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Journal of Integrative Agriculture  2025, Vol. 24 Issue (3): 1044-1064    DOI: 10.1016/j.jia.2024.04.016
Special Issue: 小麦耕作栽培Wheat Physiology · Biochemistry · Cultivation · Tillage
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Response of wheat to winter night warming based on physiological and transcriptome analyses

Yonghui Fan1, Yue Zhang1, Yu Tang1, Biao Xie2, Wei He1, Guoji Cui1, Jinhao Yang1, 3, Wenjing Zhang1, Shangyu Ma1, Chuanxi Ma1, Haipeng Zhang1#, Zhenglai Huang1#

1 College of Agronomy, Anhui Agricultural University/Key Laboratory of Wheat Biology and Genetic Improvement in South Yellow & Huai River Valley, Ministry of Agriculture and Rural Affairs, Hefei 230000, China

2 Office of Social Cooperation, Anhui Agricultural University, Hefei 230000, China

3 Xianyang Central Station for Agricultural Technology Extension, Xianyang 712000, China

 Highlights 
Night warming during the tillering–jointing stage enhanced the grain yield of winter wheat. 
Effects of warming on wheat physiological activities are mediated by the differentially expressed genes related to temperature in various metabolic pathways.  
Comparison between groups identified 14 differentially expressed genes related to temperature.
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摘要  
全球变暖的主要特征是非对称性增温,即冬春季和夜间增温幅度大于夏秋季和白天的增温幅度。为明确夜间增温对小麦叶片产生的影响,于2020~2021年的小麦生长季,以春性品种扬麦18和半冬性品种烟农19为试验材料,研究冬季夜间增温对小麦顶展叶的影响。结果表明,处理组夜间平均温度较对照组环境温度增加了1.27℃,并且冬季夜间增温提高了两个小麦品种的产量,提高了两个品种小麦花后蔗糖合成酶(SS)和蔗糖磷酸合成酶(SPS)活性,促进了糖类和可溶性糖的合成。以q-value<0.05和Fold-change>2为筛选标准对差异基因进行分析,对已筛选的差异表达基因进行GO功能注释和KEGG pathway富集分析可知,对照与夜间增温处理下小麦叶片中的差异表达基因主要参与了淀粉和蔗糖代谢、氨基酸的生物合成、碳代谢、植物激素信号转导、氨基糖和核苷酸糖的代谢。经过各个比较组的比对,最终鉴定了14个可能与温度相关的差异表达基因。这些结果通过多种途径展示了小麦对冬季夜间增温条件下植物发育的影响。为小麦对冬季夜间增温反应的分子机制以及小麦对冬季夜间增温响应所需的潜在候选基因提供了新的见解。


Abstract  

Global warming is primarily characterized by asymmetric temperature increases, with greater temperature rises in winter/spring and at night compared to summer/autumn and the daytime.  We investigated the impact of winter night warming on the top expanded leaves of the spring wheat cultivar Yangmai 18 and the semi-winter wheat cultivar Yannong 19 during the 2020–2021 growing season.  Results showed that the night-time mean temperature in the treatment group was 1.27°C higher than the ambient temperature, and winter night warming increased the yields of both wheat cultivars, the activities of sucrose synthase and sucrose phosphate synthase after anthesis, and the biosynthesis of sucrose and soluble sugars.  Differentially expressed genes (DEGs) were identified using criteria of P-value<0.05 and fold change>2, and they were subjected to Gene Ontology (GO) annotation and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analyses.  Genes differentially expressed in wheat leaves treated with night warming were primarily associated with starch and sucrose metabolism, amino acid biosynthesis, carbon metabolism, plant hormone signal transduction, and amino sugar and nucleotide sugar metabolism.  Comparisons between the groups identified 14 DEGs related to temperature.  These results highlight the effects of winter night warming on wheat development from various perspectives.  Our results provide new insights into the molecular mechanisms of the response of wheat to winter night warming and the candidate genes involved in this process.


