- -

Identification of tomato accessions as source of new genes for improving heat tolerance: from controlled experiments to field

RiuNet: Repositorio Institucional de la Universidad Politécnica de Valencia

Compartir/Enviar a

Citas

Estadísticas

  • Estadisticas de Uso

Identification of tomato accessions as source of new genes for improving heat tolerance: from controlled experiments to field

Mostrar el registro sencillo del ítem

Ficheros en el ítem

dc.contributor.author Gonzalo, María José es_ES
dc.contributor.author Nájera, Inmaculada es_ES
dc.contributor.author Baixauli, Carlos es_ES
dc.contributor.author Gil, David es_ES
dc.contributor.author Montoro, Teresa es_ES
dc.contributor.author Soriano, Vicky es_ES
dc.contributor.author Olivieri, Fabrizio es_ES
dc.contributor.author Rigano, Maria Manuela es_ES
dc.contributor.author Ganeva, Daniela es_ES
dc.contributor.author Grozeva-Tileva, Stanislava es_ES
dc.contributor.author Pevicharova, Galina es_ES
dc.contributor.author Barone, Amalia es_ES
dc.contributor.author GRANELL RICHART, ANTONIO es_ES
dc.contributor.author Monforte Gilabert, Antonio José es_ES
dc.date.accessioned 2022-04-29T18:04:08Z
dc.date.available 2022-04-29T18:04:08Z
dc.date.issued 2021-07-22 es_ES
dc.identifier.issn 1471-2229 es_ES
dc.identifier.uri http://hdl.handle.net/10251/182301
dc.description.abstract [EN] Background Due to global warming, the search for new sources for heat tolerance and the identification of genes involved in this process has become an important challenge as of today. The main objective of the current research was to verify whether the heat tolerance determined in controlled greenhouse experiments could be a good predictor of the agronomic performance in field cultivation under climatic high temperature stress. Results Tomato accessions were grown in greenhouse under three temperature regimes: control (T1), moderate (T2) and extreme heat stress (T3). Reproductive traits (flower and fruit number and fruit set) were used to define heat tolerance. In a first screening, heat tolerance was evaluated in 219 tomato accessions. A total of 51 accessions were identified as being potentially heat tolerant. Among those, 28 accessions, together with 10 accessions from Italy (7) and Bulgaria (3), selected for their heat tolerance in the field in parallel experiments, were re-evaluated at three temperature treatments. Sixteen tomato accessions showed a significant heat tolerance at T3, including five wild species, two traditional cultivars and four commercial varieties, one accession from Bulgaria and four from Italy. The 15 most promising accessions for heat tolerance were assayed in field trials in Italy and Bulgaria, confirming the good performance of most of them at high temperatures. Finally, a differential gene expression analysis in pre-anthesis (ovary) and post-anthesis (developing fruit) under heat stress among pairs of contrasting genotypes (tolerant and sensitive from traditional and modern groups) showed that the major differential responses were produced in post-anthesis fruit. The response of the sensitive genotypes included the induction of HSP genes, whereas the tolerant genotype response included the induction of genes involved in the regulation of hormones or enzymes such as abscisic acid and transferases. Conclusions The high temperature tolerance of fifteen tomato accessions observed in controlled greenhouse experiments were confirmed in agronomic field experiments providing new sources of heat tolerance that could be incorporated into breeding programs. A DEG analysis showed the complex response of tomato to heat and deciphered the different mechanisms activated in sensitive and tolerant tomato accessions under heat stress. es_ES
dc.description.sponsorship This work was supported by the European Commission H2020 Research and Innovation Programme through the TomGEM project, grant agreement No. 679796, and HARNESSTOM, grant agreement No. 101000716. es_ES
dc.language Inglés es_ES
dc.publisher Springer (Biomed Central Ltd.) es_ES
dc.relation.ispartof BMC Plant Biology es_ES
dc.rights Reconocimiento (by) es_ES
dc.subject Climate change es_ES
dc.subject Germplasm es_ES
dc.subject Abiotic stress es_ES
