It is established that, besides the cold, incident light also has a crucial role in the cold acclimation process. To elucidate the interaction between these two external hardening factors, barley plantlets were grown under different light conditions with low, normal, and high light intensities at 5 and 15 °C. The expression of the HvCBF14 gene and two well-characterized members of the C-repeat binding factor (CBF)-regulon HvCOR14b and HvDHN5 were studied. In general, the expression level of the studied genes was several fold higher at 5 °C than that at 15 °C independently of the applied light intensity or the spectra. The complementary far-red (FR) illumination induced the expression of HvCBF14 and also its target gene HvCOR14b at both temperatures. However, this supplementation did not affect significantly the expression of HvDHN5. To test the physiological effects of these changes in environmental conditions, freezing tests were also performed. In all the cases, we found that the reduced R:FR ratio increased the frost tolerance of barley at every incident light intensity. These results show that the combined effects of cold, light intensity, and the modification of the R:FR light ratio can greatly influence the gene expression pattern of the plants, which can result in increased plant frost tolerance.

Agricultural Institute Centre for Agricultural Research 2462 Martonvásár Hungary

Department of Genetics and Plant Breeding Crop Research Institute 161 06 Prague 6 Czech Republic

Festetics Doctoral School Georgikon Faculty University of Pannonia 8360 Keszthely Hungary

Zobrazit více v PubMed

Körner C. Plant adaptation to cold climates. F1000Research. 2016;5:1–5. doi: 10.12688/f1000research.9107.1. PubMed DOI PMC

Hänninen H., Tanino K. Tree seasonality in a warming climate. Trends Plant Sci. 2011;16:412–416. doi: 10.1016/j.tplants.2011.05.001. PubMed DOI

Thomashow M.F. Plant cold acclimation: Freezing Tolerance Genes and Regulatory Mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999;50:571–599. doi: 10.1146/annurev.arplant.50.1.571. PubMed DOI

Maurya J.P., Bhalerao R.P. Photoperiod-and temperature-mediated control of growth cessation and dormancy in trees: A molecular perspective. Ann. Bot. 2017;120:351–360. doi: 10.1093/aob/mcx061. PubMed DOI PMC

Maibam P., Nawkar G.M., Park J.H., Sahi V.P., Lee S.Y., Kang C.H. The influence of light quality, circadian rhythm, and photoperiod on the CBF-mediated freezing tolerance. Int. J. Mol. Sci. 2013;14:11527–11543. doi: 10.3390/ijms140611527. PubMed DOI PMC

Stockinger E.J., Gilmour S.J., Thomaschow M.F. Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc. Natl. Acad. Sci. USA. 1997;94:1035–1040. doi: 10.1073/pnas.94.3.1035. PubMed DOI PMC

Liu Q., Kasuga M., Sakuma Y., Abe H., Miura S., Yamaguchi-Shinozaki K., Shinozaki K. Two Transcription Factors, DREB1 and DREB2, with an EREBP/AP2 DNA Binding Domain Separate Two Cellular Signal Transduction Pathways in Drought-and Low-Temperature-Responsive Gene Expression, Respectively, in Arabidopsis. Plant Cell Online. 1998;10:1391–1406. doi: 10.1105/tpc.10.8.1391. PubMed DOI PMC

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

Francia E., Rizza F., Cattivelli L., Stanca A.M., Galiba G., Tóth B., Hayes P.M., Skinner J.S., Pecchioni N. Two loci on chromosome 5H determine low-temperature tolerance in a “Nure” (winter) x Tremois’ (spring) barley map. Theor. Appl. Genet. 2004;108:670–680. doi: 10.1007/s00122-003-1468-9. PubMed DOI

Miller A.K., Galiba G., Dubcovsky J. A cluster of 11 CBF transcription factors is located at the frost tolerance locus Fr-Am2 in Triticum monococcum. Mol. Genet. Genom. 2006;275:193–203. doi: 10.1007/s00438-005-0076-6. PubMed DOI

Galiba G., Vágújfalvi A., Li C., Soltész A., Dubcovsky J. Regulatory genes involved in the determination of frost tolerance in temperate cereals. Plant Sci. 2009;176:12–19. doi: 10.1016/j.plantsci.2008.09.016. DOI

