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Genotype-Dependent Gene Expression in Strawberry (Fragaria x ananassa) Plants Under High Temperature Stress

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Abstract

The differences in tolerance to high temperatures were investigated on the basis of gene expressions in two strawberry (Fragaria x ananassa Duch) cultivars which were previously determined as high temperature tolerant (Redlands Hope = R. Hope) and sensitive (Festival). Plants were exposed incrementally to 35, 40, 45, and finally 50 °C for 24 h. qRT-PCR analyses were carried out with 19 known sequences from the databases. Protein expression analyses were based on SDS-PAGE results, sequenced and then separated due to their isoelectric points. Expression levels were determined at 35, 40, and 45 °C. According to the results, tolerance of ‘R. Hope’ to high temperature stress can be explained with the coordination of Hsp70, Hsp90, and small heat shock proteins (sHsps) having a vital and supplementary role in stress response. Sensitive cultivar ‘Festival’ can respond to high temperatures only with the low molecular weight protein and transcripts that do not take a central role in high temperature stress response. Moreover, allergen gene expression triggered by high temperature were detected in both cultivars with different expression levels. The greater expression level in allergen genes observed in the sensitive cultivar ‘Festival’ under high temperature indicates that there is possibly a negative correlation between expression level in allergen genes and heat stress tolerance. Future studies addressing allergen gene expression under high temperature stress are required to confirm on these findings and to expand on the potential use as a molecular marker in breeding process for enhanced tolerance to high temperature.

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References

  • Arce DB, De Las RJ, Pratta GR (2020) Interactomic analysis of the sHSP family during tomato fruit ripening. Plant Gene 21:100208

    CAS  Google Scholar 

  • Arora R, Wisniewski ME, Scorza R (1992) Cold acclimation in genetically related (sibling) deciduous and evergreen peach (Prunus persica L. Batsch). I. Seasonal changes in cold hardiness and polypeptides of bark and xylem tissues. Plant Physiol 99:1562–1568

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arora R, Wisniewski ME (1994) Cold acclimation in genetically related (sibling) deciduous and evergreen peach (Prunus persica [L.] Batsch) (II. A 60-kilodalton bark protein in cold-acclimated tissues of peach is heat stable and related to the dehydrin family of proteins). Plant Physiol 105:95–101

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arora R, Pitchay DS, Bearce BC (1998) Water-stress-induced heat tolerance in geranium leaf tissues: a possible linkage through stress proteins? Physiol Plant 103:24–34

    CAS  Google Scholar 

  • Bösl B, Grimminger V, Walter S (2006) The molecular chaperone Hsp104-a molecular machine for protein disaggregation. J Struct Biol 156(1):139–148

    PubMed  Google Scholar 

  • Brown R, Wang H, Dennis M, Slovin J, Turechek WW (2016) The effects of heat treatment on the gene expression of several heat shock protein genes in two cultivars of strawberry. Int J Fruit Sci 16:239–248

    Google Scholar 

  • Bustin SA (2000) Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J Mol Endocrinol 25:169–193

    CAS  PubMed  Google Scholar 

  • Chen H, Li H, Lu X, Chen L, Liu J, Wu H (2019) Identification and expression analysis of GRAS transcription factors to elucidate candidate genes related to stolons, fruit ripening and abiotic stresses in woodland strawberry (Fragaria vesca). Int J Mol Sci 20:4593

    CAS  PubMed Central  Google Scholar 

  • Dafny-Yelin M, Guterman I, Menda N, Ovadis M, Shalit M, Pichersky E, Zamir D, Lewinsohn E, Adam Z, Weiss D, Vainstein A (2005) Flower proteome: changes in protein spectrum during the advanced stages of rose petal development. Planta 222:37–46

    CAS  PubMed  Google Scholar 

  • Di Donato M, Geisler M (2019) HSP90 and co-chaperones: a multitaskers’ view on plant hormone biology. FEBS Lett 593(13):1415–1430

    PubMed  Google Scholar 

  • Du X, Zhu X, Yang Y, Wang Y, Arens P, Liu H (2019) De novo transcriptome analysis of Viola ×wittrockiana exposed to high temperature stress. PLoS ONE 14(9):e0222344

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ergin S, Gülen H, Kesici M, Turhan E, İpek A, Köksal N (2016) Effects of high temperature stress on enzymatic and nonenzymatic antioxidants and proteins in strawberry plants. Turk J Agric For 40:908–917

    CAS  Google Scholar 

  • Ferreyra MLF, Pezza A, Biarc J, Burlingame AL, Casati P (2010) Plant L10 ribosomal proteins have different roles during development and translation under ultraviolet-b stress. Plant Physiol 153(4):1878–1894