dc.subject Fruit set es_ES
dc.title Identification of tomato accessions as source of new genes for improving heat tolerance: from controlled experiments to field es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1186/s12870-021-03104-4 es_ES
dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/101000716/EU es_ES
dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/679796/EU es_ES
dc.rights.accessRights Abierto es_ES
dc.contributor.affiliation Universitat Politècnica de València. Instituto Universitario Mixto de Biología Molecular y Celular de Plantas - Institut Universitari Mixt de Biologia Molecular i Cel·lular de Plantes es_ES
dc.description.bibliographicCitation Gonzalo, MJ.; Nájera, I.; Baixauli, C.; Gil, D.; Montoro, T.; Soriano, V.; Olivieri, F.... (2021). Identification of tomato accessions as source of new genes for improving heat tolerance: from controlled experiments to field. BMC Plant Biology. 21(1):1-28. https://doi.org/10.1186/s12870-021-03104-4 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.1186/s12870-021-03104-4 es_ES
dc.description.upvformatpinicio 1 es_ES
dc.description.upvformatpfin 28 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 21 es_ES
dc.description.issue 1 es_ES
dc.identifier.pmid 34294034 es_ES
dc.identifier.pmcid PMC8296629 es_ES
dc.relation.pasarela S\459188 es_ES
dc.contributor.funder European Commission es_ES
dc.description.references Battisti DS, Naylor RL. Historical warnings if future food insecurity with unprecedented seasonal heat. Science. 2009;323:240–4. es_ES
dc.description.references IPCC, 2014: Climate Change 2014: Mitigation of climate change. contribution of working group III to the fifth assessment report of the intergovernmental panel on climate change [Edenhofer, O., R. Pichs-Madruga, Y. Sokona, E. Farahani, S. Kadner, K. Seyboth, A. Adler, I. Baum, S. Brunner, P. Eickemeier, B. Kriemann, J. Savolainen, S. Schlömer, C. von Stechow, T. Zwickel and J.C. Minx (eds.)]. Cambridge and New York, Cambridge University Press es_ES
dc.description.references Schlenker W, Roberts MJ. Nonlinear temperature effects indicate severe damages to US crop yields under climate change. PNAS. 2009;106:15594–8. es_ES
dc.description.references Lohani N, Singh MB, Bhalla PL. High temperature susceptibility of sexual reproduction in crop plants. J Exp Bot. 2020;71:555–68. es_ES
dc.description.references Hasanuzzaman M, Nahar K, Alam M, Roychowdhury R, Fujita M. Physiological biochemical and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci. 2013;14:9643–84. es_ES
dc.description.references Challinor AJ, Watson J, Lobell DB, Howden SM, Smith DR, Chhetri N. A meta-analysis of crop yield under climate change and adaptation. Nat Clim Change. 2014;4:287. es_ES
dc.description.references Alsamir M, Ahmand N, Ariel V, Mahmood T, Trethiwan R. Phenotypic diversity and marker-trait association under heat stress in tomato (Solanum lycopersicum L.). Aust J Crop Sci. 2019;13:578–87. es_ES
dc.description.references Wahid A, Gelani S, Ashraf M, Foolad MR. Heat tolerance in plant: an overview. Environ Exp Bot. 2007;61:199–223. es_ES
dc.description.references Yeh CH, Kaplinsky NJ, Hu C, Charng YY. Some like it hot some like it warm: phenotyping to explore thermotolerance diversity. Plant Sci. 2012;195:10–23. es_ES
dc.description.references Camejo D, Rodriguez P, Morales MA, Dell’Amico JM, Torrecillas A, Alarcon JJ. High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. J Plant Physiol. 2005;162:281–9. es_ES
dc.description.references Sato S, Peet MM, Thomas JF. Physiological factors limit fruit set of tomato (Lycopersicon esculentum Mill.) under chronic mild heat stress. Plant Cell Environ. 2000;23:719–26. es_ES
dc.description.references Charles WB, Harris RE. Tomato fruit-set at high and low temperatures. Can J Plant Sci. 1972;52:497–506. es_ES
dc.description.references Lohar DP, Peat WE. Floral characteristics of heat-tolerant and heat-sensitive tomato (Lycopersicon esculentum Mill.) cultivars at high temperature. Sci Hortic. 1998;73:53–60. es_ES
dc.description.references Gonzalo MJ, Li YC, Chen K, Gil D, Montoro T, Nájera I, et al. Genetic control of reproductive traits in tomato under high temperature. Front Plant Sci. 2020;11:326. es_ES
