Barley TAPETAL DEVELOPMENT and FUNCTION1 (HvTDF1) gene reveals conserved and unique roles in controlling anther tapetum development in dicot and monocot plants

Hua, Miaoyuan; Yin, Wenzhe; Fernández Gómez, José; Tidy, Alison; Xing, Guangwei; Zong, Jie; Shi, Shuya; Wilson, Zoe A.

Abstract

The anther tapetum helps control microspore release and essential components for pollen wall formation. TAPETAL DEVELOPMENT and FUNCTION1 (TDF1) is an essential R2R3 MYB tapetum transcription factor in Arabidopsis thaliana; however, little is known about pollen development in the temperate monocot barley. Here, we characterize the barley (Hordeum vulgare L.) TDF1 ortholog using reverse genetics and transcriptomics. Spatial/temporal expression analysis indicates HvTDF1 has tapetum-specific expression during anther stage 7/8. Homozygous barley hvtdf1 mutants exhibit male sterility with retarded tapetum development, delayed tapetum endomitosis and cell wall degeneration, resulting in enlarged, vacuolated tapetum surrounding collapsing microspores. Transient protein expression and dual-luciferase assays show TDF1 is a nuclear-localized, transcription activator, that directly activates osmotin proteins. Comparison of hvtdf1 transcriptome data revealed several pathways were delayed, endorsing the observed retarded anther morphology. Arabidopsis tdf1 mutant fertility was recovered by HvTDF1, supporting a conserved role for TDF1 in monocots and dicots. This indicates that tapetum development shares similarity between monocot and dicots; however, barley HvTDF1 appears to uniquely act as a modifier to activate tapetum gene expression pathways, which are subsequently also induced by other factors. Therefore, the absence of HvTDF1 results in delayed developmental progression rather than pathway failure, although inevitably still results in pollen degeneration.

Citation

Hua, M., Yin, W., Fernández Gómez, J., Tidy, A., Xing, G., Zong, J., Shi, S., & Wilson, Z. A. (2023). Barley TAPETAL DEVELOPMENT and FUNCTION1 (HvTDF1) gene reveals conserved and unique roles in controlling anther tapetum development in dicot and monocot plants. New Phytologist, 240(1), 173-190. https://doi.org/10.1111/nph.19161

• Journal Article Type: Article
• Acceptance Date: Jun 20, 2023
• Online Publication Date: Aug 10, 2023
• Publication Date: 2023-10
• Deposit Date: Aug 12, 2023
• Publicly Available Date: Aug 14, 2023
• Journal: New Phytologist
• Print ISSN: 0028-646X
• Electronic ISSN: 1469-8137
• Publisher: Wiley
• Peer Reviewed: Peer Reviewed
• Volume: 240
• Issue: 1
• Pages: 173-190
• DOI: https://doi.org/10.1111/nph.19161
• Keywords: osmotin, anther, barley, TDF1, tapetum, transcriptome, male sterility, fertility
• Public URL: https://nottingham-repository.worktribe.com/output/24148908
• Publisher URL: https://nph.onlinelibrary.wiley.com/doi/10.1111/nph.19161