A molecular framework underlying low-nitrogen-induced early leaf senescence in Arabidopsis thaliana

Hongmei Fan; Shuxuan Quan; Qing Ye; Lei Zhang; Wei Liu; Ning Zhu; Xiaoqi Zhang; Wenyuan Ruan; Keke Yi; Nigel M Crawford; Yong Wang

doi:10.1016/j.molp.2023.03.006

A molecular framework underlying low-nitrogen-induced early leaf senescence in Arabidopsis thaliana

Mol Plant. 2023 Apr 3;16(4):756-774. doi: 10.1016/j.molp.2023.03.006. Epub 2023 Mar 11.

Authors

Hongmei Fan¹, Shuxuan Quan¹, Qing Ye¹, Lei Zhang¹, Wei Liu¹, Ning Zhu¹, Xiaoqi Zhang¹, Wenyuan Ruan², Keke Yi², Nigel M Crawford³, Yong Wang⁴

Affiliations

¹ State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Tai'an, Shandong 271018, China.
² Key Laboratory of Plant Nutrition and Fertilizer, Ministry of Agriculture, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 10081, China.
³ Section of Cell and Developmental Biology, Division of Biological Science, University of California at San Diego, La Jolla, CA 92093-0116, USA.
⁴ State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Tai'an, Shandong 271018, China. Electronic address: wangyong@sdau.edu.cn.

PMID: 36906802
DOI: 10.1016/j.molp.2023.03.006

Abstract

Nitrogen (N) deficiency causes early leaf senescence, resulting in accelerated whole-plant maturation and severely reduced crop yield. However, the molecular mechanisms underlying N-deficiency-induced early leaf senescence remain unclear, even in the model species Arabidopsis thaliana. In this study, we identified Growth, Development and Splicing 1 (GDS1), a previously reported transcription factor, as a new regulator of nitrate (NO₃^-) signaling by a yeast-one-hybrid screen using a NO₃^- enhancer fragment from the promoter of NRT2.1. We showed that GDS1 promotes NO₃^- signaling, absorption and assimilation by affecting the expression of multiple NO₃^- regulatory genes, including Nitrate Regulatory Gene2 (NRG2). Interestingly, we observed that gds1 mutants show early leaf senescence as well as reduced NO₃^- content and N uptake under N-deficient conditions. Further analyses indicated that GDS1 binds to the promoters of several senescence-related genes, including Phytochrome-Interacting Transcription Factors 4 and 5 (PIF4 and PIF5) and represses their expression. Interestingly, we found that N deficiency decreases GDS1 protein accumulation, and GDS1 could interact with Anaphase Promoting Complex Subunit 10 (APC10). Genetic and biochemical experiments demonstrated that Anaphase Promoting Complex or Cyclosome (APC/C) promotes the ubiquitination and degradation of GDS1 under N deficiency, resulting in loss of PIF4 and PIF5 repression and consequent early leaf senescence. Furthermore, we discovered that overexpression of GDS1 could delay leaf senescence and improve seed yield and N-use efficiency (NUE) in Arabidopsis. In summary, our study uncovers a molecular framework illustrating a new mechanism underlying low-N-induced early leaf senescence and provides potential targets for genetic improvement of crop varieties with increased yield and NUE.

Keywords: APC/C; GDS1; NUE; PIF4/PIF5; nitrate signaling; nitrogen-deficiency-induced leaf senescence; ubiquitination.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Arabidopsis Proteins* / genetics
Arabidopsis Proteins* / metabolism
Arabidopsis* / genetics
Arabidopsis* / metabolism
Gene Expression Regulation, Plant
Nitrates / metabolism
Plant Leaves / genetics
Plant Leaves / metabolism
Plant Senescence

Substances

Arabidopsis Proteins
Nitrates