Skip to main content
SpringerLink
Log in

Transcriptomic Analyses of Chilling Stress Responsiveness in Leaves of Tobacco (Nicotiana tabacum) Seedlings

  • Original Paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

Low temperature is among the most significant abiotic stresses restricting geographical distribution of plants and reducing crop productivity. However, the molecular regulatory mechanisms of tobacco plants in response to low temperature are poorly understood. To elucidate the molecular mechanisms of chilling tolerance in tobacco, the transcriptomic responses of tobacco under chilling stress were analyzed using RNA-seq analysis. A total of 1675 differentially expressed genes (DEGs) were detected from T12h vs. CK12h and T24h vs. CK24h libraries; among these genes, 1170 genes were upregulated and 505 were downregulated. Additionally, 109 genes were found to be specifically expressed in tobacco seedlings under chilling stress. Functional annotation revealed that the DEGs enriched that categories of regulating soluble sugar and polyamine content and composition to maintain cell osmotic potential, accelerating the de novo synthesis of D1 protein to promote PSII repair, regulating signal transduction such as ABA and GA, and promoting lipid metabolism and lignin synthesis to improve stability of membrane system and mechanical strength of cell wall. This work provides additional insights into the molecular basis of tobacco seedling responses to low-temperature stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P (2008) The coldinducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20(8):2117–2129

    CAS  PubMed  PubMed Central  Google Scholar 

  • Akihiro Y, Shim I-S, Fujihara S (2012) Chilling-stress responses by rice seedlings grown with different ammonium concentrations and its relationship to leaf spermidine content. Journal of Plant Biology 55(3):191–197

    Google Scholar 

  • Ali S, Charles TC, Glick BR (2014) Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiol Biochem 80:160–167

    CAS  PubMed  Google Scholar 

  • Allakhverdiev SI, Nishiyama Y, Takahashi S, Miyairi S, Suzuki I, Murata N (2005) Systematic analysis of the relation of electron transport and ATP synthesis to the photodamage and repair of photosystem II in Synechocystis. Plant Physiol 137(1):263–273

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    CAS  PubMed  PubMed Central  Google Scholar 

  • Atsushi F, Sho T, Shuichi M, Yoshihiko T, Itsuro T, Kiyoaki K (2013) The rice REDUCED CULM NUMBER11 gene controls vegetative growth under low-temperature conditions in paddy fields independent of RCN1/OsABCG5. Plant Sci 211:70–76

    Google Scholar 

  • Bajguz SH (2009) Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol Biochem 47(1):1–8

    CAS  PubMed  Google Scholar 

  • Bari R, Jones J (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69(4):473–488

    CAS  PubMed  Google Scholar 

  • Bilska A, Sowinski P (2010) Closure of plasmodesmata in maize (Zea mays) at low temperature: a new mechanism for inhibition of photosynthesis. Ann Bot 106(5):675–686

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16(1):1–18

    CAS  PubMed  Google Scholar 

  • Busov VB, Meilan R, Pearce DW, Ma C, Rood SB, Strauss SH (2003) Activation tagging of a dominant gibberellin catabolism gene (GA 2-oxidase) from poplar that regulates tree stature. Plant Physiol 132(3):1283–1291

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chang WC, Zheng HQ, Chen CN (2016) Comparative transcriptome analysis reveals a potential photosynthate partitioning mechanism between lipid and starch biosynthetic pathways in green microalgae. Algal Res 16:54–62

    Google Scholar 

  • Chang YJ, Chung WH, Kim HS et al (2017) Transcriptome profiling of sweet potato tuberous roots during low-temperature storage. Plant Physiol Biochem 112:97–108

    Google Scholar 

  • Chao WS (2008) Real-time PCR as a tool to study weed biology. Weed Sci 56:290–296

    CAS  Google Scholar 

  • Chao Wei, Zhu LX, Wen J, Yi B, Ma CZ, Tu JX, Shen JX, Fu TD (2018) Morphological, transcriptomics and biochemical characterization of new dwarf mutant of Brassica napus. Plant Science 270:97–113

