Understanding the heat resistance of cucumber through leaf transcriptomics
Min Wang
A B , Xiaoming He A B , Qin Peng C , Zhaojun Liang A , Qingwu Peng A , Wenrui Liu A B , Biao Jiang A B , Dasen Xie A B , Lin Chen A B , Jinqiang Yan A B and Yu’e Lin A C D
+ Author Affiliations
- Author Affiliations
A Vegetable Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China.
B Guangdong Key Laboratory for New Technology Research of Vegetables, Guangzhou 510640, China.
C School of Life Sciences, South China Normal University, Guangzhou, 510631, China.
D Corresponding author. Email: cucumber200@163.com
Functional Plant Biology 47(8) 704-715 https://doi.org/10.1071/FP19209
Submitted: 19 July 2019 Accepted: 26 January 2020 Published: 3 June 2020
Abstract
Heat stress is a major environmental factor limiting plant productivity and quality in agriculture. Cucumber, one of the most important vegetables among cucurbitaceae, prefers to grow in a warm environment. Until now the molecular knowledge of heat stress in cucumber remained unclear. In this study, we performed transcriptome analysis using two diverse genetic cucumber cultivars, L-9 and A-16 grown under normal and heat stress. L-9 displayed heat-tolerance phenotype with higher superoxide dismutase enzyme (SOD) enzyme activity and lower malondialdehyde (MDA) content than A-16 under heat stress. RNA-sequencing revealed that a total of 963 and 2778 genes are differentially expressed between L-9 and A-16 under normal and heat stress respectively. In addition, we found that differentially expressed genes (DEGs) associated with plant hormones signally pathway, transcription factors, and secondary metabolites showed significantly change in expression level after heat stress, which were confirmed by quantitative real-time PCR assay. Our results not only explored several crucial genes involved in cucumber heat resistance, but also provide a new insight into studying heat stress.
Additional keywords: DEGs, differentially expressed genes, heat stress, RNA-seq.
References
Akula R, Ravishankar GA (2011) Influence of abiotic stress signals on secondary metabolites in plants. Plant Signaling & Behavior 6, 1720–1731.Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of Arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. The Plant Cell 9, 1859–1868.
Barnabás B, Jäger K, Fehér A (2008) The effect of drought and heat stress on reproductive processes in cereals. Plant, Cell & Environment 31, 11–38.
Bi JL, Felton GW (1995) Foliar oxidative stress and insect herbivory, primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. Journal of Chemical Ecology 21, 1511
| Foliar oxidative stress and insect herbivory, primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance.Crossref | GoogleScholarGoogle Scholar | 24233680PubMed |
Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment, scientific fundamentals and production of heat stress-tolerant crops. Frontiers of Plant Science 4, 273
| Plant tolerance to high temperature in a changing environment, scientific fundamentals and production of heat stress-tolerant crops.Crossref | GoogleScholarGoogle Scholar |
Boyer JS (1982) Plant productivity and environment. Science 218, 443–448.
| Plant productivity and environment.Crossref | GoogleScholarGoogle Scholar | 17808529PubMed |
Castilhos G, Lazzarotto F, Spagnolo-Fonini L, Bodanese-Zanettini MH, Margis-Pinheiro M (2014) Possible roles of basic helix-loop-helix transcription factors in adaptation to drought. Plant Science 223, 1–7.
| Possible roles of basic helix-loop-helix transcription factors in adaptation to drought.Crossref | GoogleScholarGoogle Scholar | 24767109PubMed |
Challinor AJ, Watson J, Lobell DB, Howden SM, Smith DR, Chhetri N (2014) A meta-analysis of crop yield under climate change and adaptation. Nature Climate Change 4, 287–291.
| A meta-analysis of crop yield under climate change and adaptation.Crossref | GoogleScholarGoogle Scholar |
Coutinho ID, Henning LMM, Döpp SA, Nepomuceno A, Moraes LAC, Marcolino-Gomes J, Richter C, Schwalbe H, Colnago LA (2018) Flooded soybean metabolomic analysis reveals important primary and secondary metabolites involved in the hypoxia stress response and tolerance. Environmental and Experimental Botany 153, 176–187.
| Flooded soybean metabolomic analysis reveals important primary and secondary metabolites involved in the hypoxia stress response and tolerance.Crossref | GoogleScholarGoogle Scholar |
do Nascimento NC, Fett-Neto AG (2010) Plant secondary metabolism and challenges in modifying its operation, an overview. Methods in Molecular Biology 643, 1–13.
