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Identification and characterisation of candidate genes involved in chilling responses in maize (Zea mays L.)

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Abstract

Chilling stress can have severe impacts on the growth, development and productivity of maize worldwide. In the present study, cDNA amplified fragment length polymorphism (cDNA-AFLP) analysis was used to evaluate gene expression in maize during chilling treatments (6°C) over four time periods (0, 2, 6 and 12 h). A total of 441 transcript-derived fragments (TDFs) induced by low-temperature treatment were detected. Based on the sequence analysis, the 58 TDFs of known functions were involved in metabolism, photosynthesis, signal transduction and defence responses etc., suggesting that maize undergoes a complex adaptive process in response to low temperatures. Three full-length cDNA, encoding MAPKKK (mitogen-activated protein kinase kinase kinase), CLC-D (chloride channel D) and RLK (receptor-like protein kinases) homologues, were isolated from maize through in silico cloning and named as ZmMAPKKK, ZmCLC-D and ZmRLK, respectively. Finally, the expression patterns of the three genes showed a significant increase of differential expression after chilling stress as analysed by semi-quantitative RT-PCR and real-time qRT-PCR. This study provides important clues to understanding low-temperature regulation mechanisms in maize and the three candidate genes involved in chilling responses need further research to determine their usefulness in breeding new resistance cultivars.

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References

  • Akihiro T, Umezawa T, Ueki C, Lobna BM, Mizuno K, Ohta M, Fujimura T (2006) Genome wide cDNA-AFLP analysis of genes rapidly induced by combined sucrose and ABA treatment in rice cultured cells. FEBS Lett 580:5947–5952

    Article  PubMed  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Bachem CW, van der Hoeven RS, de Bruijn SM, Vreugdenhil D, Zabeau M, Visser RG (1996) Visualization of differential gene expression using a novel method of RNA fingerprinting based on AFLP: analysis of gene expression during potato tuber development. Plant J 9:745–753

    Article  PubMed  CAS  Google Scholar 

  • Baisakh N, Subudhi PK, Parami NP (2006) cDNA-AFLP analysis reveals differential gene expression in response to salt stress in a halophyte Spartina alterniflora Loisel. Plant Sci 170:1141–1149

    Article  CAS  Google Scholar 

  • Breyne P, Dreesen R, Vandepoele K, De Veylder L, Van Breusegem F, Callewaert L, Rombauts S, Raes J, Cannoot B, Engler G, Inzé D, Zabeau M (2002) Transcriptome analysis during cell division in plants. Proc Natl Acad Sci USA 99:14825–14830

    Article  PubMed  CAS  Google Scholar 

  • Carr G, Simmons N, Sayer J (2003) A role for CBS domain 2 in trafficking of chloride channel CLC-5. Biochem Biophys Res Commun 310:600–605

    Article  PubMed  CAS  Google Scholar 

  • Chapman NH, Burt C, Nicholson P (2009) The identification of candidate genes associated with Pch2 eyespot resistance in wheat using cDNA-AFLP. Theor Appl Genet 118:1045–1057

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, Zhu JK (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17:1043–1054

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Zhu JH, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    Article  PubMed  CAS  Google Scholar 

  • Craciun AR, Courbot M, Bourgis F, Salis P, Saumitou-Laprade P, Verbruggen N (2006) Comparative cDNA-AFLP analysis of Cd-tolerant and -sensitive genotypes derived from crosses between the Cd hyperaccumulator Arabidopsis halleri and Arabidopsis lyrata ssp. petraea. J Exp Bot 57:2967–2983

    Article  PubMed  Google Scholar 

  • De Angeli A, Monachello D, Ephritikhine G, Frachisse JM, Thomine S, Gambale F, Barbier-Brygoo H (2006) The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442:939–942

    Article  PubMed  Google Scholar 

  • De Paepe A, Vuylsteke M, Van Hummelen P, Zabeau M, Van Der Straeten D (2004) Transcriptional profiling by cDNA-AFLP and microarray analysis reveals novel insights into the early response to ethylene in Arabidopsis. Plant J 39:537–559

