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Metabolomic and Transcriptomic Changes Induced by Potassium Deficiency During Sarocladium oryzae Infection Reveal Insights into Rice Sheath Rot Disease Resistance.

ABSTRACT: Rice sheath rot disease caused by Sarocladium oryzae (S. oryzae) infection is an emerging disease, and infection can cause yield losses of 20-85%. Adequate potassium (K) application is a feasible strategy for rice tolerance to S. oryzae infection. However, little is known about the metabolic mechanisms regulated by K that allow rice to cope better with S. oryzae infection. The present study performed a comparative metabolome and transcriptome analysis of rice with different K nutrition statuses before and upon S. oryzae infection. Sarocladium oryzae infection triggered a hydrogen peroxide (H₂O₂) burst, and K starvation aggravated the accumulation of H₂O₂ in the flag leaf sheath (FLS), which resulted in lipid peroxidation. Likewise, K deficiency altered the lipid homeostasis of the host plants by hyperaccumulation of 1-alkyl-2-acylglycerophosphoethanolamine. K starvation decreased the content of glycoglycerolipids including monogalactosyldiacyglycerol and digalactosyldoacylglycerol during S. oryzae infection, which destroyed the stability of bilayer membranes. In contrast, sufficient K supply increased antioxidant-related transcript expression (for example, the genes related to glutathione-S-transferase biosynthesis were upregulated), which activated the antioxidant systems. Additionally, upon S. oryzae infection, K starvation amplified the negative impacts of S. oryzae infection on flag leaf photosynthetic potential. These results provide new insight into the role of K in alleviating S. oryzae infection. Adequate K supply decreased the negative impacts of sheath rot disease on rice growth by alleviating lipid peroxidation and maintaining lipid homeostasis.

SUBMITTER: Zhang J

PROVIDER: S-EPMC8448798 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundSheath rot disease caused by Sarocladium oryzae is an emerging threat for rice cultivation at global level. However, limited information with respect to genomic resources and pathogenesis is a major setback to develop disease management strategies. Considering this fact, we sequenced the whole genome of highly virulent Sarocladium oryzae field isolate, Saro-13 with 82x sequence depth.ResultsThe genome size of S. oryzae was 32.78 Mb with contig N50 18.07 Kb and 10526 protein coding genes. The functional annotation of protein coding genes revealed that S. oryzae genome has evolved with many expanded gene families of major super family, proteinases, zinc finger proteins, sugar transporters, dehydrogenases/reductases, cytochrome P450, WD domain G-beta repeat and FAD-binding proteins. Gene orthology analysis showed that around 79.80 % of S. oryzae genes were orthologous to other Ascomycetes fungi. The polyketide synthase dehydratase, ATP-binding cassette (ABC) transporters, amine oxidases, and aldehyde dehydrogenase family proteins were duplicated in larger proportion specifying the adaptive gene duplications to varying environmental conditions. Thirty-nine secondary metabolite gene clusters encoded for polyketide synthases, nonribosomal peptide synthase, and terpene cyclases. Protein homology based analysis indicated that nine putative candidate genes were found to be involved in helvolic acid biosynthesis pathway. The genes were arranged in cluster and structural organization of gene cluster was similar to helvolic acid biosynthesis cluster in Metarhizium anisophilae. Around 9.37 % of S. oryzae genes were identified as pathogenicity genes, which are experimentally proven in other phytopathogenic fungi and enlisted in pathogen-host interaction database. In addition, we also report 13212 simple sequences repeats (SSRs) which can be deployed in pathogen identification and population dynamic studies in near future.ConclusionsLarge set of pathogenicity determinants and putative genes involved in helvolic acid and cerulenin biosynthesis will have broader implications with respect to Sarocladium disease biology. This is the first genome sequencing report globally and the genomic resources developed from this study will have wider impact worldwide to understand Rice-Sarocladium interaction.

Project description:Bacterial leaf blight (BLB), caused by Xanthomonas oryzae pv. oryzae (Xoo), gives rise to devastating crop losses in rice. Disease resistant rice cultivars are the most economical way to combat the disease. The TP309 cultivar is susceptible to infection by Xoo strain PXO99. A transgenic variety, TP309_Xa21, expresses the pattern recognition receptor Xa21, and is resistant. PXO99 big up tri, openraxST, a strain lacking the raxST gene, is able to overcome Xa21-mediated immunity. We used a single extraction solvent to demonstrate comprehensive metabolomics and transcriptomics profiling under sample limited conditions, and analyze the molecular responses of two rice lines challenged with either PXO99 or PXO99 big up tri, openraxST. LC-TOF raw data file filtering resulted in better within group reproducibility of replicate samples for statistical analyses. Accurate mass match compound identification with molecular formula generation (MFG) ranking of 355 masses was achieved with the METLIN database. GC-TOF analysis yielded an additional 441 compounds after BinBase database processing, of which 154 were structurally identified by retention index/MS library matching. Multivariate statistics revealed that the susceptible and resistant genotypes possess distinct profiles. Although few mRNA and metabolite differences were detected in PXO99 challenged TP309 compared to mock, many differential changes occurred in the Xa21-mediated response to PXO99 and PXO99 big up tri, openraxST. Acetophenone, xanthophylls, fatty acids, alkaloids, glutathione, carbohydrate and lipid biosynthetic pathways were affected. Significant transcriptional induction of several pathogenesis related genes in Xa21 challenged strains, as well as differential changes to GAD, PAL, ICL1 and Glutathione-S-transferase transcripts indicated limited correlation with metabolite changes under single time point global profiling conditions. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1007/s11306-010-0218-7) contains supplementary material, which is available to authorized users.