    CAS  PubMed  Google Scholar 

  • Chen N, Yang Q, Hu D, Pan L, Chi X, Chen M, Yang Z, Wang T, Wang M, He Y, Yu S (2014) Gene expression profiling and identification of resistance genes to low temperature in leaves of peanut (Arachis hypogaea L.). Sci Hortic 169:214–225

    CAS  Google Scholar 

  • Chen J, Zhang H, Feng M, Zuo D, Hu Y, Jiang T (2016) Transcriptome analysis of woodland strawberry (Fragaria vesca) response to the infection by strawberry vein banding virus (SVBV). Virol J 13:128

    PubMed  PubMed Central  Google Scholar 

  • Cheng L, Chen X, Jiang C, Ma B, Ren M, Cheng Y, Liu D, Geng R, Yang A (2019) High-density SNP genetic linkage map construction and quantitative trait locus mapping for resistance to cucumber mosaic virus in tobacco (Nicotiana tabacum L.). Crop Journal 7(4):539–547

    Google Scholar 

  • Clarke SM, Cristescu SM, Miersch O, Harren FJM, Wasternack C, Mur LA (2009) Jasmonates act with salicylic acid to confer basal thermotolerance in Arabidopsis thaliana. New Phytol 182:175–187

    CAS  PubMed  Google Scholar 

  • Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11(1):163

    PubMed  PubMed Central  Google Scholar 

  • Cushman JC, Bohnert HJ (2000) Genomic approaches to plant stress tolerance. Curr Opin Plant Biol 3(2):117–124

    CAS  PubMed  Google Scholar 

  • Dametto A, Sperotto AR, Adamski MJ et al (2015) Cold tolerance in rice germinating seeds revealed by deep RNAseq analysis of contrasting indica genotypes. Plant Sci 238:1–12

    CAS  PubMed  Google Scholar 

  • Dang X, Thi TGT, Dong G, Wang H, Edzesi WM, Hong D (2014) Genetic diversity and association mapping of seed vigor in rice (Oryza sativa L.). Planta 239(6):1309–1319

    CAS  PubMed  Google Scholar 

  • Diao GP, Wang YC, Wang C, Yang CP (2011) Cloning and functional characterization of a novel glutathione S-transferase gene from Limonium bicolor. Plant Mol Biol Report 29(1):77–87

    CAS  Google Scholar 

  • Edner C, Li J, Albrecht T, Mahlow S, Hejazi M, Hussain H, Kaplan F, Guy C, Smith SM, Steup M, Ritte G (2007) Glucan, water dikinase activity stimulates the breakdown of starch granules by plastidial beta-amylases. Plant Physiol 145:17–28

    CAS  PubMed  PubMed Central  Google Scholar 

  • Flohé L (1989) The selenoprotein glutathione peroxidase. In: Glutathione: Dophin D (eds) chemical, biochemical, and medical aspects, part a. John Wiley & Sons, Chichester-New York, pp 643–731

    Google Scholar 

  • Fujii H, Chinnusamy V, Rodrigues A et al (2009) In vitro reconstitution of an abscisic acid signalling pathway. Nature 462(72, 73):660–664

    CAS  PubMed  PubMed Central  Google Scholar 

  • Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2006) Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc Natl Acad Sci 103(6):1988–1993

    CAS  PubMed  PubMed Central  Google Scholar 

  • Greco M, Chiappetta A, Bruno L, Bitonti MB (2012) In Posidonia oceanica cadmium induces changes in DNA methylation and chromatin patterning. J Exp Bot 63(2):3523–3544

    Google Scholar 

  • Gu XB, Chen YH, Gao ZH, Qiao YS, Wang XY (2015) Transcription factors and anthocyanin genes related to low-temperature tolerance in rd29A:RdreB1BI transgenic strawberry. Plant Physiol Biochem 89:31–43

    CAS  PubMed  Google Scholar 

  • Guschina IA, Harwood JL (2006) Mechanisms of temperature adaptation in poikilotherms. FEBS Lett 580(23):5477–5483

