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

. 2021 Apr 16 ; 10 (4) : . [epub] 20210416

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid33923804

Grantová podpora
MZe CR RO0418; QK1710302; QK1910269 Ministerstvo Zemědělství

Low temperatures in the autumn induce enhanced expression/relative accumulation of several cold-inducible transcripts/proteins with protective functions from Late-embryogenesis-abundant (LEA) superfamily including dehydrins. Several studies dealing with plants grown under controlled conditions revealed a correlation (significant quantitative relationship) between dehydrin transcript/protein relative accumulation and plant frost tolerance. However, to apply these results in breeding, field experiments are necessary. The aim of the review is to provide a summary of the studies dealing with the relationships between plant acquired frost tolerance and COR/LEA transcripts/proteins relative accumulation in cereals grown in controlled and field conditions. The impacts of cold acclimation and vernalisation processes on the ability of winter-type Triticeae to accumulate COR/LEA proteins are discussed. The factors determining dehydrin relative accumulation under controlled cold acclimation treatments versus field trials during winter seasons are discussed. In conclusion, it can be stated that dehydrins could be used as suitable indicators of winter survival in field-grown winter cereals but only in plant prior to the fulfilment of vernalisation requirement.

Zobrazit více v PubMed

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

Chouard P. Vernalization and its relations to dormancy. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1960;11:191–238. doi: 10.1146/annurev.pp.11.060160.001203. 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

Danyluk J., Kane N.A., Breton G., Limin A.E., Fowler D.B., Sarhan F. TaVRT-1, a putative transcription factor associated with vegetative to reproductive transition in cereals. Plant Physiol. 2003;132:1849–1860. doi: 10.1104/pp.103.023523. PubMed DOI PMC

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

Knox A.K., Li C.X., Vagujfalvi A., Galilba G., Stockinger E.J., Dubcovsky J. Identification of candidate CBF genes for the frost tolerance locus Fr-A(m)2 in Triticum monococcum. Plant Mol. Biol. 2008;67:257–270. doi: 10.1007/s11103-008-9316-6. PubMed DOI

Dure L., Greenway S.C., Galau G.A. Developmental biochemistry of cottonseed embryogenesis and germination: Changing messenger ribonucleic acid populations as shown by in vitro and in vivo protein synthesis. Biochemistry. 1981;20:4162–4168. doi: 10.1021/bi00517a033. PubMed DOI

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

Close T.J., Fenton R.D., Moonan F. A view of plant dehydrins using antibodies specific to the carboxy-terminal peptide. Plant Mol. Biol. 1993;23:279–286. doi: 10.1007/BF00029004. PubMed DOI

Close T.J. Dehydrins: Emergence of a biochemical role of a family of plant dehydration proteins. Physiol. Plant. 1996;97:795–803. doi: 10.1111/j.1399-3054.1996.tb00546.x. DOI

Close T.J. Dehydrins: A commonality in the response of plants to dehydration and low temperature. Physiol. Plant. 1997;100:291–296. doi: 10.1111/j.1399-3054.1997.tb04785.x. DOI

Brini F., Hanin M., Lumbreras V., Irar S., Pages M., Masmoudi K. Functional characterization of DHN-5, a dehydrin showing a differential phosphorylation pattern in two Tunisian durum wheat (Triticum durum Desf.) varieties with marked differences in salt and drought tolerance. Plant Sci. 2007;172:20–28. doi: 10.1016/j.plantsci.2006.07.011. DOI

Tompa P. Intrinsically unstructured proteins. Trends Biochem. Sci. 2002;27:527–533. doi: 10.1016/S0968-0004(02)02169-2. PubMed DOI

Hara M. The multifunctionality of dehydrins: An overview. Plant Signal. Behav. 2010;5:503–508. doi: 10.4161/psb.11085. PubMed DOI PMC

Hanin M., Brini F., Ebel C., Toda Y., Takeda S., Masmoudi K. Plant dehydrins and stress tolerance: Versatile proteins for complex mechanisms. Plant Signal. Behav. 2011;6:1503–1509. doi: 10.4161/psb.6.10.17088. PubMed DOI PMC

Graether S.P., Boddington K.F. Disorder and function: A review of the dehydrin protein family. Front. Plant Sci. 2014;5:576. doi: 10.3389/fpls.2014.00576. PubMed DOI PMC

