The miR3367–lncRNA67–GhCYP724B module regulates male sterility by modulating brassinosteroid biosynthesis and interacting with Aorf27 in Gossypium hirsutum

doi:10.1111/jipb.13802

J Integr Plant Biol. ›› 2025, Vol. 67 ›› Issue (1): 169-190.DOI: 10.1111/jipb.13802 cstr: 32098.14.jipb.13802

• Plant Reproductive Biology • Previous Articles

The miR3367–lncRNA67–GhCYP724B module regulates male sterility by modulating brassinosteroid biosynthesis and interacting with Aorf27 in Gossypium hirsutum

Anhui Guo^1†, Hushuai Nie^1†, Huijing Li¹, Bin Li¹, Cheng Cheng¹, Kaiyun Jiang¹, Shengwei Zhu², Nan Zhao¹ and Jinping Hua^1*

1. Laboratory of Cotton Genetics, Genomics and Breeding/Joint Laboratory for International Cooperation in Crop Molecular Breeding, Ministry of Education/Beijing Key Laboratory of Crop Genetic Improvement, College of Agronomy and Biotechnology, China Agricultural University, Beijing 100193, China
2. Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China
^†These authors contributed equally.
^*Correspondence: Jinping Hua (jinping_hua@cau.edu.cn)

Received:2024-05-02 Accepted:2024-09-16 Online:2024-11-11 Published:2025-01-01
Supported by:
This work was supported by the National Natural Science Foundation of China (32372128 to J.H., 32201713 to A.G.), and the China Postdoctoral Science Foundation (2020M680766 to H.N.).

Abstract

Abstract: Cytoplasmic male sterile (CMS) lines play a crucial role in utilization of heterosis in crop plants. However, the mechanism underlying the manipulation of male sterility in cotton by long non-coding RNA (lncRNA) and brassinosteroids (BRs) remains elusive. Here, using an integrative approach combining lncRNA transcriptomic profiles with virus-induced gene silencing experiments, we identify a flower bud-specific lncRNA in the maintainer line 2074B, lncRNA67, negatively modulating with male sterility in upland cotton (Gossypium hirsutum). lncRNA67 positively regulates cytochrome P274B (GhCYP724B), which acted as an eTM (endogenous target mimic) for miR3367. The suppression of GhCYP724B induced symptoms of BR deficiency and male semi-sterility in upland cotton as well as in tobacco, which resulted from a reduction in the endogenous BR contents. GhCYP724B regulates BRs synthesis by interacting with GhDIM and GhCYP90B, two BRs biosynthesis proteins. Additionally, GhCYP724B suppressed a unique chimeric open reading frame (Aorf27) in 2074A mitochondrial genome. Ectopic expression of Aorf27 in yeast inhibited cellular growth, and over expression of Aorf27 in tobacco showed male sterility. Overall, the results proved that the miR3367–lncRNA67–GhCYP724B module positively regulates male sterility by modulating BRs biosynthesis. The findings uncovered the function of lncRNA67–GhCYP724B in male sterility, providing a new mechanism for understanding male sterility in upland cotton.

Key words: brassinosteroids, GhCYP724B, lncRNA67, male sterility, mitochondrial Aorf27, upland cotton (G. hirsutum)

Anhui Guo, Hushuai Nie, Huijing Li, Bin Li, Cheng Cheng, Kaiyun Jiang, Shengwei Zhu, Nan Zhao, Jinping Hua. The miR3367–lncRNA67–GhCYP724B module regulates male sterility by modulating brassinosteroid biosynthesis and interacting with Aorf27 in Gossypium hirsutum[J]. J Integr Plant Biol., 2025, 67(1): 169-190.

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The miR3367–lncRNA67–GhCYP724B module regulates male sterility by modulating brassinosteroid biosynthesis and interacting with Aorf27 in Gossypium hirsutum

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