UNLABELLED: Low temperatures represent a crucial environmental factor determining winter survival (WS) of barley and wheat winter-type varieties. In laboratory experiments, low temperatures induce an active plant acclimation response, which is associated with an enhanced accumulation of several stress-inducible proteins including dehydrins. Here, dehydrin accumulations in sampled wheat (WCS120 protein family, or WCS120 and WDHN13 transcripts) and barley (DHN5 protein) varieties grown in two locations for two winters were compared with the variety WS evaluated by a provocation wooden-box test. A high correlation between dehydrin transcripts or protein relative accumulation and variety WS score was found only in samples taken prior vernalization fulfillment, when high tolerant varieties accumulated dehydrins earlier and to higher level than less tolerant varieties, and the plants have not yet been vernalized. After vernalization fulfillment, the correlation was weak, and the apical development indicated that plants reached double ridge (DR) in barley or stayed before DR in wheat. Dehydrin proteins and transcripts can be thus used as reliable markers of wheat or barley variety winter hardiness in the field conditions; however, only at the beginning of winter, when the plants have not yet finished vernalization. In wheat, a higher correlation was obtained for the total amount of dehydrins than for the individual dehydrin proteins. HIGHLIGHTS: -More tolerant winter-type wheat and barley plants reveal higher threshold induction temperatures for dehydrin accumulation in comparison to less tolerant varieties. Thus, more tolerant winter cereals have higher dehydrin levels than the less tolerant ones upon the same ambient temperature in November samplings.-A significant correlation between dehydrin transcript/protein accumulation and winter survival was found in both winter wheat and winter barley plants in the field conditions, but only prior to vernalization fulfillment.

Department of Crop Science Breeding and Plant Medicine Faculty of AgriSciences Mendel University Brno Czechia

Department of Genetics and Plant Breeding Crop Research Institute Prague Czechia

Research Centre SELTON Ltd Stupice Czechia

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Battaglia M., Olvera-Carrillo Y., Garciarrubio A., Campos F., Covarrubias A. A. (2008). The enigmatic LEA proteins and other hydrophilins. Plant Physiol. 148 6–24. 10.1104/pp.108.120725 PubMed DOI PMC

Chouard P. (1960). Vernalization and its relations to dormancy. Annu. Rev. Plant Physiol. Plant Mol. Biol. 11 191–238. 10.1146/annurev.pp.11.060160.001203 PubMed DOI

Crosatti C., Mare C., Mazzucotelli E., Selioni S., Barilli S., Bassi R., et al. (2003). Genetic analysis of the expression of the cold-regulated gene cor14b: a way toward the identification of components of the cold response signal transduction in Triticeae. Can. J. Bot. 81 1162–1167. 10.1139/B03-114 DOI

Crosatti C., Pagani D., Cattivelli L., Stanca A. M., Rizza F. (2008). Effects of growth stage and hardening conditions on the association between frost resistance and the expression of the cold-induced protein COR14b in barley. Environ. Exp. Bot. 62 93–100. 10.1016/j.envexpbot.2007.07.008 DOI

Danyluk J., Houde M., Rassart E., Sarhan F. (1994). Differential expression of a gene encoding an acidic dehydrin in chilling sensitive and freezing tolerant gramineae species. FEBS Lett. 344 20–24. 10.1016/0014-5793(94)00353-X PubMed DOI

Danyluk J., Perron A., Houde M., Limin A., Fowler B., Benhamou N., et al. (1998). Accumulation of an acidic dehydrin in the vicinity of the plasma membrane during cold acclimation of wheat. Plant Cell 10 623–638. 10.1105/tpc.10.4.623 PubMed DOI PMC

Deng W. W., Casao M. C., Wang P. H., Sato K., Hayes P. M., Finnegan E. J., et al. (2015). Direct links between the vernalization response and other key traits of cereal crops. Nat. Commun. 6:5882. 10.1038/ncomms6882 PubMed DOI

Dhillon T., Pearce S. P., Stockinger E. J., Distelfeld A., Li C. X., Knox A. K., et al. (2010). Regulation of freezing tolerance and flowering in temperate cereals: the VRN-1 connection. Plant Physiol. 153 1846–1858. 10.1104/pp.110.159079 PubMed DOI PMC

Fowler D. B. (2008). Cold acclimation threshold induction temperatures in cereals. Crop Sci. 48 1147–1154. 10.2135/cropsci2007.10.0581 PubMed DOI

