Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Dehydrin, alcohol dehydrogenase, and central metabolite levels are associated with cold tolerance in diploid strawberry (Fragaria spp.)

Abstract

The use of artificial freezing tests, identification of biomarkers linked to or directly involved in the low-temperature tolerance processes, could prove useful in applied strawberry breeding. This study was conducted to identify genotypes of diploid strawberry that differ in their tolerance to low-temperature stress and to investigate whether a set of candidate proteins and metabolites correlate with the level of tolerance. 17 Fragaria vesca, 2 F. nilgerrensis, 2 F. nubicola, and 1 F. pentaphylla genotypes were evaluated for low-temperature tolerance. Estimates of temperatures where 50 % of the plants survived (LT50) ranged from −4.7 to −12.0 °C between the genotypes. Among the F. vesca genotypes, the LT50 varied from −7.7 °C to −12.0 °C. Among the most tolerant were three F. vesca ssp. bracteata genotypes (FDP821, NCGR424, and NCGR502), while a F. vesca ssp. californica genotype (FDP817) was the least tolerant (LT50 −7.7 °C). Alcohol dehydrogenase (ADH), total dehydrin expression, and content of central metabolism constituents were assayed in select plants acclimated at 2 °C. The LT50 estimates and the expression of ADH and total dehydrins were highly correlated (r adh = −0.87, r dehyd = −0.82). Compounds related to the citric acid cycle were quantified in the leaves during acclimation. While several sugars and acids were significantly correlated to the LT50 estimates early in the acclimation period, only galactinol proved to be a good LT50 predictor after 28 days of acclimation (r galact = 0.79). It is concluded that ADH, dehydrins, and galactinol show great potential to serve as biomarkers for cold tolerance in diploid strawberry.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Abbreviations

ABA:

Abscisic acid

ADH:

Alcohol dehydrogenase

CBF:

C-repeat/dehydration responsive element binding factor

FDP:

Fragaria diploid project

GC–MS:

Gas chromatography and mass spectrometry

LT50 :

Temperature where 50 % of the plants are killed

NCGR:

National Clonal Germplasm Repository

PCA:

Principal component analyses

PPFD:

Photosynthetic photon flux density

References

  1. Artlip TS, Callahan AM, Bassett CL, Wisniewski ME (1997) Seasonal expression of a dehydrin gene in sibling deciduous and evergreen genotypes of peach (Prunus persica [L.] Batsch). Plant Mol Biol 33:61–70

  2. Bassett CL, Wisniewski ME, Artlip TS, Richart G, Norelli JL, Farrell RE (2009) Comparative expression and transcript initiation of three peach dehydrin genes. Planta 230:107–118

  3. Campbell SA, Close TJ (1997) Dehydrins: genes, proteins, and associations with phenotypic traits. New Phytol 137:61–74

  4. Christie PJ, Hahn M, Walbot V (1991) Low-temperature accumulation of alcohol dehydrogenase-1 mRNA and protein activity in maize and rice seedlings. Plant Physiol 95:699–706

  5. Close TJ (1996) Dehydrins: emergence of a biochemical role of a family of dehydration proteins. Physiol Plant 97:795–803

  6. Close TJ (1997) Dehydrins: a commonality in the response of plants to dehydration and low temperature. Physiol Plant 100:291–296

  7. Coles S (2001) An introduction to statistical modeling of extreme values. Springer, Berlin

  8. Cook D, Fowler S, Fiehn O, Thomashow MF (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc Natl Acad Sci USA 101:15243–15248

  9. 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. Davik J, Daugaard H, Svensson B (2000) Strawberry production in the Nordic countries. Adv Strawb Prod 19:13–18

  11. Davis TM, Yu H (1997) A linkage map of the diploid strawberry, Fragaria vesca. J Hered 88:215–221

  12. de Bruxelles GL, Peacock WJ, Dennis ES, Dolferus R (1996) Abscisic acid induces the alcohol dehydrogenase gene in Arabidopsis. Plant Physiol 111:381–391

  13. Diab AA, Kantety RV, Ozturk NZ, Benscher D, Nachit MM, Sorrells ME (2008) Drought-inducible genes and differentially expressed sequence tags associated with components of drought tolerance in durum wheat. Sci Res Essays 3:9–26

  14. Dolferus R, Jacobs M, Peacock WJ, Dennis ES (1994) Differential interactions of promoter elements in stress responses of the Arabidopsis Adh gene. Plant Physiol 105:1075–1087