    CAS  PubMed Central  Google Scholar 

  • Folta KM, Dhingra A (2006) Invited review: transformation of strawberry: the basis for translational genomics in Rosaceae. In Vitro Cell Dev Biol 42(6):482–490

    CAS  Google Scholar 

  • Franz-Oberdorf K, Eberlein B, Edelmann K, Bleicher P, Kurze E, Helm D, Olbricht K, Darsow U, Ring J, Schwab W (2017) White-fruited strawberry genotypes are not per so hypoallergenic. Food Res Int 100:748–756

    CAS  PubMed  Google Scholar 

  • Gulen H, Eris A (2003) Some physiological changes in strawberry (Fragaria x ananassa ‘Camarosa’) plants under heat stress. JHSB 78:894–898

    Google Scholar 

  • Gulen H, Eris A (2004) Effect of heat stress on peroxidase activity and total protein content in strawberry plants. Plant Sci 166:739–744

    CAS  Google Scholar 

  • Gulen H, Kuden A, Postman J, Arora R (2005) Total protein and SDS-PAGE in pear scions grafted on quince and pear seedling rootstocks. Turk J Agric For 29:91–96

    Google Scholar 

  • Gupta SC, Sharma A, Mishra M, Mishra RK, Chowdhuri DK (2010) Heat shock proteins in toxicology: how close and how far? Life Sci 13:377–384

    Google Scholar 

  • Hahn A, Bublak D, Schleiff E, Scharf KD (2011) Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. Plant Cell 23:741–755

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hashemi-petroudi SH, Nematzadeh G, Mohammadi S, Kuhlmann M (2019) Analysis of expression pattern of genome and analysis of Hsp90 gene family in Aeluropus littoralis under salinity stress. J Crop Breed 11(31):134–143

    Google Scholar 

  • Hjernø K, Alm R, Canback B, Matthiesen R, Trajkovski K, Björk L, Roepstorff P, Emanuelsson C (2006) Down-regulation of the strawberry Bet v 1-homologous allergen in concert with the flavonoid biosynthesis pathway in colorless strawberry mutant. Proteomics 6:1574–1587

    PubMed  Google Scholar 

  • Hoepflinger MC, Reitsamer J, Geretschlaeger AM, Mehlmer N, Tenhaken R (2013) The effect of translationally controlled tumour protein (TCTP) on programmed cell death in plants. BMC Plant Biol 13:135

    PubMed  PubMed Central  Google Scholar 

  • Hu Y, Han Y-T, Wei W, Li Y-J, Zhang K, Gao Y-R, Zhao F-L, Feng J-Y (2015) Identification, isolation, and expression analysis of heat shock transcription factors in the diploid woodland strawberry Fragaria vesca. Front Plant Sci 6:736

    PubMed  PubMed Central  Google Scholar 

  • Huber AE, Bauerle TL (2016) Long-distance plant signalling pathways in response multiple stressors: the gap in knowledge. J Exp Bot 67:2063–2079

    CAS  PubMed  Google Scholar 

  • Johnson MS, Lim FL, Finkler A, Fromm H, Slabas AR, Knight MR (2014) Transcriptomic analysis of Sorghum bicolor responding to combined heat and drought stress. BMC Genom 15:456

    Google Scholar 

  • Jelenska J, van Hal JA, Greenberg JT (2010) Pseudomonas syringae hijacks plant stress chaperone machinery for virulence. Proc Natl Acad Sci USA 107(29):13177–13182

    CAS  PubMed  Google Scholar 

  • Kesici M, Gulen H, Ergin S, Turhan E, İpek A, Köksal N (2013) Heat-stress tolerance of some strawberry (Fragaria × ananassa) cultivars. Not Bot Horti Agrobo 41(1):1–6

    Google Scholar 

  • Kim M, Jung Y, Lee K, Kim C (2000) Identification of the calcium binding sites in translationally controlled tumor protein. Arch Pharm Res 23:633–636

    CAS  PubMed  Google Scholar 

  • Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316

    CAS  PubMed  Google Scholar 

  • Langer SE, Oviedo NC, Marina M, Burgos JL, Martinez GA, Civello PM, Villarreal NM (2018) Effects of heat treatment on enzyme activity and expression of key genes controlling cell wall remodeling in strawberry fruit. Plant Physiol Biochem 130:334–344

    CAS  PubMed  Google Scholar 

  • Ledesma NA, Kawabata S, Sugiyama N (2004) Effect of high temperature on protein expression in strawberry plants. Biol Plant 48:73–79