dc.description.references Bitta CE, Gerads T. Plant tolerance to high temperatures in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci. 2013;4:273. es_ES
dc.description.references Dane F, Hunter AG, Chambliss OL. Fruit set pollen fertility and combining ability of selected tomato genotypes under high-temperature field conditions. J Amer Soc Hort Sci. 1991;116:906–10. es_ES
dc.description.references Paupière MJ, van Haperen P, Rieu I, Visser RGF, Tikunov YM, Bovy AG. Screening for pollen tolerance to high temperatures in tomato. Euphytica. 2017;213:130. es_ES
dc.description.references Driedonks N, Wolter-Arts M, Huber H, de Boer G-J, Vriezen W, Mariani C, et al. Exploring the natural variation for reproductive thermotolerance in wild tomato species. Euphytica. 2018;214:67. es_ES
dc.description.references Barnabás B, Jäger K, Fehér A. The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ. 2008;31:11–38. es_ES
dc.description.references Lang-Mladek C, Popova O, Kiok K, Berlinger M, Rakic B, Auf-satz W, et al. Transgenerational inheritance and resetting of stress-induced loss of epigenetic gene silencing in Arabidopsis. Mol Plant. 2010;3:594–602. es_ES
dc.description.references Pecinka A, Dinh HQ, Baubec T, Rosa M, Lettner N, Scheid OM. Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. Plant Cell. 2010;22:3118–29. es_ES
dc.description.references Ayenan MAT, Danquah A, Hanson P, Ampomah-Dwamena C, Sodedji FAK, Asante IK, et al. Accelerating breeding for heat tolerance in tomato (Solanum lycopersicum L.): an integrated approach. Agronomy. 2019;9:720. es_ES
dc.description.references Grandillo S, Chetelat R, Knapp S, Spooner D, Peralta I, Cammareri M, et al. Solanum sect Lycopersicon. In: Kole C editor. Wild Crop Relatives: Genomic and Breeding Resources. Berlin; Heidelberg: Springer. https://doi.org/10.1007/978-3-642-20450-0_9 es_ES
dc.description.references Alam M, Sultana N, Ahmad S, Hossain M, Islam A. Performance of heat tolerant tomato hybrid lines under hot, humid conditions. Bangladesh J Agr Res. 2010;35:367–73. es_ES
dc.description.references Golam F, Phorhan ZH, Nezhadahmani A, Rahman M. Heat tolerance in tomato. Life Sci J. 2012;9:4. es_ES
dc.description.references Nahar K, Ullah SM. Effect of water stress on moisture content distribution in soil and morphological characters of two tomato (Lycopersicon esculentum Mill.) cultivars. J Sci Res. 2011;3:677–82. es_ES
dc.description.references Nahar K, Ullah SM. Morphological and physiological characters of tomato (Lycopersicon esculentum Mill.) cultivars under water stress. Bangladesh J Agri Res. 2012;37:355–60. es_ES
dc.description.references Arena C, Conti S, Francesca S, Melchionna G, Hájek J, Barták M, et al. Eco-physiological screening of different tomato genotypes in response to high temperatures: A combined field-to-laboratory approach. Plants. 2020;9:508. es_ES
dc.description.references Poudyal D, Rosengvist E, Ottosen C-O. Phenotyping from lab to field- tomato lines screened for heat stress using Fv/Fm maintain high fruit yield during thermal stress in the field. Funct Plant Biol. 2018;46:44–55. es_ES
dc.description.references Zhou R, Wu Z, Wang X. Evaluation of temperature stress tolerance in cultivated and wild tomatoes using photosynthesis and chlorophyll fluorescence. Hortic Environ Biotechnol. 2018;59:499–509. es_ES
dc.description.references Jump AS, Peñuelas J. Running to stand still: adaptation and the response of plants to rapid climate change. Ecol Lett. 2005;8:1010–20. es_ES
dc.description.references Kusmec A, de Leon N, Schnable P-S. Harnessing phenotypic plasticity to improve maize yields. Front Plant Sci. 2018;9:1377. es_ES
dc.description.references Mangin B, Casadebaig P, Cadic E, Blanchet N, Boniface MC, Carrère S, et al. Genetic control of plasticity of oil yield for combined abiotic stresses using a joint approach of crop modelling and genome-wide association. Plant Cell Environ. 2017;40:2276–91. es_ES
dc.description.references Diouf I, Derivot L, Koussevitzky S, Carretero Y, Bitton F, Moreau L, et al. Genetic basis of phenotypic plasticity and genotype x environment interaction in multi-parental population. J Exp Bot. 2020;71:5365–76. es_ES