  15. Drew MC (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annu Rev Plant Physiol Plant Mol Biol 48:223–250

  16. Folta KM, Davis TM (2006) Strawberry genes and genomics. Crit Rev Plant Sci 25:399–415

  17. Garcia-Bañuelos ML, Gardea AA, Winzerling JJ, Vazquez-Moreno L (2009) Characterization of a midwinter-expressed dehydrin (DHN) gene from apple trees (Malus domestica). Plant Mol Biol Rep 27:476–487

  18. Gusta LV, OConnor BJ, MacHutcheon MG (1997) The selection of superior winter-hardy genotypes using a prolonged freeze test. Can J Plant Sci 77:15–21

  19. Guy C, Kaplan F, Kopka J, Selbig J, Hincha DK (2008) Metabolomics of temperature stress. Physiol Plant 132:220–235

  20. Hannah MA, Wiese D, Freund S, Fiehn O, Heyer AG, Hincha DK (2006) Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiol 142:98–112

  21. Heide OM, Sønsteby A (2007) Interactions of temperature and photoperiod in the control of flowering of latitudinal and altitudinal populations of wild strawberry (Fragaria vesca). Physiol Plant 130:280–289

  22. Houde M, Dallaire S, N’Dong D, Sarhan F (2004) Overexpression of the acidic dehydrin WCOR410 improves freezing tolerance in transgenic strawberry leaves. Plant Biotechnol J 2:381–387

  23. Hummel J, Strehmel N, Selbig J, Walther D, Kopka J (2010) Decision tree supported substructure prediction of metabolites from GC–MS profiles. Metabolomics 6:322–333

  24. Jarillo JA, Leyva A, Salinas J, Martinez-Zapater JM (1993) Low temperature induces the accumulation of alcohol dehydrogenase mRNA in Arabidopsis thaliana, a chilling-tolerant plant. Plant Physiol 101:833–837

  25. Kaplan RS, Pedersen PL (1985) Determination of microgram quantities of protein in the presence of milligram levels of lipid with amido black B-10. Anal Biochem 150:97–104

  26. Kaplan F, Kopka J, Sung DY, Zhao W, Popp M, Porat R, Guy CL (2007) Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J 50:967–981

  27. Koehler G, Wilson RC, Goodpaster JV et al (2012) Proteomic study of low temperature responses in strawberry cultivars (Fragaria × ananassa Duschesne) that differ in cold tolerance. Plant Physiol 159:1787–1805

  28. Korn M, Gärtner T, Erban A, Kopka J, Selbig J, Hincha DK (2010) Predicting Arabidopsis freezing tolerance and heterosis in freezing tolerance from metabolite composition. Mol Plant 3:224–235

  29. Kurz M (2008) Compatible solute influence on nucleic acids: many questions but few answers. Saline Syst 4:6

  30. Lim CC, Krebs SL, Arora R (1999) A 25-kDa dehydrin associated with genotype- and age-dependent leaf freezing-tolerance in Rhododendron: a genetic marker for cold hardiness? Theor Appl Genet 99:912–920

  31. Lindlöf A, Bräutigam M, Chawade A, Olsson B, Olsson O (2007) Identification of cold-induced genes in cereal crops and Arabidopsis through comparative analysis of multiple EST sets. In: Hochreiter S, Wagner R (eds) Bioinformatics research and development—first international conference BIRD ‘07, LNBI, vol 4414. Springer, Berlin, pp 48–65

  32. Marini RP, Boyce BR (1977) Susceptibility of crown tissues of ‘Catskill’ strawberry plants to low-temperature injury. J Am Soc Hortic Sci 102:515–516

  33. Marini RP, Boyce BR (1979) Influence of low temperatures during dormancy on growth and development of ‘Catskill’ strawberry plants. J Am Soc Hortic Sci 104:159–162

  34. Nestby R, Bjørgum R (1999) Freeze injury to strawberry plants as evaluated by crown tissue browning, regrowth and yield parameters. Sci Hortic 81:321–329

  35. Nestby R, Bjørgum R, Nes A, Wikdahl T, Hageberg B (2000) Winter cover affecting freezing injury in strawberries in a coastal and continental climate. J Hortic Sci Biotech 75:119–125

  36. Oosumi T, Gruszewski HA, Blischak LA, Baxter AJ, Wadl PA, Shuman JL, Veilleux RE, Shulev V (2006) High-efficiency transformation of the diploid strawberry (Fragaria vesca) for functional genomics. Planta 223:1219–1230

  37. Potter D, Luby JJ, Harrison RE (2000) Phylogenetic relationships among species of Fragaria (Rosaceae) inferred from non-coding nuclear and chloroplast DNA sequences. Syst Bot 25:337–348

  38. Roessner U, Luedemann A, Brust D, Fiehn O, Linke T, Willmitzer L, Fernie AR (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13:11–29