    CAS  Google Scholar 

  • Ledesma NA, Nakata M, Sugiyama N (2008) Effect of high temperature stress on the reproductive growth of strawberry cvs. ‘Nyoho’ and ‘Toyonoka’. Sci Hortic 116:186–193

    Google Scholar 

  • Ledesma NA, Kawabata S (2016) Responses of two strawberry cultivars to severe high temperature stress at different flower development stages. Sci Hortic 211:319–327

    Google Scholar 

  • Lee JH, Schöffl F (1996) AnHsp70 antisense gene affects the expression of HSP70/HSC70, the regulation of HSF, and the acquisition of thermotolerance in transgenic Arabidopsis thaliana. Mol Gen Genet MGG 252:11–19

    CAS  PubMed  Google Scholar 

  • Li S, Liu J, Liu Z, Li X, Wu F, He Y (2014) Heat-Induced TAS1 TARGET1 mediates thermotolerance via heat stress transcription factor A1a-directed pathways in Arabidopsis. Plant Cell 26:1764–1780

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liao WY, Lin LF, Jheng JL, Wang CC, Yang JH, Chou ML (2016) Identification of heat shock transcription factor genes involved in thermotolerance of octoploid cultivated strawberry. Int J Mol Sci 17(12):2130

    PubMed Central  Google Scholar 

  • Liu H, Xie WF, Zhang L, Valpuesta V, Ye ZW, Gao QH, Duan K (2014) Auxin biosynthesis by the YUCCA6 flavin monooxygenase gene in woodland strawberry. J Integr Plant Biol 56:350–363

    CAS  PubMed  Google Scholar 

  • Lim CC, Krebs SL, Arora RA (1999) 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

    CAS  Google Scholar 

  • Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62:670–684

    CAS  PubMed  PubMed Central  Google Scholar 

  • Merret R, Carpentier MC, Favory JJ, Picart C, Decombin J, Bousquet-Antonelli C, Tiilard P, Lejay L, Deragon JM, Charng YY (2017) Heat shock protein Hsp101 affects the release of ribosomal protein mRNAs for recovery after heat shock. Plant Physiol 174:1216–1225

    CAS  PubMed  PubMed Central  Google Scholar 

  • Muneer S, Park YG, Kim S, Jeong BR (2017) Foliar or subirrigation silicon supply mitigates high temperature stress in strawberry by maintaining photosynthetic and stress-responsive proteins. J Plant Growth Regul 36:836–845

    CAS  Google Scholar 

  • Ohama N, Kusakabe K, Mizoi J, Zhao H, Kidokoro S, Koizumi S, Takahashi F, Ishida T, Yanagisawa S, Shinozaki K, Yamaguchi-Shinozaki K (2016) The transcriptional cascade in the heat stress response of Arabidopsis is strictly regulated at the level of transcription factor expression. Plant Cell 28:181–201

    CAS  PubMed  Google Scholar 

  • Ohama N, Sato H, Shinozaki K, Yamaguchi-Shinozaki K (2017) Transcriptional regulatory network of plant heat stress response. Trends Plant Sci 22:53–65

    CAS  PubMed  Google Scholar 

  • Rhoads AR, Friedberg F (1997) Sequence motifs for calmodulin recognition. FASEB J 11(5):331–340

    CAS  PubMed  Google Scholar 

  • Qu AL, Ding YF, Jiang Q, Zhu C (2013) Molecular mechanisms of the plant heat stress response. Biochem Biophys Res Commun 432:203–207

    CAS  PubMed  Google Scholar 

  • van Montfort RL, Basha E, Friedrich KL, Slingsby C, Vierling E (2001) Crystal structure and assembly of a eukaryotic small heat shock protein. Nat Struct Biol 8(12):1025–1030

    PubMed  Google Scholar 

  • Scharf KD, Nover L (1982) Heat shock induced alterations of ribosomal protein phosphorylation in plant cell cultures. Cell 30:427–437

    CAS  PubMed  Google Scholar 

  • Serçe S, Hancock JF (2005) The temperature and photoperiod regulation of flowering and runnering in the strawberries, Fragaria chiloensis, F. virginiana, and F. x ananssa. Sci Hortic 103(2):167–177

    Google Scholar 

  • Shulaev V, Korban SS, Sosinski B, Abbott AG, Aldwinckle HS, Folta KM, Iezzoni A, Main D, Arus P, Dandekar AM, Lewers K, Brown SK, Davis TM, Gardiner SE, Potter D, Veilleux RE (2008) Multiple models for Rosaceae genomics. Plant Physiol 147:985–1003