Keywords:  differentially expressed genes       physiology and transcriptome        wheat        winter night warming  
Received: 16 June 2023   Accepted: 11 August 2023
Fund: 
This work was supported by the Natural Science Foundation of Anhui Province, China (2008085qc118), the National Natural Science Foundation of China (U19A2021), the Major Science and Technology Special Project of Anhui Province, China (S202003a06020035), and the Jiangsu Collaborative Innovation Center for Modern Crop Production, China (JCIC-MCP).
About author:  Yonghui Fan, E-mail: yonghuifan66@163.com; #Correspondence Zhenglai Huang, E-mail: ahauhzl@163.com; Haipeng Zhang, E-mail: nxyzhp@163.com

Cite this article: 

Yonghui Fan, Yue Zhang, Yu Tang, Biao Xie, Wei He, Guoji Cui, Jinhao Yang, Wenjing Zhang, Shangyu Ma, Chuanxi Ma, Haipeng Zhang, Zhenglai Huang. 2025.

Response of wheat to winter night warming based on physiological and transcriptome analyses
. Journal of Integrative Agriculture, 24(3): 1044-1064.

Ahmadi A, Baker D A. 2001. The effect of water stress on the activities of key regulatory enzymes of the sucrose to starch pathway in wheat. Plant Growth Regulation35, 81–91.

Anders S, Huber W. 2012. Differential expression of RNA-Seq data at the gene level - The DESeq package. European Molecular Biology23, 536–550.

Anders S, Pyl P T, Huber W. 2015. HTSeq - A Python framework to work with high-throughput sequencing data. Bioinformatics31, 166–169.

Asseng S, Foster I, Turner N C. 2011. The impact of temperature variability on wheat yields. Global Change Biology17, 997–1012.

Bernstein L, Bosch P, Canziani O, Chen Z, Christ R, Riahi K. 2007. Climate Change 2007: Synthesis Report, Summary for Policy Makers. Intergovernmental Panel on Climate Change, Geneva, Switzerland.

Chen L P, Chen Q Y, Wei W H. 2019. Effects of low temperature freezing damage on wheat yield and cold resistance gene expression. In: Abstracts of the 10th National Conference on Wheat Genomics and Molecular Breeding. Yantai, Shandong, China.

Colodete C M, Ruas K F, Barbirato J O, Barroso A L P, Dobbss L B. 2015. Biochemistry characterization of proteins defense against oxidative stress in plants and their biosynthetic pathways of secondary metabolites. Natureza13, 195–204.

Djanaguiraman M, Narayanan S, Erdayani E, Prasad P V V. 2020. Effects of high temperature stress during anthesis and grain filling periods on photosynthesis, lipids and grain yield in wheat. BMC Plant Biology20, 268–279.

Espineda C E, Linford A S, Devine D, Brusslan J A. 1999. The AtCAO gene, encoding chlorophyll a oxygenase, is required for chlorophyll b synthesis in Arabidopsis thalianaProceedings of the National Academy of Sciences of the United States of America96, 10507–10511.

Fan Y H, Lv Z Y, Ge T, Li Y X, Yang W, Zhang W J, Ma S Y, Dai T B, Huang Z L. 2021. Night-warming priming at the vegetative stage alleviates damage to the flag leaf caused by post-anthesis warming in winter wheat (Triticum aestivum L.). Frontiers in Plant Science12, 706567–706579.

Fan Y H, Lv Z Y, Zhang Y, Ma L L, Qin B Y, Liu Q X, Zhang W J, Ma S Y, Ma C X, Huang Z L. 2022. Pre-anthesis night warming improves post-anthesis physiological activity and plant productivity to post-anthesis heat stress in winter wheat (Triticum aestivum L.). Environmental and Experimental Botany197, 104819–104827.

Fan Y H, Ma C X, Huang Z L, Abid M, Jiang S Y, Dai T B, Zhang W J, Ma S Y, Jiang D G, Han X. 2018. Heat priming during early reproductive stages enhances thermo-tolerance to post-anthesis heat stress via improving photosynthesis and plant productivity in winter wheat (Triticum aestivum L.). Frontiers in Plant Science9, 805–811.

Fan Y H, Qin B Y, Yang J H, Ma L L, Cui G J, He W, Tang Y, Zhang W J, Ma S Y, Ma C X, Huang Z L. 2024. Night warming increases wheat yield by improving pre-anthesis grain starch biosynthesis. Journal of Integrative Agriculture23, 536–550.

