Combined Transcriptomic and Metabolomic Analysis of Spinach under Cold and Heat Stress

doi:10.7668/hbnxb.20195231

Abstract

Abstract:

Temperature stress is one of the main nonbiological stresses that affect the quality and yield of spinach.Investigating the molecular response mechanism of spinach to temperature stress is crucial for spinach stress tolerance breeding.To provide a theoretical basis for the research of the mechanism of spinach resistant to cold stress and heat stress,this study used the cold-tolerant inbred line D3 and the heat-tolerant inbred line M10 of spinach as experimental materials and analyzed their transcriptomes and metabolomes under cold and heat stress to explore the transcriptional and metabolic mechanisms underlying spinach tolerance.Transcriptomic analysis showed that the pathways in which the DEGs were the most enriched in D3 and M10 were essentially the same under cold stress and heat stress.Metabolomics analysis showed that under cold stress,they were coenriched in the pyrimidine metabolism and lysine degradation in KEGG pathways.Under heat stress,these were mainly enriched in the tryptophan metabolism,toluene degradation,biosynthesis of various other secondary metabolites,and glycine,serine and threonine metabolism in KEGG pathways.The joint transcriptomic and metabolomic analysis indicated that through data analysis and gene annotation.SpADH(sov2g036390),SpSHMT(sov1g001130)and SpALDH-1(sov4g007150)were identified as the candidate genes for cold stress tolerance in spinach.SpALDH-1(sov4g007150),SpALDH-2(sov1g043320)and SpNPC(sov1g040610)were identified as candidate genes for heat stress in spinach.Among them,SpALDH-1(sov4g007150),which may be a regulatory gene for spinach stress tolerance,was significantly expressed under both cold and heat stress.

Key words: Spinach, Cold stress, Heat stress, Transcriptome, Metabolome, Candidate gene

GONG Rui, ZHANG Linlin, CUI Yanling, CHEN Haili, LI Ranhong, QIAN Zongwei. Combined Transcriptomic and Metabolomic Analysis of Spinach under Cold and Heat Stress[J]. Acta Agriculturae Boreali-Sinica, 2024, 39(6): 27-39. doi: 10.7668/hbnxb.20195231.

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http://www.hbnxb.net/EN/Y2024/V39/I6/27

Figures/Tables 11

Fig.1 Spinach D3,M10 inbred lines

Fig.2 KEGG pathway enrichment analysis of differentially expressed genes of D3(A)and M10(B)under cold stress A.KEGG pathway enrichment analysis of differentially expressed genes of D3 under cold stress:1.Endocytosis,2.Peroxisome,3.Phagosome,4.Plant hormone signal transduction,5.MAPK signaling pathway-plant,6.Phosphatidylinositol signaling system,7.ABC transporters,8.Ribosome,9.Protein processing in endoplasmic reticulum,10.Spliceosome,11.RNA transport,12.Carbon metabolism,13.Starch and sucrose metabolism,14.Biosynthesis of amino acids,15.Phenylpropanoid biosynthesis,16.Plant-pathogen interaction,17.Circadian rhythm-plant;B.KEGG pathway enrichment analysis of differentially expressed genes of M10 under cold stress:1.Endocytosis,2.Phagosome,3.Peroxisome,4.Plant hormone signal transduction,5.MAPK signaling pathway-plant,6.Phosphatidylinositol signaling system,7.ABC transporters,8.Protein processing in endoplasmic reticulum,9.Spliceosome,10.Ribosome,11.RNA transport,12.Carbon metabolism,13.Starch and sucrose metabolism,14.Biosynthesis of amino acids,15.Phenylpropanoid biosynthesis,16.Plant-pathogen interaction,17.Circadian rhythm-plant.

Fig.3 KEGG pathway enrichment analysis of differentially expressed genes D3(A)and M10(B)under heat stress A.KEGG pathway enrichment analysis of differentially expressed genes of D3 under heat stress:1.Endocytosis,2.Peroxisome,3.Plant hormone signal transduction,4.MAPK signaling pathway-plant,5.ABC transporters,6.Phosphatidylinositol signaling system,7.Ribosome,8.Protein processing in endoplasmic reticulum,9.RNA transport,10.Ubiquitin mediated proteolysis,11.Carbon metabolism,12.Biosynthesis of amino acids,13.Starch and sucrose metabolism,14.Phenylpropanoid biosynthesis,15.Plant-pathogen interaction,16.Circadian rhythm-plant;B.KEGG pathway enrichment analysis of differentially expressed genes of M10 under heat stress:1.Endocytosis,2.Peroxisome,3.Phagosome,4.Plant hormone signal transduction,5.MAPK signaling pathway-plant,6.ABC transporters,7.Phosphatidylinositol signaling system,8.Ribosome,9.Protein processing in endoplasmic reticulum,10.Spliceosome,11.RNA transport,12.Carbon metabolism,13.Starch and sucrose metabolism,14.Biosynthesis of amino acids,15.Phenylpropanoid biosynthesis,16.Plant-pathogen interaction,17.Circadian rhythm-plant.

