Male Sterility in Maize: A Precise Dialogue between the Mitochondria and Nucleus

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Male sterility has been widely utilized in plant hybrid breeding. Genic male sterility (GMS) and cytoplasmic male sterility (CMS) are two types of male sterility in plants. GMS is caused by nuclear genes alone, but CMS is determined by the mitochondrial genome, whereas the latter can be suppressed or counteracted by nuclear genes known as restorer-of-fertility (Rf) genes. In maize, three types (C, S, and T) of CMS have been identified according to their mitochondrial DNA genotypes and Rf genes. It has been reported previously that the co-transcribed orf355-orf77 region of the mitochondrial genome is associated with S-type CMS (CMS-S) in maize (Zabala et al., 1997Zabala G. Gabay-Laughnan S. Laughnan J.R. The nuclear gene Rf3 affects the expression of the mitochondrial chimeric sequence R implicated in S-type male sterility in maize.Genetics. 1997; 147: 847-860PubMed Google Scholar; Xiao et al., 2006Xiao H. Zhang F. Zheng Y. The 5′ stem-loop and its role in mRNA stability in maize S cytoplasmic male sterility.Plant J. 2006; 47: 864-872Crossref PubMed Scopus (13) Google Scholar). However, the regulatory mechanism underlying the interaction of mitochondrial-nuclear genes in CMS-S in maize remains largely unclear. In a recent study, Xiao et al., 2020Xiao S. Zang J. Pei Y. Liu J. Liu J. Song W. Shi Z. Su A. Zhao J. Chen H. Activation of mitochondrial orf355 gene expression by a nuclear-encoded DREB transcription factor causes cytoplasmic male sterility in maize.Mol. Plant. 2020; https://doi.org/10.1016/j.molp.2020.07.002Abstract Full Text Full Text PDF Scopus (2) Google Scholar identified orf355 as the causal gene of maize CMS-S. They discovered that the accumulation of orf355 transcripts in microspores caused mitochondrial abnormality and enhanced retrograde responses at the large vacuole stage in the CMS-S maize, which could significantly enhance the expression of genes involved in mitochondrial retrograde responses. Interestingly, through yeast one-hybrid screening, they identified a nuclear-encoded DREB family transcription factor, ZmDREB1.7, which could bind to the C-repeat/dehydration responsive (CRT/DRE) motif of orf355 promoter and promoted its transcription, indicating a role of ZmDREB1.7 in anterograde regulation. Furthermore, they found that the expression of ZmDREB1.7 was positively regulated by mitochondrial reactive oxygen species (ROS) signals. They identified some inbred lines with ZmDREB1.7 gene lacking the unfolded protein response (UPR) motif in its promoter. The expression of ZmDREB1.7 in these lines becomes unresponsive to mitochondrial ROS signals, but these lines could partially restore the fertility of S-type cytoplasm without the present of Rf3 restorer, suggesting that ZmDREB1.7 is involved in the sterility determination in CMS-S maize. In conclusion, this study reveals a novel regulatory module controlling male sterility of CMS-S maize, in which the nuclear-encoded ZmDREB1.7 regulates maize CMS by modulating the transcription of a mitochondrial gene orf355 and in turn the orf355-mediated mitochondrial retrograde signals enhance the expression of ZmDREB1.7, forming a positive feedback loop between the nucleus and mitochondria (Figure 1). The findings from this study shed new light on the regulation of plant male sterility and provide potential molecular targets for hybrid breeding in maize.