Fan M, Huang Y, Zhong YQ, Kong QS, Xie JJ, Niu ML, Xu Y, Bie ZL (2014) Comparative transcriptome profiling of potassium starvation responsiveness in two contrasting watermelon genotypes. Planta 239, 397–410.
| Comparative transcriptome profiling of potassium starvation responsiveness in two contrasting watermelon genotypes.Crossref | GoogleScholarGoogle Scholar | 24185372PubMed |
Fang Y, Liao K, Du H, Xu Y, Song H, Li X, Xiong L (2015) A stress-responsive NAC transcription factor SNAC3 confers heat and drought tolerance through modulation of reactive oxygen species in rice. Journal of Experimental Botany 66, 6803–6817.
| A stress-responsive NAC transcription factor SNAC3 confers heat and drought tolerance through modulation of reactive oxygen species in rice.Crossref | GoogleScholarGoogle Scholar | 26261267PubMed |
Fehlmann T, Reinheimer S, Geng CY, Su XS, Drmanac S, Alexeev A, Zhang CY, Backes C, Ludwig N, Hart M, An D, Zhu ZZ, Xu CJ, Chen A, Ni M, Liu J, Li YX, Poulter M, Li YP, Stähler C, Drmanac R, Xu X, Meese E, Keller A (2016) cPAS-based sequencing on the BGISEQ-500 to explore small non-coding RNAs. Clinical Epigenetics 8, 123
| cPAS-based sequencing on the BGISEQ-500 to explore small non-coding RNAs.Crossref | GoogleScholarGoogle Scholar | 27895807PubMed |
Fischer U, Droge-Laser W (2004) Overexpression of NtERF5, a new member of the tobacco ethylene response transcription factor family enhances resistance to Tobacco mosaic virus. Molecular Plant-Microbe Interactions 17, 1162–1171.
| Overexpression of NtERF5, a new member of the tobacco ethylene response transcription factor family enhances resistance to Tobacco mosaic virus.Crossref | GoogleScholarGoogle Scholar | 15497409PubMed |
Frova C (1997) Genetics dissection of thermotolerance in maize. In ‘Physical stress in plants’. (Eds S Grillo, A Leone) pp. 31–38 (Springer-Verlag: New York)
Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LP, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. The Plant Journal 39, 863–876.
| A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway.Crossref | GoogleScholarGoogle Scholar | 15341629PubMed |
Gan X, Stegle O, Behr J, Steffen JG, Drewe P, Hildebrand KL, Lyngsoe R, Schultheiss SJ, Osborne EJ, Sreedharan VT, Kahles A, Bohnert R, Jean G, Derwent P, Kersey P, Belfield EJ, Harberd NP, Kemen E, Toomajian C, Kover PX, Clark RM, Rätsch G, Mott R (2011) Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477, 419–423.
| Multiple reference genomes and transcriptomes for Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 21874022PubMed |
Gao F, Xiong A, Peng R, Jin XF, Xu J, Zhu B, Chen JM, Yao QH (2010) OsNAC52, a rice NAC transcription factor, potentially responds to ABA and confers drought tolerance in transgenic plants. Plant Cell, Tissue and Organ Culture 100, 255–262.