Fowler D. B., Breton G., Limin A. E., Mahfoozi S., Sarhan F. (2001). Photoperiod and temperature interactions regulate low-temperature-induced gene expression in barley. Plant Physiol. 127 1676–1681. 10.1104/pp.127.4.1676 PubMed DOI PMC

Ganeshan S., Denesik T., Fowler D. B., Chibbar R. N. (2009). Quantitative expression analysis of selected low temperature-induced genes in autumn-seeded wheat (Triticum aestivum L.) reflects changes in soil temperature. Environ. Exp. Bot. 66 46–53. 10.1016/j.envexpbot.2008.12.013 DOI

Giorni E., Crosatti C., Baldi P., Grossi M., Mare C., Stanca A. M., et al. (1999). Cold-regulated gene expression during winter in frost tolerant and frost susceptible barley cultivars grown under field conditions. Euphytica 106 149–157. 10.1023/A:1003564503628 DOI

Holková L., Prášil I. T., Bradáčová M., Vitámvás P., Chloupek O. (2009). Screening for frost tolerance in wheat using the expression of dehydrine genes Wcs120 and Wdhn13 at 17°C. Plant Breed. 128 420–422. 10.1111/j.1439-0523.2008.01606.x DOI

Houde M., Danyluk J., Laliberte J. F., Rassart E., Dhindsa R. S., Sarhan F. (1992a). Cloning, characterization, and expression of a cDNA encoding a 50-kilodalton protein specifically induced by cold acclimation in wheat. Plant Physiol. 99 1381–1387. 10.1104/pp.99.4.1381 PubMed DOI PMC

Houde M., Dhindsa R. S., Sarhan F. (1992b). A molecular marker to select for freezing tolerance in Gramineae. Mol. Gen. Genet. 234 43–48. PubMed

Janáček J., Prášil I. T. (1991). Quantification of plant frost injury by nonlinear fitting of an S-shaped function. Cryo-Lett. 12 47–52.

Kobayashi F., Takumi S., Kume S., Ishibashi M., Ohno R., Murai K., et al. (2005). Regulation by Vrn-1/Fr-1 chromosomal intervals of CBF-mediated Cor/Lea gene expression and freezing tolerance in common wheat. J. Exp. Bot. 56 887–895. 10.1093/jxb/eri081 PubMed DOI

Kosová K., Holková L., Prášil I. T., Prášilová P., Bradáčová M., Vitámvás P., et al. (2008). Expression of dehydrin 5 during the development of frost tolerance in barley (Hordeum vulgare). J. Plant. Physiol. 165 1142–1151. 10.1016/j.jplph.2007.10.009 PubMed DOI

Kosová K., Prášil I. T., Prášilová P., Vítámvás P., Chrpová J. (2010). The development of frost tolerance and DHN5 protein accumulation in barley (Hordeum vulgare) doubled haploid lines derived from Atlas 68 x Igri cross during cold acclimation. J. Plant. Physiol. 167 343–350. 10.1016/j.jplph.2009.09.020 PubMed DOI

Kosová K., Vitámvás P., Prášil I. T. (2007). The role of dehydrins in plant response to cold. Biol. Plant. 51 601–617. 10.1007/s10535-007-0133-6 DOI

Kosová K., Vitámvás P., Prášilová P., Prášil I. T. (2013). Accumulation of WCS120 and DHN5 proteins in differently frost-tolerant wheat and barley cultivars grown under a broad temperature scale. Biol. Plant. 57 105–112. 10.1007/s10535-012-0237-5 DOI

Laemmli U. K. (1970). Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature 227 680–685. 10.1038/227680a0 PubMed DOI

Nátrová Z., Jokeš M. (1993). A proposal for a decimal scale of the inflorescence development of wheat. Rost. Výroba 39 315–328.

Pfaffl M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45 10.1093/nar/29.9.e45 PubMed DOI PMC

Pomortsev A. V., Dorofeev N. V., Katysheva N. B., Peshkova A. A. (2017). Changes in dehydrin composition in winter cereal crowns during winter survival. Biol. Plant. 61 394–398. 10.1007/s10535-016-0673-8 DOI

Prášil I. T., Palovský R., Rogalewicz V., Zámečník J. (1989). Classification of wheat cultivars for winterhardiness from multi-year trials. Sci. Agric. Bohemoslov. 21 85–90.

