Comprehensive analysis of the gene expression profile of wheat at the crossroads of heat, drought and combined stress

Alsamman M. Alsamman, Ratiba Bousba, Michael Baum, Aladdin Hamwieh, Nourhan Fouad


Heat and drought are among the leading environmental stresses which have a major impact on plant development. In our research, identification and characterization of differentially expressed genes (DEGs) regulating the response of wheat to drought, heat and combined stress was carried out. We analyzed data from the Gene Expression Omnibus database (GEO) microarrays containing 24 samples of wheat, which were categorized by different treatments (control: ctrl, drought: D, heat: H, and mixed: HD). Significant DEGs were examined for gene annotation, gene ontology, co-expression, protein-protein interaction (PPI) and their heterogeneity and consistency through drought, heat and combined stress was also studied. Genes such as gyrB, C6orf132 homolog, PYR1 were highly associated with wheat response to drought with P-value (-log10) of 9.3, 7.3, 6.4, and logFC of -3.9, 2.0, 1.6, respectively. DEGs associated with drought tolerance were highly related to the protein domains of lipid-transfer (LTP). Wheat response to heat stress was strongly associated with genes such as RuBisCO activase B, small heat shock, LTP3, YLS3, At2g33490, PETH with p-values (-log10) ranging from 9.3 to 12.3. In addition, a relatively high number of protein interactions involved the SDH, PEPCK, and G6PD genes under heat stress.


Wheat, Drought, Heat, Combined stress, Gene expression

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Faostat F. Statistical databases. Food and Agriculture Organization of the United Nations. 2017;.

Carraro C, Edenhofer O, Flachsland C, Kolstad C, Stavins R, Stowe R. The IPCC at a crossroads: Opportunities for reform. Science. 2015;350(6256):34–35.

Lobell DB, Howden SM, Smith DR, Chhetri N. A meta-analysis of crop yield under climate change and adaptation, Nat. Clim Change. 2014;4(4):287–291.

Daryanto S, Wang L, Jacinthe PA. Global synthesis of drought effects on maize and wheat production. PloS one. 2016;11(5).

Lobell DB, Gourdji SM. The influence of climate change on global crop productivity. Plant physiology. 2012;160(4):1686–1697.

Trenberth KE, Dai A, Van Der Schrier G, Jones PD, Barichivich J, Briffa KR, et al. Global warming and changes in drought. Nature Climate Change. 2014;4(1):17–22.

Hakeem KR, Chandna R, Ahmad P, Iqbal M, Ozturk M. Relevance of proteomic investigations in plant abiotic stress physiology. Omics: a journal of integrative biology. 2012;16(11):621–635.

Al-Khatib K, Paulsen GM. Mode of high temperature injury to wheat during grain development. Physiologia plantarum. 1984; 61(3) :363–368.

Tack J, Barkley A, Nalley LL. Effect of warming temperatures on US wheat yields. Proceedings of the National Academy of Sciences. 2015;112(22):6931–6936.

Abhinandan K, Skori L, Stanic M, Hickerson N, Jamshed M, Samuel MA. Abiotic stress signaling in wheat–an inclusive over- view of hormonal interactions during abiotic stress responses in wheat. Frontiers in plant science. 2018;9:734.

Braun HJ, Atlin G, Payne T, et al. Multi-location testing as a tool to identify plant response to global climate change. Climate change and crop production. 2010;1:115–138.

DeSA UN, Others. World population prospects: the 2012 revision. Population division of the department of economic and social affairs of the United Nations Secretariat, New York. 2013;18.

Aiqing S, Somayanda I, Sebastian SV, Singh K, Gill K, Prasad PVV, et al. Heat stress during flowering affects time of day of flowering, seed set, and grain quality in spring wheat. Crop Science. 2018;58(1):380–392.

Farooq M, Bramley H, Palta JA, Siddique KHM. Heat stress in wheat during reproductive and grain-filling phases. Critical Reviews in Plant Sciences. 2011;30(6):491–507.

Sairam RK, Srivastava GC, Saxena DC. Increased antioxidant activity under elevated temperatures: a mechanism of heat stress tolerance in wheat genotypes. Biologia Plantarum. 2000;43(2):245–251.

Perdomo JA, Capó-Bauçà S, Carmo-Silva E, Galmés J. Rubisco and rubisco activase play an important role in the biochemical limitations of photosynthesis in rice, wheat, and maize under high temperature and water deficit. Frontiers in plant science. 2017;8:490.

