Rui Xu, Xianglan Yin, Keli Qiu, Jianyu Li, Lingling Li, Jiankai Zhou, Hao Li, Xueyang Dang, Wenjing Xu, Jiale Zhang, Biao Xie, Weina Si, Yang Feng, Zhengpeng Ren, Zhong Zhao, Pengcheng Wei, Beijiu Cheng, Yunfei Li, Haiyang Jiang, Pengfei Jiang
Efficient hybrid seed production requires controllable male sterility systems, yet how developmental processes can be selectively manipulated to disrupt male fertility while preserving vegetative growth remains poorly understood. Whether filament elongation represents a distinct hormonal sensitivity checkpoint and how its regulation can be exploited to uncouple male fertility from vegetative growth remain largely unknown. Here, we identify a series of gibberellin-sensitive genic male sterililty (GGMS) mutants carrying allelic variations in the maize GA biosynthetic gene ZmKAO. Unlike previously characterized GA-deficient mutants with broad defects in reproductive development, ggms mutants exhibit male sterility primarily due to defective filament elongation, while anther development, pollen maturation, and female fertility remain largely unaffected even under severe GA deficiency. Notably, filament elongation in GGMS mutants can be restored by a single GA application after tasseling. Genetic, biochemical, and molecular analyses support a model in which reduced D9 accumulation relieves D9-mediated repression of the filament-preferential transcription factor ZmMYB53, thereby enhancing ZmBXL7 expression and promoting filament cell elongation. Quantification of endogenous GA levels across a series of ZmKAO alleles with different functional strengths reveals a graded relationship between GA reduction and developmental outputs. While strong alleles (ggms1/2) cause severe growth defects, weak alleles (ggms3/4) uncouple vegetative growth from male fertility by selectively disrupting filament elongation. Based on these findings, we propose a three-threshold model in which different developmental processes exhibit distinct sensitivities to GA reduction. This framework enables rational selection and engineering of GGMS materials for maize hybrid seed production. Together, our study reveals a hierarchical GA sensitivity mechanism underlying maize reproductive development and provides both conceptual insights into hormone-regulated fertility and practical strategies for engineering controllable GGMS systems in maize.