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OsMS1 functions as a transcriptional activator to regulate programmed tapetum development and pollen exine formation in rice

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OsMS1 functions as a transcriptional activator and interacts with known tapetal regulatory factors through its plant homeodomain (PHD) regulating tapetal programmed cell death (PCD) and pollen exine formation in rice.

Abstract

The tapetum, a hallmark tissue in the stamen, undergoes degradation triggered by PCD during post-meiotic anther development. This degradation process is indispensable for anther cuticle and pollen exine formation. Previous study has shown that PTC1 plays a critical role in the regulation of tapetal PCD. However, it remained unclear how this occurs. To further investigate the role of this gene in rice, we used CRISPR/Cas9 system to generate the homozygous mutant named as osms1, which showed complete male sterility with slightly yellow and small anthers, as well as invisible pollen grains. In addition, cytological observation revealed delayed tapetal PCD, defective pollen exine formation and a lack of DNA fragmentation according to a TUNEL analysis in the anthers of osms1 mutant. OsMS1, which encodes a PHD finger protein, was located in the nucleus of rice protoplasts and functioned as a transcription factor with transcriptional activation activity. Y2H and BiFC assays demonstrated that OsMS1 can interact with OsMADS15 and TDR INTERACTING PROTEIN2 (TIP2). It has been reported that TIP2 coordinated with TDR to modulate the expression of EAT1 and further regulated tapetal PCD in rice. Results of qPCR suggested that the expression of the genes associated with tapetal PCD and pollen wall biosynthesis, such as EAT1, AP37, AP25, OsC6 and OsC4, were significantly reduced in osms1 mutant. Taken together, our results demonstrate that the interaction of OsMS1 with known tapetal regulatory factors through its PHD finger regulates tapetal PCD and pollen exine formation in rice.

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Funding

This work was supported by the National Key Transform Program (#2016ZX08001-002), the National Natural Science Foundation of China (#31501290), the Zhejiang Provincial Natural Science Foundation of China (Grant #LQ14C130003), and the Super Rice Breeding Innovation Team and Rice Heterosis Mechanism Research Innovation Team of the Chinese Academy of Agricultural Sciences Innovation Project (CAAS-ASTIP-2013-CNRRI), Bill & Melinda Gates Foundation Project (OPP1130530).

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  1. Zhengfu Yang and Ling Liu contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory for Zhejiang Super Rice Research & State Key Laboratory of Rice Biology, China National Rice Research Institute, Hangzhou, 310006, China

    Zhengfu Yang, Ling Liu, Lianping Sun, Ping Yu, Peipei Zhang, Adil Abbas, Xiaojiao Xiang, Weixun Wu, Yingxin Zhang, Liyong Cao & Shihua Cheng

  2. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China

    Zhengfu Yang, Peipei Zhang & Xiaojiao Xiang

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  1. Zhengfu Yang
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Contributions

Study conception and design: YZF, LL, CLY, and CSH; acquisition of data: YZF, LL, SLP, and YP; analysis and interpretation of data: YZF, LL, ZPP and XXJ; drafting of manuscript: YZF, LL, YP, AA, WWX, ZYX, and CSH; critical revision: YZF, LL, CLY, and CSH. All authors have read and approved to submit it to your journal.

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Correspondence to Liyong Cao or Shihua Cheng.

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Yang, Z., Liu, L., Sun, L. et al. OsMS1 functions as a transcriptional activator to regulate programmed tapetum development and pollen exine formation in rice. Plant Mol Biol 99, 175–191 (2019). https://doi.org/10.1007/s11103-018-0811-0

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