GIF1 controls ear inflorescence architecture and floral development by regulating key genes in hormone biosynthesis and meristem determinacy in maize

Inflorescence architecture and floral development in flowering plants are determined by genetic control of meristem identity, determinacy, and maintenance. The ear inflorescence meristem in maize (Zea mays) initiates short branch meristems called spikelet pair meristems, thus unlike the tassel inflorescence, the ears lack long branches. Maize growth-regulating factor (GRF)-interacting factor1 (GIF1) regulates branching and size of meristems in the tassel inflorescence by binding to Unbranched3. However, the regulatory pathway of gif1 in ear meristems is relatively unknown. In this study, we found that loss-of-function gif1 mutants had highly branched ears, and these extra branches repeatedly produce more branches and florets with unfused carpels and an indeterminate floral apex. In addition, GIF1 interacted in vivo with nine GRFs, subunits of the SWI/SNF chromatin-remodeling complex, and hormone biosynthesis-related proteins. Furthermore, key meristem-determinacy gene RAMOSA2 (RA2) and CLAVATA signaling-related gene CLV3/ENDOSPERM SURROUNDING REGION (ESR) 4a (CLE4a) were directly bound and regulated by GIF1 in the ear inflorescence. Our findings suggest that GIF1 working together with GRFs recruits SWI/SNF chromatin-remodeling ATPases to influence DNA accessibility in the regions that contain genes involved in hormone biosynthesis, meristem identity and determinacy, thus driving the fate of axillary meristems and floral organ primordia in the ear-inflorescence of maize.

显花植物的花序构型与花发育过程，由分生组织身份、决定性及维持性的遗传调控机制所决定。玉米（Zea mays）的雌花序分生组织会起始产生被称为小穗对分生组织的短分支分生组织，因此与雄花序不同，雌穗不会产生长分支。玉米生长调控因子（growth-regulating factor，缩写GRF）互作因子1（GRF-interacting factor1，缩写GIF1）可通过结合Unbranched3，调控雄花序中分生组织的分支数量与大小。然而，GIF1在雌穗分生组织中的调控通路仍不甚明确。本研究发现，功能丧失型gif1突变体的雌穗出现严重分支过多的表型，这些额外分支会持续产生更多分支与小花，且心皮未融合、花序顶端失去决定性。此外，GIF1在体内可与9种GRF、SWI/SNF染色质重塑复合物的亚基，以及激素生物合成相关蛋白发生相互作用。进一步研究表明，关键分生组织决定性基因RAMOSA2 (RA2) 与CLAVATA信号通路相关基因CLV3/胚乳环绕区域（ENDOSPERM SURROUNDING REGION，缩写ESR）4a（CLE4a），可在玉米雌花序中被GIF1直接结合并调控。本研究结果提示，GIF1与GRFs协同作用，招募SWI/SNF染色质重塑ATP酶，以影响激素生物合成、分生组织身份及决定性相关基因所在区域的DNA可及性，进而驱动玉米雌花序中腋生分生组织与花器官原基的命运决定。