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Putative Transcription Factor Genes Associated with Regulation of Carotenoid Biosynthesis in Chili Pepper Fruits Revealed by RNA-Seq Coexpression Analysis.

ABSTRACT: During the ripening process, the pericarp of chili pepper (Capsicum spp.) fruits accumulates large amounts of carotenoids. Although the carotenoid biosynthesis pathway in the Capsicum genus has been widely studied from different perspectives, the transcriptional regulation of genes encoding carotenoid biosynthetic enzymes has not been elucidated in this fruit. We analyzed RNA-Seq transcriptomic data from the fruits of 12 accessions of Capsicum annuum during the growth, development, and ripening processes using the R package named Salsa. We performed coexpression analyses between the standardized expression of genes encoding carotenoid biosynthetic enzymes (target genes (TGs)) and the genes of all expressed transcription factors (TFs). Additionally, we analyzed the promoter region of each biosynthetic gene to identify putative binding sequences for each selected TF candidate. We selected 83 TFs as putative regulators of the carotenogenic structural genes. From them, putative binding sites in the promoters of the carotenoid-biosynthesis-related structural genes were found for only 54 TFs. These results could guide the search for transcription factors involved in the regulation of the carotenogenic pathway in chili pepper fruits and might facilitate the collection of corresponding experimental evidence to corroborate their participation in the regulation of this biosynthetic pathway in Capsicum spp.

SUBMITTER: Villa-Rivera MG

PROVIDER: S-EPMC9569626 | biostudies-literature | 2022 Oct

REPOSITORIES: biostudies-literature

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Putative Transcription Factor Genes Associated with Regulation of Carotenoid Biosynthesis in Chili Pepper Fruits Revealed by RNA-Seq Coexpression Analysis.

Villa-Rivera Maria Guadalupe MG Martínez Octavio O Ochoa-Alejo Neftalí N

International journal of molecular sciences 20221004 19

During the ripening process, the pericarp of chili pepper (Capsicum spp.) fruits accumulates large amounts of carotenoids. Although the carotenoid biosynthesis pathway in the Capsicum genus has been widely studied from different perspectives, the transcriptional regulation of genes encoding carotenoid biosynthetic enzymes has not been elucidated in this fruit. We analyzed RNA-Seq transcriptomic data from the fruits of 12 accessions of Capsicum annuum during the growth, devel ...[more]

PMID: 36233073

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Project description:Chlorophylls and carotenoids are synthesized in the chloroplast and chromoplast, respectively. Even though the two pigments are generated from the same precursor, the genetic correlation between chlorophyll and carotenoid biosynthesis has not yet been fully understood. We investigated the genetic correlation of chlorophyll and carotenoid biosynthesis during fruit ripening. Two recombinant inbred lines populations, "Long Sweet" × "AC2212" ("LA") RILs derived from a cross between Capsicum annuum "Long Sweet" with light-green and light-red fruit and C. annuum "AC2212" with dark-green and brown-fruit and "3501 (F)" × "3509 (C)" ("FC") RILs from C. annuum "3501" with dark-green and dark-red fruit and C. annuum "3509" with intermediate green and light-red fruit, were used. As the fruit ripened, three accessions produced high levels of xanthophyll. The dark-green immature fruit accumulated more total carotenoids than the light-green fruit. This trend corresponded to the expression pattern of 1-deoxy-d-xylulose 5-phosphate synthase (DXS) and CaGLK2 genes during fruit development. The expression levels of DXS and CaGLK2 in the dark-green accession "3501" were significantly higher than those of "3509" and "Long Sweet" during the early stages of fruit development. Furthermore, the genotype analysis of the transcription factor controlling chloroplast development (CaGLK2) in LA RILs revealed that CaGLK2 expression affected both carotenoid and chlorophyll contents. The single nucleotide polymorphism (SNP) linkage maps were constructed using genotyping-by-sequencing (GBS) for the two populations, and QTL analysis was performed for green fruit color intensity and carotenoid content. The QTL (LA_BG-CST10) for capsanthin content in LA RILs located at 24.4 to 100.4 Mbp on chromosome 10 was overlapped with the QTL (FC15-Cap10) for capsanthin content in FC RILs. Three QTLs for capsanthin content, American spice trade association (ASTA) value, and immature green fruit color intensity were also overlapped from 178.2 to 204 Mbp on chromosome 10. At the location, 151.6 to 165 Mbp on chromosome 8, QTLs (FC15-tcar8, FC17-ASTA8.1, and FC17-ASTA8.2) for total carotenoid content and ASTA value were discovered, and this region contained 2-C-methyl-d-erythritol 4-phosphate cytidylyltransferase (MCT), which is involved in the MEP pathway. This result is the first report to show the correlation between carotenoid and chlorophyll biosynthesis in pepper. This research will expand our understanding of the mechanism of the chloroplast-to-chromoplast transition and the development of high pigment pepper varieties.

Project description:Background The set of all mRNA molecules present in a cell constitute the transcriptome. The transcriptome varies depending on cell type as well as in response to internal and external stimuli during development. Chili pepper is an economically and culturally important horticultural crop as well as a good model for the study of secondary metabolism during fruit development. Here we present a study of the changes that occur in the transcriptome of chili pepper fruit during development and ripening. Results RNA-Seq was used to obtain transcriptomes of whole Serrano-type chili pepper fruits (Capsicum annuum L.; 'Tampiqueno 74') collected at 10, 20, 40 and 60 days after anthesis (DAA). 15,550,468 Illumina MiSeq reads were assembled de novo into 34,066 chili genes. We classified the expression patterns of individual genes as well as genes grouped into Biological Process ontologies and Metabolic Pathway categories using statistical criteria. For the analyses of gene groups we added the weighted expression of individual genes. This method was effective in interpreting general patterns of expression changes and increased the statistical power of the analyses. Subsets of genes were expressed only at a single time point sampled (1,278, 1,596, 1,519 and 1,583 genes at 10, 20, 40 and 60 DAA, respectively). We also estimated the variation in diversity and specialization of the transcriptome during chili pepper development. Approximately 17% of genes exhibited a significant change of expression in at least one of the intervals sampled. In contrast, significant differences in approximately 63% of the Biological Processes and 80% of the Metabolic Pathways studied were detected in at least one interval. Confirming previous reports, genes related to capsaicinoid and ascorbic acid biosynthesis were significantly upregulated at 20 DAA while those related to carotenoid biosynthesis were highly expressed in the last period of fruit maturation (40-60 DAA). Our RNA-Seq data was validated by examining the expression of nine genes involved in carotenoid biosynthesis by qRT-PCR. Conclusions In general, more profound changes in the chili fruit transcriptome were observed in the intervals between 10 to 20 and 40 to 60 DAA. The last interval, between 40 to 60 DAA, included 49% of all significant changes detected, and was characterized predominantly by a global decrease in gene expression. This period signals the end of maturation and the beginning of senescence of chili pepper fruit. The transcriptome at 60 DAA was the most specialized and least diverse of the four states sampled.

Dataset Information

Putative Transcription Factor Genes Associated with Regulation of Carotenoid Biosynthesis in Chili Pepper Fruits Revealed by RNA-Seq Coexpression Analysis.

Publications

Putative Transcription Factor Genes Associated with Regulation of Carotenoid Biosynthesis in Chili Pepper Fruits Revealed by RNA-Seq Coexpression Analysis.

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