Molecular Biology Reports

, Volume 46, Issue 2, pp 2427–2445 | Cite as

Transcriptomic response of durum wheat to cold stress at reproductive stage

  • Marina L. DíazEmail author
  • Daniela S. Soresi
  • Jessica Basualdo
  • Selva J. Cuppari
  • Alicia Carrera
Original Article


Understanding the genetic basis of cold tolerance is a key step towards obtaining new and improved crop varieties. Current geographical distribution of durum wheat in Argentina exposes the plants to frost damage when spikes have already emerged. Biochemical pathways involved in cold tolerance are known to be early activated at above freezing temperatures. In this study we reported the transcriptome of CBW0101 spring durum wheat by merging data from untreated control and cold (5 °C) treated plant samples at reproductive stage. A total of 128,804 unigenes were predicted. Near 62% of the unigenes were annotated in at least one database. In total 876 unigenes were differentially expressed (DEGs), 562 were up-regulated and 314 down-regulated in treated samples. DEGs are involved in many critical processes including, photosynthetic activity, lipid and carbohydrate synthesis and accumulation of amino acids and seed proteins. Twenty-eight transcription factors (TFs) belonging to 14 families resulted differentially expressed from which eight families comprised of only TFs induced by cold. We also found 31 differentially expressed Long non-coding RNAs (lncRNAs), most of them up-regulated in treated plants. Two of these lncRNAs could operate via microRNAs (miRNAs) target mimic. Our results suggest a reprogramming of expression patterns in CBW0101 that affects a number of genes that is closer to the number reported in winter genotypes. These observations could partially explain its moderate tolerance (low proportion of frost-damaged spikes) when exposed to freezing days in the field.


Cold tolerance Differentially expressed genes Durum wheat RNA-seq Transcriptome Reproductive stage 



We thank Lic. Santiago Revale for his technical assistance in the use of Illumina HiSeq 1500 platform and in the preliminary bioinformatic analysis of reads. We are also thankful to Engineer C. Jensen and Dra A. Larsen (INTA Barrow) for providing the seeds of wheat accession and the pedigree information. The authors would also like to thank Dr. Freda Anderson for providing language help.

Author contributions

MLD and DSS performed the analyses and wrote the manuscript; JB generated the dataset; SJC performed gene qRT-PCR validation. AC supervised the work and helped to discuss the results. All authors read and approved the article.


This research was granted by the Agencia Nacional de Promoción Científica y Tecnológica (PICT 2011–2188 grant awarded to Dr. A. Carrera) and Universidad Nacional del Sur and Comisión de Investigaciones Científicas de la Pcia. de Buenos Aires (grants awarded to Dr. M. Díaz).

Compliance with ethical standards

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Supplementary material

11033_2019_4704_MOESM1_ESM.docx (165 kb)
Supplementary material 1 (DOCX 165 KB)


