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Journal of Integrative Agriculture  2025, Vol. 24 Issue (12): 4588-4612    DOI: 10.1016/j.jia.2024.04.001
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Transcriptome-metabolome and anatomy conjoint analysis of vital component change of photosynthesis in foxtail millet under different drought conditions

Jing Wang1*, Zexin Sun1*, Lei Tian3, Wei Sun3, Xinning Wang1, Zhihao Wang1, Zhiying Wang1, Zhao Li1, Wei Liu1, Qianchi Ma1, Chuanyou Ren1, Xining Gao1, Yue Li1, Liwei Wang1, Xiaoguang Wang1, Chunji Jiang1, Chao Zhong1, Xinhua Zhao1, Haiqiu Yu1, 2#

1 College of Agronomy, Shenyang Agricultural University, Shenyang 110866, China

2 Liaoning Agricultural Vocational and Technical College, Yingkou 115009, China

3 Linyi Academy of Agricultural Sciences, Linyi 276000, China

 Highlights 
Light and heavy drought stress was performed both at elongation and booting stages to dig out the effects on the leaf of foxtail millet.
Drought had severe negative effect on morphological and anatomical leaves at booting stage.
Drought also conducted harmful to ATP synthesis and photosynthetic CO2 assimilation.
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摘要  
极端气候变化引起的干旱越来越严重且不可预测性增强,干旱会对谷子叶片光合作用产生潜在的影响。为深入探究不同干旱强度对谷子光合作用的损伤差异,本文在拔节期(Y)和孕穗期分别进行了轻度干旱(LD)和重度干旱(HD)处理,并从形态特征、解剖结构、生理特性、转录组和代谢组水平进行综合分析。干旱胁迫下,两个生育时期的谷子叶片长度和面积均减少,但孕穗期HD处理显著下降。孕穗期LD和HD处理,叶肉细胞和大维管束面积显著减少,维管束和花环解剖结构逐渐模糊。拔节期Y-LD和Y-HD处理,叶肉细胞数量和维管束面积均下降,但无显著性差异。孕穗期不同干旱胁迫处理,叶片净光合速率、气孔导度、蒸腾速率、细胞间CO2浓度和光系统II(PS II)的电子转移效率显著降低,表明孕穗期干旱胁迫对叶片光合功能损伤严重。利用转录组和代谢组联合分析探索孕穗期不同干旱胁迫下光合作用变化的分子机制。结果表明, LD处理,转录组和代谢组中无共同差异富集通路,但HD处理,转录组和代谢组中共有32条通路富集;其中,精氨酸、脯氨酸代谢、酪氨酸代谢、泛醌和其他萜类醌生物合成途径在转录组和代谢组中差异富集。干旱胁迫, Homogentisate、Salidroside、Homoprotocatechuate、L-DOPA、Tyramine和L-Tyrosine积累量增加。虽然LD处理下调控PSII和卡尔文循环基因的表达量略有上调,但在HD处理下均下调。LD和HD处理,Ribose-5P、Glycerate-3P、D-Fructosel 1,6P2和D-Fructose-6P代谢物均下降,特别是D-Fructose-6P降幅较大,表明干旱胁迫对光合作用中的卡尔文循环影响较大。因此,无论干旱程度强弱,谷子叶片不仅在形态特征和组织解剖水平上发生变化,并且ATP合酶受损和光合CO2同化受到抑制,最终导致其光合功能受损。


Abstract  

Drought caused by extreme climate change has become more severe and unpredictable, causing imperceptible effects on leaf photosynthesis in foxtail millet.  To investigate the damage, we performed light drought (LD) and heavy drought (HD) treatments at both the elongation (Y) and booting stages to obtain a comprehensive understanding of the morphological, anatomical, physiological, transcriptome, and metabolome levels.  Under drought stress, the length and area of leaves decreased, especially during the HD treatment at the booting stage.  The number of mesophyll cells and the area of large vascular bundles decreased under LD and HD treatments at the booting stage, with more blurring vascular bundle structure and Kranz anatomy.  However, these numbers decreased with no significance under Y-LD and Y-HD treatments at the elongation stage.  The net photosynthetic rate, stomatal conductivity, transpiration rate, and intercellular CO2 concentration significantly decreased at the booting stage.  In addition, the efficiency of electron transfers in photosystem II (PSII) decreased.  Conjunction analyses of the transcriptome and metabolome were utilized to uncover the underlying mechanism at the booting stage.  The results showed no common differentially enriched pathway in the transcriptome and metabolome under LD treatment.  However, 32 pathways were enriched in both the transcript and metabolome under HD treatment.  Among these, three pathways, including arginine and proline metabolism, tyrosine metabolism, and ubiquinone, along with other terpenoid-quinone biosynthesis pathways, were differentially enriched in both the transcript and metabolome.  The accumulation of homogentisate, salidroside, homoprotocatechuate, L-DOPA, tyramine, and L-tyrosine increased under drought stress.  Although genes related to PSII and the Calvin cycle were slightly up-regulated under LD conditions, they were down-regulated under HD conditions.  The metabolites of ribose-5P, glycerate-3P, D-fructose-1, 6P2, and D-fructose-6P were all decreased in both the LD and HD treatments, especially D-fructose-6P, confirming that drought stress harmed the Calvin cycle.  The results revealed that regardless of the severity of drought, the photosynthetic function was compromised not only at the morphological and anatomical levels but also in terms of impaired ATP synthase and inhibited photosynthetic CO2 assimilation.

Keywords:  foxtail millet        drought stress        RNA-seq        metabolites        photosynthesis  
Received: 12 December 2023   Accepted: 05 March 2024 Online: 02 April 2024  
Fund: This work was supported by the National Key Research and Development Program of China (2019YFD1002204), the National Natural Science Foundation for Youth of China (31901505), and the Shenyang Agricultural University Introduced Talent Research Project, China (20153042).
About author:  #Correspondence Haiqiu Yu, Tel: +86-24-88487135, E-mail: yuhaiqiu@syau.edu.cn * These authors contributed equally to this study.

Cite this article: 

Jing Wang, Zexin Sun, Lei Tian, Wei Sun, Xinning Wang, Zhihao Wang, Zhiying Wang, Zhao Li, Wei Liu, Qianchi Ma, Chuanyou Ren, Xinning Gao, Yue Li, Liwei Wang, Xiaoguang Wang, Chunji Jiang, Chao Zhong, Xinhua Zhao, Haiqiu Yu. 2025. Transcriptome-metabolome and anatomy conjoint analysis of vital component change of photosynthesis in foxtail millet under different drought conditions. Journal of Integrative Agriculture, 24(12): 4588-4612.

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