dc.description.references Wang HJ, Rutishauser T, Tao ZX, Zhong SY, Ge QS, Dai JH. Impacts of global warming on phenology of spring leaf unfolding remain stable in the long run. Int J Biometeorol. 2017;61:287–92. es_ES
dc.description.references Wen J, Jiang F, Weng Y. Identification of heat-tolerance QTLs and high-temperature stress-responsive genes through conventional QTL mapping QTL-seq and RNA-seq in tomato. BMC Plant Biol. 2019;19:398. es_ES
dc.description.references Feder ME, Hofmann GE. Heat-shock proteins molecular chaperones and the stress response: evolutionary and ecological physiology. Annu Rev Physiol. 1999;61:243–82. es_ES
dc.description.references Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf KD. Complexity of the heat stress response in plants. Curr Opin Plant Biol. 2007;10:310–6. es_ES
dc.description.references Krishna P. Plant responses to heat stress. In: Hirt H, Shinozaki K, editors. Plant responses to abiotic stress topics in current genetics. Berlin Heidelberg: Springer; 2003. https://doi.org/10.1007/978-3-540-39402-0_4. es_ES
dc.description.references Paupière MJ, van Heusden AW, Bovy AG. The metabolic basis of pollen thermo-tolerance: perspectives for breeding. Metabolites. 2014;4:889–920. es_ES
dc.description.references Fragkostefanakis S, Mesihovic A, Simm S, Paupière MJ, Hu Y, Paul P, et al. HsfA2 controls the activity of developmentally and stress-regulated heat stress protection mechanisms in tomato male reproductive tissues. Plant Physiol. 2016;170:2461–77. es_ES
dc.description.references Balyan S, Rao S, Jha S, Bansal C, Das JR, Mathur S. Characterization of novel regulators for heat stress tolerance in tomato from Indian sub-continent. Plant Biotechnol J. 2020;18:2118–32. es_ES
dc.description.references Giorno F, Wolters-Arts M, Grillo S, Scharf KD, Vriezen WH, Mariani C. Developmental and heat stress-regulated expression of HsfA2 and small heat shock proteins in tomato anthers. J Exp Bot. 2010;61:453–62. es_ES
dc.description.references Ruggieri V, Calafiore R, Schettini C, Rigano MM, Olivieri F, Frusciante L, et al. Exploiting genetic and genomic resources to enhance heat tolerance in tomatoes. Agronomy. 2019;9:22. es_ES
dc.description.references Scarano A, Oliveri F, Gerardi C, Liso M, Chiesa M, Chieppa M, et al. Selection of tomato landraces with high fruit yield and nutritional quality under elevated temperatures. J Sci Food Agric. 2020;100:2791–9. es_ES
dc.description.references Xu J, Wolters-Ars M, Mariani C, Huber H, Rieu I. Heat stress affects vegetative and reproductive performance and trait correlations in tomato (Solanum lycopersicum). Euphytica. 2017;213:156. es_ES
dc.description.references Sato S, Peet MM, Gardnet RG. Altered flower retention and developmental patterns in nine tomato cultivars under elevated temperatures. Sci Hortic. 2004;101:95–101. es_ES
dc.description.references Sato S, Kamiyama M, Iwata T, Makita H, Furukawa H, Ikeda H. Moderate increase of mean daily temperature adversely affects fruit set of Lycopersicon esculentum by disrupting specific physiological processes in male reproductive development. Ann Bot. 2006;97:731–8. es_ES
dc.description.references Abdul-Baki AA. Tolerance of tomato cultivars and selected germplasm to heat stress. J Amer Soc Hort Sci. 1991;116:1113–6. es_ES
dc.description.references Hazra P, Ansary SH. Genetics of heat tolerance for floral and fruit set to high temperature stress in tomato (Lycopersicon esculentum Mill.). SABRAO J Breed Genet. 2008;40:117–25. es_ES
dc.description.references Panthee DR, Kressin JP, Piotrowski A. Heritability of flower number and fruit set under heat stress in tomato. Hortscience. 2018;53:1294–9. es_ES
dc.description.references Beaman JE, White CR, Seebacher F. Evolution of plasticity: mechanistic link between development and reversible acclimation. Trends Ecol Evol. 2016;31:237–49. https://doi.org/10.1016/jtree201601004. es_ES
dc.description.references Hazra P, Ansary SH, Sikder D, Peter KV. Breeding tomato (Lycopersicon esculentum Mill) resistant to high temperature stress. Int J Plant Breed. 2007;1:31–40. es_ES
dc.description.references Villalta I, Bernet GP, Carbonell EA, Asins MJ. Comparative QTL analysis of salinity tolerance in terms of fruit yield using two Solanum populations of F7 lines. Theor Appl Genet. 2007;114:1001–17. es_ES