    CAS  PubMed  Google Scholar 

  • Guy C, Kaplan F, Kopka J, Selbig J, Hincha DK (2008) Metabolomics of temperature stress. Physiol Plant 132:220–235

    CAS  PubMed  Google Scholar 

  • Hao Li, YanLing Mo, Qi Cui, et al (2019) Transcriptomic and physiological analyses reveal drought adaptation strategies in drought-tolerant and - susceptible watermelon genotypes. Plant Science 278:32–43

    CAS  PubMed  Google Scholar 

  • Hedden P, Phillips AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5(12):523–530

    CAS  PubMed  Google Scholar 

  • Hershkovitz V, Friedman H, Goldschmidt EE, Feygenberg O, Pesis E (2009) Induction of ethylene in avocado fruit in response to chilling stress on the tree. J Plant Physiol 166(17):1855–1862

    CAS  PubMed  Google Scholar 

  • Kang NY, Cho C, Kim NY, Kim J (2012) Cytokinin receptor-dependent and receptor-independent pathways in the dehydration response of Arabidopsis thaliana. J Plant Physiol 169(14):1382–1391

    CAS  PubMed  Google Scholar 

  • Kaplan F, Guy CL (2004) β-Amylase induction and the protective role of maltose during temperature shock. Plant Physiol 135:1674–1684

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kaplan F, Guy CL (2005) RNA interference of Arabidopsis beta-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. Plant J 44:730–743

    CAS  PubMed  Google Scholar 

  • Kobayashi Y, Murata M, Minami H, Yamamoto S, Kagaya Y, Hobo T, Yamamoto A, Hattori T (2005) Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. Plant J 44(6):939–949

    CAS  PubMed  Google Scholar 

  • Koiwa H, Bressan RA, Hasegawa PM (2006) Identification of plant stress-responsive determinants in arabidopsis by large-scale forward genetic screens. J Exp Bot 57(5):1119–1128

    CAS  PubMed  Google Scholar 

  • Lee BH, Henderson DA, Zhu JK (2005) The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17:3155–3175

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu CW, Hsu YK, Cheng YH, Yen HC, Wu YP, Wang CS, Lai CC (2012) Proteomic analysis of salt-responsive ubiquitin-related proteins in rice roots. Rapid Commun Mass Spectrom 26:1649–1660

    CAS  PubMed  Google Scholar 

  • Livak JK, Schmittgen GT (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408

    CAS  PubMed  Google Scholar 

  • Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009a) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068

    CAS  PubMed  Google Scholar 

  • Ma YY, Zhang YL, Lu J, Shao H (2009b) Roles of plant soluble sugars and their responses to plant cold stress. Afr J Biotechnol 8:2004–2010

    CAS  Google Scholar 

  • Maksymiec W, Wianowska D, Dawidowicz AL, Radkiewicz S, Mardarowicz M, Krupa Z (2005) The level of jasmonic acid in Arabidopsis thaliana and Phaseolus coccineus plants under heavy metal stress. J Plant Physiol 162(12):1338–1346

    CAS  PubMed  Google Scholar 

  • Mao XZ, Cai T, Olyarchuk JG, Wei LP (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21(19):3787–3793

    CAS  PubMed  Google Scholar 

  • Martone PT, Estevez JM, Lu F, Ruel K, Denny MW, Somerville C, Ralph J (2009) Discovery of lignin in seaweed reveals convergent evolution of cell-wall architecture. Curr Biol 19(2):169–175

    CAS  PubMed  Google Scholar 

  • Matthew DY, Matthew JW, Gordon KS, Alicia O (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11(2):R14

    Google Scholar 

  • Miura K, Furumoto T (2013) Cold signaling and cold response in plants. Int J Mol Sci 14(3):5312–5337. https://doi.org/10.3390/ijms14035312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mustafa RM, Abeer MA, James G, Song JY, Benildo GR (2005) The OsLti6 genes encoding low-molecular-weight membrane proteins are differentially expressed in rice cultivars with contrasting sensitivity to low temperature. Gene 344:171–180

