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SiMADS34, an E-class MADS-box transcription factor, regulates inflorescence architecture and grain yield in Setaria italica

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A novel MADS-box member SiMADS34 is essential for regulating inflorescence architecture and grain yield in Setaria italica.

Abstract

MADS-box transcription factors participate in regulating various developmental processes in plants. Inflorescence architecture is one of the most important agronomic traits and is closely associated with grain yield in most staple crops. Here, we isolated a panicle development mutant simads34 from a foxtail millet (Setaria italica (L.) P. Beauv.) EMS mutant library. The mutant showed significantly altered inflorescence architecture and decreased grain yield. Investigation of agronomic traits revealed increased panicle width by 16.8%, primary branch length by 10%, and number of primary branches by 30.9%, but reduced panicle length by 25.2%, and grain weight by 25.5% in simads34 compared with wild-type plants. Genetic analysis of a simads34 × SSR41 F2 population indicated that the simads34 phenotype was controlled by a recessive gene. Map-based cloning and bulked-segregant analysis sequencing demonstrated that a single G-to-A transition in the fifth intron of SiMADS34 in the mutant led to an alternative splicing event and caused an early termination codon in this causal gene. SiMADS34 mRNA was expressed in all of the tissues tested, with high expression levels at the heading and panicle development stages. Subcellular localization analysis showed that simads34 predominantly accumulated in the nucleus. Transcriptome sequencing identified 241 differentially expressed genes related to inflorescence development, cell expansion, cell division, meristem growth and peroxide stress in simads34. Notably, an SPL14–MADS34–RCN pathway was validated through both RNA-seq and qPCR tests, indicating the putative molecular mechanisms regulating inflorescence development by SiMADS34. Our study identified a novel MADS-box member in foxtail millet and provided a useful genetic resource for inflorescence architecture and grain yield research.

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Acknowledgements

This work was supported by National Key R&D Program of China (Grant Nos. 2019YFD1000700 and 2019YFD1000704), the National Natural Science Foundation of China (31871692), Fundamental Research Funds of CAAS (S2018PY03 to Sha Tang), the China Agricultural Research System (CARS06-13.5-A04), and the Agricultural Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences. We thank Huw Tyson, PhD in Plant Biochemistry, graduated from University of Cambridge, for editing the English text of a draft of this manuscript.

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  1. Shareif Hammad Hussin, Hailong Wang, and Sha Tang have contributed equally to this work.

Authors and Affiliations

  1. Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing, 100081, China

    Shareif Hammad Hussin, Hailong Wang, Sha Tang, Hui Zhi, Chanjuan Tang, Wei Zhang, Guanqing Jia & Xianmin Diao

  2. Geneina Research Station, Agricultural Research Corporation (ARC), P.O. Box 126, Wad Madani, Sudan

    Shareif Hammad Hussin

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  1. Shareif Hammad Hussin
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Contributions

SHH, HW, HZ performed the molecular and field experiments; SHH, ST, CT, WZ extracted the data; SHH, ST analyzed the data; SHH, ST wrote the manuscript; SHH, ST, GJ were responsible for research methodology; ST, XD, HZ for review and editing; XD, ST for conceptualization, funding acquisition, supervision, project administration.

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Correspondence to Xianmin Diao.

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Hussin, S.H., Wang, H., Tang, S. et al. SiMADS34, an E-class MADS-box transcription factor, regulates inflorescence architecture and grain yield in Setaria italica. Plant Mol Biol 105, 419–434 (2021). https://doi.org/10.1007/s11103-020-01097-6

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