    Article  PubMed  Google Scholar 

  • Diédhiou CJ, Golldack D (2006) Salt-dependent regulation of chloride channel transcripts in rice. Plant Sci 170:793–800

    Article  Google Scholar 

  • Ditt RF, Nester EW, Comai L (2001) Plant gene expression response to Agrobacterium tumefaciens. Proc Natl Acad Sci USA 98:10954–10959

    Article  PubMed  CAS  Google Scholar 

  • Dutzler R (2004) Structural basis for ion conduction and gating in ClC chloride channels. FEBS Lett 564:229–233

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Mata C, Gay R, Sokolovski S, Hills A, Lamattina L, Blatt MR (2003) Nitric oxide regulates K+ and Cl− channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc Natl Acad Sci USA 100:11116–111121

    Article  PubMed  CAS  Google Scholar 

  • Gou XP, He K, Yang H, Yuan T, Lin HH, Clouse SD, Li J (2010) Genome-wide cloning and sequence analysis of leucine-rich repeat receptor-like protein kinase genes in Arabidopsis thaliana. BMC Genomics 11:19

    Article  PubMed  Google Scholar 

  • Guan B, Jiang G-Q, Wang Y-X, Wang Z-C, Haxim Y, Bao Q, Hu Y-Z, Zhang F-C, Wang Y (2010) Identification of differentially expressed transcripts involved in the salt-stress response of Salsola ferganica by suppression subtractive hybridization. Plant Cell Tissue Organ Cult 103:343–352

    Article  CAS  Google Scholar 

  • He K, Gou XP, Powell RA, Yang H, Yuan T, Guo ZX, Li J (2008) Receptor-like protein kinases, BAK1 and BKK1, regulate a light-dependent cell-death control pathway. Plant Signal Behav 3:813–815

    Article  PubMed  Google Scholar 

  • Hebeisen S, Biela A, Giese B, Muller-Newen G, Hidalgo P, Fahlke C (2004) The role of the carboxyl terminus in ClC chloride channel function. J Biol Chem 279:13140–13147

    Article  PubMed  CAS  Google Scholar 

  • Hechenberger M, Schwappach B, Fischer WN, Frommer WB, Jentsch TJ, Steinmeyer K (1996) A family of putative chloride channels from Arabidopsis and functional complementation of a yeast strain with a CLC gene disruption. J Biol Chem 271:33632–33638

    Article  PubMed  CAS  Google Scholar 

  • Hirt H (2000) Connecting oxidative stress, auxin, and cell cycle regulation through a plant mitogen-activated protein kinase pathway. Proc Natl Acad Sci USA 97:2405–2407

    Article  PubMed  CAS  Google Scholar 

  • Hong SW, Jon JH, Kwak JM, Nam HG (1997) Identification of a receptor-like protein kinase gene rapidly induced by abscisic acid, dehydration, high salt, and cold treatments in Arabidopsis thaliana. Plant Physiol 113:1203–1212

    Article  PubMed  CAS  Google Scholar 

  • Huang J, Bachem C, Jacobsen E, Visser RGF (2001) Molecular analysis of differentially expressed genes during postharvest deterioration in cassava (Manihot eseulenta Crantz) tuberous roots. Euphytica 120:85–93

    Article  CAS  Google Scholar 

  • Isayenkov S, Isner JC, Maathuis FJM (2010) Vacuolar ion channels: roles in plant nutrition and signalling. FEBS Lett 584:1982–1988

    Article  PubMed  CAS  Google Scholar 

  • Jiang W, Fu F-L, Zhang S-Z, Wu L, Li W-C (2010) Cloning and characterization of functional trehalose-6-phosphate synthase gene in maize. J Plant Biol 53:134–141

    Article  CAS  Google Scholar 

  • Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    Article  PubMed  CAS  Google Scholar 

  • Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97:2940–2945

    Article  PubMed  CAS  Google Scholar 

  • Lease KA, Lau NY, Schuster RA, Torii KU, Walker JC (2001) Receptor serine/threonine protein kinases in signalling: analysis of the erecta receptor-like kinase of Arabidopsis thaliana. New Phytologist 151:133–143