| OsNAC52, a rice NAC transcription factor, potentially responds to ABA and confers drought tolerance in transgenic plants.Crossref | GoogleScholarGoogle Scholar |
Garg R, Shankar R, Thakkar B, Kudapa H, Krishnamurthy L, Mantri N, Varshney RK, Bhatia S, Jain M (2016) Transcriptome analyses reveal genotype-and developmental stage-specific molecular responses to drought and salinity stresses in chickpea. Scientific Reports 6, 19228
| Transcriptome analyses reveal genotype-and developmental stage-specific molecular responses to drought and salinity stresses in chickpea.Crossref | GoogleScholarGoogle Scholar | 26759178PubMed |
Gershenzon J (1984) Changes in the levels of plant secondary metabolites under water and nutrient stress. In ‘Phytochemical adaptations to stress’. (Eds BN Timmermann, C Steelink, FA Loewus) pp.273–320. (Springer: Boston, MA, USA) https://doi.org/10.1007/978-1-4684-1206-2_10
Guan Q, Yue X, Zeng H, Zhu JH (2014) The protein phosphatase RCF2 and its interacting partner NAC019 are critical for heat stress-responsive gene regulation and thermotolerance in Arabidopsis. The Plant Cell 26, 438–453.
| The protein phosphatase RCF2 and its interacting partner NAC019 are critical for heat stress-responsive gene regulation and thermotolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 24415771PubMed |
Hays DB, Do JH, Mason RE, Morgan G, Finlayson SA (2007) Heat stress induced ethylene production in developing wheat grains induces kernel abortion and increased maturation in a susceptible cultivar. Plant Science 172, 1113–1123.
| Heat stress induced ethylene production in developing wheat grains induces kernel abortion and increased maturation in a susceptible cultivar.Crossref | GoogleScholarGoogle Scholar |
Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Research 36, 480–484.
| KEGG for linking genomes to life and the environment.Crossref | GoogleScholarGoogle Scholar |
Kim J, Kim HY (2006) Functional analysis of a calcium-binding transcription factor involved in plant salt stress signaling. FEBS Letters 580, 5251–5256.
| Functional analysis of a calcium-binding transcription factor involved in plant salt stress signaling.Crossref | GoogleScholarGoogle Scholar | 16962584PubMed |
Kiribuchi K, Jikumaru Y, Kaku H, Minami E, Hasegawa M, Kodama O, et al (2005) Involvement of the basic Helix-Loop-Helix transcription factor RERJ1 in wounding and drought stress responses in rice plants. Bioscience, Biotechnology, and Biochemistry 69, 1042–1044.
| Involvement of the basic Helix-Loop-Helix transcription factor RERJ1 in wounding and drought stress responses in rice plants.Crossref | GoogleScholarGoogle Scholar | 15914931PubMed |
Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, Hirai N, Koshiba T, Kamiya Y, Nambara E (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′-hydroxylases: key enzymes in ABA catabolism. The EMBO Journal 23, 1647–1656.
| The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′-hydroxylases: key enzymes in ABA catabolism.Crossref | GoogleScholarGoogle Scholar | 15044947PubMed |
Lafitte HR, Yongsheng G, Yan S, Li ZK (2007) Whole plant responses, key processes, and adaptation to drought stress, the case of rice. Journal of Experimental Botany 58, 169–175.
| Whole plant responses, key processes, and adaptation to drought stress, the case of rice.Crossref | GoogleScholarGoogle Scholar | 16997901PubMed |
Ledent V, Vervoort M (2001) The basic Helix-Loop-Helix protein family, comparative genomics and phylogenetic analysis. Genome Research 11, 754–770.
| The basic Helix-Loop-Helix protein family, comparative genomics and phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar | 11337472PubMed |
Li B, Dewey CN (2011) RSEM, Accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinformatics 12, 323
| RSEM, Accurate transcript quantification from RNA-seq data with or without a reference genome.Crossref | GoogleScholarGoogle Scholar | 21816040PubMed |
Li ZG, Gong M (2009) Involvement of calcium and calmodulin in mechanical stimulation- induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension cultured cells. Plant Physiol. Commun 45, 363–365.
Li ZG, Du CK, Gong M (2005) Involvement of Ca2+ and calmodulin in the regulation of H2O2-induced heat tolerance in maize seedlings. J. Plant Physiol. Mol. Biol 31, 515–519.