Koag M.C., Wilkens S., Fenton R.D., Resnik J., Vo E., Close T.J. The K-Segment of maize DHN1 mediates binding to anionic phospholipid vesicles and concomitant structural changes. Plant Physiol. 2009;150:1503–1514. doi: 10.1104/pp.109.136697. PubMed DOI PMC

Houde M., Daniel C., Lachapelle M., Allard F., Laliberte S., Sarhan F. Immunolocalization of freezing-tolerance-associated proteins in the cytoplasm and nucleoplasm of wheat crown tissues. Plant J. 1995;8:583–593. doi: 10.1046/j.1365-313X.1995.8040583.x. PubMed DOI

Bravo L.A., Gallardo J., Navarrete A., Olave N., Martinez J., Alberdi M., Close T.J., Corcuera L.J. Cryoprotective activity of a cold-induced dehydrin purified from barley. Physiol. Plant. 2003;118:262–269. doi: 10.1034/j.1399-3054.2003.00060.x. DOI

Kosová K., Prášil I.T., Vitámvás P. Role of dehydrins in plant stress response. In: Pessarakli M., editor. Handbook of Plant and Crop Stress. 4th ed. CRC Press, Taylor and Francis; Boca Raton, FL, USA: 2019. pp. 239–286.

Danyluk J., Houde M., Rassart E., 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

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

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

Houde M., Dhindsa R.S., Sarhan F. A molecular marker to select for freezing tolerance in Gramineae. Mol. Gen. Genet. 1992;234:43–48. doi: 10.1007/BF00272343. 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., Holková L., Prášil I.T., Prášilová P., Bradáčová M., Vitámvás 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., Kosová K., Prášilová P., Prášil I.T. Accumulation of WCS120 protein in wheat cultivars grown at 9 °C or 17 °C in relation to their winter survival. Plant Breed. 2010;129:611–616. doi: 10.1111/j.1439-0523.2010.01783.x. DOI

Kosová K., Vitámvás 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. Cold acclimation threshold induction temperatures in cereals. Crop Sci. 2008;48:1147–1154. doi: 10.2135/cropsci2007.10.0581. DOI

Vítámvás P., Kosová K., Musilová J., Holková L., Mařík P., Smutná P., Klíma M., Prášil I.T. Relationship between dehydrin accumulation and winter survival in winter wheat and barley grown in the field. Front. Plant Sci. 2019;10:7. doi: 10.3389/fpls.2019.00007. PubMed DOI PMC

Ruelland E., Vaultier M.N., Zachowski A., Hurry V. Cold signalling and cold acclimation in plants. Adv. Bot. Res. 2009;49:35–150.

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

Prášil I., Zámečník J. The use of a conductivity measurement method for assessing freezing injury I. Influence of leakage time, segment number, size and shape in a sample on evaluation of the degree of injury. Environ. Exp. Bot. 1998;40:1–10. doi: 10.1016/S0098-8472(98)00010-0. 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

Kumar S.V., Wigge P.A. H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell. 2010;140:136–147. doi: 10.1016/j.cell.2009.11.006. PubMed DOI

Janská A., Aprile A., Zámečník J., Cattivelli L., Ovesná J. Transcriptional responses of winter barley to cold indicate nucleosome remodelling as a specific feature of crown tissues. Funct. Integr. Genom. 2011;11:307–325. doi: 10.1007/s10142-011-0213-8. PubMed DOI PMC

Tarkowski L.P., Van den Ende W. Cold tolerance triggered by soluble sugars: A multifaceted countermeasure. Front. Plant Sci. 2015;6:203. doi: 10.3389/fpls.2015.00203. PubMed DOI PMC

Bertrand A., Bipfubusa M., Claessens A., Rocher S., Castonguay Y. Effect of photoperiod prior to cold acclimation on freezing tolerance and carbohydrate metabolism in alfalfa (Medicago sativa L.) Plant Sci. 2017;264:122–128. doi: 10.1016/j.plantsci.2017.09.003. PubMed DOI

Murata N., Los D.A. Membrane fluidity and temperature perception. Plant Physiol. 1997;115:875–879. doi: 10.1104/pp.115.3.875. PubMed DOI PMC

Suzuki I., Los D.A., Kanesaki Y., Mikami K., Murata N. The pathway for perception and transduction of low-temperature signals in Synechocystis. EMBO J. 2000;19:1327–1334. doi: 10.1093/emboj/19.6.1327. PubMed DOI PMC