    Article  CAS  Google Scholar 

  • Leymarie J, Bruneaux E, Gibot-Leclerc S, Corbineau F (2007) Identification of transcripts potentially involved in barley seed germination and dormancy using cDNA-AFLP. J Exp Bot 58:425–437

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lv QD, Tang RJ, Liu H, Gao XS, Li YZ, Zheng HQ, Zhang HX (2009) Cloning and molecular analyses of the Arabidopsis thaliana chloride channel gene family. Plant Sci 176:650–661

    Article  CAS  Google Scholar 

  • Lv DK, Bai X, Li Y, Ding XD, Ge Y, Cai H, Ji W, Wu N, Zhu YM (2010) Profiling of cold-stress-responsive miRNAs in rice by microarrays. Gene 459:39–47

    Article  PubMed  CAS  Google Scholar 

  • Manickavelu A, Kambara K, Mishina K, Koba T (2007) An efficient method for purifying high quality RNA from wheat pistils. Colloids Surf B Biointerfaces 54:254–258

    Article  PubMed  CAS  Google Scholar 

  • Mishra NS, Tuteja R, Tuteja N (2006) Signaling through MAP kinase networks in plants. Arch Biochem Biophys 452:55–68

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Jin JB, Lee J, Yoo CY, Stirm V, Miura T, Ashworth EN, Bressan RA, Yun DJ, Hasegawa PM (2007) SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 19:1403–1414

    Article  PubMed  CAS  Google Scholar 

  • Nakagami H, Kiegerl S, Hirt H (2004) OMTK1, a novel MAPKKK, channels oxidative stress signaling through direct MAPK interaction. J Biol Chem 279:26959–26966

    Article  PubMed  CAS  Google Scholar 

  • Nguyen HT, Leipner J, Stamp P, Guerra-Peraza O (2009) Low temperature stress in maize (Zea mays L.) induces genes involved in photosynthesis and signal transduction as studied by suppression subtractive hybridization. Plant Physiol Biochem 47:116–122

    Article  PubMed  Google Scholar 

  • Ning J, Li XH, Hicks LM, Xiong LZ (2010) A Raf-Like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol 152:876–890

    Article  PubMed  CAS  Google Scholar 

  • Oufir M, Legay S, Nicot N, Van Moer K, Hoffmann L, Renaut J, Hausman J-F, Evers D (2008) Gene expression in potato during cold exposure: changes in carbohydrate and polyamine metabolisms. Plant Sci 175:839–852

    Article  CAS  Google Scholar 

  • Polesani M, Desario F, Ferrarini A, Zamboni A, Pezzotti M, Kortekamp A, Polverari A (2008) cDNA-AFLP analysis of plant and pathogen genes expressed in grapevine infected with Plasmopara viticola. BMC Genomics 9:142

    Article  PubMed  Google Scholar 

  • Qin F, Sakuma Y, Li J, Liu Q, Li YQ, Shinozaki K, Yamaguchi-Shinozaki K (2004) Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol 45:1042–1052

    Article  PubMed  CAS  Google Scholar 

  • Sarosh BR, Meijer J (2007) Transcriptional profiling by cDNA-AFLP reveals novel insights during methyl jasmonate, wounding and insect attack in Brassica napus. Plant Mol Biol 64:425–438

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223

    PubMed  CAS  Google Scholar 

  • Shiu SH, Bleecker AB (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132:530–543

    Article  PubMed  CAS  Google Scholar 

  • Shou HX, Bordallo P, Fan JB, Yeakley JM, Bibikova M, Sheen J, Wang K (2004) Expression of an active tobacco mitogen-activated protein kinase kinase kinase enhances freezing tolerance in transgenic maize. Proc Natl Acad Sci USA 101:3298–3303

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Steinwand BJ, Kieber JJ (2010) The role of receptor-like kinases in regulating cell wall function. Plant Physiol 153:479–484

