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Transgenerational conditioned male fertility of HD-ZIP IV transcription factor mutant ocl4: impact on 21-nt phasiRNA accumulation in pre-meiotic maize anthers

Abstract

Key message

Maize Outer cell layer 4 (ocl4) encodes an HD-ZIP IV transcription factor required for robust male fertility and 21-nt phasiRNA biogenesis. ocl4 fertility is favored in warm conditions, and phasiRNAs are partially restored.

Abstract

Environment-sensitive male-sterile plants have been described before and can result from different molecular mechanisms and biological processes, but putative environment-conditioned, transgenerational rescue of their male fertility is a rather new mystery. Here, we report a derivative line of the male-sterile outer cell layer 4 (ocl4) mutant of maize, in which fertility was restored and perpetuated over several generations. Conditioned fertile ocl4 anthers exhibit the anatomical abnormality of a partially duplicated endothecial layer, just like their sterile counterparts. We profiled the dynamics of phased, small interfering RNAs (phasiRNAs) during pre-meiotic development in fully sterile and various grades of semi-fertile ocl4 anthers. The conditioned fertile anthers accumulated significantly higher 21-nt phasiRNAs compared to ocl4 sterile samples, suggesting a partial restoration of phasiRNAs in conditioned fertility. We found that the biogenesis of 21-nt phasiRNAs is largely dependent on Ocl4 at three key steps: (1) production of PHAS precursor transcripts, (2) expression of miR2118 that modulates precursor processing, and (3) accumulation of 21-nt phasiRNAs.

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Availability of data and materials

The data reported in this paper have been deposited in the Gene Expression Omnibus (GEO) database, Series GSE150446, accession nos. GSM4550675 to GSM4550682 for RNA-seq data, GSM4550683 to GSM4550690 for small RNA data.

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Funding

This study was supported by U.S. National Science Foundation Plant Genome Research Project (Award # 1754097) to BCM and VW. PY was supported by a Fulbright-Nehru grant from United-States India Educational Foundation (Award No. 2200/FNPDR/2016).

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Correspondence to Virginia Walbot.

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Yadava, P., Tamim, S., Zhang, H. et al. Transgenerational conditioned male fertility of HD-ZIP IV transcription factor mutant ocl4: impact on 21-nt phasiRNA accumulation in pre-meiotic maize anthers. Plant Reprod 34, 117–129 (2021). https://doi.org/10.1007/s00497-021-00406-3

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Keywords

  • Male sterility
  • Conditioned fertility
  • PhasiRNA
  • Ocl4
  • Maize