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Parallel evolution of dominant pistil-side self-incompatibility suppressors in Arabidopsis.

ABSTRACT: Selfing is a frequent evolutionary trend in angiosperms, and is a suitable model for studying the recurrent patterns underlying adaptive evolution. Many plants avoid self-fertilization by physiological processes referred to as self-incompatibility (SI). In the Brassicaceae, direct and specific interactions between the male ligand SP11/SCR and the female receptor kinase SRK are required for the SI response. Although Arabidopsis thaliana acquired autogamy through loss of these genes, molecular evolution contributed to the spread of self-compatibility alleles requires further investigation. We show here that in this species, dominant SRK silencing genes have evolved at least twice. Different inverted repeat sequences were found in the relic SRK region of the Col-0 and C24 strains. Both types of inverted repeats suppress the functional SRK sequence in a dominant fashion with different target specificities. It is possible that these dominant suppressors of SI contributed to the rapid fixation of self-compatibility in A. thaliana.

SUBMITTER: Fujii S

PROVIDER: S-EPMC7075917 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Parallel evolution of dominant pistil-side self-incompatibility suppressors in Arabidopsis.

Fujii Sota S Shimosato-Asano Hiroko H Kakita Mitsuru M Kitanishi Takashi T Iwano Megumi M Takayama Seiji S

Nature communications 20200316 1

Selfing is a frequent evolutionary trend in angiosperms, and is a suitable model for studying the recurrent patterns underlying adaptive evolution. Many plants avoid self-fertilization by physiological processes referred to as self-incompatibility (SI). In the Brassicaceae, direct and specific interactions between the male ligand SP11/SCR and the female receptor kinase SRK are required for the SI response. Although Arabidopsis thaliana acquired autogamy through loss of these genes, molecular evo ...[more]

PMID: 32179752

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Project description:Self-incompatibility (SI) is a major issue in dragon fruit (Selenicereus spp.) breeding and production. Therefore, a better understanding of the dragon fruit SI mechanism is needed to improve breeding efficiency and ultimate production costs. To reveal the underlying mechanisms of SI in dragon fruit, plant anatomy, de novo RNA sequencing-based transcriptomic analysis, and multiple bioinformatic approaches were used to analyze gene expression in the pistils of the self-pollinated and cross-pollinated dragon fruit flowers at different intervals of time after pollination. Using fluorescence microscopy, we observed that the pollen of 'Hongshuijing', a self-incompatible dragon fruit variety (S. monacanthus), germinated on its own stigma. However, the pollen tube elongation has ceased at 1/2 of the style, confirming that dragon fruit experiences gametophyte self-incompatibility (GSI). We found that the pollen tube elongation in vitro was inhibited by self-style glycoproteins in the SI variety, indicating that glycoproteins were involved in SI. That is to say the female S factor should be homologous of S-RNase or PrsS (P. rhoeas stigma S factor), both of which are glycoproteins and are the female S factors of the two known GSI mechanism respectively. Bioinformatics analyses indicated that among the 43,954 assembled unigenes from pistil, there were six S-RNase genes, while 158 F-box genes were identified from a pollen transcriptomic dataset. There were no P. rhoeas type S genes discovered. Thus, the identified S-RNase and F-box represent the candidate female and male S genes, respectively. Analysis of differentially expressed genes (DEGs) between the self and cross-pollinated pistils at different time intervals led to the identification of 6,353 genes. We then used a weighted gene co-expression network analysis (WGCNA) to find some non-S locus genes in SI responses in dragon fruit. Additionally, 13 transcription factors (TFs) (YABBY4, ANL2, ERF43, ARF2, BLH7, KNAT6, PIF3, two OBF1, two HY5 and two LHY/CCA) were identified to be involved in dragon fruit GSI. Thus, we uncovered candidate S and non-S genes and predicted more SI-related genes for a more detailed investigation of the molecular mechanism of dragon fruit SI. Our findings suggest that dragon fruit possesses a GSI system and involves some unique regulators. This study lays the groundwork for future research into SI mechanisms in dragon fruit and other plant species.

Project description:BackgroundPollen-pistil interactions are an essential prelude to fertilization in angiosperms and determine compatibility/incompatibility. Pollen-pistil interactions have been studied at a molecular and cellular level in relatively few families. Self-incompatibility (SI) is the best understood pollen-pistil interaction at a molecular level where three different molecular mechanisms have been identified in just five families. Here we review studies of pollen-pistil interactions and SI in the Asteraceae, an important family that has been relatively understudied in these areas of reproductive biology.ScopeWe begin by describing the historical literature which first identified sporophytic SI (SSI) in species of Asteraceae, the SI system later identified and characterized at a molecular level in the Brassicaceae. Early structural and cytological studies in these two families suggested that pollen-pistil interactions and SSI were similar, if not the same. Recent cellular and molecular studies in Senecio squalidus (Oxford ragwort) have challenged this belief by revealing that despite sharing the same genetic system of SSI, the Brassicaceae and Asteraceae molecular mechanisms are different. Key cellular differences have also been highlighted in pollen-stigma interactions, which may arise as a consequence of the Asteraceae possessing a 'semi-dry' stigma, rather than the 'dry' stigma typical of the Brassicaceae. The review concludes with a summary of recent transcriptomic analyses aimed at identifying proteins regulating pollen-pistil interactions and SI in S. squalidus, and by implication the Asteraceae. The Senecio pistil transcriptome contains many novel pistil-specific genes, but also pistil-specific genes previously shown to play a role in pollen-pistil interactions in other species.ConclusionsStudies in S. squalidus have shown that stigma structure and the molecular mechanism of SSI in the Asteraceae and Brassicaceae are different. The availability of a pool of pistil-specific genes for S. squalidus offers an opportunity to elucidate the molecular mechanisms of pollen-pistil interactions and SI in the Asteraceae.

Dataset Information

Parallel evolution of dominant pistil-side self-incompatibility suppressors in Arabidopsis.

Publications

Parallel evolution of dominant pistil-side self-incompatibility suppressors in Arabidopsis.

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