Key divisions and cell specification during embryo pattern formation require SMU1-mediated splicing of <i>CAK</i> genes in Arabidopsis

Xiaoyi Huang; Yue Liu; Yajun Cai; Xiaogang Long; Emily Xu; Xiaoming Zhong; Jingyuan Zhang; Man Wang; Guoyong Xu; Peng Zhao; Kun Wang; Limin Pi; Arp Schnittger; Hongchun Yang

doi:10.1016/j.jgg.2025.10.008

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Key divisions and cell specification during embryo pattern formation require SMU1-mediated splicing of CAK genes in Arabidopsis

doi: 10.1016/j.jgg.2025.10.008

a. State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, Hubei 430072, China;
b. Hubei Hongshan Laboratory, Wuhan, Hubei 430070, China;
c. College of Literature, Science and Arts, University of Michigan, Ann Arbor, Michigan 48109, USA;
d. State Key Laboratory of Hybrid Rice, Institute for Advanced Studies (IAS), Wuhan University, Wuhan, Hubei 430072, China;
e. Department of Developmental Biology, University of Hamburg, Hamburg D-22609, Germany;
f. RNA Institute, Wuhan University, Wuhan, Hubei 430072, China

Funds:

We thank Liping Niu, Qin Lu, and Xinlian Liu from the Core Facility of State Key Laboratory of Hybrid Rice and Wenxuan Zou from the Core Facility of College of Life Sciences at Wuhan University for their technical support

Professor Yangjie Hu and Xiongbo Peng (Wuhan University) for critical reading and comments, and all the members of the Yang research group for discussions. This work was supported by the National Natural Science Foundation of China (32570654 and 32370619), the earmarked fund for China Agriculture Research System (CARS) (CARS-01-02), the Natural Science Foundation of Hubei Province (2024AFA010 and 2024AFE007), and Hubei Hongshan Laboratory.

Received Date: 2025-08-29
Accepted Date: 2025-10-26
Rev Recd Date: 2025-10-18

Available Online: 2025-11-14

Abstract

Abstract

Embryonic pattern formation and cell specification require precise cell division and cell cycle regulation. Splicing factors and the splicing of precursor mRNA (pre-mRNA) play significant roles in embryo development. However, how splicing factors control embryonic patterning via RNA splicing remains unclear. Here, we show that the mutation of SUPPRESSORS OF MEC-8 AND UNC-52 1 (SMU1), a conserved subunit of the spliceosomal B complex, causes compromised cell fate of the hypophysis and quiescent center (QC), failed embryonic root apical meristem (RAM) formation, as evidenced by altered WUSCHEL-RELATED HOMEOBOX 5 (WOX5) expression and perturbed auxin signaling. This results in smu1 embryo lethality. The splicing efficiency of three out of four CYCLIN-DEPENDENT KINASE ACTIVATOR (CAK) genes is decreased, leading to reduced protein levels in smu1 embryos. These CAK genes are required for hypophysis specification and embryonic RAM formation. SMU1 binds CAK transcripts in vitro and in vivo. Restoring the expression of either CAK gene partially rescues the defects in smu1 embryos, leading to the formation of QC-like cells, continued embryo development, and even the production of viable seeds. Our data suggest that SMU1 binds to CAK transcripts and promotes their splicing, enabling cell cycle progression to promote embryonic RAM formation.
- SMU1,
- CDK-ACTIVATING KINASES (CAKs),
- RNA splicing,
- Embryonic pattern formation,
- Cell cycle,
- Auxin,
- Quiescent center (QC)

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