    Article  PubMed  CAS  Google Scholar 

  • Sun J, Li LS, Liu MQ, Wang MJ, Ding MQ, Deng SR, Lu CF, Zhou XY, Shen X, Zheng XJ, Chen SL (2010) Hydrogen peroxide and nitric oxide mediate K+/Na+ homeostasis and antioxidant defense in NaCl-stressed callus cells of two contrasting poplars. Plant Cell Tissue Organ Cult 103:205–215

    Article  CAS  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599

    Article  PubMed  CAS  Google Scholar 

  • Thomashow MF (2001) So what’s new in the field of plant cold acclimation? Lots!. Plant Physiol 125:89–93

    Article  PubMed  CAS  Google Scholar 

  • Trzcinska-Danielewicz J, Bilska A, Fronk J, Zielenkiewicz P, Jarochowska E, Roszczyk M, Jończyk M, Axentowicz E, Skoneczny M, Sowiński P (2009) Global analysis of gene expression in maize leaves treated with low temperature: I. Moderate chilling (14°C). Plant Sci 177:648–658

    Article  CAS  Google Scholar 

  • Van de Velde W, Guerra JC, De Keyser A, De Rycke R, Rombauts S, Maunoury N, Mergaert P, Kondorosi E, Holsters M, Goormachtig S (2006) Aging in legume symbiosis. A molecular view on nodule senescence in Medicago truncatula. Plant Physiol 141:711–720

    Article  PubMed  Google Scholar 

  • van der Biezen EA, Juwana H, Parker JE, Jones JD (2000) cDNA-AFLP display for the isolation of Peronospora parasitica genes expressed during infection in Arabidopsis thaliana. Mol Plant Microbe Interact 13:895–898

    Article  PubMed  Google Scholar 

  • Vuylsteke M, Daele H, Vercauteren A, Zabeau M, Kuiper M (2006) Genetic dissection of transcriptional regulation by cDNA-AFLP. Plant J 45:439–446

    Article  PubMed  CAS  Google Scholar 

  • Wang JP, Bughrara SS (2007) Monitoring of gene expression profiles and identification of candidate genes involved in drought responses in Festuca mairei. Mol Genet Genomics 277:571–587

    Article  PubMed  CAS  Google Scholar 

  • Wrzaczek M, Brosché M, Salojarvi J, Kangasjärvi S, Idanheimo N, Mersmann S, Robatzek S, Karpiński S, Karpińska B, Kangasjarvi J (2010) Transcriptional regulation of the CRK/DUF26 group of receptor-like protein kinases by ozone and plant hormones in Arabidopsis. BMC Plant Biol 10:95

    Article  PubMed  Google Scholar 

  • Zhang Y, Fu JJ, Gu RL, Wang JH, Chen XP, Jia JP, Zhang JP, Wang GY (2009a) Isolation and analysis of cold stress inducible genes in Zea mays by suppression subtractive hybridization and cDNA macroarray. Plant Mol Biol Rep 27:38–49

    Article  Google Scholar 

  • Zhang J, Xu Y, Huan Q, Chong K (2009b) Deep sequencing of Brachypodium small RNAs at the global genome level identifies microRNAs involved in cold stress response. BMC Genomics 10:449

    Article  PubMed  Google Scholar 

  • Zhou XF, Wang GD, Sutoh K, Zhu JK, Zhang WX (2008) Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochim Biophys Acta 1779:780–788

    PubMed  CAS  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 10:290–295

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This research was supported by the National Key Technology R&D Program of China (2006BAD13B03).

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  1. College of Plant Science, Jilin University, 5333 Xi’an Road, 130062, Changchun, China

    Guang Yang, Hongda Zou, Ying Wu, Hongkui Liu & Yaping Yuan

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  1. Guang Yang
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  2. Hongda Zou
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Correspondence to Yaping Yuan.

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Yang, G., Zou, H., Wu, Y. et al. Identification and characterisation of candidate genes involved in chilling responses in maize (Zea mays L.). Plant Cell Tiss Organ Cult 106, 127–141 (2011). https://doi.org/10.1007/s11240-010-9900-8

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