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Comparative analysis of the root transcriptomes of cultivated and wild rice varieties in response to Magnaporthe oryzae infection revealed both common and species-specific pathogen responses.

ABSTRACT: BACKGROUND:Magnaporthe oryzae, the causal fungus of rice blast disease, negatively impacts global rice production. Wild rice (Oryza rufipogon), a relative of cultivated rice (O. sativa), possesses unique attributes that enable it to resist pathogen invasion. Although wild rice represents a major resource for disease resistance, relative to current cultivated rice varieties, no prior studies have compared the immune and transcriptional responses in the roots of wild and cultivated rice to M. oryzae. RESULTS:In this study, we showed that M. oryzae could act as a typical root-infecting pathogen in rice, in addition to its common infection of leaves, and wild rice roots were more resistant to M. oryzae than cultivated rice roots. Next, we compared the differential responses of wild and cultivated rice roots to M. oryzae using RNA-sequencing (RNA-seq) to unravel the molecular mechanisms underlying the enhanced resistance of the wild rice roots. Results indicated that both common and genotype-specific mechanisms exist in both wild and cultivated rice that are associated with resistance to M. oryzae. In wild rice, resistance mechanisms were associated with lipid metabolism, WRKY transcription factors, chitinase activities, jasmonic acid, ethylene, lignin, and phenylpropanoid and diterpenoid metabolism; while the pathogen responses in cultivated rice were mainly associated with phenylpropanoid, flavone and wax metabolism. Although modulations in primary metabolism and phenylpropanoid synthesis were common to both cultivated and wild rice, the modulation of secondary metabolism related to phenylpropanoid synthesis was associated with lignin synthesis in wild rice and flavone synthesis in cultivated rice. Interestingly, while the expression of fatty acid and starch metabolism-related genes was altered in both wild and cultivated rice in response to the pathogen, changes in lipid acid synthesis and lipid acid degradation were dominant in cultivated and wild rice, respectively. CONCLUSIONS:The response mechanisms to M. oryzae were more complex in wild rice than what was observed in cultivated rice. Therefore, this study may have practical implications for controlling M. oryzae in rice plantings and will provide useful information for incorporating and assessing disease resistance to M. oryzae in rice breeding programs.

SUBMITTER: Tian L

PROVIDER: S-EPMC5910329 | biostudies-literature | 2018 Apr

REPOSITORIES: biostudies-literature

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Comparative analysis of the root transcriptomes of cultivated and wild rice varieties in response to Magnaporthe oryzae infection revealed both common and species-specific pathogen responses.

Tian Lei L Shi Shaohua S Nasir Fahad F Chang Chunling C Li Weiqiang W Tran Lam-Son Phan LP Tian Chunjie C

Rice (New York, N.Y.) 20180420 1

<h4>Background</h4>Magnaporthe oryzae, the causal fungus of rice blast disease, negatively impacts global rice production. Wild rice (Oryza rufipogon), a relative of cultivated rice (O. sativa), possesses unique attributes that enable it to resist pathogen invasion. Although wild rice represents a major resource for disease resistance, relative to current cultivated rice varieties, no prior studies have compared the immune and transcriptional responses in the roots of wild and cultivated rice to ...[more]

PMID: 29679239

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Project description:BackgroundRice, which serves as a staple food for more than half of the world's population, is very susceptible to the pathogenic fungus, Magnaporthe oryzae. However, common wild rice (Oryza rufipogon), which is the ancestor of Asian cultivated rice (O. sativa), has significant potential as a genetic source of resistance to M. oryzae. Recent studies have shown that the domestication of rice has altered its relationship to symbiotic arbuscular mycorrhizae. A comparative response of wild and domestic rice inhabited by mycorrhizae to infection by M. oryzae has not been documented.ResultsIn the current study, roots of wild and cultivated rice colonized with the arbuscular mycorrhizal (AM) fungus (AMF) Rhizoglomus intraradices were used to compare the transcriptomic responses of the two species to infection by M. oryzae. Phenotypic analysis indicated that the colonization of wild and cultivated rice with R. intraradices improved the resistance of both genotypes to M. oryzae. Wild AM rice, however, was more resistant to M. oryzae than the cultivated AM rice, as well as nonmycorrhizal roots of wild rice. Transcriptome analysis indicated that the mechanisms regulating the responses of wild and cultivated AM rice to M. oryzae invasion were significantly different. The expression of a greater number of genes was changed in wild AM rice than in cultivated AM rice in response to the pathogen. Both wild and cultivated AM rice exhibited a shared response to M. oryzae which included genes related to the auxin and salicylic acid pathways; all of these play important roles in pathogenesis-related protein synthesis. In wild AM rice, secondary metabolic and biotic stress-related analyses indicated that the jasmonic acid synthesis-related α-linolenic acid pathway, the phenolic and terpenoid pathways, as well as the phenolic and terpenoid syntheses-related mevalonate (MVA) pathway were more affected by the pathogen. Genes related to these pathways were more significantly enriched in wild AM rice than in cultivated AM rice in response to M. oryzae. On the other hand, genes associated with the 'brassinosteroid biosynthesis' were more enriched in cultivated AM rice.ConclusionsThe AMF R. intraradices-colonized rice plants exhibited greater resistance to M. oryzae than non-AMF-colonized plants. The findings of the current study demonstrate the potential effects of crop domestication on the benefits received by the host via root colonization with AMF(s), and provide new information on the underlying molecular mechanisms. In addition, results of this study can also help develop guidelines for the applications of AMF(s) when planting rice.