  1. 1.
    Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599. CrossRefGoogle Scholar
  2. 2.
    Gott MB (1957) Vernalization of green plants of a winter wheat. Nature 180:714–715. CrossRefGoogle Scholar
  3. 3.
    Fowler DB, Limin AE (2004) Interactions among factors regulating phenological development and acclimation rate determine low temperature tolerance in wheat. Ann Bot 94:717–724. CrossRefGoogle Scholar
  4. 4.
    Francia E, Rizza F, Cattivelli L, Stanca AM, Galiba G, Tóth B, Hayes PM, Skinner JS, Pecchioni N (2004) Two loci on chromosome 5H determine low-temperature tolerance in a ‘Nure’ (winter) x ‘Tremois’ (spring) barley map. Theor Appl Genet 108:670–680. CrossRefGoogle Scholar
  5. 5.
    Zinn K, Tunc-Ozdemir M, Harper J (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. J Exp Bot 61:1959–1968. CrossRefGoogle Scholar
  6. 6.
    Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403. CrossRefGoogle Scholar
  7. 7.
    Liu Z, Xin M, Qin J, Peng H, Ni Z, Yao Y, Sun Q (2015) Temporal transcriptome profiling reveals expression partitioning of homeologous genes contributing to heat and drought acclimation in wheat (Triticum aestivum L.). BMC Plant Biol 15:152. CrossRefGoogle Scholar
  8. 8.
    Calzadilla P, Maiale S, Ruiz O, Escaray F (2016) Transcriptome response mediated by cold stress in Lotus japonicus. Front Plant Sci 7:374. CrossRefGoogle Scholar
  9. 9.
    Wang J, Yang Y, Liu X, Huang J, Wang Q, Gu J, Lu Y (2014) Transcriptome profiling of the cold response and signaling pathways in Lilium lancifolium. BMC Genom 15:203. CrossRefGoogle Scholar
  10. 10.
    Lu X, Zhou X, Cao Y, Zhou M, McNeil D, Liang S, Yang C (2017) RNA-seq Analysis of cold and drought responsive transcriptomes of Zea mays ssp. Mexicana L. Front Plant Sci 8:136. Google Scholar
  11. 11.
    Monroy AF, Dryanova A, Malette B, Oren DH, Farajalla MR, Liu W, Danyluk J, Ubayasena LWC, Kane K, Scoles GJ, Sarhan F, Gulick PJ (2007) Regulatory gene candidates and gene expression analysis of cold acclimation in winter and spring wheat. Plant Mol Biol 64:409–423. CrossRefGoogle Scholar
  12. 12.
    Ganeshan S, Vitamvas P, Fowler DB, Chibbar RN (2008) Quantitative expression analysis of selected COR genes reveals their differential expression in leaf and crown tissues of wheat (Triticum aestivum L.) during an extended low temperature acclimation regimen. J Exp Bot 59:2393–2402. CrossRefGoogle Scholar
  13. 13.
    Skinner DZ (2015) Genes upregulated in winter wheat (Triticum aestivum L.) during mild freezing and subsequent thawing suggest sequential activation of multiple response mechanisms. PLoS ONE. Google Scholar
  14. 14.
    Zhang S, Song G, Gao J, Li Y, Guo D, Fan Q, Sui X, Chu X, Huang C, Liu J, Li G (2014) Transcriptome characterization and differential expression analysis of cold-responsive genes in young spikes of common wheat. J Biotechnol 189:48–57. CrossRefGoogle Scholar
  15. 15.
    Song G, Zhang R, Zhang S, Li Y, Gao J, Han X, Chen M, Wang J, Li W, Li G (2017) Response of microRNAs to cold treatment in the young spikes of common wheat. BMC Genom 18:212. CrossRefGoogle Scholar
  16. 16.
    Marcussen T, Sandve S, Heier L, Spannagl M, Pfeifer M, Jakobsen K, Wulff B, Steuernagel B, Mayer K, Olsen O (2014) Ancient hybridizations among the ancestral genomes of bread wheat. Science. Google Scholar
  17. 17.
    Larsen AO, Jensen CA (2014) Evaluación de cultivares de trigo candeal en Barrow - Campaña 2013–2014. EEAI INTA Barrow.
  18. 18.
