizal plants show two transcriptomic "signatures": genes characteristic of a climacteric fleshy fruit, and genes characteristic of mycorrhizal status, like phosphate and sulphate transporters. Moreover, mycorrhizal plants under low nutrient conditions produce fruits with a nutrient content similar to those from non-mycorrhizal plants under high nutrient conditions, indicating that AM fungi can help replace exogenous fertilizer for fruit crops.

Dataset Information

Dual RNA-seq reveals large-scale non-conserved genotype?×?genotype-specific genetic reprograming and molecular crosstalk in the mycorrhizal symbiosis.

Publications

Dual RNA-seq reveals large-scale non-conserved genotype × genotype-specific genetic reprograming and molecular crosstalk in the mycorrhizal symbiosis.

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