RNase ZS1 processes UbL40 mRNAs and controls thermosensitive genic male sterility in rice

Abstract

Thermosensitive genic male-sterile (TGMS) lines, which are male-sterile at restrictive (high) temperatures but male-fertile at permissive (low) temperatures, have been widely used in breeding two-line hybrid rice (Oryza sativa L.). Here we find that mutation of thermosensitive genic male sterile 5 (tms5) in rice causes the TGMS trait through a loss of RNase Z S1 function. We show that RNase Z S1 processes the mRNAs of three ubiquitin fusion ribosomal protein L40 (Ub L40 ) genes into multiple fragments in vitro and in vivo. In tms5 mutants, high temperature results in increased levels of Ub L40 mRNAs. Overaccumulation of Ub L40 mRNAs causes defective pollen production and male sterility. Our results uncover a novel mechanism of RNase Z S1 -mediated Ub L40 mRNA regulation and shows that loss of this regulation produces TGMS in rice, a finding with potential applications in hybrid crop breeding.

Construction of a male sterility system for hybrid rice breeding and seed production using a nuclear male sterility gene

“…Photoperiod-sensitive and thermo-sensitive lines are the two major types of rice PTGMS germplasm resources (5)(6)(7)(8). Two widely used PTGMS genes have been cloned: one is a noncoding RNA gene (6,7), and the other codes for RNase Z S1 (8).…”

“…Two widely used PTGMS genes have been cloned: one is a noncoding RNA gene (6,7), and the other codes for RNase Z S1 (8). The male fertility of PTGMS lines is reversible in response to environmental conditions, which enables the PTGMS lines to propagate via selfpollination under environmental conditions restoring the male fertility and to outcross with restorer lines for hybrid seed production under conditions suppressing male fertility (5)(6)(7)(8). Because PTGMS traits are controlled by nuclear recessive genes and male fertility can be restored by any normal rice cultivars (5-8), broader genetic resources can be explored for strong heterosis (1,5).…”

Understanding a key gene for thermosensitive genic male sterility in rice

“…Recently, a joint research team led by Chuxiong Zhuang of South China Agricultural University and Xiaofeng Cao of Institute of Genetics and Development Biology, Chinese Academy of Sciences published their work on the cloning and molecular characterization of the gene thermosensitive genic male sterile 5 (tms5) in rice in Nature Communications [1]. This is the result of a long-term collaboration representing an important advance in male sterility research in crops.…”

Growth Phase-dependent Variation of RNase BN/Z Affects Small RNAs

“…These RNases generally participate in the 3Ј processing of tRNA precursors lacking an encoded CCA sequence, cleaving right after the discriminator nucleotide to generate a substrate for CCA addition by tRNA nucleotidyltransferase (1). In addition to tRNA precursors, some mRNAs have also been identified as substrates including some in rice (2) and Escherichia coli (3), raising the possibility of other putative substrates (4). This is of particular significance in E. coli, because the precursors of all 86 tRNAs already contain the CCA trinucleotide (5), obviating a need for the action of RNase Z.…”

“…Ribonucleases play an important role in cellular RNA metabolism, and recent studies have revealed that these enzymes may act as important regulators of small RNAs (sRNAs) 2 by participating in their maturation or turnover (12,13). 6S RNA, a stable sRNA, is an important transcription regulator that acts by binding to the sigma 70-containing holoenzyme of RNA polymerase (E 70 ) and reducing its activity (14).…”