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RNA-Seq analysis reveals insight into enhanced rice Xa7-mediated bacterial blight resistance at high temperature.

ABSTRACT: Plant disease is a major challenge to agriculture worldwide, and it is exacerbated by abiotic environmental factors. During some plant-pathogen interactions, heat stress allows pathogens to overcome host resistance, a phenomenon which could severely impact crop productivity considering the global warming trends associated with climate change. Despite the importance of this phenomenon, little is known about the underlying molecular mechanisms. To better understand host plant responses during simultaneous heat and pathogen stress, we conducted a transcriptomics experiment for rice plants (cultivar IRBB61) containing Xa7, a bacterial blight disease resistance (R) gene, that were infected with Xanthomonas oryzae, the bacterial blight pathogen of rice, during high temperature stress. Xa7-mediated resistance is unusual relative to resistance mediated by other R genes in that it functions better at high temperatures. Using RNA-Seq technology, we identified 8,499 differentially expressed genes as temperature responsive in rice cultivar IRBB61 experiencing susceptible and resistant interactions across three time points. Notably, genes in the plant hormone abscisic acid biosynthesis and response pathways were up-regulated by high temperature in both mock-treated plants and plants experiencing a susceptible interaction and were suppressed by high temperature in plants exhibiting Xa7-mediated resistance. Genes responsive to salicylic acid, an important plant hormone for disease resistance, were down-regulated by high temperature during both the susceptible and resistant interactions, suggesting that enhanced Xa7-mediated resistance at high temperature is not dependent on salicylic acid signaling. A DNA sequence motif similar to known abscisic acid-responsive cis-regulatory elements was identified in the promoter region upstream of genes up-regulated in susceptible but down-regulated in resistant interactions. The results of our study suggest that the plant hormone abscisic acid is an important node for cross-talk between plant transcriptional response pathways to high temperature stress and pathogen attack. Genes in this pathway represent an important focus for future study to determine how plants evolved to deal with simultaneous abiotic and biotic stresses.

SUBMITTER: Cohen SP

PROVIDER: S-EPMC5673197 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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RNA-Seq analysis reveals insight into enhanced rice Xa7-mediated bacterial blight resistance at high temperature.

Cohen Stephen P SP Liu Hongxia H Argueso Cristiana T CT Pereira Andy A Vera Cruz Casiana C Verdier Valerie V Leach Jan E JE

PloS one 20171106 11

Plant disease is a major challenge to agriculture worldwide, and it is exacerbated by abiotic environmental factors. During some plant-pathogen interactions, heat stress allows pathogens to overcome host resistance, a phenomenon which could severely impact crop productivity considering the global warming trends associated with climate change. Despite the importance of this phenomenon, little is known about the underlying molecular mechanisms. To better understand host plant responses during simu ...[more]

PMID: 29107972

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Project description:Bacterial blight, blast, and sheath blight are the commonest diseases causing substantial yield loss in rice around the world. Stacking of broad-spectrum resistance genes/QTLs into popular cultivars is becoming a major objective of any disease resistance breeding program. The varieties ASD 16 and ADT 43 are the two popular, high yielding, and widely grown rice cultivars of South India, which are susceptible to bacterial blight (BB), blast, and sheath blight diseases. The present study was carried out to improve the cultivars (ASD 16 and ADT 43) through introgression of bacterial blight (xa5, xa13, and Xa21), blast (Pi54), and sheath blight (qSBR7-1, qSBR11-1, and qSBR11-2) resistance genes/QTLs by MABB (marker-assisted backcross breeding). IRBB60 (xa5, xa13, and Xa21) and Tetep (Pi54; qSBR7-1, qSBR11-1, and qSBR11-2) were used as donors to introgress BB, blast, and sheath blight resistance into the recurrent parents (ASD 16 and ADT 43). Homozygous (BC3F3 generation), three-gene bacterial blight pyramided (xa5 + xa13 + Xa21) lines were developed, and these lines were crossed with Tetep to combine blast (Pi54) and sheath blight (qSBR7-1, qSBR11-1, and qSBR11-2) resistance. In BC3F3 generation, the improved pyramided lines carrying a total of seven genes/QTLs (xa5 + xa13 + Xa21 + Pi54 + qSBR7-1 + qSBR11-1 + qSBR11-2) were selected through molecular and phenotypic assay, and these were evaluated for resistance against bacterial blight, blast, and sheath blight pathogens under greenhouse conditions. We have selected nine lines in ASD 16 background and 15 lines in ADT 43 background, exhibiting a high degree of resistance to BB, blast, and sheath blight diseases and also possessing phenotypes of recurrent parents. The improved pyramided lines are expected to be used as improved varieties or used as a potential donor in breeding programs. The present study successfully introgressed Pi54, and qSBR QTLs (qSBR7-1, qSBR11-1, and qSBR11-2) from Tetep and major effective BB-resistant genes (xa5, xa13, and Xa21) from IRBB60 into the commercial varieties for durable resistance to multiple diseases.

Project description:BackgroundSpotted leaf mutants show typical necrotic lesions that appear spontaneously in the absence of any pathogen attack. These mutants are often characterized to exhibit programmed cell death (PCD) and activation of plant defense responses resulting in enhanced disease resistance to multiple pathogens. Here, we reported a novel spotted-leaf mutant, spl40 that showed enhanced disease resistance response.ResultsInitially lesions appeared at leaf tips during seedling stage and gradually covered the whole leaf at the tillering stage. The lesion development was light-dependent. spl40 showed obvious cell death at and around the lesion, and burst of reactive oxygen species (ROS) was accompanied by disturbed ROS scavenging system. Photosynthetic capacity was compromised as evidenced by significant reductions in chlorophyll content, important photosynthesis parameters and downregulated expression of photosynthesis-related genes which ultimately led to poor performance of major agronomic traits. spl40 exhibited enhanced resistance to 14 out of 16 races of bacterial blight pathogen of rice, caused by Xanthomonas oryzae pv. oryzae, most probably though activation of SA and JA signaling pathways, owing to upregulated expression of SA and JA signaling genes, though the exact mechanism remain to be elucidated. The spotted-leaf phenotype was controlled by a novel single recessive nuclear gene. Genetic mapping combined with high throughput sequencing analysis identified Os05G0312000 as the most probable candidate gene. Sequencing of ORF revealed a single SNP change from C to T that resulted in non-synonymous change in amino acid residue from leucine to phenylalanine. Interestingly, the complementation plants did not display lesions before heading but showed lesions at the heading stage and the transgenic T1 progenies could be classified into 3 categories based on their lesion intensity, indicating the complex genetic nature of the spl40 mutation.ConclusionThe results obtained here clearly show that genes related to defense and PCD were upregulated in accordance with enhanced disease resistance and occurrence of PCD, whereas the photosynthetic capacity and overall ROS homeostasis was compromised in spl40. Our data suggest that a novel spotted-leaf mutant, spl40, would help to elucidate the mechanism behind lesion development involving programmed cell death and associated defense responses.

Dataset Information

RNA-Seq analysis reveals insight into enhanced rice Xa7-mediated bacterial blight resistance at high temperature.

Publications

RNA-Seq analysis reveals insight into enhanced rice Xa7-mediated bacterial blight resistance at high temperature.

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