    Google Scholar 

  • Nese S, Harshavardhan VT, Govind G, Seiler C, Kohli A (2012) Contrapuntal role of ABA: does it mediate stress tolerance or plant growth retardation under long-term drought stress? Gene 506(2):265–273

    Google Scholar 

  • Ogawa A, Audo F, Toyofuku K, Kawashima C (2009) Sucrose metabolism for the development of seminal root in maize seedlings. Plant Prod Sci 12:9–16

    CAS  Google Scholar 

  • Park JE, Park JY, Kim YS, Staswick PE, Jeon J, Yun J, Kim SY, Kim J, Lee YH, Park CM (2007) GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J Biol Chem 282(13):10036–10046

    CAS  PubMed  Google Scholar 

  • Patel D, Franklin KA (2009) Temperature-regulation of plant architecture. Plant Signal Behav 4:577–579

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peilu Z, Qiyao L, Guangliang L, Xu N, Yang Y, Wenlong Z, Aiguo C, Wang S (2019) Integrated analysis of transcriptomic and metabolomic data reveals critical metabolic pathways involved in polyphenol biosynthesis in Nicotiana tabacum under chilling stress. Funct Plant Biol 46(1):30

    Google Scholar 

  • Peters D (2007) Raw materials. Adv Biochem Eng Biotechnol 105:1–30

    CAS  PubMed  Google Scholar 

  • Rintamäki E, Kettunen R, Aro EM (1996) Differential D1 dephosphorylation in functional and photodamaged photosystem II centers. Dephosphorylation is a prerequisite for degradation of damaged D1. J Biol Chem 271(25):14870–148755

    PubMed  Google Scholar 

  • Ruelland E, Zachowski A (2010) How plants sense temperature. Environ Exp Bot 69:225–232

    Google Scholar 

  • Ruelland E, Cantrel C, Gawer M, Kader J-C, Zachowski A (2002) Activation of phospholipases C and D is an early response to a cold exposure in Arabidopsis suspension cells. Plant Physiol 130(2):999–1007

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sanghera GS, Wani SH, Hussain W, Singh NB (2011) Engineering cold stress tolerance in crop plants. Current Genomics 12:30–43

    Google Scholar 

  • Savitch LV, Ivanov AG, Loreta GS, Huner NPA, John S (2011) Cold stress effects on PSI photochemistry in Zea mays: differential increase of FQR-dependent cyclic electron flow and functional implications. Plant Cell Physiol 52(6):1042–1054

    CAS  PubMed  Google Scholar 

  • Sharma R, Yang Y, Sharma A, Awasthi S, Awasthi YC (2004) Antioxidant role of glutathione S-transferases: protection against oxidant toxicity and regulation of stress-mediated apoptosis. Antioxid Redox Signal 6(2):289–300

    CAS  PubMed  Google Scholar 

  • Shi Y, Tian S, Hou L, Huang X, Zhang X, Guo H, Yang S (2012) Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis. Plant Cell 24:2578–2595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi YL, Wang QF, Hou YH et al (2014) Molecular cloning, expression and enzymatic characterization of glutathione S-transferase from Antarctic sea-ice bacteria Pseudoalteromonas sp.ANT506. Microbiol Res 169(2–3):179–184

    CAS  PubMed  Google Scholar 

  • Shu S, Guo SR, Sun J, Yuan LY (2012) Effects of salt stress on the structure and function of the photosynthetic apparatus in Cucumis sativus and its protection by exogenous putrescine. Physiol Plant 146(3):285–296

    CAS  PubMed  Google Scholar 

  • Siritantikorn A, Johansson K, Ahlen K et al (2007) Protection of cells from oxidative stress by microsomal glutathione transferase1. Biochem Biophys Res Commun 355(2):592–596

    CAS  PubMed  Google Scholar 

  • Solanke AU, Sharma AK (2008) Signal transduction during cold stress in plants. Physiol Mol Biol Plants 14(1–2):69–79