Project description:BackgroundUtilizating the plant microbiome to enhance pathogen resistance in crop production is an emerging alternative to the use of chemical pesticides. However, the diversity and structure of the microbiota, and the assembly mechanisms of root-associated microbial communities of plants are still poorly understood.ResultsWe invstigated the microbiota of the root endosphere and rhizosphere soils of the rice cultivar Nipponbare (NPB) and its Piz-t-transgenic line (NPB-Piz-t) when infected with the filamentous fungus Magnaporthe oryzae (M. oryzae) isolate KJ201, using 16S rRNA and internal transcribed spacer 1 (ITS1) amplicon sequencing. The rhizosphere soils showed higher bacterial and fungal richness and diversity than the endosphere except for fungal richness in the rhizosphere soils of the mock treatment. Bacteria richness and diversity increased in the endospheric communities of NPB and Piz-t under inoculation with KJ201 (referred to as 'NPB-KJ201' and 'Piz-t-KJ201', respectively) compared with the corresponding mock treatments, with the NPB-KJ201 showing the highest diversity in the four bacterial endocompartments. In contrast, fungal richness and diversity decreased in the endospheric communities of NPB-KJ201 and Piz-t-KJ201, relative to the corresponding mock treatments, with NPB-KJ201 and Piz-t-KJ201 having the lowest richness and diversity, respectively, across the four fungal endocompartments. Principal component analysis (PCA) indicated that the microbiota of Piz-t-KJ201 of root endophytes were mostly remarkablely distinct from that of NPB-KJ201. Co-occurrence network analysis revealed that the phyla Proteobacteria and Ascomycota were the key contributors to the bacterial and fungal communities, respectively. Furthermore, a comparative metabolic analysis showed that the contents of tryptophan metabolism and indole alkaloid biosynthesis were significantly lower in the Piz-t-KJ201 plants.ConclusionsIn this study, we compared the diversity, composition, and assembly of microbial communities associated with the rhizosphere soils and endosphere of Piz-t-KJ201 and NPB-KJ201. On the basis of the different compositions, diversities, and assemblies of the microbial communities among different compartments, we propose that the host genotype and inoculation pattern of M. oryzae played dominant roles in determining the microbial community assemblage. Further metabolomics analysis revealed that some metabolites may influence changes in bacterial communities. This study improves our understanding of the complex interactions between rice and M. oryzae, which could be useful in developing new strategies to improve rice resistance through the manipulation of soil microorganisms.

Project description:Rice blast (Magnaporthe oryzae) is a key concern in combating global food insecurity given the disease is responsible for approximately 30% of rice production losses globally-the equivalent of feeding 60 million people. These losses increase the global rice price and reduce consumer welfare and food security. Rice is the staple crop for more than half the world's population so any reduction in rice blast would have substantial beneficial effects on consumer livelihoods. In 2012, researchers in the US began analyzing the feasibility of creating blast-resistant rice through cisgenic breeding. Correspondingly, our study evaluates the changes in producer, consumer, and environmental welfare, if all the rice produced in the Mid-South of the US were blast resistant through a process like cisgenics, using both international trade and environmental assessment modeling. Our results show that US rice producers would gain 69.34 million dollars annually and increase the rice supply to feed an additional one million consumers globally by eliminating blast from production in the Mid-South. These results suggest that blast alleviation could be even more significant in increasing global food security given that the US is a small rice producer by global standards and likely experiences lower losses from blast than other rice-producing countries because of its ongoing investment in production technology and management. Furthermore, results from our detailed life cycle assessment (LCA) show that producing blast-resistant rice has lower environmental (fossil fuel depletion, ecotoxicity, carcinogenics, eutrophication, acidification, global warming potential, and ozone depletion) impacts per unit of rice than non-blast resistant rice production. Our findings suggest that any reduction in blast via breeding will have significantly positive impacts on reducing global food insecurity through increased supply, as well as decreased price and environmental impacts in production.