Fig.4 KEGG pathways of the top 20 significantly enriched differentially enriched metabolites in D3(A)and M10(B)under cold stress A.KEGG of the top 20 significantly enriched differentially enriched metabolites in D3 under cold stress:1.Pyrimidine metabolism,2.Tryptophan metabolism,3.Methane metabolism,4.Lysine degradation,5.HIF-1 signaling pathway,6.Proximal tubule bicarbonate reclamation,7.Renal cell carcinoma,8.Carbon fixation in photosynthetic organisms,9.Ascorbate and aldarate metabolism,10.Fatty acid degradation,11.Drug metabolism-other enzymes,12.Glucagon signaling pathway,13.Citrate cycle(TCA cycle),14.Lysine biosynthesis,15.Pyruvate metabolism,16.Two-component system,17.Taste transduction,18.Pathways in cancer,19.Glutathione metabolism,20.Glyoxylate and dicarboxylate metabolism;B.KEGG of the top 20 significantly enriched differentially enriched metabolites in M10 under cold stress:1.Benzoate degradation,2.Lysine degradation,3.Pyrimidine metabolism,4.Phenylpropanoid biosynthesis,5.Stilbenoid,diarylheptanoid and gingerol biosynthesis,6.Lysine biosynthesis,7.Pyruvate metabolism,8.Glyoxylate and dicarboxylate metabolism,9.Carbon fixation pathways in prokaryotes,10.Toluene degradation,11.Diterpenoid biosynthesis,12.Biosynthesis of various other secondary metabolites,13.Vaine,leucine and isoleucine degradation,14.Zeatin biosynthesis,15.Polycyclic aromatic hydrocarbon degradation,16.Phosphatidylinositol signaling system,17.Proximal tubule bicarbonate reclamation,18.Renal cell carcinoma,19.Galactose metabolism,20.Carbon fixation in photosynthetic organism.

Fig.5 KEGG pathways of the first 20 significantly enriched differential metabolites of D3(A)and M10(B)under heat stress A.KEGG pathways of the top 20 significantly enriched differentially enriched metabolites in D3 under heat stress:1.Pyrimidine metabolism,2.Caprolactam degradation,3.Toluene degradation,4.Biosynthesis of various other secondary metabolites,5.Glycine,serine and threonine metabolism,6.Furfural degradation,7.C5-Branched dibasic acid metabolism,8.Indole alkaloid biosynthesis,9.Chemical carcinogenesis-reactive oxygen species,10.Choline metabolism in cancer,11.Chlorocyclohexane and chlorobenzene degradation,12.Teichoic acid biosynthesis,13.Glycerophospholipid metabolism,14.Axon regeneration,15.African trypanosomiasis,16.Naphthalene degradation,17.Styrene degradation,18.Isoflavonoid biosynthesis,19.Dopaminergic synapse,20.Prolactin signaling pathway;B.KEGG pathways of the top 20 significantly enriched differentially enriched metabolites in M10 under heat stress:1.Biosynthesis of plant hormones,2.Biosynthesis of plant secondary metabolites,3.Tryptophan metabolism,4.α-Linolenic acid metabolism,5.Purine metabolism,6.Limonene and pinene degradation,7.Aminoacyl-tRNA biosynthesis,8.Benzoate degradation,9.Carbon fixation pathways in prokaryotes,10.Plant hormone signal transduction,11.Neomycin,kanamycin and gentamicin biosynthesis,12.Toluene degradation,13.Biosynthesis of various other secondary metabolites,14.Zeatin biosynthesis,15.Biosynthesis of various alkaloids,16.Biosynthesis of unsaturated fatty acids,17.Glycine,serine and threonine metabolism,18.Indole alkaloid biosynthesis,19.Chemical carcinogenesis-reactive oxygen species,20.Fatty acid degradation.