García G A, Dreccer M F, Miralles D J, Serrago R A. 2015. High night temperatures during grain number determination reduce wheat and barley grain yield: A field study. Global Change Biology21, 4153–4164.

Gong Z, Zhang W. 2001. Plant resources of taraxacum in China. Chinese Wild Plant Resources3, 9–15. (in Chinese)

Hennig B, Watkins B A. 1989. Linoleic acid and linolenic acid: Effect on permeability properties of cultured endothelial cell monolayers. The American Journal of Clinical Nutrition49, 301–305.

Ilagan R P, Chapp T W, Hiller R G, Sharples F P, Polivka T, Frank H A. 2006. Optical spectroscopic studies of light-harvesting by pigment-reconstituted peridinin-chlorophyll-proteins at cryogenic temperatures. Photosynthesis Research90, 5–15.

Jia W S, Zhang J H. 2008. Stomatal movements and longdistance signaling in plants. Plant Signaling & Behavior3, 772–777.

Kolattukudy P E. 1980. Cutin, suberin and waxes. Biochemistry of Plants A Comprehensive Treatise18, 571–645.

Kopečná J, Sobotka R, Komenda J. 2013. Inhibition of chlorophyll biosynthesis at the protochlorophyllide reduction step results in the parallel depletion of Photosystem I and Photosystem II in the cyanobacterium Synechocystis PCC. Planta237, 497–508.

Król M, Spangfort M D, Huner N P, Öquist G, Gustafsson P, Jansson S. 1995. Chlorophyll a/b-binding proteins, pigment conversions, and early light-induced proteins in a chlorophyll b-

less barley mutant. Plant Physiology107, 873–883.

Kumar R R, Goswami S, Sharma S K, kala Y K, Rai G K, Mishra D C, Grover M, Singh G P, Pathak H, Rai A, Chinnusamy V, Rai R D. 2015. Harnessing next generation sequencing in climate change: RNA-Seq analysis of heat stress-responsive genes in wheat (Triticum aestivum L.). OmicsA Journal of Integrative Biology19, 632–647.

Li D M, Wu W, Zhang D, Liu X R, Liu X F, Lin Y J. 2015. Floral transcriptome analyses of four Paphiopedilum Orchids with distinct flowering behaviors and development of simple sequence repeat markers. Plant Molecular Biology Reporter33, 1928–1952.

Li J, Liu H L, Xia W W, Mu J Q, Feng Y J, Liu R N, Yan P Y, Wang A Y, Lin Z P, Guo Y. 2017. De novo transcriptome sequencing and the hypothetical cold response mode of Saussurea involucrata in extreme cold environments. International Journal of Molecular Sciences18, 1155–1170.

Li Q, Chang X H, Meng X H, Li D, Zhao M H, Sun S L, Li H M, Qiao W C. 2020. Heat stability of winter wheat depends on cultivars, timing and protective methods. Journal of Integrative Agriculture19, 1984–1997.

Li X, Jiang D, Liu F. 2016. Winter soil warming exacerbates the impacts of spring low temperature stress on wheat. Journal of Agronomy and Crop Science202, 554–563.

Li Y F, Wang Y X, Tang Y HKakani V G, Mahalingam R. 2013. Transcriptome analysis of heat stress response in switchgrass (Panicum virgatum L.). BMC Plant Biology13, 153–164.

Liu L T, Hu C S, Olesen J E, Ju Z Q, Yang P P, Zhang Y M. 2013. Warming and nitrogen fertilization effects on winter wheat yields in northern China varied between four years. Field Crops Research151, 56–64.

Liu W, Lin L P, Zhang Z Y, Liu S Q, Gao K, Lv Y B, Tao H, He H Q. 2019. Gene co-expression network analysis identifies trait-related modules in Arabidopsis thalianaPlanta249, 1487–1501.

Lobell D B. 2007. Changes in diurnal temperature rand and national cereal yields. Agricultural and Forest Meteorology145, 229–238.

Lobell D B, Schlenker W, Costa-Roberts J. 2011. Climate trends and global crop production since 1980. Science333, 616–620.

