Double-Locking Mechanism of Self-Compatibility in Arabidopsis thaliana: The Synergistic Effect of Transcriptional Depression and Disruption of Coding Region in the Male Specificity Gene

Keita Suwabe; Kaori Nagasaka; Endang Ayu Windari; Chihiro Hoshiai; Takuma Ota; Maho Takada; Ai Kitazumi; Hiromi Masuko-Suzuki; Yasuaki Kagaya; Kentaro Yano; Takashi Tsuchimatsu; Kentaro K Shimizu; Seiji Takayama; Go Suzuki; Masao Watanabe

doi:10.3389/fpls.2020.576140

Double-Locking Mechanism of Self-Compatibility in Arabidopsis thaliana: The Synergistic Effect of Transcriptional Depression and Disruption of Coding Region in the Male Specificity Gene

Front Plant Sci. 2020 Sep 11:11:576140. doi: 10.3389/fpls.2020.576140. eCollection 2020.

Authors

Affiliations

¹ Graduate School of Bioresources, Mie University, Tsu, Japan.
² Department of Plant and Soil Science, Texas Tech University, TX, United States.
³ Graduate School of Life Sciences, Tohoku University, Sendai, Japan.
⁴ Life Science Research Center, Mie University, Tsu, Japan.
⁵ School of Agriculture, Meiji University, Kawasaki, Japan.
⁶ Graduate School of Science, The University of Tokyo, Tokyo, Japan.
⁷ Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland.
⁸ Kihara Institute for Biological Studies, Yokohama City University, Yokohama, Japan.
⁹ Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan.
¹⁰ Division of Natural Science, Osaka Kyoiku University, Kashiwara, Japan.

Abstract

Self-compatibility in Arabidopsis thaliana represents the relatively recent disruption of ancestral obligate cross pollination, recognized as one of the prevalent evolutionary pathways in flowering plants, as noted by Darwin. Our previous study found that inversion of the male specificity gene (SP11/SCR) disrupted self-incompatibility, which was restored by overexpressing the SCR with the reversed inversion. However, SCR in A. thaliana has other mutations aside from the pivotal inversion, in both promoter and coding regions, with probable effects on transcriptional regulation. To examine the functional consequences of these mutations, we conducted reciprocal introductions of native promoters and downstream sequences from orthologous loci of self-compatible A. thaliana and self-incompatible A. halleri. Use of this inter-species pair enabled us to expand the scope of the analysis to transcriptional regulation and deletion in the intron, in addition to inversion in the native genomic background. Initial analysis revealed that A. thaliana has a significantly lower basal expression level of SCR transcripts in the critical reproductive stage compared to that of A. halleri, suggesting that the promoter was attenuated in inducing transcription in A. thaliana. However, in reciprocal transgenic experiments, this A. thaliana promoter was able to restore partial function if coupled with the functional A. halleri coding sequence, despite extensive alterations due to the self-compatible mode of reproduction in A. thaliana. This represents a synergistic effect of the promoter and the inversion resulting in fixation of self-compatibility, primarily enforced by disruption of SCR. Our findings elucidate the functional and evolutionary context of the historical transition in A. thaliana thus contributing to the understanding of the molecular events leading to development of self-compatibility.

Keywords: Arabidopsis thaliana; S-locus protein 11/S-locus cysteine rich protein gene; artificial chimeric gene; evolutionary process; flower development; promoter activity; self-compatibility.