  39. Rohloff J, Kopka J, Erban A et al (2009) Metabolic, transcriptional, and proteomic profiling of cold response in Fragaria vesca. Acta Hortic 842:785–788

  40. Rohloff J, Kopka J, Erban A, Winge P, Wilson RC, Bones AM, Davik J, Randall SK, Alsheikh MK (2012) Metabolite profiling reveals novel multi-level cold responses in the diploid model Fragaria vesca (woodland strawberry). Phytochemistry 77:99–109

  41. Rousseau-Gueutin M, Lerceteau-Köhler E, Barrot L, Sargent DJ, Monfort A, Simpson D, Arús P, Guérin G, Denoyes-Rothan B (2008) Comparative genetic mapping between octoploid and diploid Fragaria species reveals a high level of colinearity between their genomes and the essentially disomic behavior of the cultivated octoploid strawberry. Genetics 179:2045–2060

  42. Rousseau-Gueutin M, Gaston A, Aïnouche A, Ainouche ML, Olbricht K, Staudt G, Richard L, Denoyes-Rothan B (2009) Tracking the evolutionary history of polyploidy in Fragaria L. (strawberry): new insights from phylogenetic analyses of low-copy nuclear genes. Mol Phylgenet Evol 51:515–530

  43. Saito M, Yoshida M (2011) Expression analysis of the gene family associated with raffinose accumulation in rice seedlings under cold stress. J Plant Physiol 168:2268–2271

  44. Sargent DJ, Davis TM, Tobutt KR, Wilkinson MJ, Battey NH, Simpson DW (2004) A genetic linkage map of microsatellite, gene-specific and morphological markers in diploid Fragaria. Theor Appl Genet 109:1385–1391

  45. Sargent DJ, Fernandéz-Fernandéz F, Ruiz-Roja JJ, Sutherland BG, Passey A, Whitehouse AB, Simpson DW (2009) A genetic linkage map of the cultivated strawberry (Fragaria × ananassa) and its comparison to the diploid Fragaria reference map. Mol Breed 24:293–303

  46. SAS Institute Inc. (2008) SAS/STAT® 9.2 User’s guide. SAS Institute Inc., Cary

  47. Sasaki H, Ichimura K, Yamaki S (2001) Sucrose synthase and sucrose phosphate synthase, but not acid invertase, are regulated by cold acclimation and deacclimation in cabbage seedlings. J Plant Physiol 158:847–852

  48. Schulze WX, Schneider T, Starck S, Martinola E, Trentmann O (2011) Cold acclimation induces changes in Arabidopsis tonoplast protein abundance and activity and alters phosphorylation of tonoplast monosaccharide transporters. Plant J 69:529–541

  49. Shulaev V, Sargent DJ, Crowhurst RN et al (2011) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43:109–116

  50. Sønsteby A, Heide OM (2011) Environmental regulation of dormancy and frost hardiness in Norwegian populations of wood strawberry (Fragaria vesca L.). In: Nestby R (ed) Plant science and biotechnology in Norway. Eur J Plant Sci Biotech 5(special issue 1):42–48

  51. Teutonico RA, Palta JP, Osborn TC (1993) In vitro freezing tolerance in relation to winter survival of rapeseed cultivars. Crop Sci 33:103–107

  52. Zuther E, Büchel K, Hundertmark M, Stitt M, Hincha DK, Heyer AG (2004) The role of raffinose in the cold acclimation response of Arabidopsis thaliana. FEBS Lett 576:169–173

Download references

Acknowledgments

This work was supported by the Norwegian Research Council (RCN) grant No. 199554 (BiP, user-driven innovation awarded to Muath Alsheikh; Graminor Breeding Ltd.). Support from Graminor AS, Norwegian Institute for Agricultural and Environmental Research and Hedmark University College is also greatly acknowledged. Support was also provided by an International Development Fund (IDF) grant awarded by IUPUI to Stephen K. Randall. We thank the National Clonal Germplasm Repository (NCGR), USA, and East Malling Research (EMR), UK, for providing the seeds. Anne Langerud and Ragnhild Sween provided excellent technical assistance with plant maintenance and for performing the low-temperature experiments.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Correspondence to Jahn Davik.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 1231 kb)

Supplementary material 2 (XLS 47 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Davik, J., Koehler, G., From, B. et al. Dehydrin, alcohol dehydrogenase, and central metabolite levels are associated with cold tolerance in diploid strawberry (Fragaria spp.). Planta 237, 265–277 (2013). https://doi.org/10.1007/s00425-012-1771-2

Download citation

Keywords

  • Galactinol
  • Hierarchical clustering
  • Lethal temperature 50
  • Metabolite profiling
  • Raffinose pathway
  • Survival analysis