Project description:BackgroundRice, which serves as a staple food for more than half of the world's population, is grown worldwide. The hybridization of wild and cultivated rice has enabled the incorporation of resistance to varying environmental conditions. Endophytic microbiota are known to be transferred with their host plants. Although some studies have reported on the endophytic microbiota of wild and cultivated rice, the inheritance from wild and cultivated rice accessions in next generations, in terms of endophytic microbiota, has not been examined.ResultsIn the present study, the endophytic microbial community structures of Asian and African wild and cultivated rice species were compared with those of their F1 offspring. High-throughput sequencing data of bacterial 16S rDNA and fungal internal transcribed spacer regions were used to classify the endophytic microbiota of collected samples of rice. Results indicated that when either African or Asian wild rice species were crossed with cultivated rice accessions, the first generation harbored a greater number of root endophytic fungi than the cultivated parent used to make the crosses. Network analysis of the bacterial and fungal operational taxonomic units revealed that Asian and African wild rice species clustered together and exhibited a greater number of significant correlations between fungal taxa than cultivated rice. The core bacterial genus Acidovorax and the core fungal order Pleosporales, and genera Myrothecium and Bullera connected African and Asian wild rice accessions together, and both the wild rice accessions with their F1 offspring. On the other hand, the core bacterial genus Bradyrhizobium and the core fungal genera Dendroclathra linked the African and Asian cultivated rice accessions together.ConclusionsThis study has theoretical significance for understanding the effect of breeding on the inheritance of endophytic microbiota of rice and identifying beneficial endophytic bacteria and fungi among wild and cultivated rice species, and their F1 offspring.

Project description:The role of ?-oxidation and the glyoxylate cycle in fungal pathogenesis is well documented. However, an ambiguity still remains over their interaction in peroxisomes to facilitate fungal pathogenicity and virulence. In this report, we characterize a gene encoding an alanine, glyoxylate aminotransferase 1 (AGT1) in Magnaporthe oryzae, the causative agent of rice blast disease, and demonstrate that AGT1 is required for pathogenicity of M. oryzae. Targeted deletion of AGT1 resulted in the failure of penetration via appressoria; therefore, mutants lacking the gene were unable to induce blast symptoms on the hosts rice and barley. This penetration failure may be associated with a disruption in lipid mobilization during conidial germination as turgor generation in the appressorium requires mobilization of lipid reserves from the conidium. Analysis of enhanced green fluorescent protein expression using the transcriptional and translational fusion with the AGT1 promoter and open reading frame, respectively, revealed that AGT1 expressed constitutively in all in vitro grown cell types and during in planta colonization, and localized in peroxisomes. Peroxisomal localization was further confirmed by colocalization with red fluorescent protein fused with the peroxisomal targeting signal 1. Surprisingly, conidia produced by the ?agt1 mutant were unable to form appressoria on artificial inductive surfaces, even after prolonged incubation. When supplemented with nicotinamide adenine dinucleotide (NAD(+))+pyruvate, appressorium formation was restored on an artificial inductive surface. Taken together, our data indicate that AGT1-dependent pyruvate formation by transferring an amino group of alanine to glyoxylate, an intermediate of the glyoxylate cycle is required for lipid mobilization and utilization. This pyruvate can be converted to non-fermentable carbon sources, which may require reoxidation of NADH generated by the ?-oxidation of fatty acids to NAD(+) in peroxisomes. Therefore, it may provide a means to maintain redox homeostasis in appressoria.

Dataset Information

Comparative analysis of the root transcriptomes of cultivated and wild rice varieties in response to Magnaporthe oryzae infection revealed both common and species-specific pathogen responses.

Publications

Comparative analysis of the root transcriptomes of cultivated and wild rice varieties in response to Magnaporthe oryzae infection revealed both common and species-specific pathogen responses.

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