RNase ZS1 Mediates UbL40 mRNAs Decay Controlling Thermo-Sensitive Genic Male Sterility in Rice

Male sterility is an important trait and plays a key role in hybrid breeding in crops. Thermo-sensitive genic male sterility (TGMS) lines, which are male-sterile at high temperatures but convert to male-fertile at low temperatures, have been widely used in two-line hybrid rice breeding. However, the molecular mechanism underlying TGMS remains unclear. Here, we show that a rice (Oryza sativa L.) thermo-sensitive genic male sterile gene 5 (tms5) locus confers the TGMS trait through a loss-of-function mutation of RNase Z^S1, which belongs to the metallo-β-lactamase superfamily, resulting in failing to mediate the mRNA decay of a temperature-responsive ubiquitin-encoding gene family. RNase Z^S1 is a short version of the RNase Z family originally involved in tRNA 3'-end processing in nucleus. RNase Z^S1 retains the endonuclease activity in tRNA processing in vitro, however, it does not play a role in vivo due to its localization in cytoplasm. RNase Z^S1 specifically cleaves the mRNAs of an ubiquitin-60S ribosomal protein L40 family. Defective RNase Z^S1 in tms5 plants leads to over accumulation of the Ubi_L40 mRNAs in young anthers at high but not at low temperature. Overexpression and RNAi of Ub_L40s in transgenic rice results in male sterility and restored fertility, respectively. Our results uncover a novel function of the RNase Z family member and reveal the molecular mechanism for rice TGMS by a new post-transcriptional regulatory machinery for ubiquitin homeostasis, an essential process for cell viability. Moreover, this study provides applied potential for not only rice but also other crops in hybrid breeding.