The apple GARP family gene MdHHO3 regulates the nitrate response and leaf senescence

Binbin Wen; Binbin Wen; Xingyao Gong; Xingyao Gong; Wenpeng Deng; Wenpeng Deng; Xiude Chen; Xiude Chen; Xiude Chen; Dongmei Li; Dongmei Li; Dongmei Li; Xiling Fu; Xiling Fu; Xiling Fu; Ling Li; Ling Li; Ling Li; Qiuping Tan; Qiuping Tan; Qiuping Tan

doi:10.3389/fpls.2022.932767

Frontiers in Plant Science (Aug 2022)

The apple GARP family gene MdHHO3 regulates the nitrate response and leaf senescence

Binbin Wen,
Binbin Wen,
Xingyao Gong,
Xingyao Gong,
Wenpeng Deng,
Wenpeng Deng,
Xiude Chen,
Xiude Chen,
Xiude Chen,
Dongmei Li,
Dongmei Li,
Dongmei Li,
Xiling Fu,
Xiling Fu,
Xiling Fu,
Ling Li,
Ling Li,
Ling Li,
Qiuping Tan,
Qiuping Tan,
Qiuping Tan

Affiliations

Binbin Wen: College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an, China
Binbin Wen: State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, China
Xingyao Gong: College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an, China
Xingyao Gong: State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, China
Wenpeng Deng: College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an, China
Wenpeng Deng: State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, China
Xiude Chen: College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an, China
Xiude Chen: State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, China
Xiude Chen: Shandong Collaborative Innovation Center for Fruit and Vegetable Production With High Quality and Efficiency, Shandong Agricultural University, Tai’an, China
Dongmei Li: College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an, China
Dongmei Li: State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, China
Dongmei Li: Shandong Collaborative Innovation Center for Fruit and Vegetable Production With High Quality and Efficiency, Shandong Agricultural University, Tai’an, China
Xiling Fu: College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an, China
Xiling Fu: State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, China
Xiling Fu: Shandong Collaborative Innovation Center for Fruit and Vegetable Production With High Quality and Efficiency, Shandong Agricultural University, Tai’an, China
Ling Li: College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an, China
Ling Li: State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, China
Ling Li: Shandong Collaborative Innovation Center for Fruit and Vegetable Production With High Quality and Efficiency, Shandong Agricultural University, Tai’an, China
Qiuping Tan: College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an, China
Qiuping Tan: State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, China
Qiuping Tan: Shandong Collaborative Innovation Center for Fruit and Vegetable Production With High Quality and Efficiency, Shandong Agricultural University, Tai’an, China

DOI: https://doi.org/10.3389/fpls.2022.932767
Journal volume & issue: Vol. 13

Abstract

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The regulation of plant gene expression by nitrate is a complex regulatory process. Here, we identified 90 GARP family genes in apples by genome-wide analysis. As a member of the GARP gene family, the expression of MdHHO3 (Malus domestica HYPERSENSITIVITY TO LOW PHOSPHATE-ELICITED PRIMARY ROOT SHORTENING1 HOMOLOG 3) is upregulated under N (nitrogen) supply. The results of DNA-binding site analysis and electrophoretic mobility shift assays (EMSA) showed that MdHHO3 binds to the motif-containing GAATC. Furthermore, MdHHO3 binds to its promoter sequence and inhibits its activity. In addition, the overexpression of MdHHO3 in apple calli resulted in less accumulation of nitrate in 35S:MdHHO3-GFP calli and downregulated the expression of the nitrate transport-related genes but upregulated the expression of the nitrate assimilation-related genes. Similarly, the expression of the nitrate transport-related genes was downregulated and the expression of the nitrate assimilation-related genes was upregulated in MdHHO3 overexpression Arabidopsis and tobacco plants. Interaction experiments showed that MdHHO3 could bind to the promoter MdNRT2.1 (NITRATE TRANSPORTER 2.1) and negatively regulate its expression. Moreover, the exposure of MdHHO3-overexpressing Arabidopsis and tobacco to nitrate deficiency resulted in an early senescence phenotype as compared to the WT plants. These results show that MdHHO3 can not only negatively regulate nitrate accumulation in response to nitrate but also promote early leaf senescence under nitrate deficiency. This information may be useful to further reveal the mechanism of the nitrate response and demonstrates that nitrate deficiency induces leaf senescence in apples.

Published in Frontiers in Plant Science

ISSN: 1664-462X (Online)
Publisher: Frontiers Media S.A.
Country of publisher: Switzerland
LCC subjects: Agriculture: Plant culture
Website: https://www.frontiersin.org/journals/plant-science

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