    Basualdo J, Díaz ML, Cuppari S, Cardone S, Soresi D, Pérez Camargo G, Carrera A (2015) Allelic variation and differential expression of VRN-A1 in durum wheat genotypes varying in the vernalization response. Plant Breed 134:520–528. CrossRefGoogle Scholar
  19. 19.
    Basualdo J (2013) Estudio de la variabilidad de la tolerancia a bajas temperaturas en trigo candeal (Triticum turgidum L. var. durum) y genes asociados. Tesis para optar al grado de doctora en Ciencias Biológicas. Universidad Nacional del Sur.
  20. 20.
    Andrews S (2010) FastQC: a quality control tool for high throughput sequence data.
  21. 21.
    Grabherr MG, Hass BJ, Yassour M, Levin JZ, Thompson DA, Amit L et al (2011) Full length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652. CrossRefGoogle Scholar
  22. 22.
    Trapnell C, Williams A, Pertea G, Mortazavi A, Kwan G, Baren M, Salzberg S, Wold B, Pachter L (2010) Transcript assembly and quantification by rNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515. CrossRefGoogle Scholar
  23. 23.
    Wang LK, Feng ZX, Wang X, Wang XW, Zhang XG (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138. CrossRefGoogle Scholar
  24. 24.
    Conesa A, Götz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676. CrossRefGoogle Scholar
  25. 25.
    Jin JP, Tian F, Yang DC, Meng YQ, Kong L, Luo JC, Gao G (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 45:D1040–D1045. CrossRefGoogle Scholar
  26. 26.
    Paytuví Gallart A, Hermoso Pulido A, Anzar Martínez de Lagrán I, Sanseverino W, Cigliano A, R (2016) GREENC: a Wiki-based database of plant lncRNAs. Nucleic Acids Res 44:D1161–D1166. CrossRefGoogle Scholar
  27. 27.
    Ye J, Fang L, Zheng HK, Zhang Y, Chen J, Zhang ZJ et al (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–W297. CrossRefGoogle Scholar
  28. 28.
    Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408. CrossRefGoogle Scholar
  29. 29.
    Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2010) InfoStat, versión 2010, Grupo InfoStat.
  30. 30.
    Pearce S, Zhu J, Boldizsár Á, Vágújfalvi A, Burke A, Garland-Campbell K, Galiba G, Dubcovsky J (2013) Large deletions in the CBF gene cluster at the Fr-B2 locus are associated with reduced frost tolerance in wheat. Theor Appl Genet 126:2683–2697. CrossRefGoogle Scholar
  31. 31.
    Fowler D (2008) Cold acclimation threshold induction temperatures in cereals. Crop Sci 48:1147–1154. CrossRefGoogle Scholar
  32. 32.
    Zou H, Tzarfati R, Hübner S, Krugman T, Fahima T, Abbo S, Saranga Y, Korol AB (2015) Transcriptome profiling of wheat glumes in wild emmer, hulled landraces and modern cultivars. BMC Genom 16:777. CrossRefGoogle Scholar
  33. 33.
    Avni R, Nave M, Barad O, Baruch K, Twardziok S et al (2017) Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science 357:93–97. CrossRefGoogle Scholar
  34. 34.
    Oono Y, Kobayashi F, Kawahara Y, Yazawa T, Handa H, Itoh T, Matsumoto T (2013) Characterisation of the wheat (Triticum aestivum L.) transcriptome by de novo assembly for the discovery of phosphate starvation-responsive genes: gene expression in Pi-stressed wheat. BMC Genom 14:77. CrossRefGoogle Scholar
  35. 35.
    Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ (2010) Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnol J 8:749–771. CrossRefGoogle Scholar
  36. 36.
    Li Q, Byrns B, Badawi M, Diallo A, Danyluk J, Sarhan F, Laudencia-Chingcuanco D, Zou J, Fowler B (2018) Transcriptomic insights into phenological development and cold tolerance of wheat grown in the field. Plant Physiol 176:2376–2394. CrossRefGoogle Scholar
  37. 37.
