Comparative transcriptome analysis identifies key regulators of nitrogen use efficiency in chrysanthemum

doi:10.1016/j.jia.2024.11.003

Journal of Integrative Agriculture

2025, Vol. 24

Issue (1): 176-195 DOI: 10.1016/j.jia.2024.11.003

Horticulture

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Comparative transcriptome analysis identifies key regulators of nitrogen use efficiency in chrysanthemum

Lijiao Ge^{1, 2, 3}, Weihao Miao^{1, 2}, Kuolin Duan^{1, 2}, Tong Sun^{1, 2}, Xinyan Fang^{1, 2}, Zhiyong Guan^{1, 2}, Jiafu Jiang^{1, 2}, Sumei Chen^{1, 2},Weimin Fang^{1, 2}, Fadi Chen^{1, 2}, Shuang Zhao^{1, 2#}

¹College of Horticulture, Nanjing Agricultural University, Nanjing 210095, China

²Key Laboratory of Landscaping, Ministry of Agriculture and Rural Affairs, Nanjing 210095, China

³Jiangsu Yanjiang Institute of Agricultural Sciences, Nantong 226012, China

Highlights
● Genes are more sensitive to changes in nitrogen (N) conditions in N-efficient genotype.
● Several candidate genes related to N use efficiency are identified.
● Eight hub genes involved in resistance to low N stress resistance are revealed.

Abstract
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摘要

氮（N）是决定菊花产量和品质的限制因子。不同基因型菊花的氮利用效率(NUE)存在遗传变异。为探究影响菊花NUE的遗传因子，我们应用转录组技术分析了氮高效基因型‘南农丽黄’（‘LH’）和氮低效基因型‘南农雪峰’(‘XF’)经低氮（0.4 mM·L^-1 N）、正常氮（8 mM·L^-1 N)处理15 d和氮恢复处理12 h（低氮处理15 d后转正常氮处理12 h）的根系基因表达特征。结果显示，两种基因型对不同氮处理表现出响应差异。正常氮和低氮处理下，氮高效基因型‘LH’在农艺性状、氮累积量和谷氨酰胺合成酶活性中展现显著优势。低氮处理促进了‘LH’的根系生长，但抑制了‘XF’的根系生长。转录组分析发现，低氮处理增加了两基因型根系中部分N代谢、生长素和脱落酸信号转导相关基因的表达以及‘LH’根系中赤霉素信号转导相关基因的表达，氮恢复处理则仅增加了‘LH’根系细胞分裂素信号转导相关基因的表达。不同氮处理下，‘LH’根系中NRT2.1、AMT1.1、Gln1、赤霉素和细胞分裂素信号转导相关基因的表达量均高于‘XF’，说明‘LH’根中与N代谢和激素（生长素、脱落酸、赤霉素和细胞分裂素）信号转导相关的基因对不同氮处理响应比‘XF’更为敏感。共表达网络分析结果显示，bZIP43、bHLH93、NPF6.3、IBR10、MYB62、PP2C、PP2C06和NLP7等八个枢纽基因可能是菊花氮素介导应答的关键调控因子，在氮高效基因型菊花抵御低氮胁迫、提高NUE的过程中发挥重要作用。本研究结果在遗传水平上揭示了调控菊花NUE的关键因素，为菊花氮高效利用这一复杂机理的理解提供了新视角，同时也为菊花基因型改良和氮高效菊花基因型育种提供了有益依据。

Abstract

Nitrogen (N) is a limiting factor that determines the yield and quality of chrysanthemum. Genetic variation in N use efficiency (NUE) has been reported among chrysanthemum genotypes. We performed a transcriptome analysis of two chrysanthemum genotypes, ‘Nannonglihuang’ (LH, N-efficient genotype) and ‘Nannongxuefeng’ (XF, N-inefficient genotype), under low N (0.4 mmol L^–1 N) and normal N (8 mmol L^–1 N) treatments for 15 d and an N recovery treatment for 12 h (low N treatment for 15 d and then normal N treatment for 12 h) to understand the genetic factors impacting NUE in chrysanthemum. The two genotypes exhibited contrasting responses to the different N treatments. The N-efficient genotype LH had significant superiority in agronomic traits, N accumulation and glutamine synthase activity under both normal N and low N treatments. Low N treatment promoted root growth in LH, but inhibited root growth in XF. Transcriptome analysis revealed that the low N treatment increased the expression of some N metabolism genes, genes related to auxin and abscisic acid signal transduction in the roots of both genotypes, as well as genes related to gibberellin signal transduction in roots of LH. The N recovery treatment just increased the expression of genes related to cytokinin signal transduction in roots of LH. The expression levels of the NRT2.1, AMT1.1, and Gln1 genes related to gibberellin and cytokinin signal transduction were higher in roots of LH than in XF under different N treatments, suggesting that the genes related to N metabolism and hormone (auxin, abscisic acid, gibberellin, and cytokinin) signal transduction in roots of LH are more sensitive to different N treatments than those of XF. Co-expression network analysis (WGCNA) also identified hub genes like bZIP43, bHLH93, NPF6.3, IBR10, MYB62, PP2C, PP2C06 and NLP7, which may be the key regulators of N-mediated responses in chrysanthemum and play crucial roles in enhancing NUE and resistance to low N stress in the N-efficient chrysanthemum genotype. These results revealed the key factors involved in regulating NUE in chrysanthemum at the genetic level, which provides new insights into the complex mechanism of efficient nitrogen utilization in chrysanthemum, and can be useful for the improvement and breeding of high NUE chrysanthemum genotypes.

Keywords: chrysanthemum genotype NUE gene expression transcriptome analysis

Received: 13 March 2023 Accepted: 27 September 2024

Fund:

This study was supported by the National Key R&D Program of China (2020YFD1000400), the National Natural Science Foundation of China (32072603), the Jiangsu Agriculture Science and Technology Innovation Fund, China (CX(21)2004), and the JBGS Project of Seed Industry Revitalization in Jiangsu Province, China (JBGS[2021]020).

About author: Lijiao Ge, E-mail: 2019104112@njau.edu.cn; #Correspondence Shuang Zhao, E-mail: zhaoshuang@njau.edu.cn

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Lijiao Ge, Weihao Miao, Kuolin Duan, Tong Sun, Xinyan Fang, Zhiyong Guan, Jiafu Jiang, Sumei Chen, Weimin Fang, Fadi Chen, Shuang Zhao. 2025. Comparative transcriptome analysis identifies key regulators of nitrogen use efficiency in chrysanthemum. Journal of Integrative Agriculture, 24(1): 176-195.

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