Lv L H, Liang S B, Zhang J T, Yao Y R, Dong Z Q, Zhang L H, Jia X L. 2017. Yield and radiation utilization of different wheat varieties in response to accumulated temperature before winter. Journal of Triticeae Crops37, 1047–1055. (in Chinese)

Ma Q, Zhou H J, Sui X Y, Su C X, Yu Y C, Yang H B, Dong C H. 2021. Generation of new salt-tolerant wheat lines and transcriptomic exploration of the responsive genes to ethylene and salt stress. Plant Growth Regulation94, 33–48.

Mezreb K, Goullieux A, Ralainirina R, Queneudec M. 2006. Effect of sucrose on the textural properties of corn and wheat extrudates. Carbohydrate Polymers64, 1–8.

Mirosavljević M, Mikić S, Župunski V, Špika A K, Trkulja D, Ottosen C, Zhou R, Abdelhakim L. 2021. Effects of high temperature during anthesis and grain filling on physiological characteristics of winter wheat cultivars. Journal of Agronomy and Crop Science207, 823–832.

Mukherjee S, Liu A H, Deol K K, Kulichikhin K, Stasolla C, Brûlé-Babel A, Ayele Bm T. 2015. Transcriptional coordination and abscisic acid mediated regulation of sucrose transport and sucrose-to-starch metabolism related genes during grain filling in wheat (Triticum aestivum L.). Plant Science240, 143–160.

Noel J P, Austin M B, Bomati E K. 2005. Structure-function relationships in plant phenylpropanoid biosynthesis. Current Opinion in Plant Biology8, 249–253.

Onaga G, Wydra K, Koopmann B, Chebotarov D, Séré Y, Tiedemann A V. 2017. High temperature effects on Pi54 conferred resistance to Magnaporthe oryzae in two genetic backgrounds of Oryza sativaJournal of Plant Physiology212, 80–93.

Panda B B, Badoghar A K, Das K, Panigrahi R, Kariali E, Das S R, Dash S K, Shaw B P, Mohapatra P K. 2015. Compact panicle architecture is detrimental for growth as well as sucrose synthase activity of developing rice kernels. Functional Plant Biology42, 875–887.

Paul S, Duhan J S, Jaiswal S, Angadi U B, Sharma R, Raghav N. Gupta O P, Sheoran S, Sharma P, Singh R, Rai A, Singh G P, Kumar D, Iquebal M A, Tiwari R. 2022. RNA-Seq analysis of developing grains of wheat to intrigue into the complex molecular mechanism of the heat stress response. Frontiers in Plant Science13, 904392–904407.

Pelleschi S, Rocher J P, Prioul J L. 1997. Effect of water restriction on carbohydrate metabolism and photosynthesis in mature maize leaves. Plant Cell and Environment20, 493–503.

Pepin N, Bradley R S, Diaz H F, Baraer M, Caceres E B, Forsythe N, Fowler H, Greenwood G, Hashmi M Z, Liu X D. 2015. Elevation-dependent warming in mountain regions of the world. Nature Climate Change5, 424–430.

Porter J R, Gawith M. 1999. Temperatures and the growth and development of wheat: A review. European Journal of Agronomy10, 23–36.

Qi Y X, Liu Y B, Rong W H. 2011. RNA-Seq and its applications: A new technology for transcriptomics. Hereditas33, 1191–1202. (in Chinese)

Qiao Q, Wang Q, Han X, Guan Y L, Sun H, Zhong Y, Huang J L, Zhang T C. 2016. Transcriptome sequencing of Crucihimalaya himalaica (Brassicaceae) reveals how Arabidopsis close relative adapt to the Qinghai–Tibet Plateau. Scientific Reports6, 212729–212736.

Shi S B, Chen T, Zhao X M. 2010. Transcriptome platforms and applications to metabolic engineering. Chinese Journal of Biotechnology26, 1187–1198.

Tanaka R, Koshino Y, Sawa S, Ishiguro S, Okada K, Tanaka A. 2010. Overexpression of chlorophyllide a oxygenase (CAO) enlarges the antenna size of photosystem II in Arabidopsis thalianaThe Plant Journal26, 365–373.

Tian J S, Hu Y Y, Gan X X, Zhang Y L, Hu X B, Gou L, Luo H H, Zhang W F. 2013. Effects of increased night temperature on cellulose synthesis and the activity of sucrose metabolism enzymes in cotton fiber. Journal of Integrative Agriculture12, 979–988.