Prasad PVV, Pisipati SR, Momčilović I, Ristic Z. Independent and combined effects of high temperature and drought stress during grain filling on plant yield and chloroplast EF-Tu expression in spring wheat. Journal of Agronomy and Crop Science. 2011;197(6):430–441.

Awasthi R, Kaushal N, Vadez V, Turner NC, Berger J, Siddique KHM, et al. Individual and combined effects of transient drought and heat stress on carbon assimilation and seed filling in chickpea. Functional Plant Biology. 2014;41(11):1148–1167.

Kang WH, Sim YM, Koo N, Nam JY, Lee J, Kim N, et al. Transcriptome profiling of abiotic responses to heat, cold, salt, and osmotic stress of Capsicum annuum L. Scientific Data. 2020;7(1):1–7.

Johnson SM, Lim FL, Finkler A, Fromm H, Slabas AR, Knight MR. Transcriptomic analysis of Sorghum bicolor responding to combined heat and drought stress. BMC genomics. 2014;15(1):456.

Liu Z, Xin M, Qin J, Peng H, Ni Z, Yao Y, et al. Temporal transcriptome profiling reveals expression partitioning of homeologous genes contributing to heat and drought acclimation in wheat (Triticum aestivum L.). BMC plant biology. 2015;15(1):152.

Tilman D, Balzer C, Hill J, Befort BL. Global food demand and the sustainable intensification of agriculture. Proceedings of the national academy of sciences. 2011;108(50):20260–20264.

Aprile A, Havlickova L, Panna R, Marè C, Borrelli GM, Marone D, et al. Different stress responsive strategies to drought and heat in two durum wheat cultivars with contrasting water use efficiency. BMC genomics. 2013;14(1):821.

Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic acids research. 1997;25(17):3389–3402.

Szklarczyk D, Morris JH, Cook H, Kuhn M, Wyder S, Simonovic M, et al. The STRING database in 2017: quality-controlled protein–protein association networks, made broadly accessible. Nucleic acids research. 2016;p. gkw937.

Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome research. 2003;13(11):2498–2504.

Cho HS, Lee SS, Kim KD, Hwang I, Lim JS, Park YI, et al. DNA gyrase is involved in chloroplast nucleoid partitioning. The Plant Cell. 2004;16(10):2665–2682.

Evans-Roberts KM, Breuer C, Wall MK, Sugimoto-Shirasu K, Maxwell A. Arabidopsis thaliana GYRB3 does not encode a DNA gyrase subunit. PloS one. 2010;5(3).

Manjulatha M, Sreevathsa R, Kumar AM, Sudhakar C, Prasad TG, Tuteja N, et al. Overexpression of a pea DNA helicase (PDH45) in peanut (Arachis hypogaea L.) confers improvement of cellular level tolerance and productivity under drought stress. Molecular biotechnology. 2014;56(2):111–125.

Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, et al. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. science. 2009;324(5930):1068–1071.

Dorosh L, Kharenko OA, Rajagopalan N, Loewen MC, Stepanova M. Molecular mechanisms in the activation of abscisic acid receptor PYR1. PLoS computational biology. 2013;9(6).

Hlaváčková I, V’itámvás P, Šantruuček J, Kosová K, Zelenková S, Prášil IT, et al. Proteins involved in distinct phases of cold hardening process in frost resistant winter barley (Hordeum vulgare L.) cv Luxor. International journal of molecular sciences. 2013;14(4):8000–8024.

V’itámvás P, Urban MO, Škodáček Z, Kosová K, Pitelková I, V’itámvás J, et al. Quantitative analysis of proteome extracted from barley crowns grown under different drought conditions. Frontiers in plant science. 2015;6:479.

González-Candelas L, Alamar S, Sánchez-Torres P, Zacar’ias L, Marcos JF. A transcriptomic approach highlights induction of secondary metabolism in citrus fruit in response to Penicillium digitatuminfection. BMC plant biology. 2010;10(1):194.

Attila C, Ueda A, Cirillo SLG, Cirillo JD, Chen W, Wood TK. Pseudomonas aeruginosa PAO1 virulence factors and poplar tree response in the rhizosphere. Microbial biotechnology. 2008;1(1):17–29.

Sui J, Li G, Chen G, Zhao C, Kong X, Hou X, et al. RNA-seq analysis reveals the role of a small GTP-binding protein, Rab7, in regulating clathrin-mediated endocytosis and salinity-stress resistance in peanut. Plant Biotechnology Reports. 2017;11(1):43–52.