Greenup A., Peacock W.J., Dennis E.S., Trevaskis B. The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals. Ann. Bot. 2009;103:1165–1172. doi: 10.1093/aob/mcp063. PubMed DOI PMC

Tondelli A., Pagani D., Ghafoori I.N., Rahimi M., Ataei R., Rizza F., Flavell A.J., Cattivelli L. Allelic variation at Fr-H1/Vrn-H1 and Fr-H2 loci is the main determinant of frost tolerance in spring barley. Environ. Exp. Bot. 2014;106:148–155. doi: 10.1016/j.envexpbot.2014.02.014. DOI

Vágújfalvi A., Aprile A., Miller A., Dubcovsky J., Delugu G., Galiba G., Cattivelli L. The expression of several Cbf genes at the Fr-A2 locus is linked to frost resistance in wheat. Mol. Genet. Genom. 2005;274:506–514. doi: 10.1007/s00438-005-0047-y. PubMed DOI

Tondelli A., Francia E., Barabaschi D., Aprile A., Skinner J.S., Stockinger E.J., Stanca A.M., Pecchioni N. Mapping regulatory genes as candidates for cold and drought stress tolerance in barley. Theor. Appl. Genet. 2006;112:445–454. doi: 10.1007/s00122-005-0144-7. PubMed DOI

Francia E., Barabaschi D., Tondelli A., Laidò G., Rizza F., Stanca A.M., Busconi M., Fogher C., Stockinger E.J., Pecchioni N. Fine mapping of a HvCBF gene cluster at the frost resistance locus Fr-H2 in barley. Theor. Appl. Genet. 2007;115:1083–1091. doi: 10.1007/s00122-007-0634-x. PubMed DOI

Stockinger E.J., Skinner J.S., Gardner K.G., Francia E., Pecchioni N. Expression levels of barley Cbf genes at the Frost resistance-H2 locus are dependent upon alleles at Fr-H1 and Fr-H2. Plant J. 2007;51:308–321. doi: 10.1111/j.1365-313X.2007.0141.x. PubMed DOI

Wisniewski M., Norelli J., Bassett C., Artlip T., Macarisin D. Ectopic expression of a novel peach (Prunus persica) CBF transcription factor in apple (Malus × domestica) results in short-day induced dormancy and increased cold hardiness. Planta. 2011;233:971–983. doi: 10.1007/s00425-011-1358-3. PubMed DOI

Soltész A., Smedley M., Vashegyi I., Galiba G., Harwood W., Vágújfalvi A. Transgenic barley lines prove the involvement of TaCBF14 and TaCBF15 in the cold acclimation process and in frost tolerance. J. Exp. Bot. 2013;64:1849–1862. doi: 10.1093/jxb/ert050. PubMed DOI PMC

Fricano A., Rizza F., Faccioli P., Donata P., Pavan P., Stella A., Rossini L., Piffanelli P., Cattivelli L. Genetic variants of hvcbf14 are statistically associated with frost tolerance in a european germplasm collection of Hordeum vulgare. Theor. Appl. Genet. 2009;119:1335–1348. doi: 10.1007/s00122-009-1138-7. PubMed DOI PMC

Franklin K.A., Whitelam G.C. Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nat. Genet. 2007;39:1410–1413. doi: 10.1038/ng.2007.3. PubMed DOI

Lee C.M., Thomashow M.F. Photoperiodic regulation of the C-repeat binding factor (CBF) cold acclimation pathway and freezing tolerance in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA. 2012;109:15054–15059. doi: 10.1073/pnas.1211295109. PubMed DOI PMC

Novák A., Boldizsár Á., Ádám É., Kozma-Bognár L., Majláth I., Båga M., Tóth B., Chibbar R., Galiba G. Light-quality and temperature-dependent CBF14 gene expression modulates freezing tolerance in cereals. J. Exp. Bot. 2016;67:1285–1295. doi: 10.1093/jxb/erv526. PubMed DOI