Tian Z W, Yin Y Y, Li B W, Zhong K T, Liu X X, Jiang D, Cao W X, Dai T B. 2024. Optimizing planting density and nitrogen application to mitigate yield loss and improve grain quality of late-sown wheat under rice–wheat rotation. Journal of Integrative Agriculture23, 2095–3119.

Volder A, Edwards E J, Evans J R, Robertson B C, Schortemeyer M, Gifford R M. 2004. Does greater night-time, rather than constant, warming alter growth of managed pasture under under ambient and elevated atmospheric CO2New Phytologist162, 397–411.

Wang F, Sanz A, Brenner M L, Smith A. 1993. Sucrose synthase, starch accumulation, and tomato fruit sink strength. Plant Physiology101, 321–327.

Wang W J, Wang G J, Wang Y H. 2007. Dynamic changes of activities of key enzymes involved in sucrose metabolism during grain filling in wheat and the relationship with starch accumulation in grain. Journal of Crop Science33, 1122–1128. (in Chinese)

Wang X, Cai J, Liu F, Jin M. 2011. Pre-anthesis high-temperature acclimation alleviates damage to the flag leaf caused by post-anthesis heat stress in wheat. Journal of Plant Physiology168, 585–593.

Wang X, Cai J, Liu F L, Jin M, Yu H X, Jiang D, Wollenweber B, Dai T B, Cao W X. 2012. Preanthesis high temperature acclimation alleviates the negative effects of post-anthesis heat stress on stem stored carbohydrates remobilization and grain starch accumulation in wheat. Journal of Cereal Science55, 331–336.

Wang X J, Liang H Y, Guo D L, Guo L L, Duan X G, Jia Q S, Hou X G. 2019. Integrated analysis of transcriptomic and proteomic data from tree peony (Postii) seeds reveals key developmental stages and candidate genes related to oil biosynthesis and fatty acid metabolism. Horticulture Research6, 111–129.

Xin M, Wang Y, Yao Y, Xie C, Peng H, Ni Z, Sun Q. 2010. Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). BMC Plant Biology10, 123–133.

Xiong W, Holman I P, You L Z, Yang J, Wu W B. 2014. Impacts of observed growing-season warming trends since 1980 on crop yields in China. Regional Environmental Change14, 7–16.

Yamakawa H, Hakata M. 2010. Atlas of rice grain filling-related metabolism under high temperature: Joint analysis of metabolome and transcriptome demonstrated inhibition of starch accumulation and induction of amino acid accumulation. Plant & Cell Physiology51, 795–809.

Zhai L C, Wang Z, Song S J, Zhang L H, Zhang Z B, Jia X L. 2020. Tillage practices affects the grain filling of inferior kernel of summer maize by regulating soil water content and photosynthetic capacity. Agricultural Water Management245, 106600–106611.

Zhang C. 2011. Effect of sucrose metabolism and starch accumulation on different wheat under drought or re-water during filing stage. MSc thesis, Northwest A&F University. (in Chinese)

Zhang D, Duan X L, Shang B, Hong Y, Sun H. 2021. Analysis of lipidomics profile of rice and changes during storage by UPLC-Q-Extractive Orbitrap mass spectrometry. Food Research International142, 110214–110221.

Zhang W, Voloudakis G, Rajagopal V M, Readhead B, Dudley J T, Schadt E E, Björkegren J L M, Kim Y, Fullard J F, Hoffman G E, Roussos P. 2019. Integrative transcriptome imputation reveals tissue-specific and shared biological mechanisms mediating susceptibility to complex traits. Nature Communications10, 3834–3846.

Zhang Y J, Shou W K, Maucieri C, Lin F. 2021. Rainfall increasing offsets the negative effects of nighttime warming on GHGs and wheat yield in North China Plain. Scientific Reports11, 6505–6514.

Zhang Z Z, Cheng S, Fan P, Zhou N B, Xing Z P, Hu Y J, Xu F F, Guo B W, Wei H Y, Zhang H C. 2023. Effects of sowing date and ecological points on yield and the temperature and radiation resources of semi-winter wheat. Journal of Integrative Agriculture22, 1366–1380.

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