Ma Y., Dai X., Xu Y., Luo W., Zheng X., Zeng D., Pan Y., Lin X., Liu H., Zhang D., et al. COLD1 confers chilling tolerance in rice. Cell. 2015;160:1209–1221. doi: 10.1016/j.cell.2015.01.046. 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

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

Zarka D.G., Vogel J.T., Cook D., Thomashow M.F. Cold induction of Arabidopsis CBF genes involves multiple ICE (Inducer of CBF expression) promoter elements and a cold-regulatory circuit that is desensitized by low temperature. Plant Physiol. 2003;133:910–918. doi: 10.1104/pp.103.027169. PubMed DOI PMC

Ding Y.L., Li H., Zhang X.Y., Xie Q., Gong Z.Z., Yang S.H. OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Dev. Cell. 2015;32:278–289. doi: 10.1016/j.devcel.2014.12.023. PubMed DOI

Ohno R., Takumi S., Nakamura C. Kinetics of transcript and protein accumulation of a low-molecular-weight wheat LEA D-11 dehydrin in response to low temperature. J. Plant Physiol. 2003;160:193–200. doi: 10.1078/0176-1617-00925. PubMed DOI

Ganeshan S., Vítámvás P., Fowler D.B., Chibbar R.N. 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. 2008;59:2393–2402. doi: 10.1093/jxb/ern112. PubMed DOI PMC

Urban M.O., Klíma M., Vítámvás P., Vašek J., Hilgert-Delgado A.A., Kučera V. Significant relationships among frost tolerance and net photosynthetic rate, water use efficiency and dehydrin accumulation in cold-treated winter oilseed rapes. J. Plant Physiol. 2013;170:1600–1608. doi: 10.1016/j.jplph.2013.07.012. PubMed DOI

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

Ahres M., Gierczik K., Boldizsár A., Vítámvás P., Galiba G. Temperature and light-quality dependent regulation of freezing tolerance in barley. Plants. 2020;9:83. doi: 10.3390/plants9010083. PubMed DOI PMC

Tondelli A., Francia E., Barabaschi D., Pasquariello M., Pecchioni N. Inside the CBF locus in Poaceae. Plant Sci. 2011;180:39–45. doi: 10.1016/j.plantsci.2010.08.012. PubMed DOI

Kume S., Kobayashi F., Ishibashi M., Ohno R., Nakamura C., Takumi S. Differential and coordinated expression of Cbf and Cor/Lea genes during long-term cold acclimation in two wheat cultivars showing distinct levels of freezing tolerance. Genes Genet. Syst. 2005;80:185–197. doi: 10.1266/ggs.80.185. PubMed DOI

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

Campoli C., Matus-Cadiz M.A., Pozniak C.J., Cattivelli L., Fowler D.B. Comparative expression of Cbf genes in the Triticeae under different acclimation induction temperatures. Mol. Genet. Genom. 2009;282:141–152. doi: 10.1007/s00438-009-0451-9. PubMed DOI PMC

Badawi M., Danyluk J., Boucho B., Houde M., Sarhan F. The CBF gene family in hexaploid wheat and its relationship to the phylogenetic complexity of cereal CBFs. Mol. Genet. Genom. 2007;277:533–554. doi: 10.1007/s00438-006-0206-9. PubMed DOI PMC

Achard P., Gong F., Cheminant S., Alioua M., Hedden P., Genschik P. The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell. 2008;20:2117–2129. doi: 10.1105/tpc.108.058941. PubMed DOI PMC

Kosová K., Prášil I.T., Vítámvás P., Dobrev P., Motyka V., Floková K., Novák O., Turečková V., Rolčik J., Pešek B., et al. Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra. J. Plant Physiol. 2012;169:567–576. doi: 10.1016/j.jplph.2011.12.013. PubMed DOI

Vanková R., Kosová K., Dobrev P., Vítámvás P., Trávníčková A., Cvikrová M., Pešek B., Gaudinová A., Přerostová S., Musilová J., et al. Dynamics of cold acclimation and complex phytohormone responses in Triticum monococcum lines G3116 and DV92 differing in vernalization and frost tolerance level. Env. Exp. Bot. 2014;101:12–25. doi: 10.1016/j.envexpbot.2014.01.002. DOI

Kalapos B., Novák A., Dobrev P., Vítámvás P., Marincs F., Galiba G., Vanková R. Effect of the winter wheat Cheyenne 5A substituted chromosome on dynamics of abscisic acid and cytokinins in freezing-sensitive Chinese spring genetic background. Front. Plant Sci. 2017;8:2033. doi: 10.3389/fpls.2017.02033. PubMed DOI PMC

