Abstract
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.
Similar content being viewed by others
References
Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599. https://doi.org/10.1146/annurev.arplant.50.1.571
Gott MB (1957) Vernalization of green plants of a winter wheat. Nature 180:714–715. https://doi.org/10.1038/180714a0
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. https://doi.org/10.1093/aob/mch196
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. https://doi.org/10.1007/s00122-003-1468-9
Zinn K, Tunc-Ozdemir M, Harper J (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. J Exp Bot 61:1959–1968. https://doi.org/10.1093/jxb/erq053
Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403. https://doi.org/10.1146/annurev.arplant.47.1.377
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. https://doi.org/10.1186/s12870-015-0511-8
Calzadilla P, Maiale S, Ruiz O, Escaray F (2016) Transcriptome response mediated by cold stress in Lotus japonicus. Front Plant Sci 7:374. https://doi.org/10.3389/fpls.2016.00374
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. https://doi.org/10.1186/1471-2164-15-203
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. https://doi.org/10.3389/fpls.2017.00136
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. https://doi.org/10.1007/s11103-007-9161-z
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. https://doi.org/10.1093/jxb/ern112
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. https://doi.org/10.1371/journal.pone.0133166
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. https://doi.org/10.1016/j.jbiotec.2014.08.032
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. https://doi.org/10.1186/s12864-017-3556-2
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. https://doi.org/10.1126/science.1250092
Larsen AO, Jensen CA (2014) Evaluación de cultivares de trigo candeal en Barrow - Campaña 2013–2014. EEAI INTA Barrow. http://inta.gob.ar/documentos/evaluacion-de-cultivares-de-trigocandeal-en-barrow-campana-2013-2014
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. https://doi.org/10.1111/pbr.12292
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. http://repositoriodigital.uns.edu.ar/handle/123456789/607
Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/
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. https://doi.org/10.1038/nbt.1883
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. https://doi.org/10.1038/nbt.1621
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. https://doi.org/10.1093/bioinformatics/btp612
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. https://doi.org/10.1093/bioinformatics/bti610
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. https://doi.org/10.1093/nar/gkw982
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. https://doi.org/10.1093/nar/gkv1215
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. https://doi.org/10.1093/nar/gkl031
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. https://doi.org/10.1006/meth.2001.1262
Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2010) InfoStat, versión 2010, Grupo InfoStat. http://www.infostat.com.ar/
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. https://doi.org/10.1007/s00122-013-2165-y
Fowler D (2008) Cold acclimation threshold induction temperatures in cereals. Crop Sci 48:1147–1154. https://doi.org/10.1186/1471-2164-12-299
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. https://doi.org/10.1186/s12864-015-1996-0
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. https://doi.org/10.1126/science.aan0032
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. https://doi.org/10.1186/1471-2164-14-77
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. https://doi.org/10.1111/j.1467-7652.2010.00536.x
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. https://doi.org/10.1104/pp.17.01311
Mancinelli A (1983) The photoregulation of anthocyanin synthesis. In: Pirson A, Zimmermann MH (eds) Encyclopaedia of plant physiology. Springer-Verlag, Berlin, pp 640–661
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. https://doi.org/10.1104/pp.108.1.39
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. https://doi.org/10.3389/fpls.2017.00374
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. https://doi.org/10.3390/ijms160613561
Choudhury F, Rivero R, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867. https://doi.org/10.1111/tpj.13299
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. https://doi.org/10.1111/j.1438-8677.2012.00718.x
Dixon D, Lapthorn A, Edward R (2002) Plant glutathione transferases. Genome Biol. https://doi.org/10.1186/gb-2002-3-3-reviews3004
Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5:218–223. https://doi.org/10.1016/S1369-5266(02)00256-X
Kramer D, Evans J (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol 155:70–78. https://doi.org/10.1104/pp.110.166652
Kaplan F, Sung DY, Guy CL (2006) Roles of β-amylase and starch breakdown during temperatures stress. Physiol Plant 126:120–128. https://doi.org/10.1111/j.1399-3054.2006.00604.x