    Mancinelli A (1983) The photoregulation of anthocyanin synthesis. In: Pirson A, Zimmermann MH (eds) Encyclopaedia of plant physiology. Springer-Verlag, Berlin, pp 640–661Google Scholar
  38. 38.
    Leyva A, Jarillo JA, Salinas J, Martínez-Zapater JM (1995) Low temperature induces the accumulation of phenylalanine ammonia-lyase and chalcone synthase mRNAs of Arabidopsis thaliana in a light-dependent manner. Plant Physiol 108:39–46. CrossRefGoogle Scholar
  39. 39.
    Gupta O, Karkute S, Banerjee S, Meena N, Dahuja A (2017) Contemporary understanding of miRNA-based regulation of secondary metabolites biosynthesis in plants. Front Plant Sci 29:374. Google Scholar
  40. 40.
    Sofo A, Scopa A, Nuzzaci M, Vitti A (2015) Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. Int J Mol Sci 16:13561–13578. CrossRefGoogle Scholar
  41. 41.
    Choudhury F, Rivero R, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867. CrossRefGoogle Scholar
  42. 42.
    Distelbarth H, Nägele T, Heyer AG (2013) Responses of antioxidant enzymes to cold and high light are not correlated to freezing tolerance in natural accessions of Arabidopsis thaliana. Plant Biol 15:982–990. CrossRefGoogle Scholar
  43. 43.
    Dixon D, Lapthorn A, Edward R (2002) Plant glutathione transferases. Genome Biol. Google Scholar
  44. 44.
    Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5:218–223. CrossRefGoogle Scholar
  45. 45.
    Kramer D, Evans J (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol 155:70–78. CrossRefGoogle Scholar
  46. 46.
    Kaplan F, Sung DY, Guy CL (2006) Roles of β-amylase and starch breakdown during temperatures stress. Physiol Plant 126:120–128. CrossRefGoogle Scholar
  47. 47.
    Castonguay Y, Nadeau P, Lechasseur P, Chouinard L (1995) Differential accumulation of carbohydrates in alfalfa cultivars of contrasting winterhardiness. Crop Sci 35(2):509–516. CrossRefGoogle Scholar
  48. 48.
    Pennycooke JC, Jones ML, Stushnoff C (2003) Down-regulating α-Galactosidase enhances freezing tolerance in transgenic petunia. Plant Physiol 133:901–909. CrossRefGoogle Scholar
  49. 49.
    Zuther E, Büchel K, Hundertmark M, Stitt M, Hincha DK, Heyer AG (2004) The role of raffinose in the cold acclimation of Arabidopsis thaliana. FEBS Lett 576:169–173. CrossRefGoogle Scholar
  50. 50.
    Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M et al (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426. CrossRefGoogle Scholar
  51. 51.
    Hong Z, Lakkineni K, Zhang Z, Verma DPS (2000) Removal of feedback inhibition of delta 1-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 122:1129–1136. CrossRefGoogle Scholar
  52. 52.
    Syed N, Kalyna M, Marquez Y, Barta A, Brown W (2012) Alternative splicing in plants—coming of age. Trends Plant Sci 17:616–623. CrossRefGoogle Scholar
  53. 53.
    Mastrangelo AM, Belloni S, Barilli S, Ruperti B, Di Fonzo N, Stanca AM, Cattivelli L (2005) Low temperature promotes intron retention in two e-cor genes of durum wheat. Planta 221:705–715. CrossRefGoogle Scholar
  54. 54.
    Kawakami A, Yoshida M (2002) Molecular characterization of sucrose:sucrose 1-fructosyltransferase and sucrose:fructan 6-fructosyltransferase associated with fructan accumulation in winter wheat during cold hardening. Biosci Biotechnol Biochem 66:2297–2305. CrossRefGoogle Scholar
  55. 55.
    Giuliani M, Palermo C, De Santis M, Mentana A, Pompa M, Giuzio L, Masci S, Centonze D, Flagella Z (2015) Differential expression of durum wheat gluten proteome under water stress during grain filling. J Agric Food Chem 63:6501–6512. CrossRefGoogle Scholar
  56. 56.
