H+-pyrophosphatases enhance low nitrogen stress tolerance in transgenic Arabidopsis and wheat by interacting with a receptor-like protein kinase

IntroductionNitrogen is a major abiotic stress that affects plant productivity. Previous studies have shown that plant H+-pyrophosphatases (H+-PPases) enhance plant resistance to low nitrogen stress. However, the molecular mechanism underlying H+-PPase-mediated regulation of plant responses to low n...

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Main Authors: Huijuan Zhang, Ming Chen, Chengjie Xu, Rongbang Liu, Wensi Tang, Kai Chen, Yongbin Zhou, Zhaoshi Xu, Jun Chen, Youzhi Ma, Weiguo Chen, Daizhen Sun, Hua Fan
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-01-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1096091/full
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author Huijuan Zhang
Huijuan Zhang
Ming Chen
Chengjie Xu
Chengjie Xu
Rongbang Liu
Wensi Tang
Kai Chen
Yongbin Zhou
Zhaoshi Xu
Jun Chen
Youzhi Ma
Weiguo Chen
Daizhen Sun
Hua Fan
author_facet Huijuan Zhang
Huijuan Zhang
Ming Chen
Chengjie Xu
Chengjie Xu
Rongbang Liu
Wensi Tang
Kai Chen
Yongbin Zhou
Zhaoshi Xu
Jun Chen
Youzhi Ma
Weiguo Chen
Daizhen Sun
Hua Fan
author_sort Huijuan Zhang
collection DOAJ
description IntroductionNitrogen is a major abiotic stress that affects plant productivity. Previous studies have shown that plant H+-pyrophosphatases (H+-PPases) enhance plant resistance to low nitrogen stress. However, the molecular mechanism underlying H+-PPase-mediated regulation of plant responses to low nitrogen stress is still unknown. In this study, we aimed to investigate the regulatory mechanism of AtAVP1 in response to low nitrogen stress.Methods and ResultsAtAVP1 in Arabidopsis thaliana and EdVP1 in Elymus dahuricus belong to the H+-PPase gene family. In this study, we found that AtAVP1 overexpression was more tolerant to low nitrogen stress than was wild type (WT), whereas the avp1-1 mutant was less tolerant to low nitrogen stress than WT. Plant height, root length, aboveground fresh and dry weights, and underground fresh and dry weights of EdVP1 overexpression wheat were considerably higher than those of SHI366 under low nitrogen treatment during the seedling stage. Two consecutive years of low nitrogen tolerance experiments in the field showed that grain yield and number of grains per spike of EdVP1 overexpression wheat were increased compared to those in SHI366, which indicated that EdVP1 conferred low nitrogen stress tolerance in the field. Furthermore, we screened interaction proteins in Arabidopsis; subcellular localization analysis demonstrated that AtAVP1 and Arabidopsis thaliana receptor-like protein kinase (AtRLK) were located on the plasma membrane. Yeast two-hybrid and luciferase complementary imaging assays showed that the AtRLK interacted with AtAVP1. Under low nitrogen stress, the Arabidopsis mutants rlk and avp1-1 had the same phenotypes.DiscussionThese results indicate that AtAVP1 regulates low nitrogen stress responses by interacting with AtRLK, which provides a novel insight into the regulatory pathway related to H+-pyrophosphatase function in plants.
