ZmMs33 promotes anther elongation via modulating cell elongation regulators, metabolic homeostasis, and cell wall remodeling in maize

Plant cell elongation depends on well-defined gene regulations, adequate nutrients, and timely cell wall modifications. Anther size is positively correlated with the number and viability of pollen grains, while little is known about molecular mechanisms underlying anther cell elongation. Here, we found that properly activated cell elongation regulators at transcriptional levels in loss-of-function ZmMs33 mutant (ms33-6038) anthers failed to promote maize anther elongation. ZmMs33 deficiency disrupted metabolic homeostasis mainly by inhibiting both photosynthesis in anther endothecium and lipid accumulation in anther tapetum. Importantly, ms33-6038 anthers displayed ectopic, premature and excessive secondary cell wall thickening in anther middle layer, which constrained cell elongation structurally and blocked nutrient flows across different anther wall layers. The metabolic disorder was only found in ms33-6038 mutant rather than several representative male-sterility lines at transcriptional and post-translational levels. Collectively, the disordered metabolisms and blocked nutrient flows defeated the activated cell elongation regulators, and finally inhibited anther elongation and growth with a unique “idling effect” in ms33-6038 mutant.