Gierczik K., Novák A., Ahres M., Székely A., Soltész A., Boldizsár Á., Gulyás Z., Kalapos B., Monostori I., Kozma-Bognár L., et al. Circadian and light regulated expression of CBFs and their upstream signalling genes in barley. Int. J. Mol. Sci. 2017;18:1828. doi: 10.3390/ijms18081828. PubMed DOI PMC

Apostol S., Szalai G., Sujbert L., Popova L.P., Janda T. Non-invasive monitoring of the light-induced cyclic photosynthetic electron flow during cold hardening in wheat leaves. Z. Naturforsch. C J. Biosci. 2006;61:734–740. doi: 10.1515/znc-2006-9-1021. PubMed DOI

Gilmour S.J., Fowler S.G., Thomashow M.F. Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol. Biol. 2004;54:767–781. doi: 10.1023/B:PLAN.0000040902.06881.d4. PubMed DOI

Thomashow M.F. 30 Arabidopsis thaliana as a Model for Studying Mechanisms of Plant Cold Tolerance. Cold Spring Harb. Monogr. Arch. 1994;27:807–834.

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

Jaglo-Ottosen K.R., Gilmour S.J., Zarka D.G., Schabenberger O., Thomashow M.F. Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science. 1998;280:104–106. doi: 10.1126/science.280.5360.104. PubMed DOI

Choi D.W., Zhu B., Close T.J. The barley (Hordeum vulgare L.) dehydrin multigene family: Sequences, allele types, chromosome assignments, and expression characteristics of 11 Dhn genes of cv Dicktoo. Theor. Appl. Genet. 1999;98:1234–1247. doi: 10.1007/s001220051189. DOI

Dal Bosco C., Busconi M., Govoni C., Baldi P., Michele Stanca A., Crosatti C., Bassi R., Cattivelli L. Cor Gene Expression in Barley Mutants Affected in Chloroplast Development and Photosynthetic Electron Transport. Plant Physiol. 2003;131:793–802. doi: 10.1104/pp.014530. PubMed DOI PMC

Yamaguchi-Shinozaki K., Shinozaki K. A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell. 1994;6:251–264. PubMed PMC

Kim H.J., Kim Y.K., Park J.Y., Kim J. Light signalling mediated by phytochrome plays an important role in cold-induced gene expression through the C-repeat/dehydration responsive element (C/DRE) in Arabidopsis thaliana. Plant J. 2002;29:693–704. doi: 10.1046/j.1365-313X.2002.01249.x. PubMed DOI

Crosatti C., Marè C., Mazzucotelli E., Belloni S., Barilli S., Bassi R., Dubcovskyi J., Galiba G., Stanca A.M., Cattivelli L. 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. 2003;81:1162–1167. doi: 10.1139/b03-114. DOI

Vágújfalvi A., Galiba G., Dubcovsky J., Cattivelli L. 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. 2000;263:194–200. doi: 10.1007/s004380051160. PubMed DOI

Sarhan F., Ouellet F., Vazquez-Tello A. The wheat wcs120 gene family. A useful model to understand the molecular genetics of freezing tolerance in cereals. Physiol. Plant. 1997;101:439–445. doi: 10.1111/j.1399-3054.1997.tb01019.x. DOI

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

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

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

Fowler D.B., Breton G., Limin A.E., Mahfoozi S., Sarhan F. Photoperiod and temperature interactions regulate low-temperature-induced gene expression in barley. Plant Physiol. 2001;127:1676–1681. doi: 10.1104/pp.010483. PubMed DOI PMC

Rizza F., Karsai I., Morcia C., Badeck F.W., Terzi V., Pagani D., Kiss T., Stanca A.M. Association between the allele compositions of major plant developmental genes and frost tolerance in barley (Hordeum vulgare L.) germplasm of different origin. Mol. Breed. 2016;36:156. doi: 10.1007/s11032-016-0571-y. DOI

Liu Y., Dang P., Liu L., He C. Cold acclimation by the CBF–COR pathway in a changing climate: Lessons from Arabidopsis thaliana. Plant Cell Rep. 2019;38:511–519. doi: 10.1007/s00299-019-02376-3. PubMed DOI PMC