Fig.6 KEGG enrichment of the top 30 metabolic pathways with significant enrichment of D3(A)and M10(B)differential genes/metabolites under cold stress A.KEGG enrichment of the top 30 metabolic pathways with significant enrichment of D3 differential genes/metabolites under cold stress:1.Phenylalanine metabolism,2.Tryptophan metabolism,3.Terpenoid backbone biosynthesis,4.Phenylalanine,tyrosine and tryptophan biosynthesis,5.Phenylpropanoid biosynthesis,6.Riboflavin metabolism,7.Cysteine and methionine metabolism,8.Vitamin B6 metabolism,9.Histidine metabolism,10.Biosynthesis of amino acids,11.Pyrimidine metabolism,12.Ubiquinone and other terpenoid-quinone biosynthesis,13.Tyrosine metabolism,14.Monobactam biosynthesis,15.Arginine and proline metabolism,16.Citrate cycle(TCA cycle),17.Purine metabolism,18.Butanoate metabolism,19.Pyruvate metabolism,20.Alanine,aspartate and glutamate metabolism,21.β-Alanine metabolism,22.α-Linolenic acid metabolism,23.Glyoxylate and dicarboxylate metabolism,24.Thiamine metabolism,25.Valine,leucine and isoleucine degradation,26.Glycine,serine and threonine metabolism,27.Fatty acid degradation,28.Propanoate metabolism,29.Carbon fixation in photosynthetic organisms,30.Carbon metabolism;B:KEGG enrichment of the top 30 metabolic pathways with significant enrichment of M10 differential genes/metabolites under cold stress:1.Diterpenoid biosynthesis,2.Biosynthesis of amino acids,3.Limonene and pinene degradation,4.Thiamine metabolism,5.lsoquinoline alkaloid biosynthesis,6.Pyruvate metabolism,7.Alanine,aspartate and glutamate metabolism,8.Tyrosine metabolism,9.Nicotinate and nicotinamide metabolism,10.Vitamin B6 metabolism,11.Folate biosynthesis,12.Purine metabolism,13.β-Alanine metabolism,14.Arachidonic acid metabolism,15.One carbon pool by folate,16.Glycine,serine and threonine metabolism,17.Fatty acid degradation,18.Cysteine and methionine metabolism,19.Phosphatidylinositol signaling system,20.Photosynthesis,21.Steroid biosynthesis,22.Fatty acid metabolism,23.Inositol phosphate metabolism,24.Valine,leucine and isoleucine degradation,25.Glyoxylate and dicarboxylate metabolism,26.Propanoate metabolism,27.Carbon fixation in photosynthetic organisms,28.α-Linolenic acid metabolism,29.Citrate cycle(TCA cycle),30.Carbon metabolism.

Fig.7 Correlation network of DEGs and DAMs of D3 in the α-Linolenic acid metabolism pathway under cold stress The circles represent metabolites,the squares represent genes,and the numbers on the line represent correlation coefficients.Positive correlations are red,negative correlations are green,and the larger the correlation coefficients,the wider the lines and the darker the colors.The same as Fig.9.