    CAS  PubMed  PubMed Central  Google Scholar 

  • Soon FF, Ng LM, Zhou XE, West GM, Kovach A, Tan MHE, Suino-Powell KM, He Y, Xu Y, Chalmers MJ, Brunzelle JS, Zhang H, Yang H, Jiang H, Li J, Yong EL, Cutler S, Zhu JK, Griffin PR, Melcher K, Xu HE (2012) Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science 335(6064):85–88

    CAS  PubMed  Google Scholar 

  • Sreenivasulu N, Harshavardhan VT, Govind G, Seiler C, Kohli A (2012) Contrapuntal role of ABA: does it mediate stress tolerance or plant growth retardation under long-term drought stress? Gene 506(2):265–273

    CAS  PubMed  Google Scholar 

  • Sun XM, Zhu ZZF, Zhang LL et al (2019) Overexpression of ethylene response factors VaERF080 and VaERF087 from Vitis amurensis enhances cold tolerance in Arabidopsis. Sci Hortic 243:320–326

    CAS  Google Scholar 

  • Takahashi S, Murata N (2005) Interruption of the Calvin cycle inhibits the repair of photosystem II from photodamage. BBA-Bioenergetics 1708(3):352–361

    CAS  PubMed  Google Scholar 

  • Takano A, Kakehi J, Takahashi T (2012) Thermospermine is not a minor polyamine in the plant kingdom. Plant Cell Physiol 53(4):606–616

    CAS  PubMed  Google Scholar 

  • Tiburcio AF, Altabella T, Bitrián M, Alcázar R (2014) The roles of polyamines during the lifespan of plants: from development to stress. Planta 240(1):1–18

    CAS  PubMed  Google Scholar 

  • Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28(5):511–515. https://doi.org/10.1038/nbt.1621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trebitsh T, Danon A (2001) Translation of chloroplast psbA mRNA is regulated by signals initiated by both photosystems II and I. Proc Natl Acad Sci 98(21):12289–12294. https://doi.org/10.1073/pnas.211440698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Ishihama Y, Hirayama T, Shinozaki K (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc Natl Acad Sci 106:17588–17593

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vass I, Styring S, Hundal T, Koivuniemi A, Aro E, Andersson B (1992) Reversible and irreversible intermediates during photoinhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation. Proc Natl Acad Sci 89(4):1408–1412

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang SK, YouHuang B, Shen CJ, Wu YR, SaiNa Z, DeAn J, Guilfoyle TJ, Ming C, YanHua Q (2010) Auxin-related gene families in abiotic stress response in Sorghum bicolor. Functional & Integrative Genomics 10(4):533–546

    CAS  Google Scholar 

  • Wasternack C (2014) Action of jasmonates in plant stress responses and development-applied aspects. Biotechnol Adv 32(1):31–39

    CAS  PubMed  Google Scholar 

  • Wei SJ, Du ZL, Gao F et al (2015) Global transcriptome profiles of 'Meyer' Zoysiagrass in response to cold stress. PLoS One 10(6):e0131153

    PubMed  PubMed Central  Google Scholar 

  • Wongsheree T, Ketsa S, van Doorn WG (2009) The relationship between the chilling injury and membrane damage in lemon basil (Ocimumcitriodourum) leaves. Postharvest Biol Technol 51(1):91–96

    CAS  Google Scholar 

  • Yamaguchi S, Kamiya Y (2000) Gibberellin biosynthesis: its regulation by endogenous and environmental signals. Plant Cell Physiol 41(3):251–257

    CAS  PubMed  Google Scholar 

  • Yamamoto A, Shim IS, Fujihara S (2012) Chilling-stress responses by rice seedlings grown with different ammonium concentrations and its relationship to leaf spermidine content. J Plant Biol 55(3):191–197