Sutka J. Genetic studies of frost resistance in wheat. Theor. Appl. Genet. 1981;59:145–152. doi: 10.1007/BF00264968. PubMed DOI

Galiba G., Quarrie S.A., Sutka J., Morgounov A., Snape J.W. RFLP mapping of the vernalization (Vrn1) and frost resistance (Fr1) genes on chromosome 5A of wheat. Theor. Appl. Genet. 1995;90:1174–1179. doi: 10.1007/BF00222940. PubMed DOI

Jeknić Z., Pillman K.A., Dhillon T., Skinner J.S., Veisz O., Cuesta-Marcos A., Hayes P.M., Jacobs A.K., Chen T.H.H., Stockinger E.J. Hv-CBF2A overexpression in barley accelerates COR gene transcript accumulation and acquisition of freezing tolerance during cold acclimation. Plant Mol. Biol. 2014;84:67–82. doi: 10.1007/s11103-013-0119-z. PubMed DOI

Li X., Ma D., Lu S.X., Hu X., Huang R., Liang T., Xu T., Tobin E.M., Liu H. Blue light-and low temperature-regulated COR27 and COR28 play roles in the arabidopsis circadian clock. Plant Cell. 2016;28:2755–2769. doi: 10.1105/tpc.16.00354. PubMed DOI PMC

Lindlöf A. Interplay between low-temperature pathways and light reduction. Plant Signal. Behav. 2010;5:820–825. doi: 10.4161/psb.5.7.11701. PubMed DOI PMC

Franklin K.A., Toledo-Ortiz G., Pyott D.E., Halliday K.J. Interaction of light and temperature signalling. J. Exp. Bot. 2014;65:2859–2871. doi: 10.1093/jxb/eru059. PubMed DOI

Wang F., Guo Z., Li H., Wang M., Onac E., Zhou J., Xia X., Shi K., Yu J., Zhou Y. Phytochrome a and b function antagonistically to regulate cold tolerance via abscisic acid-dependent jasmonate signaling 1. Plant Physiol. 2016;170:459–471. doi: 10.1104/pp.15.01171. PubMed DOI PMC

Kobayashi F., Takumi S., Nakata M., Ohno R., Nakamura T., Nakamura C. Comparative study of the expression profiles of the Cor/Lea gene family in two wheat cultivars with contrasting levels of freezing tolerance. Physiol. Plant. 2004;120:585–594. doi: 10.1111/j.0031-9317.2004.0293.x. PubMed DOI

Crosatti C., De Laureto P.P., Bassi R., Cattivelli L. The interaction between cold and light controls the expression of the cold-regulated barley gene cor14b and the accumulation of the corresponding protein. Plant Physiol. 1999;119:671–680. doi: 10.1104/pp.119.2.671. PubMed DOI PMC

Zolotarov Y., Strömvik M. De novo regulatory motif discovery identifies significant motifs in promoters of five classes of plant dehydrin genes. PLoS ONE. 2015;10:e0129016. doi: 10.1371/journal.pone.0129016. PubMed DOI PMC

Cellier F., Conéjéro G., Casse F. Dehydrin transcript fluctuations during a day/night cycle in drought-stressed sunflower. J. Exp. Bot. 2000;51:299–304. doi: 10.1093/jexbot/51.343.299. PubMed DOI

Welling A., Rinne P., Viherä-Aarnio A., Kontunen-Soppela S., Heino P., Palva E.T. Photoperiod and temperature differentially regulate the expression of two dehydrin genes during overwintering of birch (Betula pubescens Ehrh.) J. Exp. Bot. 2004;55:507–516. doi: 10.1093/jxb/erh045. PubMed DOI

Szalai G., Pap M., Janda T. Light-induced frost tolerance differs in winter and spring wheat plants. J. Plant Physiol. 2009;166:1826–1831. doi: 10.1016/j.jplph.2009.04.016. PubMed DOI

Gray G.R., Chauvin L.P., Sarhan F., Huner N.P.A. Cold acclimation and freezing tolerance. A complex interaction of light and temperature. Plant Physiol. 1997;114:467–474. doi: 10.1104/pp.114.2.467. PubMed DOI PMC