Fig.8 KEGG enrichment for the top 30 pathways significantly enriched in D3(A) and M10(B)differential genes/metabolites under heat stress A.KEGG enrichment of the top 30 metabolic pathways with significant enrichment of D3 differential genes/metabolites under heat stress:1.Monobactam biosynthesis,2.Purine metabolism,3.Limonene and pinene degradation,4.Photosynthesis,5.Tyrosine metabolism,6.Citrate cycle(TCA cycle),7.Plant hormone signal transduction,8.Stilbenoid,diarylheptanoid and gingerol biosynthesis,9.Arginine and proline metabolism,10.Phenylalanine,tyrosine and tryptophan biosynthesis,11.Ubiquinone and other terpenoid-quinone biosynthesis,12.Glycine,serine and threonine metabolism,13.Biosynthesis of unsaturated fatty acids,14.Isoflavonoid biosynthesis,15.Phosphonate and phosphinate metabolism,16.Biosynthesis of amino acids,17.β-Alanine metabolism,18.Cysteine and methionine metabolism,19.Steroid biosynthesis,20.Sulfur metabolism,21.Thiamine metabolism,22.Vitamin B6 metabolism,23.Amino sugar and nucleotide sugar metabolism,24.Propanoate metabolism,25.Glycerophospholipid metabolism,26.Valine,leucine and isoleucine degradation,27.α-Linolenic acid metabolism,28.Carbon fixation in photosynthetic organisms,29.Glyoxylate and dicarboxylate metabolism,30.Carbon metabolism;B:KEGG enrichment of the top 30 metabolic pathways with significant enrichment of M10 differential genes/metabolites under heat stress:1.Betalain biosynthesis,2.ABC transporters,3.Vitamin B6 metabolism,4.Linoleic acid metabolism,5.Pantothenate and CoA biosynthesis,6.Monoterpenoid biosynthesis,7.Propanoate metabolism,8.Cysteine and methionine metabolism,9.Amino sugar and nucleotide sugar metabolism,10.Monobactam biosynthesis,11.Biosynthesis of unsaturated fatty acids,12.Terpenoid backbone biosynthesis,13.Ubiquinone and other terpenoid-quinone biosynthesis,14.Plant hormone signal transduction,15.Limonene and pinene degradation,16.Butanoate metabolism,17.Thiamine metabolism,18.Steroid biosynthesis,19.β-Alanine metabolism,20.Histidine metabolism,21.Arginine and proline metabolism,22.Flavonoid biosynthesis,23.Folate biosynthesis,24.Arachidonic acid metabolism,25.Nicotinate and nicotinamide metabolism,26.Valine,leucine and isoleucine degradation,27.Glycerophospholipid metabolism,28.Fatty acid metabolism,29.α-Linolenic acid metabolism,30.Fatty acid degradation.

Fig.9 Correlation network of DEGs and DAMs in the α-Linolenic acid metabolism pathway of D3 under heat stress

Fig.10 Relative expression of D3 and M10 candidate genes under cold stress Different lowercase letters indicate significant differences(P<0.05).The same as Fig.11.