Li SJ, Fu QT, Huang WD, Yu DQ (2009) Functional analysis of an Arabidopsis transcription factor WRKY25 in heat stress. Plant Cell Reports 28, 683–693.
| Functional analysis of an Arabidopsis transcription factor WRKY25 in heat stress.Crossref | GoogleScholarGoogle Scholar |
Li SJ, Zhou X, Chen LG, Huang WD, Yu DQ (2010) Functional characterization of Arabidopsis thaliana WRKY39 in heat stress. Molecules and Cells 29, 475–483.
| Functional characterization of Arabidopsis thaliana WRKY39 in heat stress.Crossref | GoogleScholarGoogle Scholar |
Li H, Liu SS, Yi CY, Wang F, Zhou J, Xia XJ, Shi K, Zhou YH, Yu JQ (2014) Hydrogen peroxide mediates abscisic acid-induced HSP70 accumulation and heat tolerance in grafted cucumber plants. Plant, Cell & Environment 37, 2768–2780.
| Hydrogen peroxide mediates abscisic acid-induced HSP70 accumulation and heat tolerance in grafted cucumber plants.Crossref | GoogleScholarGoogle Scholar |
Malepszy S (1988) Cucumber (Cucumis sativus L.). Biotech Agric. Forestry 6, 277–293.
| Cucumber (Cucumis sativus L.).Crossref | GoogleScholarGoogle Scholar |
Miller G (2008) Reactive oxygen signaling and abiotic stress. Physiologia Plantarum 133, 481–489.
Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends in Biochemical Sciences 37, 118–125.
| How do plants feel the heat?Crossref | GoogleScholarGoogle Scholar | 22236506PubMed |
Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. BBA-Gene Regulatory Mechanisms 1819, 0–96.
Morgan PW, Drew MC (1997) Ethylene and plant responses to stress. Physiologia Plantarum 100, 620–630.
| Ethylene and plant responses to stress.Crossref | GoogleScholarGoogle Scholar |
Morison JIL, Lawlor DW (1999) Interactions between increasing CO2 concentration and temperature on plant growth. Plant, Cell & Environment 22, 659–682.
| Interactions between increasing CO2 concentration and temperature on plant growth.Crossref | GoogleScholarGoogle Scholar |
Paranidharan V, Palaniswami A, Vidhyasekaran P, Velazhahan R (2005) A host-specific toxin of Rhizoctonia solani triggers superoxide dismutase (SOD) activity in rice. Archiv für Pflanzenschutz 38, 151–157.
| A host-specific toxin of Rhizoctonia solani triggers superoxide dismutase (SOD) activity in rice.Crossref | GoogleScholarGoogle Scholar |
Qin F, Kakimoto M, Sakuma Y, Maruyama K, Osakabe Y, Tran LSP, Shinozaki K, Yamaguchi-Shinozaki K (2007) Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. The Plant Journal 50, 54–69.
| Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L.Crossref | GoogleScholarGoogle Scholar | 17346263PubMed |
Ray DK, Gerber JS, MacDonald GK, West PC (2015) Climate variation explains a third of global crop yield variability. Nature Communications 6, 5989
| Climate variation explains a third of global crop yield variability.Crossref | GoogleScholarGoogle Scholar | 25609225PubMed |
Rizhsky L (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiology 130, 1143–1151.
| The combined effect of drought stress and heat shock on gene expression in tobacco.Crossref | GoogleScholarGoogle Scholar | 12427981PubMed |
Saito S, Hirai N, Matsumoto C, Ohigashi H, Ohta D, Sakata K, Mizutani M (2004) Arabidopsis CYP707As encode (+)-abscisic acid 8′-hydroxylase, a key enzyme in the oxidative catabolism of abscisic acid. Plant Physiology 134, 1439–1449.
| Arabidopsis CYP707As encode (+)-abscisic acid 8′-hydroxylase, a key enzyme in the oxidative catabolism of abscisic acid.Crossref | GoogleScholarGoogle Scholar | 15064374PubMed |
Sangwan V, Orvar BL, Beyerly J, Hirt H, Dhindsa RS (2002) Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. The Plant Journal 31, 629–638.
| Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways.Crossref | GoogleScholarGoogle Scholar | 12207652PubMed |
Sanjukta D, Corina VA (2015) Ethylene responsive factors in the orchestration of stress responses in monocotyledonous plants. Frontiers of Plant Science 6, 640.