Wanner L.A., Junttila O. Cold-induced freezing tolerance in arabidopsis. Plant Physiol. 1999;120:391–399. doi: 10.1104/pp.120.2.391. PubMed DOI PMC

Janda T., Szalai G., Leskó K., Yordanova R., Apostol S., Popova L.P. Factors contributing to enhanced freezing tolerance in wheat during frost hardening in the light. Phytochemistry. 2007;68:1674–1682. doi: 10.1016/j.phytochem.2007.04.012. PubMed DOI

Affandi F.Y., Verdonk J.C., Ouzounis T., Ji Y., Woltering E.J., Schouten R.E. Far-red light during cultivation induces postharvest cold tolerance in tomato fruit. Postharvest Biol. Technol. 2020;159:111019. doi: 10.1016/j.postharvbio.2019.111019. DOI

Zhu H., Li X., Zhai W., Liu Y., Gao Q., Liu J., Ren L., Chen H., Zhu Y. Effects of low light on photosynthetic properties, antioxidant enzyme activity, and anthocyanin accumulation in purple pak-choi (Brassica campestris ssp. Chinensis Makino) PLoS ONE. 2017;12:e0179305. doi: 10.1371/journal.pone.0179305. PubMed DOI PMC

Szalai G., Majláth I., Pál M., Gondor O.K., Rudnóy S., Oláh C., Vanková R., Kalapos B., Janda T. Janus-faced nature of light in the cold acclimation processes of maize. Front. Plant Sci. 2018;9:850. doi: 10.3389/fpls.2018.00850. PubMed DOI PMC

Williams B.J., Pellett N.E., Klein R.M. Phytochrome Control of Growth Cessation and Initiation of Cold Acclimation in Selected Woody Plants. Plant Physiol. 1972;50:262–265. doi: 10.1104/pp.50.2.262. PubMed DOI PMC

McKenzie J.S., Weiser C.J., Burke M.J. Effects of Red and Far Red Light on the Initiation of Cold Acclimation in Cornus stolonifera Michx. Plant Physiol. 1974;53:783–789. doi: 10.1104/pp.53.6.783. PubMed DOI PMC

Wang X., Wu D., Yang Q., Zeng J., Jin G., Chen Z.H., Zhang G., Dai F. Identification of mild freezing shock response pathways in barley based on transcriptome profiling. Front. Plant Sci. 2016;7:106. doi: 10.3389/fpls.2016.00106. PubMed DOI PMC

Burton R.A., Shirley N.J., King B.J., Harvey A.J., Fincher G.B. The CesA Gene Family of Barley. Quantitative Analysis of Transcripts Reveals Two Groups of Co-Expressed Genes. Plant Physiol. 2004;134:224–236. doi: 10.1104/pp.103.032904. PubMed DOI PMC

Morran S., Eini O., Pyvovarenko T., Parent B., Singh R., Ismagul A., Eliby S., Shirley N., Langridge P., Lopato S. Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. Plant Biotechnol. J. 2011;9:230–249. doi: 10.1111/j.1467-7652.2010.00547.x. PubMed DOI

Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 2001;25:402–408. doi: 10.1006/meth.2001.1262. PubMed DOI

Webb M.S., Uemura M., Steponkus P.L. A comparison of freezing injury in oat and rye: Two cereals at the extremes of freezing tolerance. Plant Physiol. 1994;104:467–478. doi: 10.1104/pp.104.2.467. PubMed DOI PMC

The Effect of White Light Spectrum Modifications by Excess of Blue Light on the Frost Tolerance, Lipid- and Hormone Composition of Barley in the Early Pre-Hardening Phase

Light Quality Modulates Plant Cold Response and Freezing Tolerance

Crosstalk between Light- and Temperature-Mediated Processes under Cold and Heat Stress Conditions in Plants

COR/LEA Proteins as Indicators of Frost Tolerance in Triticeae: A Comparison of Controlled versus Field Conditions

The Impact of Far-Red Light Supplementation on Hormonal Responses to Cold Acclimation in Barley