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spelling doaj.art-48a970ed859d4da98c3b84e84d3aa33d2023-01-27T15:02:45ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-01-011410.3389/fpls.2023.10960911096091H+-pyrophosphatases enhance low nitrogen stress tolerance in transgenic Arabidopsis and wheat by interacting with a receptor-like protein kinaseHuijuan Zhang0Huijuan Zhang1Ming Chen2Chengjie Xu3Chengjie Xu4Rongbang Liu5Wensi Tang6Kai Chen7Yongbin Zhou8Zhaoshi Xu9Jun Chen10Youzhi Ma11Weiguo Chen12Daizhen Sun13Hua Fan14College of Agriculture, Shanxi Agricultural University, Shanxi, ChinaInstitute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing, ChinaInstitute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing, ChinaCollege of Agriculture, Shanxi Agricultural University, Shanxi, ChinaInstitute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing, ChinaInstitute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing, ChinaInstitute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing, ChinaInstitute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing, ChinaInstitute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing, ChinaInstitute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing, ChinaInstitute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing, ChinaInstitute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing, ChinaCollege of Agriculture, Shanxi Agricultural University, Shanxi, ChinaCollege of Agriculture, Shanxi Agricultural University, Shanxi, ChinaCollege of Agriculture, Shanxi Agricultural University, Shanxi, ChinaIntroductionNitrogen is a major abiotic stress that affects plant productivity. Previous studies have shown that plant H+-pyrophosphatases (H+-PPases) enhance plant resistance to low nitrogen stress. However, the molecular mechanism underlying H+-PPase-mediated regulation of plant responses to low nitrogen stress is still unknown. In this study, we aimed to investigate the regulatory mechanism of AtAVP1 in response to low nitrogen stress.Methods and ResultsAtAVP1 in Arabidopsis thaliana and EdVP1 in Elymus dahuricus belong to the H+-PPase gene family. In this study, we found that AtAVP1 overexpression was more tolerant to low nitrogen stress than was wild type (WT), whereas the avp1-1 mutant was less tolerant to low nitrogen stress than WT. Plant height, root length, aboveground fresh and dry weights, and underground fresh and dry weights of EdVP1 overexpression wheat were considerably higher than those of SHI366 under low nitrogen treatment during the seedling stage. Two consecutive years of low nitrogen tolerance experiments in the field showed that grain yield and number of grains per spike of EdVP1 overexpression wheat were increased compared to those in SHI366, which indicated that EdVP1 conferred low nitrogen stress tolerance in the field. Furthermore, we screened interaction proteins in Arabidopsis; subcellular localization analysis demonstrated that AtAVP1 and Arabidopsis thaliana receptor-like protein kinase (AtRLK) were located on the plasma membrane. Yeast two-hybrid and luciferase complementary imaging assays showed that the AtRLK interacted with AtAVP1. Under low nitrogen stress, the Arabidopsis mutants rlk and avp1-1 had the same phenotypes.DiscussionThese results indicate that AtAVP1 regulates low nitrogen stress responses by interacting with AtRLK, which provides a novel insight into the regulatory pathway related to H+-pyrophosphatase function in plants.https://www.frontiersin.org/articles/10.3389/fpls.2023.1096091/fulllow nitrogen stressreceptor-like protein kinasearabidopsistransgenic wheatH+-pyrophosphatase
spellingShingle Huijuan Zhang
Huijuan Zhang
Ming Chen
Chengjie Xu
Chengjie Xu
Rongbang Liu
Wensi Tang
Kai Chen
Yongbin Zhou
Zhaoshi Xu
Jun Chen
Youzhi Ma
Weiguo Chen
Daizhen Sun
Hua Fan
H+-pyrophosphatases enhance low nitrogen stress tolerance in transgenic Arabidopsis and wheat by interacting with a receptor-like protein kinase
Frontiers in Plant Science
low nitrogen stress
receptor-like protein kinase
arabidopsis
transgenic wheat
H+-pyrophosphatase
title H+-pyrophosphatases enhance low nitrogen stress tolerance in transgenic Arabidopsis and wheat by interacting with a receptor-like protein kinase
title_full H+-pyrophosphatases enhance low nitrogen stress tolerance in transgenic Arabidopsis and wheat by interacting with a receptor-like protein kinase
title_fullStr H+-pyrophosphatases enhance low nitrogen stress tolerance in transgenic Arabidopsis and wheat by interacting with a receptor-like protein kinase
title_full_unstemmed H+-pyrophosphatases enhance low nitrogen stress tolerance in transgenic Arabidopsis and wheat by interacting with a receptor-like protein kinase
title_short H+-pyrophosphatases enhance low nitrogen stress tolerance in transgenic Arabidopsis and wheat by interacting with a receptor-like protein kinase
title_sort h pyrophosphatases enhance low nitrogen stress tolerance in transgenic arabidopsis and wheat by interacting with a receptor like protein kinase
topic low nitrogen stress
receptor-like protein kinase
arabidopsis
transgenic wheat
H+-pyrophosphatase
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1096091/full
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