OsNPF3.1, a nitrate, abscisic acid and gibberellin transporter gene, is essential for rice tillering and nitrogen utilization efficiency
Low-affinity nitrate transporter genes have been identified in subfamilies 4–8 of the rice nitrate transporter 1 (NRT1)/peptide transporter family (NPF), but the OsNPF3 subfamily responsible for nitrate and phytohormone transport and rice growth and development remains unknown. In this study, we des...
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Elsevier
2024-04-01
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author | Junnan Hang Bowen Wu Diyang Qiu Guo Yang Zhongming Fang Mingyong Zhang |
author_facet | Junnan Hang Bowen Wu Diyang Qiu Guo Yang Zhongming Fang Mingyong Zhang |
author_sort | Junnan Hang |
collection | DOAJ |
description | Low-affinity nitrate transporter genes have been identified in subfamilies 4–8 of the rice nitrate transporter 1 (NRT1)/peptide transporter family (NPF), but the OsNPF3 subfamily responsible for nitrate and phytohormone transport and rice growth and development remains unknown. In this study, we described OsNPF3.1 as an essential nitrate and phytohormone transporter gene for rice tillering and nitrogen utilization efficiency (NUtE). OsNPF3.1 possesses four major haplotypes of its promoter sequence in 517 cultivars, and its expression is positively associated with tiller number. Its expression was higher in the basal part, culm, and leaf blade than in other parts of the plant, and was strongly induced by nitrate, abscisic acid (ABA) and gibberellin 3 (GA3) in the root and shoot of rice. Electrophysiological experiments demonstrated that OsNPF3.1 is a pH-dependent low-affinity nitrate transporter, with rice protoplast uptake assays showing it to be an ABA and GA3 transporter. OsNPF3.1 overexpression significantly promoted ABA accumulation in the roots and GA accumulation in the basal part of the plant which inhibited axillary bud outgrowth and rice tillering, especially at high nitrate concentrations. The NUtE of OsNPF3.1-overexpressing plants was enhanced under low and medium nitrate concentrations, whereas the NUtE of OsNPF3.1 clustered regularly interspaced short palindromic repeats (CRISPR) plants was increased under high nitrate concentrations. The results indicate that OsNPF3.1 transports nitrate and phytohormones in different rice tissues under different nitrate concentrations. The altered OsNPF3.1 expression improves NUtE in the OsNPF3.1-overexpressing and CRISPR lines at low and high nitrate concentrations, respectively. |
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spelling | doaj.art-5c63ca2e5e2643b3bd777970e033d26a2024-04-06T04:39:47ZengElsevierJournal of Integrative Agriculture2095-31192024-04-0123410871104OsNPF3.1, a nitrate, abscisic acid and gibberellin transporter gene, is essential for rice tillering and nitrogen utilization efficiencyJunnan Hang0Bowen Wu1Diyang Qiu2Guo Yang3Zhongming Fang4Mingyong Zhang5Institute of Rice Industry Technology Research/Key Laboratory of Functional Agriculture, Guizhou Provincial Department of Education/Key Laboratory of Plant Resource Conservation and Germplasm Innovation in Mountainous Region, Ministry of Education/Key Laboratory of Molecular Breeding for Grain and Oil Crops in Guizhou Province/College of Agricultural Sciences, Guizhou University, Guiyang 550025, ChinaInstitute of Rice Industry Technology Research/Key Laboratory of Functional Agriculture, Guizhou Provincial Department of Education/Key Laboratory of Plant Resource Conservation and Germplasm Innovation in Mountainous Region, Ministry of Education/Key Laboratory of Molecular Breeding for Grain and Oil Crops in Guizhou Province/College of Agricultural Sciences, Guizhou University, Guiyang 550025, ChinaKey Laboratory of South China Agricultural Plant Molecular Analysis and Genetic Improvement/Guangdong Provincial Key Laboratory of Applied Botany/South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China; Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, ChinaInstitute of Rice Industry Technology Research/Key Laboratory of Functional Agriculture, Guizhou Provincial Department of Education/Key Laboratory of Plant Resource Conservation and Germplasm Innovation in Mountainous Region, Ministry of