Project description:Potassium ions (K+) are important for plant growth and crop yield. However, the effects of K+ deficiency on the biomass of coconut seedlings and the mechanism by which K+ deficiency regulates plant growth remain largely unknown. Therefore, in this study, we compared the physiological, transcriptome, and metabolite profiles of coconut seedling leaves under K+-deficient and K+-sufficient conditions using pot hydroponic experiments, RNA-sequencing, and metabolomics technologies. K+ deficiency stress significantly reduced the plant height, biomass, and soil and plant analyzer development value, as well as K content, soluble protein, crude fat, and soluble sugar contents of coconut seedlings. Under K+ deficiency, the leaf malondialdehyde content of coconut seedlings were significantly increased, whereas the proline (Pro) content was significantly reduced. Superoxide dismutase, peroxidase, and catalase activities were significantly reduced. The contents of endogenous hormones such as auxin, gibberellin, and zeatin were significantly decreased, whereas abscisic acid content was significantly increased. RNA-sequencing revealed that compared to the control, there were 1003 differentially expressed genes (DEGs) in the leaves of coconut seedlings under K+ deficiency. Gene Ontology analysis revealed that these DEGs were mainly related to "integral component of membrane," "plasma membrane," "nucleus", "transcription factor activity," "sequence-specific DNA binding," and "protein kinase activity." Kyoto Encyclopedia of Genes and Genomes pathway analysis indicated that the DEGs were mainly involved in "MAPK signaling pathway-plant," "plant hormone signal transduction," "starch and sucrose metabolism," "plant-pathogen interaction," "ABC transporters," and "glycerophospholipid metabolism." Metabolomic analysis showed that metabolites related to fatty acids, lipidol, amines, organic acids, amino acids, and flavonoids were generally down-regulated in coconut seedlings under K+ deficiency, whereas metabolites related to phenolic acids, nucleic acids, sugars, and alkaloids were mostly up-regulated. Therefore, coconut seedlings respond to K+ deficiency stress by regulating signal transduction pathways, primary and secondary metabolism, and plant-pathogen interaction. These results confirm the importance of K+ for coconut production, and provide a more in-depth understanding of the response of coconut seedlings to K+ deficiency and a basis for improving K+ utilization efficiency in coconut trees.

Project description:BackgroundXanthomonas oryzae pv oryzae is a devastating pathogen of rice and has been extensively studied as a model pathogen of monocotyledons. Expressional studies in both the contenders have been undertaken in past to understand the molecular mechanism underlying the compatible and incompatible interactions in the pathosystem. Continuous update on database and gene annotations necessitates constant updating on the roles of the new entities as well as reinterpretation of regulations of the previous ones. Moreover the past endeavors have addressed the middle or late defense responses of the rice plant whereas in the present study an attempt has been made to investigate the early defense responses taking place immediately after inoculation.ResultsMicroarray was used to study the transcriptional modulations in eighteen days old rice seedling leaves of both susceptible and resistant genotypes one hour after inoculation. In resistant plants as compared to susceptible ones 274 genes were found to be differentially expressed. Annotations could be assigned to 112 up- and 73 down-regulated transcripts and gene interaction maps were generated for 86 transcripts. Expressional data and interaction maps were used to develop a hypothetical scheme of the molecular events taking place during early defense response. Network analysis with the differential transcripts showed up-regulation of major clusters of cell signaling proteins and transcription factors while growth and basal metabolic components were largely found to be down-regulated.ConclusionsThis study provides an understanding of the early defense signaling in rice cells. Components of the calcium and lipid signaling as well as MAPK cascade were modulated, by signals from surface receptors and cytosolic R-proteins, to arouse jasmonic acid and ethylene signaling and suppress auxin signaling through various transcription factors. Abscisic acid modulation was also evident through the expression regulation of transcription factors involved with its functions. Moreover adjustments in expression levels of components of primary as well as secondary metabolism, protein trafficking and turnout were apparent, highlighting the complexity of defense response.

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Metabolomic and Transcriptomic Changes Induced by Potassium Deficiency During Sarocladium oryzae Infection Reveal Insights into Rice Sheath Rot Disease Resistance.

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