Prášil I. T., Prášilová P., Mařík P. (2007). Comparative study of direct and indirect evaluations of frost tolerance in barley. Field Crop. Res. 102 1–8. 10.1016/j.fcr.2006.12.012 DOI

Prášil I. T., Prášilová P., Pánková K. (2004). Relationships among vernalization, shoot apex development and frost tolerance in wheat. Ann. Bot. 94 413–418. 10.1093/aob/mch158 PubMed DOI PMC

Prášil I. T., Rogalewicz V. (1989). Accuracy of wheat winterhardines evaluation by a provocation method in natural conditions. Genet. Šlechtìní 25 223–230.

Rizza F., Pagani D., Gut M., Prášil I. T., Lago C., Tondelli A., et al. (2011). Diversity in the response to low temperature in representative barley genotypes cultivated in Europe. Crop Sci. 51 2759–2779. 10.2135/cropsci2011.01.0005 DOI

Ruelland E., Vaultier M. N., Zachowski A., Hurry V. (2009). Cold signalling and cold acclimation in plants. Adv. Bot. Res. 49 35–150. 10.1016/S0065-2296(08)00602-2 DOI

Sarhan F., Ouellet F., Vazqueztello A. (1997). The wheat wcs120 gene family. A useful model to understand the molecular genetics of freezing tolerance in cereals. Physiol. Plant. 101 439–445. 10.1034/j.1399-3054.1997.1010226.x DOI

Solařová E., Holková L., Bradáčová M., Smutná P. (2016). Osmotic adjustment and activity of stress-related genes in wheats of different origin exposed to water stress. Russ. J. Plant Physiol. 63 532–541. 10.1134/S1021443716030146 DOI

Sung S. B., Amasino R. M. (2004). Vernalization and epigenetics: how plants remember winter. Curr. Opin. Plant Biol. 7 4–10. 10.1016/j.pbi.2003.11.010 PubMed DOI

Thomashow M. F. (1999). Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50 571–599. 10.1146/annurev.arplant.50.1.571 PubMed DOI

Tommasini L., Svensson J. T., Rodriguez E. M., Wahid A., Malatrasi M., Kato K., et al. (2008). Dehydrin gene expression provides an indicator of low temperature and drought stress: transcriptome-based analysis of barley (Hordeum vulgare L.). Funct. Integr. Genomics 8 387–405. 10.1007/s10142-008-0081-z PubMed DOI

Vágújfalvi A., Crosatti C., Galiba G., Dubcovsky J., Cattivelli L. (2000). Two loci on wheat chromosome 5A regulate the differential cold-dependent expression of the cor14b gene in frost-tolerant and frost-sensitive genotypes. Mol. Gen. Genet. 263 194–200. 10.1007/s004380051160 PubMed DOI

Vágújfalvi A., Galiba G., Cattivelli L., Dubcovsky J. (2003). The cold-regulated transcriptional activator Cbf3 is linked to the frost-tolerance locus Fr-A2 on wheat chromosome 5A. Mol. Genet. Genomics 269 60–67. 10.1007/s00438-003-0806-6 PubMed DOI PMC

Vítámvás P., Kosová K., Prášilová P., Prášil I. T. (2010). Accumulation of WCS120 protein in wheat cultivars grown at 9°C or 17°C in relation to their winter survival. Plant Breed. 129 611–616. 10.1111/j.1439-0523.2010.01783.x DOI

Vitámvás P., Prášil I. T. (2008). WCS120 protein family and frost tolerance during cold acclimation, deacclimation and reacclimation of winter wheat. Plant Physiol. Biochem. 46 970–976. 10.1016/j.plaphy.2008.06.006 PubMed DOI

Vítámvás P., Saalbach G., Prášil I. T., Čapková V., Opatrná J., Ahmed J. (2007). WCS120 protein family and proteins soluble upon boiling in cold-acclimated winter wheat. J. Plant Physiol. 164 1197–1207. 10.1016/j.jplph.2006.06.011 PubMed DOI

Yan L., Fu D., Li C., Blechl A., Tranquilli G., Bonafede M., et al. (2006). The wheat and barley vernalization gene VRN3 is an orthologue of FT. Prot. Natl. Acad. Sci. U.S.A. 103 19581–19586. 10.1073/pnas.0607142103 PubMed DOI PMC

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