Exploiting Genic Male Sterility in Rice: From Molecular Dissection to Breeding Applications

Abstract

Rice (Oryza sativa L.) occupies a very salient and indispensable status among cereal crops, as its vast production is used to feed nearly half of the world's population. Male sterile plants are the fundamental breeding materials needed for specific propagation in order to meet the elevated current food demands. The development of the rice varieties with desired traits has become the ultimate need of the time. Genic male sterility is a predominant system that is vastly deployed and exploited for crop improvement. Hence, the identification of new genetic elements and the cognizance of the underlying regulatory networks affecting male sterility in rice are crucial to harness heterosis and ensure global food security. Over the years, a variety of genomics studies have uncovered numerous mechanisms regulating male sterility in rice, which provided a deeper and wider understanding on the complex molecular basis of anther and pollen development. The recent advances in genomics and the emergence of multiple biotechnological methods have revolutionized the field of rice breeding. In this review, we have briefly documented the recent evolution, exploration, and exploitation of genic male sterility to the improvement of rice crop production. Furthermore, this review describes future perspectives with focus on state-of-the-art developments in the engineering of male sterility to overcome issues associated with male sterility-mediated rice breeding to address the current challenges. Finally, we provide our perspectives on diversified studies regarding the identification and characterization of genic male sterility genes, the development of new biotechnology-based male sterility systems, and their integrated applications for hybrid rice breeding.

Keywords: anther and pollen development; biotechnology based male sterility systems; genic male sterility; hybrid breeding; regulatory mechanism; rice.

FIGURE 1

Genetic network of genic male sterility (GMS) genes for anther and pollen development including lipid and polysaccharide metabolism. E, epidermis; En, endothecium; ML, middle layer; T, tapetum; Sp, sporogenous cell; PMC, pollen mother cell; Ne, nexine; pm, plasma membrane; Te, tectum; ba, bacula; In, intine.

FIGURE 2

Molecular mechanism of fertility–sterility transition of environment-sensitive genic male sterility (EGMS) genes. (A) pms3 encodes a non-coding RNA long-day-specific male-fertility-associated RNA (LDMAR). The promoter generated psi-LDMAR follows RdDM pathway and increases DNA methylation of single-nucleotide polymorphism (SNP) carrying LDMAR resulting in secondary LDMAR structure, reduced transcript production, and male sterility under long-day (LD) conditions. While under short-day (SD) conditions, SNP does not affect transcript production and produces fertile pollen. (B) pms1 encodes a long non-coding RNA PMS1T. An SNP in the promoter of PMS1T affects the binding of miR2118 and produces higher level of 21-nt phased small-interfering RNAs (phasiRNAs), which then downregulates the target genes and cause male sterility under long-day (LD) condition. (C) miR2118 produces excess of U-rich 21-nt phasiRNAs, which, in coordination with AGO proteins, downregulates target genes and causes male sterility under SD conditions. Under LD conditions, fertility is restored. C, SNP; M, methylation; LD, long day; SG, short day; HT, high temperature; LT, low temperature; RdDM, RNA-directed DNA methylation; AGO, argonaute.

FIGURE 3

Molecular control of fertility–sterility transition of environment-sensitive genic male sterility (EGMS) genes. (A) TMS5 in TGMS lines encodes RNase Z^S1, which cleaves Ub_L40 messenger RNA (mRNA). The mutated tms5 does not encode RNase Z^S1 and is unable to cleave Ub_L40 mRNA. Higher accumulation of unprocessed Ub_L40 mRNA causes male sterility under high temperature (HT). Under low temperature, mutated tms5 encodes RNase Z^S1 and cleaves Ub_L40 mRNA to produce fertile pollen. (B) Overexpression plants of UPD-glucose pyrophosphorylase1 (Ugp1) produce abundance of unprocessed aberrant mRNA, which causes male sterility at high temperature (HT). Under low temperature (LT), the mRNA undergoes proper splicing and produces fertile pollen.

FIGURE 4

Integrative model of the epigenetic regulation of male sterility in rice. (A) Genetic disruption in epigenetic-related genes diverges DNA methylation pattern and causes impaired histone modification and unusual production of small-interfering RNAs (siRNAs). The divergent epigenetic pathways cause gene silencing/inability to activate target genes and cause male sterility. (B) The mutation in OsRDR6 causes increased production of 24-nt psiRNAs, which, in coordination with AGO proteins, downregulates target genes, affects DSB formation, and causes male sterility. RdDM, RNA-directed DNA methylation; Ac, acetylation; Ph, phosphorylation; Me, methylation; Ub, ubiquitination; MIR, microRNA locus; AGO, Argonaute; lncRNA, long non-coding RNA; dsRNA, double-stranded RNA; RISC, RNA-induced silencing complex.

FIGURE 5

Illustration of seed production technology (SPT) using transgenic construct-driven non-transgenic hybrid strategy in rice.

FIGURE 6

Work flow for the construction of transgenic male sterility. (A) Barbase/Barstar or Cysteine Protease/Cystatin. (B) Fertility restoration system. (C) Chemically induced male sterility system using argE gene.

FIGURE 7

Phytohormone genic male sterility system for two-line hybrid production. Exogenous application of MeJA on jasmonic-acid-deficient male sterile mutants rescues the fertile phenotype for sterile line propagation and hybrid production. JA, jasmonic acid; MeJA, methyl jasmonate.

FIGURE 8

Work flow for synthetic apomixes in rice. (A) Normal meiosis process promotes segregation and produces recombinant inbred embryo. (B) Triple mutant of BBM1, BBM2, and BBM3 triggers MiMe and causes embryo abortion during early fertilization in ovary, which can be rescued by male-transmitted BBM1 to produce asexual 2n seeds through parthenogenesis. (C) Triple mutant of PAIR1, OSD1, and REC8 promotes MiMe phenomenon to avoid fertilization. The MATL in quadruple mutant of MATL, PAIR1, OSD1, and REC8 promotes haploid production by eliminating parental chromosomes during fertilization and facilitates parthenogenesis to produce 2n asexual clonal seeds. MiMe, mitosis instead of meiosis.