Scharf KD, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family, structure, function and evolution. Biochimica et Biophysica Acta 1819, 104–119.
| The plant heat stress transcription factor (Hsf) family, structure, function and evolution.Crossref | GoogleScholarGoogle Scholar | 22033015PubMed |
Sun ZM, Zhou ML, Xiao XG, Tang YX, Wu YM (2014) Overexpression of a Lotus corniculatus AP2/ERF transcription factor gene, LcERF080, enhances tolerance to salt stress in transgenic Arabidopsis. Plant Biotechnology Reports 8, 315–324.
| Overexpression of a Lotus corniculatus AP2/ERF transcription factor gene, LcERF080, enhances tolerance to salt stress in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Suzuki N, Bassil E, Hamilton JS, Inupakutika MA, Zandalinas SI, Tripathy D, Luo YT, Dion E, Fukui G, Kumazaki A, Nakano R, Rivero RM, Verbeck GF, Azad RK, Blumwald E, Mittler R (2016) ABA is required for plant acclimation to a combination of salt and heat stress. PLoS One 11, e0147625
| ABA is required for plant acclimation to a combination of salt and heat stress.Crossref | GoogleScholarGoogle Scholar | 27716825PubMed |
Umezawa T, Okamoto M, Kushiro T, Nambara E, Oono Y, Seki M, Kobayashi M, Koshiba T, Kamiya Y, Kazuo Shinozaki K (2006) CYP707A3, a major ABA 8′hydroxylase involved in dehydration and rehydration response in Arabidopsis thaliana. The Plant Journal 46, 171–182.
| CYP707A3, a major ABA 8′hydroxylase involved in dehydration and rehydration response in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 16623881PubMed |
Wang YJ, Zhang ZG, He XJ, Zhou HL, Wen YX, Dai JX, Zhang JS, Chen SY (2003) A rice transcription factor OsbHLH1 is involved in cold stress response. Theoretical and Applied Genetics 107, 1402–1409.
| A rice transcription factor OsbHLH1 is involved in cold stress response.Crossref | GoogleScholarGoogle Scholar | 12920519PubMed |
Wan H, Zhao Z, Qian C, Sui Y, Abbas Malik A, Chen J (2010) Selection of appropriate reference genes for gene expression studies by quantitative real-time polymerase chain reaction in cucumber. Analytical Biochemistry 399, 257–261.
| Selection of appropriate reference genes for gene expression studies by quantitative real-time polymerase chain reaction in cucumber.Crossref | GoogleScholarGoogle Scholar | 20005862PubMed |
Wang D, Qin BX, Li X, Tang D, Zhang YE, Cheng ZK, Xue YB (2016) Nucleolar DEAD-Box RNA helicase TOGR1 regulates thermotolerant growth as a pre-rRNA chaperone in rice. PLOS Genetics 12, e1005844
| Nucleolar DEAD-Box RNA helicase TOGR1 regulates thermotolerant growth as a pre-rRNA chaperone in rice.Crossref | GoogleScholarGoogle Scholar | 26848586PubMed |
Wang M, Jiang B, Peng QW, Liu WR, He XM, Liang ZJ, Lin YE (2018) Transcriptome analyses in different cucumber cultivars provide novel insights into drought stress responses. International Journal of Molecular Sciences 19, 2067
| Transcriptome analyses in different cucumber cultivars provide novel insights into drought stress responses.Crossref | GoogleScholarGoogle Scholar |
Wang M, Jiang B, Liu WR, Lin YE, Liang ZJ, He XM, Peng QW (2019) Transcriptome analyses provide novel insights into heat stress responses in chieh-qua (Benincasa hispida Cogn. var. chieh-qua how). International Journal of Molecular Sciences 20, 883
| Transcriptome analyses provide novel insights into heat stress responses in chieh-qua (Benincasa hispida Cogn. var. chieh-qua how).Crossref | GoogleScholarGoogle Scholar |
Wilkinson S, Davies WJ (2002) ABA-based chemical signalling, the co-ordination of responses to stress in plants. Plant, Cell & Environment 25, 195–210.
