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Integrated Analysis of microRNA and mRNA Transcriptome Reveals the Molecular Mechanism of Solanum lycopersicum Response to Bemisia tabaci and Tomato chlorosis virus.

ABSTRACT: Tomato chlorosis virus (ToCV), is one of the most devastating cultivated tomato viruses, seriously threatened the growth of crops worldwide. As the vector of ToCV, the whitefly Bemisia tabaci Mediterranean (MED) is mainly responsible for the rapid spread of ToCV. The current understanding of tomato plant responses to this virus and B. tabaci is very limited. To understand the molecular mechanism of the interaction between tomato, ToCV and B. tabaci, we adopted a next-generation sequencing approach to decipher miRNAs and mRNAs that are differentially expressed under the infection of B. tabaci and ToCV in tomato plants. Our data revealed that 6199 mRNAs were significantly regulated, and the differentially expressed genes were most significantly associated with the plant-pathogen interaction, the MAPK signaling pathway, the glyoxylate, and the carbon fixation in photosynthetic organisms and photosynthesis related proteins. Concomitantly, 242 differentially expressed miRNAs were detected, including novel putative miRNAs. Sly-miR159, sly-miR9471b-3p, and sly-miR162 were the most expressed miRNAs in each sample compare to control group. Moreover, we compared the similarities and differences of gene expression in tomato plant caused by infection or co-infection of B. tabaci and ToCV. Taken together, the analysis reported in this article lays a solid foundation for further research on the interaction between tomato, ToCV and B. tabaci, and provide evidence for the identification of potential key genes that influences virus transmission in tomato plants.

SUBMITTER: Yue H

PROVIDER: S-EPMC8258350 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundWhiteflies threaten agricultural crop production worldwide, are polyphagous in nature, and transmit hundreds of plant viruses. Little is known how whitefly gene expression is altered due to feeding on plants infected with a semipersistently transmitted virus. Tomato chlorosis virus (ToCV; genus Crinivirus, family Closteroviridae) is transmitted by the whitefly (Bemisia tabaci) in a semipersistent manner and infects several globally important agricultural and ornamental crops, including tomato.ResultsTo determine changes in global gene regulation in whiteflies after feeding on tomato plants infected with a crinivirus (ToCV), comparative transcriptomic analysis was performed using RNA-Seq on whitefly (Bemisia tabaci MEAM1) populations after 24, 48, and 72 h acquisition access periods on either ToCV-infected or uninfected tomatoes. Significant differences in gene expression were detected between whiteflies fed on ToCV-infected tomato and those fed on uninfected tomato among the three feeding time periods: 447 up-regulated and 542 down-regulated at 24 h, 4 up-regulated and 7 down-regulated at 48 h, and 50 up-regulated and 160 down-regulated at 72 h. Analysis revealed differential regulation of genes associated with metabolic pathways, signal transduction, transport and catabolism, receptors, glucose transporters, α-glucosidases, and the uric acid pathway in whiteflies fed on ToCV-infected tomatoes, as well as an abundance of differentially regulated novel orphan genes. Results demonstrate for the first time, a specific and temporally regulated response by the whitefly to feeding on a host plant infected with a semipersistently transmitted virus, and advance the understanding of the whitefly vector-virus interactions that facilitate virus transmission.ConclusionWhitefly transmission of semipersistent viruses is believed to require specific interactions between the virus and its vector that allow binding of virus particles to factors within whitefly mouthparts. Results provide a broader understanding of the potential mechanism of crinivirus transmission by whitefly, aid in discerning genes or loci in whitefly that influence virus interactions or transmission, and subsequently facilitate development of novel, genetics-based control methods against whitefly and whitefly-transmitted viruses.

Project description:Tomato (Solanum lycopersicum L.) is a major Solanaceae crop worldwide and is vulnerable to bacterial wilt (BW) caused by Ralstonia solanacearum during the production process. BW has become a growing concern that could enormously deplete the tomato yield from 50 to 100% and decrease the quality. Research on the molecular mechanism of tomato regulating BW resistance is still limited. In this study, two tomato inbred lines (Hm 2-2, resistant to BW; and BY 1-2, susceptible to BW) were used to explore the molecular mechanism of tomato in response to R. solanacearum infection by RNA-sequencing (RNA-seq) technology. We identified 1923 differentially expressed genes (DEGs) between Hm 2-2 and BY 1-2 after R. solanacearum inoculation. Among these DEGs, 828 were up-regulated while 1095 were down-regulated in R-3dpi (Hm 2-2 at 3 days post-inoculation with R. solanacearum) vs. R-mock (mock-inoculated Hm 2-2); 1087 and 2187 were up- and down-regulated, respectively, in S-3dpi (BY 1-2 at 3 days post-inoculation with R. solanacearum) vs. S-mock (mock-inoculated BY 1-2). Moreover, Gene Ontology (GO) enrichment analysis revealed that the largest amount of DEGs were annotated with the Biological Process terms, followed by Cellular Component and Molecular Function terms. A total of 114, 124, 85, and 89 regulated (or altered) pathways were identified in R-3dpi vs. R-mock, S-3dpi vs. S-mock, R-mock vs. S-mock, and R-3dpi vs. S-3dpi comparisons, respectively, by Kyoto Encyclopaedia of Genes and Genomes (KEGG) pathway analysis. These clarified the molecular function and resistance pathways of DEGs. Furthermore, quantitative RT-PCR (qRT-PCR) analysis confirmed the expression patterns of eight randomly selected DEGs, which suggested that the RNA-seq results were reliable. Subsequently, in order to further verify the reliability of the transcriptome data and the accuracy of qRT-PCR results, WRKY75, one of the eight DEGs was silenced by virus-induced gene silencing (VIGS) and the defense response of plants to R. solanacearum infection was analyzed. In conclusion, the findings of this study provide profound insight into the potential mechanism of tomato in response to R. solanacearum infection, which lays an important foundation for future studies on BW.

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Integrated Analysis of microRNA and mRNA Transcriptome Reveals the Molecular Mechanism of Solanum lycopersicum Response to Bemisia tabaci and Tomato chlorosis virus.

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