    Zhou J, Liu D, Deng X, Zhen S, Wang Z, Yan Y (2018) Effects of water deficit on breadmaking quality and storage protein compositions in bread wheat (Triticum aestivum L.). J Sci Food Agric. Google Scholar
  57. 57.
    Mikic S, Ahmad S (2018) Benzoxazinoids-protective secondary metabolites in cereals: biochemistry and genetic control. Ratar povrt 55:49–57.CrossRefGoogle Scholar
  58. 58.
    Zhou S, Richter A, Jander G (2018) Beyond defense: multiple functions of benzoxazinoids in maize metabolism. Plant Cell Physiol 59:1528–1537. CrossRefGoogle Scholar
  59. 59.
    Garg R, Jhanwar S, Tyagi AK, Jain M (2010) Genome-wide survey and expression analysis suggest diverse roles of glutaredoxin gene family members during development and response to various stimuli in rice. DNA Res 17:353–367. CrossRefGoogle Scholar
  60. 60.
    Zhang J, Xu Y, Dong J, Peng L, Feng X, Wang X, Li F, Miao Y, Yao S, Zhao Q, Feng S, Hu B, Li F (2018) Genome-wide identification of wheat (Triticum aestivum) expansins and expansin expression analysis in cold-tolerant and cold-sensitive wheat cultivars. PLoS ONE 13(3):e0195138. CrossRefGoogle Scholar
  61. 61.
    Todorovska EG, Kolev S, Christov NK, Balint A, Kocsy G et al (2014) The expression of CBF genes at Fr-2 locus is associated with the level of frost tolerance in Bulgarian winter wheat cultivars. Biotechnol Biotechnol Equip 28:392–401. CrossRefGoogle Scholar
  62. 62.
    Wang D, Jin Y, Ding X, Wang W, Zhai S, Bai L, Guo Z (2017) Gene regulation and signal transduction in the ICE–CBF–COR signaling pathway during cold stress in plants. Biochemistry 82:1103–1117. Google Scholar
  63. 63.
    Loukoianov A, Yan L, Blechl A, Sanchez A, Dubcovsky J (2005) Regulation of VRN-1 vernalization genes in normal and transgenic polyploid wheat. Plant Physiol 138:2364–2373. CrossRefGoogle Scholar
  64. 64.
    Dhillon T, Pearce SP, Stockinger EJ, Distelfeld A, Li C, Knox AK et al (2010) Regulation of freezing tolerance and flowering in temperate cereals: the VRN-1 connection. Plant Physiol 153:1846–1858. CrossRefGoogle Scholar
  65. 65.
    Yousfi FE, Makhloufi E, Marande W, Ghorbel AW, Bouzayen M, Berges H (2017) Comparative analysis of WRKY genes potentially involved in salt stress responses in Triticum turgidum L. ssp. durum. Front Plant Sci 7:2034. CrossRefGoogle Scholar
  66. 66.
    Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111. CrossRefGoogle Scholar
  67. 67.
    Agarwal M, Hao Y, Kapoor A, Dong CH, Fuji H, Zheng X, Zhu JK (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281:37636–37645. CrossRefGoogle Scholar
  68. 68.
    Scharf KD, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim Biophys Acta 1819:104–119. CrossRefGoogle Scholar
  69. 69.
    Liu PP, Koizuka N, Martin RC, Nonogaki H (2005) The BME3 (Blue Micropylar End 3) GATA zinc finger transcription factor is a positive regulator of Arabidopsis seed germination. Plant J 44:960–971. CrossRefGoogle Scholar
  70. 70.
    Myers ZA, Kumimoto RW, Siriwardana CL, Gayler KK, Risinger JR, Pezzetta D, Holt BF (2016) NUCLEAR FACTOR Y, subunit C (NF-YC) transcription factors are positive regulators of photomorphogenesis in Arabidopsis thaliana. PLoS Genet 12:e1006333. CrossRefGoogle Scholar
  71. 71.
    Chen M, Ji M, Wen B, Liu L, Li S, Chen X, Gao D, Li L (2016) GOLDEN 2-LIKE Transcription Factors of Plants. Front Plant Sci 7:1509. Google Scholar
  72. 72.
    Dietz KJ, Vogel MO, Viehhauser A (2010) AP2/EREBP transcription factors are part of gene regulatory networks and integrate metabolic, hormonal and environmental signals in stress acclimation and retrograde signalling. Protoplasma 245:3–14. CrossRefGoogle Scholar