Gupta S, Singh Y, Kumar H, Raj U, Rao AR, Varadwaj PK. Identification of novel abiotic stress proteins in Triticum aestivum through functional annotation of hypothetical proteins. Interdisciplinary Sciences: Computational Life Sciences. 2018;10(1):205–220.

Kumar RR, Goswami S, Dubey K, Singh K, Singh JP, Kumar A, et al. RuBisCo activaseâ[80? ][94? ]a catalytic chaperone involved in modulating the RuBisCo activity and heat stress-tolerance in wheat. Journal of plant biochemistry and biotechnology.2019; 28 (1):63–75.

Qu M, Bunce JA, Sicher RC, Zhu X, Gao B, Chen G. An attempt to interpret a biochemical mechanism of C4 photosynthetic thermo-tolerance under sudden heat shock on detached leaf in elevated CO2 grown maize. PloS one. 2017;12(12).

Zhang M, Kim Y, Zong J, Lin H, Dievart A, Li H, et al. Genome-wide analysis of the barley non-specific lipid transfer protein gene family. The Crop Journal. 2019;7(1):65–76.

Wang F, Zang Xs, Kabir MR, Liu Kl, Liu Zs, Ni Zf, et al. A wheat lipid transfer protein 3 could enhance the basal thermotolerance and oxidative stress resistance of Arabidopsis. Gene. 2014;550(1):18–26.

Altenbach SB, Kothari KM, Tanaka CK, Hurkman WJ. Expression of 9-kDa non-specific lipid transfer protein genes in developing wheat grain is enhanced by high temperatures but not by post-anthesis fertilizer. Journal of cereal science. 2008;47(2):201–213.

Das A, Eldakak M, Paudel B, Kim DW, Hemmati H, Basu C, et al. Leaf proteome analysis reveals prospective drought and heat stress response mechanisms in soybean. BioMed research international. 2016;2016.

Werwie M, Dworak L, Bottin A, Mayer L, Basché T, Wachtveitl J, et al. Light-harvesting chlorophyll protein (LHCII) drives electron transfer in semiconductor nanocrystals. Biochimica et Biophysica Acta (BBA)-Bioenergetics. 2018;1859(3):174–181.

Panchuk II, Volkov RA, Schöffl F. Heat stress-and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant physiology. 2002;129(2) :838–853.

Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D, et al. Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. Journal of Biological Chemistry. 2008;283(49):34197–34203.

Wang W, Vinocur B, Shoseyov O, Altman A. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends in plant science. 2004;9(5):244–252.

Kumar RR, Goswami S, Sharma SK, Kala YK, Rai GK, Mishra DC, et al. Harnessing next generation sequencing in climate change: RNA-Seq analysis of heat stress-responsive genes in wheat (Triticum aestivum L.). Omics: a journal of integrative biology. 2015;19(10):632–647.

Qi Z, Xiong L. Characterization of a Purine Permease Family Gene Os PUP 7 Involved in Growth and Development Control in Rice. Journal of integrative plant biology. 2013;55(11):1119–1135.

Sun M, Shen Y, Yin K, Guo Y, Cai X, Yang J, et al. A late embryogenesis abundant protein GsPM30 interacts with a receptor like cytoplasmic kinase GsCBRLK and regulates environmental stress responses. Plant Science. 2019;283:70–82.

Xu D, Duan X, Wang B, Hong B, Ho THD, Wu R. Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant physiology. 1996;110(1):249–257.

Nagaraju M, Kumar SA, Reddy PS, Kumar A, Rao DM, Kishor PBK. Genome-scale identification, classification, and tissue specific expression analysis of late embryogenesis abundant (LEA) genes under abiotic stress conditions in Sorghum bicolor L. PloS one. 2019;14(1).

Taniguchi S, HOSOKAWA-SHINONAGA Y, Tamaoki D, Yamada S, Akimitsu K, Gomi K. Jasmonate induction of the monoterpene linalool confers resistance to rice bacterial blight and its biosynthesis is regulated by JAZ protein in rice. Plant, cell & environment. 2014;37(2):451–461.

Savoi S, Wong DCJ, Arapitsas P, Miculan M, Bucchetti B, Peterlunger E, et al. Transcriptome and metabolite profiling reveals that prolonged drought modulates the phenylpropanoid and terpenoid pathway in white grapes (Vitis vinifera L.). BMC plant biology. 2016;16(1):67.