Education/Key Laboratory of Molecular Breeding for Grain and Oil Crops in Guizhou Province/College of Agricultural Sciences, Guizhou University, Guiyang 550025, ChinaInstitute of Rice Industry Technology Research/Key Laboratory of Functional Agriculture, Guizhou Provincial Department of Education/Key Laboratory of Plant Resource Conservation and Germplasm Innovation in Mountainous Region, Ministry of Education/Key Laboratory of Molecular Breeding for Grain and Oil Crops in Guizhou Province/College of Agricultural Sciences, Guizhou University, Guiyang 550025, China; Correspondence Zhongming Fang, Mingyong ZhangKey Laboratory of South China Agricultural Plant Molecular Analysis and Genetic Improvement/Guangdong Provincial Key Laboratory of Applied Botany/South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China; Correspondence Zhongming Fang, Mingyong ZhangLow-affinity nitrate transporter genes have been identified in subfamilies 4–8 of the rice nitrate transporter 1 (NRT1)/peptide transporter family (NPF), but the OsNPF3 subfamily responsible for nitrate and phytohormone transport and rice growth and development remains unknown. In this study, we described OsNPF3.1 as an essential nitrate and phytohormone transporter gene for rice tillering and nitrogen utilization efficiency (NUtE). OsNPF3.1 possesses four major haplotypes of its promoter sequence in 517 cultivars, and its expression is positively associated with tiller number. Its expression was higher in the basal part, culm, and leaf blade than in other parts of the plant, and was strongly induced by nitrate, abscisic acid (ABA) and gibberellin 3 (GA3) in the root and shoot of rice. Electrophysiological experiments demonstrated that OsNPF3.1 is a pH-dependent low-affinity nitrate transporter, with rice protoplast uptake assays showing it to be an ABA and GA3 transporter. OsNPF3.1 overexpression significantly promoted ABA accumulation in the roots and GA accumulation in the basal part of the plant which inhibited axillary bud outgrowth and rice tillering, especially at high nitrate concentrations. The NUtE of OsNPF3.1-overexpressing plants was enhanced under low and medium nitrate concentrations, whereas the NUtE of OsNPF3.1 clustered regularly interspaced short palindromic repeats (CRISPR) plants was increased under high nitrate concentrations. The results indicate that OsNPF3.1 transports nitrate and phytohormones in different rice tissues under different nitrate concentrations. The altered OsNPF3.1 expression improves NUtE in the OsNPF3.1-overexpressing and CRISPR lines at low and high nitrate concentrations, respectively.http://www.sciencedirect.com/science/article/pii/S2095311923000941rice tilleringgrain yieldphytohormonenitratetransporternitrogen utilization efficiency |
spellingShingle | Junnan Hang Bowen Wu Diyang Qiu Guo Yang Zhongming Fang Mingyong Zhang OsNPF3.1, a nitrate, abscisic acid and gibberellin transporter gene, is essential for rice tillering and nitrogen utilization efficiency Journal of Integrative Agriculture rice tillering grain yield phytohormone nitrate transporter nitrogen utilization efficiency |
title | OsNPF3.1, a nitrate, abscisic acid and gibberellin transporter gene, is essential for rice tillering and nitrogen utilization efficiency |
title_full | OsNPF3.1, a nitrate, abscisic acid and gibberellin transporter gene, is essential for rice tillering and nitrogen utilization efficiency |
title_fullStr | OsNPF3.1, a nitrate, abscisic acid and gibberellin transporter gene, is essential for rice tillering and nitrogen utilization efficiency |
title_full_unstemmed | OsNPF3.1, a nitrate, abscisic acid and gibberellin transporter gene, is essential for rice tillering and nitrogen utilization efficiency |
title_short | OsNPF3.1, a nitrate, abscisic acid and gibberellin transporter gene, is essential for rice tillering and nitrogen utilization efficiency |
title_sort | osnpf3 1 a nitrate abscisic acid and gibberellin transporter gene is essential for rice tillering and nitrogen utilization efficiency |
topic | rice tillering grain yield phytohormone nitrate transporter nitrogen utilization efficiency |
url | http://www.sciencedirect.com/science/article/pii/S2095311923000941 |
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