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Cyclin-Dependent Kinase Inhibitor Gene TaICK1 acts as a Potential Contributor to Wheat Male Sterility induced by a Chemical Hybridizing Agent.

ABSTRACT: Heterosis has been widely accepted as an effective strategy to increase yields in plant breeding. Notably, the chemical hybridization agent SQ-1 induces male sterility in wheat, representing a critical potential tool in hybrid seed production. However, the mechanisms underlying the male sterility induced by SQ-1 still remain poorly understood. In this study, a cyclin-dependent kinase inhibitor gene, TaICK1, which encodes a 229 amino acid protein, was identified as a potential contributor to male sterility in common wheat. The expression of TaICK1 was upregulated during the development of anthers in Xinong1376 wheat treated with SQ-1. Meanwhile, the seed setting rate was found to be significantly decreased in TaICK1 transgenic rice. Furthermore, we identified two cyclin proteins, TaCYCD2;1 and TaCYCD6;1, as interactors through yeast two-hybrid screening using TaICK1 as the bait, which were validated using bimolecular fluorescence complementation. Subcellular localization revealed that the proteins encoded by TaICK1, TaCYCD2;1, and TaCYCD6;1 were localized in the cell nucleus. The expression levels of TaCYCD2;1 and TaCYCD6;1 were lower in Xinong1376 treated with SQ-1. A further analysis demonstrated that the expression levels of OsCYCD2;1 and OsCYCD6;1 were lower in transgenic TaICK1 rice lines as well. Taken together, these results suggest that the upregulation of TaICK1, induced by SQ-1, may subsequently suppress the expression of TaCYCD2;1 and TaCYCD6;1 in anthers, resulting in male sterility. This study provides new insights into the understanding of SQ-1-induced wheat male sterility, as well as the developmental mechanisms of anthers.

SUBMITTER: Zhang L

PROVIDER: S-EPMC7177297 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Cyclin-Dependent Kinase Inhibitor Gene <i>TaICK1</i> acts as a Potential Contributor to Wheat Male Sterility induced by a Chemical Hybridizing Agent.

Zhang Lili L Wang Chaojie C Yu Yongang Y Zhang Yamin Y Song Yulong Y Li Zheng Z Wang Shuping S Zhang Yanfang Y Guo Xiaofeng X Liu Dan D Li Ziliang Z Ma Shoucai S Zheng Jinjuan J Zhao Huiyan H Zhang Gaisheng G

International journal of molecular sciences 20200402 7

Heterosis has been widely accepted as an effective strategy to increase yields in plant breeding. Notably, the chemical hybridization agent SQ-1 induces male sterility in wheat, representing a critical potential tool in hybrid seed production. However, the mechanisms underlying the male sterility induced by SQ-1 still remain poorly understood. In this study, a cyclin-dependent kinase inhibitor gene, <i>TaICK1</i>, which encodes a 229 amino acid protein, was identified as a potential contributor ...[more]

PMID: 32252420

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Project description:Chemical hybridization agent (CHA)-induced male sterility is becoming one of the most useful tools for the crop heterosis in seed production. We had previously discovered monosulfuron ester sodium (Mes), an acetolactate synthase (ALS) inhibitor of the herbicide sulfonylurea family, could induce rapeseed (Brassica napus L.) male sterility. To investigate the mechanism of Mes inducing male sterility, a cytological analysis and comparative transcriptome analysis were performed between Mes-treated plants leaves and different developmental stage anthers and those of the Mock-treated plants. Cytological analysis exhibited that Mes destroyed plastids ultrastructure and depressed the materials accumulation during anther development and maturation process. Comparative transcriptome analysis identified a total of 1501 transcripts differentially expressed in the leaves and different developmental stage anthers. Subcellular localization analysis, functional analysis and pathway analysis were carried out to obtain the clues that plastid was the seriously damaged organelle, and many genes involved in carbon and lipid metabolism and cellular transport differentially expressed. Detailed expression pattern analysis of genes related with these functions were conducted and verified by RT-PCR. In addition, several transcription factors, protein kinases and hormone related genes were identified. Carbohydrate content analysis confirmed carbon metabolism were influenced by Mes. Taken together, we proposed a putative action mode that Mes inhibited activity of acetolactate synthase, which localized in plastid in plants, and then disturbed the normal supply of carbon and lipid metabolite for anther development, finally displayed male sterility. This results have important significance for uncovering the metabolic gene regulation during anther development and may provide more potential targets for developing new male sterility inducing CHAs in rapeseed breeding. Rapeseed (Brassica napus L.) plants were foliar sprayed with 0.1Î¼g mL-1 Monosulfuron ester sodium (Mes) solution containing 50ppm DMF and 5ppm Tween 80 for about 15 ml per plant. Young leaves (C2Y1, C2Y2, C2Y3; T2Y1, T2Y2, T2Y3) of the main inflorescences and developing anthers (including small buds (C2S1, C2S2, C2S3; T2S1, T2S2, T2S3), middle anthers (C2M1, C2M2, C2M3; T2M1, T2M2, T2M3), and large anthers (C2L1, C2L2, C2L3; T2L1, T2L2, T2L3)) from Mes-treated and Mock-treated plants were collected for each experiment. Each tissue has three independent biological replicates.

Dataset Information

Cyclin-Dependent Kinase Inhibitor Gene TaICK1 acts as a Potential Contributor to Wheat Male Sterility induced by a Chemical Hybridizing Agent.

Publications

Cyclin-Dependent Kinase Inhibitor Gene <i>TaICK1</i> acts as a Potential Contributor to Wheat Male Sterility induced by a Chemical Hybridizing Agent.

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