Plant genic male sterility genes and their molecular regulatory mechanisms

Plant genic male sterile (GMS) mutants constitute indispensable germplasm resources for advancing fundamental theories in plant reproductive developmental biology and enhancing crop heterosis utilization. Anther and pollen development represent an intricately regulated biological process requiring precise coordination between sporophytic and gametophytic genes. Dysregulation or functional impairment of key genes governing these processes frequently results in GMS phenotypes. Comprehensive characterization of GMS genes—encompassing their identification, mechanism elucidation, and regulatory network construction—holds critical significance for deciphering developmental cascades in microsporogenesis while enabling the engineering of next-generation biotechnological male sterility (BMS) systems. Notable applications include maize multiple-control sterility (MCS) and dominant GMS (DGMS) systems, as well as the two-line hybrid breeding paradigm in rice and other cereals. This review summarizes current knowledge on GMS gene classification, functional characterization, spatiotemporal expression profiles, and molecular regulatory mechanisms across three model plant species (Arabidopsis, rice, and maize), with particular emphasis on emerging insights into environment-sensitive GMS (EGMS) systems. Functional categorization reveals GMS genes primarily participate in archesporial cell specification, anther somatic cell differentiation, tapetum development and pollen mother cell meiosis, pollen maturation and anther dehiscence. These genes are predominantly associated with four functional modules: transcription factors (TFs; 53 genes), lipid metabolism (62 genes), carbohydrate metabolism (27 genes), and other processes (37 genes), based on comparative analysis of 76 Arabidopsis, 52 rice, and 51 maize GMS genes. Notably, lipid metabolism-associated genes constitute the largest functional cohort (42.3%), followed by transcriptional regulators (35.9%), underscoring their pivotal roles in pollen wall formation and anther development. Evolutionarily conserved orthologs were identified across all three plant species, with 34 homologous gene clusters demonstrating functional conservation during microgametogenesis. This phylogenetic conservation provides critical guidance for reverse-genetic identification of GMS candidates in non-model plant species through genome editing approaches. Current models propose a hierarchical regulatory framework wherein TF cascades coordinate downstream metabolic networks—particularly lipid and carbohydrate biosynthesis pathways—to orchestrate anther development. EGMS systems exhibit conditional fertility transitions mediated by specific environmental cues, including photoperiod/thermo-sensitive GMS (P/TGMS) and humidity-sensitive GMS (HGMS). Fertility restoration of P/TGMS under permissive conditions correlates with developmental rate modulation and reactive oxygen species (ROS) homeostasis during pollen maturation, whereas that of HGMS under elevated humidity involves restoration of pollen dehydration-hydration dynamics and cell wall plasticity. Notably, persisting limitations include fragmented understanding of early (archesporial initiation) and late (anther dehiscence) developmental phases, necessitating systems-level investigations to complete the molecular continuum of microsporogenesis. We propose a paradigm shift from reductionist gene characterization to integrative network biology, leveraging emerging technologies, such as the CRISPR-based multiplex editing for synthetic sterility circuits, single-cell omics for spatiotemporal regulatory mapping and AI-driven network modeling to predict epistatic interactions. Such multidisciplinary integration will catalyze the transition from conventional single-gene BMS designs to programmable sterility systems governed by synthetic genetic networks. This review provides both theoretical foundations for plant reproductive biology and feasible frameworks for engineering new male sterility systems in crop improvement programs.