    CAS  PubMed  PubMed Central  Google Scholar 

  • Silver N, Best S, Jiang J, Thein SL (2006) Selection of housekeeping genes for gene expression studies in human reticulocytes using real-time PCR. BMC Mol Biol 7:33

    PubMed  PubMed Central  Google Scholar 

  • Skaper SD, Facci L, Milani D, Leon A, Toffano G (1990) Culture and use of primary and clonal neural cells. Cell Cult 2:17–53

    Google Scholar 

  • Song L, Jiang Y, Zhao H, Hou M (2012) Acquired thermotolerance in plants. Plant Cell Tiss Organ Cult 111:265–276

    CAS  Google Scholar 

  • Sudhamalla B, Kumar M, Kumar RS, Sashi P, Yasin AM, Ramakrishna D, Rao PN (2013) Enzyme dimension of the ribosomal protein S4 across plant and animal kingdoms. BBA Gen Subj 11:5335–5341

    Google Scholar 

  • Sung DY, Vierling E, Guy CL (2001) Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiol 126:789–800

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vicente AR, Martinez GA, Chaves AR, Civello PM (2006) Effect of heat treatment on strawberry fruit damage and oxidative metabolism during storage. Postharv Bio Tech 40(2):116–122

    CAS  Google Scholar 

  • Virdi AS, Singh S, Singh P (2015) Abiotic stress responses in plants: roles of calmodulin-regulated proteins. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00809

    Article  PubMed  PubMed Central  Google Scholar 

  • Wahid A, Close TJ (2007) Expression of dehydrins under heat stress and their relationship with water relations of sugarcane leaves. Biol Plant 51:104–109

    CAS  Google Scholar 

  • Wang Y, Lin S, Song Q, Li K, Tao H, Huang J, Chen X, Que S, He H (2014) Genome-wide identification of heat shock proteins (Hsps) and Hsp interactors in rice: Hsp70s as a case study. BMC Genom 15:344

    Google Scholar 

  • Waters ER, Aevermann BD, Sanders-Reed Z (2008) Comparative analysis of the small heat shock proteins in three angiosperm genomes identifies new subfamilies and reveals diverse evolutionary patterns. Cell Stress Chaperones 13:127–142

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wei W, Hu Y, Han YT, Zhang K, Zhao FL, Feng JY (2016) The WRKY transcription factors in the diploid woodland strawberry Fragaria vesca: identification and expression analysis under biotic and abiotic stresses. Plant Physiol Biochem 105:129–144

    CAS  PubMed  Google Scholar 

  • Zhang L, Hu W, Gao Y, Pan H, Zhang Q (2018) A cytosolic class II small heat shock protein, PfHSP17.2, confers resistance to heat, cold, and salt stresses in transgenic Arabidopsis. Genet Mol Biol 41(3):649–660

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Tian B, Fang Y, Tong T, Zheng J, Xue D (2019) Proteome analysis and phenotypic characterization of the lesion mimic mutant bspl in barley. Plant Growth Regul. https://doi.org/10.1007/s10725-018-00474-y

    Article  Google Scholar 

  • Zhao P, Wang D, Wang R, Kong N, Zhang C, Yang C, Wu W, Ma H, Chen Q (2018) Genome-wide analysis of the potato Hsp20 gene family: identification, genomic organization and expression profiles in response to heat stress. BMC Genom 19:61

    Google Scholar 

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Acknowledgement

This research supported by Bursa Uludag University Scientific Research Committee with Project Number OUAP(Z)2012/8.

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Authors and Affiliations

  1. Department of Genetics and Bioengineering, Faculty of Engineering and Natural Sciences, Istanbul Bilgi University, Istanbul, Turkey

    Müge Kesici & Hatice Gülen

  2. Horticulture Department, Faculty of Agriculture, Bursa Uludag University, Bursa, Turkey

    Müge Kesici & Ahmet Ipek

  3. Department of Molecular Biology and Genetics, Faculty of Arts and Sciences, Bursa Uludag University, Bursa, Turkey

    Figen Ersoy

  4. Department of Agricultural Biotechnology, Faculty of Agriculture, Eskisehir Osmangazi University, Eskisehir, Turkey

    Sergül Ergin

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  1. Müge Kesici
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Kesici, M., Ipek, A., Ersoy, F. et al. Genotype-Dependent Gene Expression in Strawberry (Fragaria x ananassa) Plants Under High Temperature Stress . Biochem Genet 58, 848–866 (2020). https://doi.org/10.1007/s10528-020-09978-7

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