Baghery MA, Kamal S, Kazemitabar AD, Mehrabanjoubani P, Mehdi M, Naghizadeh AMN. Transcription Factors and micro RNA Genes Regulatory Network Construction Under Drought Stress in Sesame (Sesamum indicum L.). Research Square; 2020. DOI: 10.21203/rs.2.21135/v1.

Strathmann A, Kuhlmann M, Heinekamp T, Dröge-Laser W. BZI-1 specifically heterodimerises with the tobacco bZIP transcription factors BZI-2, BZI-3/TBZF and BZI-4, and is functionally involved in flower development. The Plant Journal. 2001; 28(4): 397–408.

Wang M, Wang Y, Zhang Y, Li C, Gong S, Yan S, et al. Comparative transcriptome analysis of salt-sensitive and salt-tolerant maize reveals potential mechanisms to enhance salt resistance. Genes & genomics. 2019;41(7):781–801.

Wu W, Zhu S, Chen Q, Lin Y, Tian J, Liang C. Cell Wall Proteins Play Critical Roles in Plant Adaptation to Phosphorus Deficiency. International journal of molecular sciences.2019; 20(21) :5259.

Atkinson D, Davison AW. The effects of phosphorus deficiency on water content and response to drought. New Phytologist. 1973;72(2):307–313.

Arce-Paredes P, Mora-Escobedo R, Luna-Arias JP, Mendoza -Hernández G, Rojas-Espinosa O. Heat, salinity, and acidity, commonly upregulate A1aB1b proglycinin in soybean embryonic axes. Soybean -Biochemistry, Chemistry and Physiology. 2011;p. 402–422.

Ruibal C, Castro A, Carballo V, Szabados L, Vidal S. Recovery from heat, salt and osmotic stress in Physcomitrella patens requires a functional small heat shock protein PpHsp16. 4. BMC plant biology. 2013;13(1):174.

Chen L, Hou Y, Hu W, Qiu X, Lu H, Wei J, et al. The molecular chaperon AKR2A increases the mulberry chilling-tolerant capacity by maintaining SOD activity and unsaturated fatty acids composition. Scientific reports. 2018;8(1):1–11.

Pritchard J, Griffiths B, Hunt EJ. Can the plant-mediated impacts on aphids of elevated CO2 and drought be predicted? Global Change Biology. 2007;13(8):1616–1629.

Cotton LM, Rodriguez CM, Suzuki K, Orgebin-Crist MC, Hinton BT. Organic cation/carnitine transporter, OCTN2, transcriptional activity is regulated by osmotic stress in epididymal cells. Molecular Reproduction and Development: Incorporating Gamete Research. 2010;77(2):114–125.

Guo L, Yang H, Zhang X, Yang S. Lipid transfer protein 3 as a target of MYB96 mediates freezing and drought stress in Arabidopsis. Journal of experimental botany. 2013;64(6):1755–1767.

Li YF, Wang Y, Tang Y, Kakani VG, Mahalingam R. Transcriptome analysis of heat stress response in switchgrass (Panicum virgatumL.). BMC Plant Biology. 2013;13(1):153.

Sarkar NK, Kim YK, Grover A. Coexpression network analysis associated with call of rice seedlings for encountering heat stress. Plant molecular biology. 2014;84(1-2):125–143.

Raabe K, Honys D, Michailidis C. The role of eukaryotic initiation factor 3 in plant translation regulation. Plant Physiology and Biochemistry. 2019;.

Hu CA, Delauney AJ, Verma DP. A bifunctional enzyme (delta 1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proceedings of the National Academy of Sciences. 1992;89(19):9354–9358.

Sidari M, Mallamaci C, Muscolo A. Drought, salinity and heat differently affect seed germination of Pinuspinea. Journal of forest research. 2008;13(5):326–330.

Hu X, Wu L, Zhao F, Zhang D, Li N, Zhu G, et al. Phosphoproteomic analysis of the response of maize leaves to drought, heat and their combination stress. Frontiers in plant science. 2015;6:298.

Janicka-Russak M. Plant plasma membrane H+-ATPase in adaptation of plants to abiotic stresses. Abiotic stress response in plants-physiological, biochemical and genetic perspectives. 2011; 1:197–218.

Wang QJ, Sun H, Dong QL, Sun TY, Jin ZX, Hao YJ, et al. The enhancement of tolerance to salt and cold stresses by modifying the redox state and salicylic acid content via the cytosolic malate dehydrogenase gene in transgenic apple plants. Plant biotechnology journal. 2016;14(10):1986–1997.



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