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. https://doi.org/10.2135/cropsci1995.0011183X003500020038x
Pennycooke JC, Jones ML, Stushnoff C (2003) Down-regulating α-Galactosidase enhances freezing tolerance in transgenic petunia. Plant Physiol 133:901–909. https://doi.org/10.1104/pp.103.024554
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. https://doi.org/10.1016/j.febslet.2004.09.006
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. https://doi.org/10.1046/j.0960-7412.2001.01227.x
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. https://doi.org/10.1104/pp.122.4.1129
Syed N, Kalyna M, Marquez Y, Barta A, Brown W (2012) Alternative splicing in plants—coming of age. Trends Plant Sci 17:616–623. https://doi.org/10.1016/j.tplants.2012.06.001
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. https://doi.org/10.1007/s00425-004-1475-3
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. https://doi.org/10.1271/bbb.66.2297
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. https://doi.org/10.1021/acs.jafc.5b01635
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. https://doi.org/10.1002/jsfa.8968
Mikic S, Ahmad S (2018) Benzoxazinoids-protective secondary metabolites in cereals: biochemistry and genetic control. Ratar povrt 55:49–57.
Zhou S, Richter A, Jander G (2018) Beyond defense: multiple functions of benzoxazinoids in maize metabolism. Plant Cell Physiol 59:1528–1537. https://doi.org/10.1093/pcp/pcy064
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. https://doi.org/10.1093/dnares/dsq023
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. https://doi.org/10.1371/journal.pone.0195138
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. https://doi.org/10.1080/13102818.2014.944401
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. https://doi.org/10.1134/S0006297917100030
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. https://doi.org/10.1104/pp.105.064287
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. https://doi.org/10.1104/pp.110.159079
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. https://doi.org/10.3389/fpls.2016.02034
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. https://doi.org/10.1016/S1360-1385(01)02223-3
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. https://doi.org/10.1074/jbc.M605895200
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. https://doi.org/10.1016/j.bbagrm.2011.10.002
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. https://doi.org/10.1111/j.1365-313X.2005.02588.x
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. https://doi.org/10.1371/journal.pgen.1006333
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. https://doi.org/10.3389/fpls.2016.01509
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. https://doi.org/10.1007/s00709-010-0142-8
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. https://doi.org/10.1016/j.plaphy.2016.12.028
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. https://doi.org/10.1038/srep23072
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. https://doi.org/10.1105/tpc.006130
Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37. https://doi.org/10.1038/353031a0
Ariel F, Manavella P, Dezar C, Chan R (2007) The true story of the HD-Zip family. Trends Plant Sci 12:419–426. https://doi.org/10.1016/j.tplants.2007.08.003
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. https://doi.org/10.3389/fpls.2018.00692
Singh KB, Foley RC, Sánchez LO (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436. https://doi.org/10.1016/S1369-5266(02)00289-3
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. https://doi.org/10.1186/1471-2229-12-22
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. https://doi.org/10.1111/nph.12291
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. https://doi.org/10.1104/pp.16.01725
Rushton P, Somssich I, Ringler P, Shen Q (2010) WRKY transcription factors. Trends Plant Sci 15:247–258. https://doi.org/10.1016/j.tplants.2010.02.006
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. https://doi.org/10.3389/fpls.2015.00615
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. https://doi.org/10.1016/j.gpb.2017.01.007
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. https://doi.org/10.1038/srep45981
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. https://doi.org/10.1371/journal.pone.0200002
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. https://doi.org/10.1016/0014-5793(94)00353-X
Acknowledgements
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.
Funding
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).
Author information
Authors and Affiliations
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.
Corresponding author
Ethics declarations
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.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Díaz, M.L., Soresi, D.S., Basualdo, J. et al. Transcriptomic response of durum wheat to cold stress at reproductive stage. Mol Biol Rep 46, 2427–2445 (2019). https://doi.org/10.1007/s11033-019-04704-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-019-04704-y