Fig.11 Relative expression of D3 and M10 candidate genes under heat stress

References 41

[1]	Khattak J Z K, Torp A M, Andersen S B. A genetic linkage map of Spinacia oleracea and localization of a sex determination locus[J]. Euphytica, 2006, 148(3):311-318.doi:10.1007/s10681-005-9031-1.
[2]	Cai X F, Sun X P, Xu C X, Sun H H, Wang X L, Ge C H, Zhang Z H, Wang Q X, Fei Z J, Jiao C, Wang Q H. Genomic analyses provide insights into spinach domestication and the genetic basis of agronomic traits[J]. Nature Communications, 2021, 12(1):7246.doi:10.1038/s41467-021-27432-z. pmid: 34903739
[3]	Huang H, Yan L, Zhang Y, Raza A, Liu Z, Lü Y, Ding X Y, Cheng Y, Zou X L. Study on the mechanism of exogenous serotonin improving cold tolerance of rapeseed(Brassica napus L.) seedlings[J]. Plant Growth Regulation, 2021, 94(2):161-170.doi:10.1007/s10725-021-00700-0.
[4]	Raza H, Khan M R, Zafar S A, Kirch H H, Bartles D. Aldehyde dehydrogenase 3I1 gene is recruited in conferring multiple abiotic stress tolerance in plants[J]. Plant Biology, 2022, 24(1):85-94.doi:10.1111/plb.13337.
[5]	罗健东, 邱梦青, 周慧敏, 解为玮, 黄海鑫, 刘洁琪, 张梓敏, 徐健, 陈程杰, 何业华, 刘朝阳. 菠萝AcZFP1的克隆及其在低温胁迫下的功能分析[J]. 园艺学报, 2024, 51(3):495-508.doi:10.16420/j.issn.0513-353x.2023-0089.
	Luo J D, Qiu M Q, Zhou H M, Xie W W, Huang H X, Liu J Q, Zhang Z M, Xu J, Chen C J, He Y H, Liu C Y. Cloning and functional analysis of pineapple AcZFP1 gene under low temperature stress[J]. Acta Horticulturae Sinica, 2024, 51(3):495-508.
[6]	Fang C X, Zhang P L, Li L L, Yang L K, Mu D, Yan X, Li Z, Lin W X. Serine hydroxymethyltransferase localised in the endoplasmic reticulum plays a role in scavenging H₂O₂ to enhance rice chilling tolerance[J]. BMC Plant Biology, 2020, 20(1):236.doi:10.1186/s12870-020-02446-9.
[7]	Wang Z Y, Zhang Y M, Hu H F, Chen L, Zhang H F, Chen R G. CabHLH79 acts upstream of CaNAC035 to regulate cold stress in pepper[J]. International Journal of Molecular Sciences, 2022, 23(5):2537.doi:10.3390/ijms23052537.
[8]	Su W H, Ren Y J, Wang D J, Su Y C, Feng J F, Zhang C, Tang H C, Xu L P, Muhammad K, Que Y X. The alcohol dehydrogenase gene family in sugarcane and its involvement in cold stress regulation[J]. BMC Genomics, 2020, 21(1):521.doi:10.1186/s12864-020-06929-9. pmid: 32727370
[9]	Cai B B, Li Q, Xu Y C, Yang L, Bi H G, Ai X Z. Genome-wide analysis of the fructose 1,6-bisphosphate aldolase(FBA)gene family and functional characterization of FBA7 in tomato[J]. Plant Physiology and Biochemistry, 2016, 108:251-265.doi:10.1016/j.plaphy.2016.07.019.
[10]	李月, 孔丽颖, 李才运, 李翔, 代培红, 刘晓东. 海岛棉GbCBF6基因克隆及其在逆境胁迫下的表达分析[J]. 西北植物学报, 2015, 35(10):1949-1955.doi:10.7606/j.issn.1000-4025.2015.10.1949.
	Li Y, Kong L Y, Li C Y, Li X, Dai P H, Liu X D. Molecular cloning of GbCBF6 gene and its expression in cotton(Gossypium barbadense L.)[J]. Acta Botanica Boreali-Occidentalia Sinica, 2015, 35(10):1949-1955.
[11]	Kaye C, Neven L, Hofig A, Li Q B, Haskell D, Guy C. Characterization of a gene for spinach CAP160 and expression of two spinach cold-acclimation proteins in tobacco[J]. Plant Physiology, 1998, 116(4):1367-1377.doi:10.1104/pp.116.4.1367. pmid: 9536054
[12]	Fan W J, Zhang M, Zhang H X, Zhang P. Improved tolerance to various abiotic stresses in transgenic sweet potato(Ipomoea batatas)expressing spinach betaine aldehyde dehydrogenase[J]. PLoS One, 2012, 7(5):e37344.doi:10.1371/journal.pone.0037344.
[13]	Krishna P, Sacco M, Cherutti J F, Hill S. Cold-induced accumulation of hsp90 transcripts in Brassica napus[J]. Plant Physiology, 1995, 107(3):915-923.doi:10.1104/pp.107.3.915. pmid: 12228411
[14]	Zhao J Y, Missihoun T D, Bartels D. The role of Arabidopsis aldehyde dehydrogenase genes in response to high temperature and stress combinations[J]. Journal of Experimental Botany, 2017, 68(15):4295-4308.doi:10.1093/jxb/erx194.