    CAS  Google Scholar 

  • Yeshvekar RK, Nitnavare RB, Chakradhar T, Bhatnagar-Mathur P, Reddy MK, Reddy PS (2017) Molecular characterization and expression analysis of pearl millet plasma membrane proteolipid 3 ( Pmp3 ) genes in response to abiotic stress conditions. Plant Gene 10:37–44

    CAS  Google Scholar 

  • Zhang Y, Ni ZF, Yao YY, Nie XL, Sun QX (2007) Gibberellins and heterosis of plant height in wheat (Triticum aestivum L.). BMC Genet 8(1):40

    PubMed  PubMed Central  Google Scholar 

  • Zhang XD, Wang RP, Zhang FJ, Tao FQ, Li WQ (2013) Lipid profiling and tolerance to low-temperature stress in Thellungiella salsuginea in comparison with Arabidopsis thaliana. Biol Plant 57(1):149–153

    CAS  Google Scholar 

  • Zheng YL, Feng YL, Lei YB, Yang CY (2009) Different photosynthetic responses to night chilling among twelve populations of Jatropha curcas. Photosynthetica 47:559–566

    CAS  Google Scholar 

  • Zhou Y, Xu Z, Duan C, Chen Y, Meng Q, Wu J, Hao Z, Wang Z, Li M, Yong H, Zhang D, Zhang S, Weng J, Li X (2016) Dual transcriptome analysis reveals insights into the response to Rice black streaked dwarf virus in maize. J Exp Bot 67(15):4593–4609

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou AM, Sun HW, Feng S et al (2018a) A novel cold-regulated gene from Phlox subulata, PsCor413im1, enhances low temperature tolerance in Arabidopsis. Biochem Biophys Res Commun 495(2):1688–1694

    CAS  PubMed  Google Scholar 

  • Zhou PL, Li QY, Liu GL, Xu N, Yang YJ, Zeng WL, Chen AG, Wang SS (2018b) Integrated analysis of transcriptomic and metabolomic data reveals critical metabolic pathways involved in polyphenol biosynthesis in Nicotiana tabacum under chilling stress. Funct Plant Biol 46:30–43

    PubMed  Google Scholar 

  • Zhu JH, Dong CH, Zhu JK (2007) Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol 10(3):290–295

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.

Funding

This research was funded by Fundamental Research Funds for Central Non-Profit Scientific Institution, grant number 1610232016019, and Agricultural Science and Technology Innovation Program, grant number ASTIP-TRIC03.

Author information

Author notes

  1. Peilu Zhou and Rayyan Khan contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Tobacco Biology and Processing, Ministry of Agriculture, Tobacco Research Institute of Chinese Academy of Agricultural Sciences, Qingdao, 266101, People’s Republic of China

    Peilu Zhou, Rayyan Khan, Qiyao Li, Guangliang Liu, Na Xu, Yinju Yang, Yi Wang, Shusheng Wang & Aiguo Chen

  2. College of Agronomy, Resources and Environment, Tianjin Agricultural University, Tianjin, 300384, People’s Republic of China

    Peilu Zhou

Authors
  1. Peilu Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rayyan Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qiyao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guangliang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Na Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yinju Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shusheng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Aiguo Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Shusheng Wang or Aiguo Chen.

Ethics declarations

Conflict of Interest

The authors declare no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

S1 Table

. List of primers used for qRT-PCR analysis (MSWord). (DOCX 14 kb)

S2 Table

. KEGG annotation analysis of upregulated DEGs responded to chilling (MSexcle). (XLS 78 kb)

S3 Table

. KEGG annotation analysis of downregulated DEGs responded to chilling (MSexcle). (XLS 41 kb)

S4 Table

. Candidate genes involved in tobacco chilling tolerance (MSexcle). (XLS 91 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, P., Khan, R., Li, Q. et al. Transcriptomic Analyses of Chilling Stress Responsiveness in Leaves of Tobacco (Nicotiana tabacum) Seedlings. Plant Mol Biol Rep 38, 1–13 (2020). https://doi.org/10.1007/s11105-019-01167-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-019-01167-0

Keywords

Search

Navigation