Dose effects of restorer gene modulate pollen fertility in cotton CMS-D2 restorer lines via auxin signaling and flavonoid biosynthesis

Rong Zang; Kashif Shahzad; Xuexian Zhang; Liping Guo; Tingxiang Qi; Huini Tang; Ruijie Wang; Hailin Wang; Xiuqin Qiao; Meng Zhang; Jianyong Wu; Chaozhu Xing

doi:10.1007/s00299-023-03053-2

Dose effects of restorer gene modulate pollen fertility in cotton CMS-D2 restorer lines via auxin signaling and flavonoid biosynthesis

Plant Cell Rep. 2023 Nov;42(11):1705-1719. doi: 10.1007/s00299-023-03053-2. Epub 2023 Sep 16.

Authors

Rong Zang^#¹, Kashif Shahzad^#¹, Xuexian Zhang¹, Liping Guo¹, Tingxiang Qi¹, Huini Tang¹, Ruijie Wang¹, Hailin Wang¹, Xiuqin Qiao¹, Meng Zhang², Jianyong Wu³, Chaozhu Xing⁴

Affiliations

¹ National Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, Institute of Cotton Research of Chinese Academy of Agricultural Sciences, Key Laboratory for Cotton Genetic Improvement, Ministry of Agriculture and Rural Affairs, 38 Huanghe Dadao, Anyang, 455000, Henan, China.
² National Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, Institute of Cotton Research of Chinese Academy of Agricultural Sciences, Key Laboratory for Cotton Genetic Improvement, Ministry of Agriculture and Rural Affairs, 38 Huanghe Dadao, Anyang, 455000, Henan, China. zhangmeng03@caas.cn.
³ National Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, Institute of Cotton Research of Chinese Academy of Agricultural Sciences, Key Laboratory for Cotton Genetic Improvement, Ministry of Agriculture and Rural Affairs, 38 Huanghe Dadao, Anyang, 455000, Henan, China. dr.wujianyong@live.cn.
⁴ National Key Laboratory of Cotton Bio-Breeding and Integrated Utilization, Institute of Cotton Research of Chinese Academy of Agricultural Sciences, Key Laboratory for Cotton Genetic Improvement, Ministry of Agriculture and Rural Affairs, 38 Huanghe Dadao, Anyang, 455000, Henan, China. chaozhuxing@126.com.

^# Contributed equally.

PMID: 37715064
DOI: 10.1007/s00299-023-03053-2

Abstract

Dose effects of Rf₁ gene regulated retrieval mechanism of pollen fertility for CMS-D2 cotton. Cytoplasmic male sterility conditioned by Gossypium harknessii cytoplasm (CMS-D2) is an economical pollination control system for producing hybrid cotton seeds compared to artificial and chemical emasculation methods. However, the unstable restoring ability of restorer lines is a main barrier in the large-scale application of "three-line" hybrid cotton in China. Our phenotypic investigation determined that the homozygous Rf₁Rf₁ allelic genotype had a stronger ability to generate fertile pollen than the heterozygous Rf₁rf₁ allelic genotype. To decipher the genetic mechanisms that control the differential levels of pollen fertility, an integrated metabolomic and transcriptomic analysis was performed at two environments using pollen grains of four cotton genotypes differing in Rf₁ alleles or cytoplasm. Totally 5,391 differential metabolite features were detected, and 369 specific differential metabolites (DMs) were identified between homozygous and heterozygous Rf₁ allelic genotypes with CMS-D2 cytoplasm. In addition, transcriptome analysis identified 2,490 differentially expressed genes (DEGs) and 96 unique hub DEGs with dynamic regulation in this comparative combination. Further integrated analyses revealed that several key DEGs and DMs involved in indole biosynthesis, flavonoid biosynthesis, and sugar metabolism had strong network linkage with fertility restoration. In vitro application of auxin analogue NAA and inhibitor Auxinole confirmed that over-activated auxin signaling might inhibit pollen development, whereas suppressing auxin signaling partially promoted pollen development in CMS-D2 cotton. Our results provide new insight into how the dosage effects of the Rf₁ gene regulate pollen fertility of CMS-D2 cotton.

Keywords: Auxin signaling; CMS-D2; Cotton (Gossypium hirsutum L.); Dose effects; Flavonoid biosynthesis; Pollen fertility restoration.

Abstract

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