[15]	Krčková Z, Brouzdová J, Daněk M, Kocourková D, Rainteau D, Ruelland E, Valentová O, Pejchar P, Martinec J. Arabidopsis non-specific phospholipase C1:characterization and its involvement in response to heat stress[J]. Frontiers in Plant Science, 2015,6:928.doi:10.3389/fpls.2015.00928.
[16]	Poonia A K, Mishra S K, Sirohi P, Chaudhary R, Kanwar M, Germain H, Chauhan H. Overexpression of wheat transcription factor(TaHsfA6b)provides thermotolerance in barley[J]. Planta, 2020, 252(4):53.doi:10.1007/s00425-020-03457-4.
[17]	Casaretto J A, El-Kereamy A, Zeng B, Stiegelmeyer S M, Chen X, Bi Y M, Rothstein S J. Expression of OsMYB55 in maize activates stress-responsive genes and enhances heat and drought tolerance[J]. BMC Genomics, 2016,17:312.doi:10.1186/s12864-016-2659-5.
[18]	董立红, 范瑞, 陈永欣, 翟广谦, 张璐, 李文和. 玉米热激转录因子基因ZmHSF05的克隆与功能分析[J]. 西北植物学报, 2020, 40(8):1294-1302.doi:10.7606/j.issn.1000-4025.2020.08.1294.
	Dong L H, Fan R, Chen Y X, Zhai G Q, Zhang L, Li W H. Cloning and functional analysis of maize heat shock transcription factor gene ZmHSF05[J]. Acta Botanica Boreali-Occidentalia Sinica, 2020, 40(8):1294-1302.
[19]	Qi C D, Lin X P, Li S T, Liu L, Wang Z R, Li Y, Bai R Y, Xie Q, Zhang N, Ren S X, Zhao B, Li X D, Fan S X, Guo Y D. SoHSC70 positively regulates thermotolerance by alleviating cell membrane damage,reducing ROS accumulation,and improving activities of antioxidant enzymes[J]. Plant Science, 2019, 283:385-395.doi:10.1016/j.plantsci.2019.03.003.
[20]	Li Y, Zhang H, Zhang Y X, Liu Y S, Li Y Y, Tian H D, Guo S Y, Sun M H, Qin Z, Dai S J. Genome-wide identification and expression analysis reveals spinach brassinosteroid-signaling kinase(BSK)gene family functions in temperature stress response[J]. BMC Genomics, 2022, 23(1):453.doi:10.1186/s12864-022-08684-5.
[21]	Collins K, Zhao K, Jiao C, Xu C X, Cai X F, Wang X L, Ge C H, Dai S J, Wang Q X, Wang Q H, Fei Z J, Zheng Y. SpinachBase:a central portal for spinach genomics[J]. Database, 2019,2019:baz072.doi:10.1093/database/baz072.
[22]	Sharif R, Raza A, Chen P, Li Y H, El-Ballat E M, Rauf A, Hano C, El-Esawi M A. HD-ZIP gene family:potential roles in improving plant growth and regulating stress-responsive mechanisms in plants[J]. Genes, 2021, 12(8):1256.doi:10.3390/genes12081256.
[23]	Naranjo-Arcos M, Srivastava M, Deligne F, Bhagat P K, Mansi M, Sadanandom A, Vert G. SUMO/deSUMOylation of the BRI1 brassinosteroid receptor modulates plant growth responses to temperature[J]. Proceedings of the National Academy of Sciences of the United States of America, 2023, 120(4):e2217255120.doi:10.1073/pnas.2217255120.
[24]	Huang J Y, Zhao X B, Bürger M, Chory J, Wang X C. The role of ethylene in plant temperature stress response[J]. Trends in Plant Science, 2023, 28(7):808-824.doi:10.1016/j.tplants.2023.03.001. pmid: 37055243
[25]	Yin Y L, Qin K Z, Song X W, Zhang Q H, Zhou Y H, Xia X J, Yu J Q. BZR1 transcription factor regulates heat stress tolerance through FERONIA receptor-like kinase-mediated reactive oxygen species signaling in tomato[J]. Plant & Cell Physiology, 2018, 59(11):2239-2254.doi:10.1093/pcp/pcy146.
[26]	Yao Y, He R J, Xie Q L, Zhao X H, Deng X M, He J B, Song L L, He J, Marchant A, Chen X Y, Wu A M. ETHYLENE RESPONSE FACTOR 74(ERF74)plays an essential role in controlling a respiratory burst oxidase homolog D(RbohD)-dependent mechanism in response to different stresses in Arabidopsis[J]. The New Phytologist, 2017, 213(4):1667-1681.doi:10.1111/nph.14278.
[27]	Wang X Y, Zhuang L L, Shi Y, Huang B R. Up-regulation of HSFA2c and HSPs by ABA contributing to improved heat tolerance in tall fescue and Arabidopsis[J]. International Journal of Molecular Sciences, 2017, 18(9):1981.doi:10.3390/ijms18091981.
[28]	Yu H S, Kong X F, Huang H, Wu W W, Park J, Yun D J, Lee B H, Shi H Z, Zhu J K. STCH₄/REIL2 confers cold stress tolerance in Arabidopsis by promoting rRNA processing and CBF protein translation[J]. Cell Reports, 2020, 30(1):229-242.e5.doi:10.1016/j.celrep.2019.12.012.
