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Male sterile 28 encodes an ARGONAUTE family protein essential for male fertility in maize

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Abstract

Male sterility is a common biological phenomenon in plants and is a useful trait for hybrid seed production. Normal tapetum development is essential for viable pollen generation. Although many genes involved in tapetum differentiation and degradation have been isolated in maize, elements that regulate tapetum development during pollen mother cell (PMC) meiosis are less studied. Here, we characterized a classical male-sterile mutant male sterile 28 (ms28) in maize. The ms28 mutant had a regular male meiosis process, while its tapetum cells showed premature vacuolation at the early meiotic prophase stage. Using map-based cloning, we cloned the Ms28 gene and confirmed its role in male fertility in maize together with two allelic mutants. Ms28 encodes the ARGONAUTE (AGO) family protein ZmAGO5c, and its transcripts primarily accumulate in premeiosis anthers, with more intense signals in PMCs. Transcriptomic analysis revealed that genes related to anther development, cell division, and reproductive structure development processes were differentially expressed between the ms28 mutant and its fertile siblings. Moreover, small RNA (sRNA) sequencing revealed that the small interfering RNA (siRNA) and microRNA (miRNA) abundances were obviously changed in ms28 meiotic anthers, which indicated that Ms28 may regulate tapetal cell development through small RNA–mediated epigenetic regulatory pathways. Taken together, our results shed more light on the functional mechanisms of the early development of the tapetum for male fertility in maize.

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Abbreviations

AGO:

ARGONAUTE

CMS:

Cytoplasmic male sterility

DAPI:

4′,6-diamino-phenylindole

DEGs:

Differentially expressed genes

GMS:

Nuclear male sterility

miRNA:

microRNA

ms28:

Male sterile 28

phasiRNAs:

Phased secondary small interfering RNAs

PMCs:

Pollen mother cells

RISC:

RNA-induced silencing complexes

SEM:

Scanning electron microscopy

siRNA:

Small interfering RNA

sRNA:

Small RNA

TEM:

Transmission electron microscopy

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Acknowledgements

The authors thank the staff of the Maize Genetics Cooperation Stock Center for their help in providing germplasm.

Funding

This work was supported by the National Natural Science Foundation of China (Grant Nos. 31701430 to WH and 31801375 to YZ).

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Authors and Affiliations

  1. State Key Laboratory of Plant Physiology and Biochemistry, National Maize Improvement Center of China, Beijing Key Laboratory of Crop Genetic Improvement, Key Laboratory of Crop Heterosis and Utilization, Ministry of Education (MOE), China Agricultural University, Beijing, 100193, China

    Yunfei Li, Yumin Huang, Lingling Pan, Yue Zhao, Wei Huang & Weiwei Jin

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  1. Yunfei Li
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  2. Yumin Huang
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  3. Lingling Pan
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  4. Yue Zhao
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Contributions

WJ and WH conceived and supervised the project; YL and WH designed the experiments; YL carried out most of the experiments; YH performed the bioinformatic analysis; LP participated in cytogenetic analysis; YL, WH, and WJ analyzed the data and wrote the article; YZ helped with the manuscript preparation.

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Correspondence to Wei Huang or Weiwei Jin.

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Li, Y., Huang, Y., Pan, L. et al. Male sterile 28 encodes an ARGONAUTE family protein essential for male fertility in maize. Chromosome Res 29, 189–201 (2021). https://doi.org/10.1007/s10577-021-09653-6

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