| ABA-based chemical signalling, the co-ordination of responses to stress in plants.Crossref | GoogleScholarGoogle Scholar |
Xin M, Wang L, Liu Y, Feng Z, Zhou X, Qin Z (2017) Transcriptome profiling of cucumber genome expression in response to long-term low nitrogen stress. Acta Physiologiae Plantarum 39, 130
| Transcriptome profiling of cucumber genome expression in response to long-term low nitrogen stress.Crossref | GoogleScholarGoogle Scholar |
Yang XH, Liang Z, Lu CM (2005) Genetic engineering of the biosynthesis of glycinebetaine enhances photosynthesis against high temperature stress in transgenic tobacco plants. Plant Physiology 138, 2299–2309.
| Genetic engineering of the biosynthesis of glycinebetaine enhances photosynthesis against high temperature stress in transgenic tobacco plants.Crossref | GoogleScholarGoogle Scholar |
Yang Y, Mo Y, Yang X, Zhang H, Wang Y, Li H, Wei CH, Zhang X (2016) Transcriptome profiling of watermelon root in response to short-term osmotic stress. PLoS One 11, e0166314
| Transcriptome profiling of watermelon root in response to short-term osmotic stress.Crossref | GoogleScholarGoogle Scholar | 28006821PubMed |
Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang ZW, Wang J, Li ST, Li RQ, Bolund L, Wang J (2006) WEGO, a web tool for plotting GO annotations. Nucleic Acids Research 34, W293
| WEGO, a web tool for plotting GO annotations.Crossref | GoogleScholarGoogle Scholar | 16845012PubMed |
Yi K, Wu Z, Zhou J, Du L, Guo L, Wu Y, Wu P (2005) OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiology 138, 2087–2096.
| OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice.Crossref | GoogleScholarGoogle Scholar | 16006597PubMed |
Yu B, Yan S, Zhou H, Dong R, Lei J, Chen C, Cao B (2018) Overexpression of CsCaM3 improves high temperature tolerance in cucumber. Frontiers of Plant Science 9, 797
| Overexpression of CsCaM3 improves high temperature tolerance in cucumber.Crossref | GoogleScholarGoogle Scholar |
Zhang N, Zhang HJ, Zhao B, Sun QQ, Cao YY, Li R, Wu XX, Weeda S, Li L, Ren SX, Reiter RJ, Guo YD (2014) The RNA-seq approach to discriminate gene expression profiles in response to melatonin on cucumber lateral root formation. Journal of Pineal Research 56, 39–50.
| The RNA-seq approach to discriminate gene expression profiles in response to melatonin on cucumber lateral root formation.Crossref | GoogleScholarGoogle Scholar | 24102657PubMed |
Zhang F, Yao J, Ke J, Zhang L, Lam VQ, Xin XF, Zhou XE, Chen J, Brunzelle J, Griffin PR, Zhou MG, Xu HE, Melcher K, He SY (2015) Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling. Nature 525, 269–273.
| Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling.Crossref | GoogleScholarGoogle Scholar | 26258305PubMed |
Zhao W, Yang X, Yu H, Jiang W, Sun N, Liu X, Zhang XM, Wang Y, Gu X (2015) RNA-Seq-based transcriptome profiling of early nitrogen deficiency response in cucumber seedlings provides new insight into the putative nitrogen regulatory network. Plant & Cell Physiology 56, 455
| RNA-Seq-based transcriptome profiling of early nitrogen deficiency response in cucumber seedlings provides new insight into the putative nitrogen regulatory network.Crossref | GoogleScholarGoogle Scholar |
Zhou J, Li F, Wang JL, Ma Y, Chong K, Xu Y (2009) Basic helix-loop-helix transcription factor from wild rice (OrbHLH2) improves tolerance to salt- and osmotic-stress in Arabidopsis. Journal of Plant Physiology 166, 1296–1306.
| Basic helix-loop-helix transcription factor from wild rice (OrbHLH2) improves tolerance to salt- and osmotic-stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 19324458PubMed |
Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167, 313–324.
| Abiotic stress signaling and responses in plants.Crossref | GoogleScholarGoogle Scholar | 27716505PubMed |
Zhu W, Lu M, Gong Z, Chen R (2011) Cloning and expression of a small heat shock protein gene CaHSP24 from pepper under abiotic stress. African Journal of Biotechnology 1025, 4968–4976.