  73. 73.
    Saidi MN, Mergby D, Brini F (2017) Identification and expression analysis of the NAC transcription factor family in durum wheat (Triticum turgidum L. ssp. durum). Plant Physiol Biochem 112:117–128. CrossRefGoogle Scholar
  74. 74.
    Wen C, Cheng Q, Zhao L, Mao A, Yang J, Yu S, Weng Y, Xu Y (2016) Identification and characterisation of Dof transcription factors in the cucumber genome. Sci Rep. Google Scholar
  75. 75.
    Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78. CrossRefGoogle Scholar
  76. 76.
    Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37. CrossRefGoogle Scholar
  77. 77.
    Ariel F, Manavella P, Dezar C, Chan R (2007) The true story of the HD-Zip family. Trends Plant Sci 12:419–426. CrossRefGoogle Scholar
  78. 78.
    Ma L, Li G (2018) FAR1-RELATED SEQUENCE (FRS) and FRS-RELATED FACTOR (FRF) family proteins in Arabidopsis growth and development. Front Plant Sci 9:692. CrossRefGoogle Scholar
  79. 79.
    Singh KB, Foley RC, Sánchez LO (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436. CrossRefGoogle Scholar
  80. 80.
    Feng XM, Zhao Q, Zhao LL, Qiao Y, Xie XB, Li HF, Yao YX, You CX, Hao YJ (2012) The cold-induced basic helix-loop-helix transcription factor gene MdCIbHLH1 encodes an ICE-like protein in apple. BMC Plant Biol 12:22. CrossRefGoogle Scholar
  81. 81.
    Licausi F, Ohme-Takagi M, Perata P (2013) APETALA2/ethylene responsive factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol 199:639–649. CrossRefGoogle Scholar
  82. 82.
    Lv Y, Yang M, Hu D, Yang Z, Ma S, Li X, Xiong L (2017) The OsMYB30 transcription factor suppresses cold tolerance by interacting with a jaz protein and suppressing b-amylase expression. Plant Physiol 173:1475–1491. CrossRefGoogle Scholar
  83. 83.
    Rushton P, Somssich I, Ringler P, Shen Q (2010) WRKY transcription factors. Trends Plant Sci 15:247–258. CrossRefGoogle Scholar
  84. 84.
    Wang X, Zeng J, Li Y, Rong X, Sun J, Sun T, Li M, Wang L, Feng Y, Chai R, Chen M, Chang J, Li K, Yang G, He G (2015) Expression of TaWRKY44, a wheat WRKY gene, in transgenic tobacco confers multiple abiotic stress tolerances. Front Plant Sci 6:615. Google Scholar
  85. 85.
    Wang J, Meng X, Dobrovolskaya O, Orlov Y, Chen M (2017) Non-coding RNAs and their roles in stress response in plants. Genom Proteom Bioinform 15:301–312. CrossRefGoogle Scholar
  86. 86.
    Li S, Yu X, Lei N, Cheng Z, Zhao P, He Y et al (2017) Genome-wide identification and functional prediction of cold and/or drought-responsive lncRNAs in cassava. Sci Rep 7:5981. CrossRefGoogle Scholar
  87. 87.
    Liu W, Cheng C, Lin Y, Xuhan X, Lai Z (2018) Genome-wide identification and characterization of mRNAs and lncRNAs involved in cold stress in the wild banana (Musa itinerans). PLoS ONE, 13:e0200002. CrossRefGoogle Scholar
  88. 88.
    Danyluk J, Houde M, Rassart E, Sarhan F (1994) Differential expresion of a gene encoding an acidic dehydrin in chilling sensitive and freezing tolerant gramineae species. FEBS Lett 344:20–24. CrossRefGoogle Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Departamento de Biología, Bioquímica y FarmaciaUniversidad Nacional del Sur (UNS), Comisión de Investigaciones Científicas (CIC)Bahía BlancaArgentina
  2. 2.Centro de Recursos Naturales Renovables de la Zona Semiárida (CERZOS)Universidad Nacional del Sur (UNS)-CONICETBahía BlancaArgentina
  3. 3.Departamento de AgronomíaUniversidad Nacional del Sur (UNS)Bahía BlancaArgentina

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