[29]	Duran Garzon C, Lequart M, Rautengarten C, Bassard S, Sellier-Richard H, Baldet P, Heazlewood J L, Gibon Y, Domon J M, Giauffret C, Rayon C. Regulation of carbon metabolism in two maize sister lines contrasted for chilling tolerance[J]. Journal of Experimental Botany, 2020, 71(1):356-369.doi:10.1093/jxb/erz421. pmid: 31557299
[30]	Shen J Z, Zhang D Y, Zhou L, Zhang X Z, Liao J R, Duan Y, Wen B, Ma Y C, Wang Y H, Fang W P, Zhu X J. Transcriptomic and metabolomic profiling of Camellia sinensis L.cv.Suchazao exposed to temperature stresses reveals modification in protein synthesis and photosynthetic and anthocyanin biosynthetic pathways[J]. Tree Physiology, 2019, 39(9):1583-1599.doi:10.1093/treephys/tpz059.
[31]	Khakimov B, Jespersen B M, Engelsen S B. Comprehensive and comparative metabolomic profiling of wheat,barley,oat and rye using gas chromatography-mass spectrometry and advanced chemometrics[J]. Foods, 2014, 3(4):569-585.doi:10.3390/foods3040569. pmid: 28234338
[32]	Wei J P, Zheng G Q, Yu X W, Liu S S, Dong X Y, Cao X D, Fang X L, Li H, Jin J J, Mi W B, Liu Z G. Comparative transcriptomics and proteomics analyses of leaves reveals a freezing stress-responsive molecular network in winter rapeseed(Brassica rapa L.)[J]. Frontiers in Plant Science, 2021,12:664311.doi:10.3389/fpls.2021.664311.
[33]	El-Kereamy A, Bi Y M, Ranathunge K, Beatty P H, Good A G, Rothstein S J. The rice R2R3-MYB transcription factor OsMYB55 is involved in the tolerance to high temperature and modulates amino acid metabolism[J]. PLoS One, 2012, 7(12):e52030.doi:10.1371/journal.pone.0052030.
[34]	Chen L, Liang Z J, Xie S Y, Liu W R, Wang M, Yan J Q, Yang S G, Jiang B, Peng Q W, Lin Y E. Responses of differential metabolites and pathways to high temperature in cucumber anther[J]. Frontiers in Plant Science, 2023,14:1131735.doi:10.3389/fpls.2023.1131735.
[35]	Wang J Y, Yuan B, Xu Y, Huang B R. Differential responses of amino acids and soluble proteins to heat stress associated with genetic variations in heat tolerance for hard fescue[J]. Journal of the American Society for Horticultural Science, 2018, 143(1):45-55.doi:10.21273/jashs04246-17.
[36]	Zhu X L, Zhang S B, Li X, Wang X Q, Li Z D, Zhu X Y, Liu X X, Li H X, Zhang J, Chen X L. Integrative analysis of high temperature-induced transcriptome and metabolome alterations in the leaves of five raspberry(Rubus ideaus L.) cultivars[J]. Environmental and Experimental Botany, 2022,203:105038.doi:10.1016/j.envexpbot.2022.105038.
[37]	Davik J, Koehler G, From B, Torp T, Rohloff J, Eidem P, Wilson R C, Sønsteby A, Randall S K, Alsheikh M. Dehydrin,alcohol dehydrogenase,and central metabolite levels are associated with cold tolerance in diploid strawberry(Fragaria spp.)[J]. Planta, 2013, 237(1):265-277.doi:10.1007/s00425-012-1771-2. pmid: 23014928
[38]	Zhu Q D, Han Y D, Yang W T, Zhu H, Li G T, Xu K, Long M X. Genome-wide identification and characterization of ADH gene family and the expression under different abiotic stresses in tomato(Solanum lycopersicum L.)[J]. Frontiers in Genetics, 2023,14:1186192.doi:10.3389/fgene.2023.1186192.
[39]	Liu Z S, Pan X J, Wang C L, Yun F H, Huang D J, Yao Y D, Gao R, Ye F J, Liu X J, Liao W B. Genome-wide identification and expression analysis of serine hydroxymethyltransferase(SHMT)gene family in tomato(Solanum lycopersicum)[J]. PeerJ, 2022,10:e12943.doi:10.7717/peerj.12943.
[40]	Chen Z, Chen M, Xu Z S, Li L C, Chen X P, Ma Y Z. Characteristics and expression patterns of the aldehyde dehydrogenase(ALDH)gene superfamily of foxtail millet(Setaria italica L.)[J]. PLoS One, 2014, 9(7):e101136.doi:10.1371/journal.pone.0101136.
[41]	Guo J B, Sun W, Liu H Y, Chi J L, Odiba A S, Li G C, Jin L P, Xin C H. Aldehyde dehydrogenase plays crucial roles in response to lower temperature stress in Solanum tuberosum and Nicotiana benthamiana[J]. Plant Science, 2020,297:110525.doi:10.1016/j.plantsci.2020.110525.

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