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Evolution of Lineage-Specific Gene Networks Underlying the Considerable Fruit Shape Diversity in Persimmon.

ABSTRACT: The shapes of plant organs reflect the evolution of each lineage and have been diversified according to lineage-specific adaptations to environment. Research on the molecular pathways responsible for organ shapes has traditionally been focused mainly on leaves or flowers. Thus, little is known about the pathways controlling fruit shapes, despite their diversity in some plant species. In this study, we analyzed oriental persimmon (Diospyros kaki), which exhibits considerable diversity in fruit shapes among cultivars, to elucidate the underlying molecular mechanism using transcriptomic data and quantitative evaluation. First, to filter the candidate genes associated with persimmon fruit shapes, the whole gene expression patterns obtained using mRNA-Seq analysis from 100 individuals, including a segregated population and various cultivars, were assessed to detect correlations with principal component scores for fruit shapes characterized with elliptic Fourier descriptors. Next, a gene co-expression network analysis with weighted gene co-expression network analysis (WGCNA) package revealed that class 1 KNOX family genes and SEEDSTICK function as integrators along with some phytohormone-related genes, to regulate the fruit shape diversity. On the other hand, the OVATE family genes also contribute to fruit shape diversity, of which pathway would be potentially shared with other plant species. Evolutionary aspects suggest that acquisition of a high lineage-specific and variable expression of class 1 KNOX gene, knotted-like homeobox of Arabidopsis thaliana 1 (KNAT1), in young fruit is important for establishing the persimmon-specific mechanism that determines fruit shape diversity.

SUBMITTER: Maeda H

PROVIDER: S-EPMC6839372 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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Evolution of Lineage-Specific Gene Networks Underlying the Considerable Fruit Shape Diversity in Persimmon.

Maeda Haruka H Akagi Takashi T Onoue Noriyuki N Kono Atsushi A Tao Ryutaro R

Plant & cell physiology 20191101 11

The shapes of plant organs reflect the evolution of each lineage and have been diversified according to lineage-specific adaptations to environment. Research on the molecular pathways responsible for organ shapes has traditionally been focused mainly on leaves or flowers. Thus, little is known about the pathways controlling fruit shapes, despite their diversity in some plant species. In this study, we analyzed oriental persimmon (Diospyros kaki), which exhibits considerable diversity in fruit sh ...[more]

PMID: 31350891

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Project description:Sex expression in plants is often flexible and contributes to the maintenance of genetic diversity within a species. In diploid persimmons (the genus Diospyros), the sexuality is controlled by the Y chromosome-encoded small-RNA gene, OGI, and its autosomal counterpart, MeGI. Hexaploid Oriental persimmon (Diospyros kaki) evolved more flexible sex expression, where genetically male individuals carrying OGI can produce both male and female flowers (monoecy). This is due to (semi-)inactivation of OGI by the Kali-SINE retrotransposon insertion on the promoter region and the resultant DNA methylations. Instead, flower sex determination in Oriental persimmon is also dependent on DNA methylation states of MeGI. Here, we focused on a cultivar, Kumemaru, which shows stable male flower production. Our results demonstrated that cv. Kumemaru carries OGI with Kali-SINE, which was highly methylated as well as in other monoecious cultivars; nevertheless, OGI gene could have a basal expression level. Transcriptomic analysis between cv. Kumemaru and 14 cultivars that predominantly produce female flowers showed differentially expressed genes (DEGs) specific to cv. Kumemaru, which is mainly involved in stress responses. Co-expression gene networks focusing on the DEGs also suggested the involvement of stress signals, mainly via gibberellin (GA), salicylic acid (SA), and especially jasmonic acid (JA) signal pathways. We also identified potential regulators of this co-expression module, represented by the TCP4 transcription factor. Furthermore, we attempted to identify cv. Kumemaru-specific transcript polymorphisms potentially contributing to derepressed OGI expression by cataloging subsequences (k-mers) in the transcriptomic reads from cv. Kumemaru and the other 14 female cultivars. Overall, although the direct genetic factor to activate OGI remains to be solved, our results implied the involvement of stress signals in the release of silenced OGI and the resultant continuous male production.

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Evolution of Lineage-Specific Gene Networks Underlying the Considerable Fruit Shape Diversity in Persimmon.

Publications

Evolution of Lineage-Specific Gene Networks Underlying the Considerable Fruit Shape Diversity in Persimmon.

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