Sung S., Amasino R.M. Remembering winter: Toward a molecular understanding of vernalization. Annu. Rev. Plant Biol. 2005;56:491–508. doi: 10.1146/annurev.arplant.56.032604.144307. PubMed DOI

Yan L., Loukoianov A., Tranquilli G., Helguera M., Fahima T., Dubcovsky J. Positional cloning of the wheat vernalization gene VRN1. Proc. Nat. Acad. Sci. USA. 2003;100:6263–6268. doi: 10.1073/pnas.0937399100. PubMed DOI PMC

Yan L., Loukoianov A., Blechl A., Tranquilli G., Ramakrishna W., SanMiguel P., Bennetzen J.L., Echenique V., Dubcovsky J. The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science. 2004;303:1640–1644. doi: 10.1126/science.1094305. PubMed DOI PMC

Von Zitzewitz J., Szücs P., Dubcovsky J., Yan L.L., Francia E., Pecchioni N., Casas A., Chen T.H.H., Hayes P.M., Skinner J.S. Molecular and structural characterization of barley vernalization genes. Plant Mol. Biol. 2005;59:449–467. doi: 10.1007/s11103-005-0351-2. PubMed DOI

Oliver S.N., Finnegan E.J., Dennis E.S., Peacock W.J., Trevaskis B. Vernalization induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene. Proc. Natl. Acad. Sci. USA. 2009;106:8386–8391. doi: 10.1073/pnas.0903566106. PubMed DOI PMC

Kane N.A., Danyluk J., Tardif G., Ouellet F., Laliberté J.F., Limin A.E., Fowler D.B., Sarhan F. TaVRT-2, a member of the StMADS-11 clade of flowering repressors is regulated by vernalization and photoperiod in wheat. Plant Physiol. 2005;138:2354–2363. doi: 10.1104/pp.105.061762. PubMed DOI PMC

Seo E., Lee H., Jeon J., Park H., Kim J., Noh Y.S., Lee I. Crosstalk between cold response and flowering in Arabidopsis is mediated through the flowering–time gene SOC1 and its upstream negative regulator FLC. Plant Cell. 2009;21:3185–3197. doi: 10.1105/tpc.108.063883. PubMed DOI PMC

Laudencia-Chingcuanco D., Ganeshan S., You F., Fowler B., Chibbar R., Anderson O. Genome-wide gene expression analysis supports a developmental model of low temperature tolerance gene regulation in wheat (Triticum aestivum L.) BMC Genom. 2011;12:299. doi: 10.1186/1471-2164-12-299. PubMed DOI PMC

Dhillon T., Pearce S.P., Stockinger E.J., Distelfeld A., Li C., Knox A.K., Vashegyi I., Vágújfalvi A., Galiba G., Dubcovsky J. Regulation of freezing tolerance and flowering in cereals: The VRN–1 connection. Plant Physiol. 2010;153:1846–1858. doi: 10.1104/pp.110.159079. PubMed DOI PMC

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

Li Q., Byrns B., Badawi M.A., Diallo A.B., Danyluk J., Sarhan F., Laudencia-Chingcuanco D., Zou J., Fowler D.B. Transcriptomic insights into phenological development and cold tolerance of wheat grown in the field. Plant Physiol. 2018;176:2376–2394. doi: 10.1104/pp.17.01311. PubMed DOI PMC

Limin A.E., Fowler D.B. Developmental traits affecting low-temperature tolerance response in near-isogenic lines for the vernalization locus Vrn-A1 in wheat (Triticum aestivum L. em Thell) Ann. Bot. 2002;89:579–585. doi: 10.1093/aob/mcf102. PubMed DOI PMC

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

Mittler R. Abiotic stress, the field environment and stress combination. Trends Plant. Sci. 2006;11:15–19. doi: 10.1016/j.tplants.2005.11.002. PubMed DOI

Crosatti C., Pagani D., Cattivelli L., Stanca A.M., Rizza F. 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. 2008;62:93–100. doi: 10.1016/j.envexpbot.2007.07.008. DOI

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

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

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

Rizza F., Pagani D., Gut M., Prášil I.T., Lago C., Tondelli A., Orru L., Mazucotelli E., Francia E., Badeck F.W., et al. Diversity in the response to low temperature in representative barley genotypes cultivated in Europe. Crop Sci. 2011;51:2759–2779. doi: 10.2135/cropsci2011.01.0005. DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...