MutS HOMOLOG1 mediates fertility reversion from cytoplasmic male sterile Brassica juncea in response to environment

• Published in: Plant, cell and environment cell and environment, 2021-01, Vol.44 (1), p.234-246
• Main Authors: Zhao, Na, Li, Zhangping, Zhang, Lili, Yang, Xiaodong, Mackenzie, Sally A., Hu, Zhongyuan, Zhang, Mingfang, Yang, Jinghua
• Format: Article
• Language: English
• Subjects: Brassica; Brassica juncea; carbonhydrate signal; Cytoplasmic male sterility; Ecological conditions; Fertility; fertility reversion; Gynodioecy; Homology; Mitochondria; MSH1; Plant reproduction; Pollination; pollination signal; Reproductive isolation; Reproductive strategy; Reversion; Signaling; Sugar; Transcription
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.13895

Spontaneous fertility reversion has been documented in cytoplasmic male sterile (CMS) plants of several species, influenced in frequency by nuclear genetic background. In this study, we found that MutS HOMOLOG1 (MSH1) mediates fertility reversion via substoichiometric shifting (SSS) of the CMS‐associated mitochondrial Open Reading Frame 220 (ORF220), a process that may be regulated by pollination signalling in Brassica juncea. We show that plants adjust their growth and development in response to unsuccessful pollination. Measurable decrease in MSH1 transcript levels and evidence of ORF220 SSS under non‐pollination conditions suggest that this nuclear‐mitochondrial interplay influences fertility reversion in CMS plants in response to physiological signals. Suppression of MSH1 expression induced higher frequency SSS in CMS plants than occurs normally. Transcriptional analysis of floral buds under pollination and non‐pollination conditions, and the response of MSH1 expression to different sugars, supports the hypothesis that carbon flux is involved in the pollination signalling of fertility reversion in CMS plants. Our findings suggest that facultative gynodioecy as a reproductive strategy may incorporate environmentally responsive genes like MSH1 as an “on–off” switch for sterility–fertility transition under ecological conditions of reproductive isolation. We show that the plant‐specific gene MutS HOMOLOG1 (MSH1) mediates fertility reversion by directing the substoichiometric shifting (SSS) of mitochondrial ORF220, a gene associated with cytoplasmic male sterility. The reversion process is influenced in frequency by pollination signaling in Brassica juncea. Our findings suggest that facultative gynodioecy is a reproductive strategy that incorporates environmental signals to regulate sterility‐fertility transitions under ecological conditions of reproductive isolation. These observations have important agricultural implications for selection and control of CMS as a hybrid seed production system.