Integrative physiological and transcriptome analysis unravels the mechanism of low nitrogen use efficiency in burley tobacco

Abstract Burley tobacco, a chlorophyll‐deficient mutant with impaired nitrogen use efficiency (NUE), generally requires three to five times more nitrogen fertilization than flue‐cured tobacco to achieve a comparable yield, which generates serious environmental pollution and negatively affects human...

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Main Authors: Yuqing Feng, Yuanyuan Zhao, Yanjun Ma, Xiaolong Chen, Hongzhi Shi
Format: Article
Language:English
Published: Wiley 2024-10-01
Series:Plant Direct
Subjects:
Online Access:https://doi.org/10.1002/pld3.70004
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author Yuqing Feng
Yuanyuan Zhao
Yanjun Ma
Xiaolong Chen
Hongzhi Shi
author_facet Yuqing Feng
Yuanyuan Zhao
Yanjun Ma
Xiaolong Chen
Hongzhi Shi
author_sort Yuqing Feng
collection DOAJ
description Abstract Burley tobacco, a chlorophyll‐deficient mutant with impaired nitrogen use efficiency (NUE), generally requires three to five times more nitrogen fertilization than flue‐cured tobacco to achieve a comparable yield, which generates serious environmental pollution and negatively affects human health. Therefore, exploring the mechanisms underlying NUE is an effective measure to reduce environmental pollution and an essential direction for burley tobacco plant improvement. Physiological and genetic factors affecting tobacco NUE were identified using two tobacco genotypes with contrasting NUE in hydroponic experiments. Nitrogen use inefficient genotype (TN90) had lower nitrogen uptake and transport efficiencies, reduced leaf and root biomass, lower nitrogen assimilation and photosynthesis capacity, and lower nitrogen remobilization ability than the nitrogen use efficient genotype (K326). Transcriptomic analysis revealed that genes associated with photosynthesis, carbon fixation, and nitrogen metabolism are implicated in NUE. Three nitrate transporter genes in the leaves (NPF2.11, NPF2.13, and NPF3.1) and three nitrate transporter genes (NPF6.3, NRT2.1, and NRT2.4) in roots were down‐regulated by nitrogen starvation, all of which showed lower expression in TN90 than in K326. In addition, the protein–protein interaction (PPI) network diagram identified eight key genes (TPIP1, GAPB, HEMB, PGK3, PSBO, PSBP2, PSAG, and GLN2) that may affect NUE. Less advantageous changes in nitrogen uptake, nitrogen assimilation in combination with nitrogen remobilization, and maintenance of photosynthesis in response to nitrogen deficiency led to a lower NUE in TN90. The key genes (TPIP1, GAPB, PGK3, PSBO, PSBP2, PSAG, and GLN2) were associated with improving photosynthesis and nitrogen metabolism in tobacco plants grown under N‐deficient conditions.
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spelling doaj-art-a315f3323ec64f05af6e5ac81e68e5502025-02-04T08:31:56ZengWileyPlant Direct2475-44552024-10-01810n/an/a10.1002/pld3.70004Integrative physiological and transcriptome analysis unravels the mechanism of low nitrogen use efficiency in burley tobaccoYuqing Feng0Yuanyuan Zhao1Yanjun Ma2Xiaolong Chen3Hongzhi Shi4College of Tobacco Henan Agricultural University Zhengzhou ChinaCollege of Tobacco Henan Agricultural University Zhengzhou ChinaTechnology Center Shanghai Tobacco Group Beijing Cigarette Factory Co., Ltd. Beijing ChinaChina Tobacco Henan Industrial Co., Ltd. Zhengzhou Henan ChinaCollege of Tobacco Henan Agricultural University Zhengzhou ChinaAbstract Burley tobacco, a chlorophyll‐deficient mutant with impaired nitrogen use efficiency (NUE), generally requires three to five times more nitrogen fertilization than flue‐cured tobacco to achieve a comparable yield, which generates serious environmental pollution and negatively affects human health. Therefore, exploring the mechanisms underlying NUE is an effective measure to reduce environmental pollution and an essential direction for burley tobacco plant improvement. Physiological and genetic factors affecting tobacco NUE were identified using two tobacco genotypes with contrasting NUE in hydroponic experiments. Nitrogen use inefficient genotype (TN90) had lower nitrogen uptake and transport efficiencies, reduced leaf and root biomass, lower nitrogen assimilation and photosynthesis capacity, and lower nitrogen remobilization ability than the nitrogen use efficient genotype (K326). Transcriptomic analysis revealed that genes associated with photosynthesis, carbon fixation, and nitrogen metabolism are implicated in NUE. Three nitrate transporter genes in the leaves (NPF2.11, NPF2.13, and NPF3.1) and three nitrate transporter genes (NPF6.3, NRT2.1, and NRT2.4) in roots were down‐regulated by nitrogen starvation, all of which showed lower expression in TN90 than in K326. In addition, the protein–protein interaction (PPI) network diagram identified eight key genes (TPIP1, GAPB, HEMB, PGK3, PSBO, PSBP2, PSAG, and GLN2) that may affect NUE. Less advantageous changes in nitrogen uptake, nitrogen assimilation in combination with nitrogen remobilization, and maintenance of photosynthesis in response to nitrogen deficiency led to a lower NUE in TN90. The key genes (TPIP1, GAPB, PGK3, PSBO, PSBP2, PSAG, and GLN2) were associated with improving photosynthesis and nitrogen metabolism in tobacco plants grown under N‐deficient conditions.https://doi.org/10.1002/pld3.70004burley tobaccocarbon and metabolismN deficiencynitrogen use efficiencyphotosynthesis
spellingShingle Yuqing Feng
Yuanyuan Zhao
Yanjun Ma
Xiaolong Chen
Hongzhi Shi
Integrative physiological and transcriptome analysis unravels the mechanism of low nitrogen use efficiency in burley tobacco
Plant Direct
burley tobacco
carbon and metabolism
N deficiency
nitrogen use efficiency
photosynthesis
title Integrative physiological and transcriptome analysis unravels the mechanism of low nitrogen use efficiency in burley tobacco
title_full Integrative physiological and transcriptome analysis unravels the mechanism of low nitrogen use efficiency in burley tobacco
title_fullStr Integrative physiological and transcriptome analysis unravels the mechanism of low nitrogen use efficiency in burley tobacco
title_full_unstemmed Integrative physiological and transcriptome analysis unravels the mechanism of low nitrogen use efficiency in burley tobacco
title_short Integrative physiological and transcriptome analysis unravels the mechanism of low nitrogen use efficiency in burley tobacco
title_sort integrative physiological and transcriptome analysis unravels the mechanism of low nitrogen use efficiency in burley tobacco
topic burley tobacco
carbon and metabolism
N deficiency
nitrogen use efficiency
photosynthesis
url https://doi.org/10.1002/pld3.70004
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AT yanjunma integrativephysiologicalandtranscriptomeanalysisunravelsthemechanismoflownitrogenuseefficiencyinburleytobacco
AT xiaolongchen integrativephysiologicalandtranscriptomeanalysisunravelsthemechanismoflownitrogenuseefficiencyinburleytobacco
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