dc.description.references Zhou R, Yu X, Ottosen C-O, Rosenqvist E, Zhao L, Wang Y, et al. Drought stress had a predominant effect over heat stress on three tomato cultivars subjected to combined stress. BMC Plant Pathol. 2017;17:24. es_ES
dc.description.references Sharma DK, Andersen SB, Ottosen CO, Rosenqvist E. Wheat cultivars selected for high Fv/Fm under heat stress maintain high photosynthesis total chlorophyll stomatal conductance transpiration and dry matter. Plant Physiol. 2015;153:284–98. es_ES
dc.description.references Zhou R, Yu X, Kjær KH, Rosenqvist E, Ottosen CO, Wu Z. Screening and validation of tomato genotypes under heat stress using Fv/Fm to reveal the physiological mechanism of heat tolerance. Environ Exp Bot. 2015;118:1–11. es_ES
dc.description.references Firon N, Shaked R, Peet MM, Pharr DM, Zamski E, Rosenfeld K, et al. Pollen grains of heat tolerant tomato cultivars retain higher carbohydrate concentration under heat stress conditions. Sci Hortic. 2006;109:212–7. es_ES
dc.description.references Arnold PA, Krunk LEB, Nicotra AB. How to analyse plant phenotypic plasticity in response to a changing climate. New Phytol. 2019;222:1235–41. es_ES
dc.description.references Gerszberg A, Hnatuszko-Konka K. Tomato tolerance to abiotic stress: a review of most often engineered target sequences. Plant Growth Regul. 2017;83:175–98. es_ES
dc.description.references He M, He C-Q, Ding N-Z. Abiotic stresses; general defences of land plants and chances for engineering multistress tolerance. Front Plant Sci. 2018;9:1771. es_ES
dc.description.references Mae L, Lawas F, Zuther E, Krishna Jagadish SV, Hincha DK. Molecular mechanisms of combined heat and drought stress resilence in cereals. Curr Opin Plant Biol. 2017;45:212–7. es_ES
dc.description.references Tricker PJ, ElHabti A, Schmidt J, Fleury D. The physiological and genetic basis of combined drought and heat tolerance in wheat. J Exp Bot. 2018;69:3195–210. es_ES
dc.description.references Abdul-Baki AA, Stommel JR. Pollen viability and fruit set of tomato genotypes under optimum-and high temperature regimens. HortSci. 1995;30:115–7. es_ES
dc.description.references Kugblenu YO, Oppong DE, Ofori K, Andersen M, Abenney-Mickson S, Sabi E, et al. Screening tomato genotypes for adaptation to high temperature in West Africa. Acta Agric Scand B Plant Soil Sci. 2013;63:516–22. es_ES
dc.description.references Opeña RT, Chen JT, Kuo CG, Chen HM. Genetic and physiological aspects of tropical adaptation in tomato. In: Adaptation of food crops to temperature and water stress. Taiwan: AVRDC; 1992. p. 257–70. es_ES
dc.description.references Rohrmann J, McQuinn R, Giovannoni JJ, Fernie AR, Tohge T. Tissue specificity and differential expression of transcription factors in tomato provide hints of unique regulatory networks during fruit ripening. Plant Signal Behav. 2012;7:1639–47. es_ES
dc.description.references Zhang SS, Yang H, Ding L, Song ZT, Ma H, Chang F, et al. Tissue-specific transcriptomics reveals an important role of the unfolded protein response in maintain in fertility upon heat stress in Arabidopsis. Plant Cell. 2017;29:1007–23. es_ES
dc.description.references Sherzod R, Yang E, Cho M, Chae S, Chae W. Physiological traits associated with high temperature tolerance differ by fruit types and sizes in tomato (Solanum lycopersicum L.). Hortic Environ Biotechnol. 2020; https://doi.org/10.1007/s13580-020-00280-4 es_ES
dc.description.references Foodlad MR. Breeding for abiotic stress tolerances in tomato. In: Ashraf M, Harris PJC, editors. Abiotic Stresses: Plant Resistance Through Breeding and Molecular Approaches. New York: The Haworth Press Inc; 2005. p. 613–84. es_ES
dc.description.references Peet MM, Willits DH. The effect of night temperature on greenhouse grown tomato yields in warm climate. Agric Forest Meteorol. 1998;92:191–202. es_ES
dc.description.references Su PH, Li HM. Arabidopsis stromal 70-kD heat shock proteins are essential for plant dev elopment and important for thermotolerance of germinating seeds. Plant Physiol. 2008;146:1231–41. es_ES
dc.description.references Jacob P, Hirt H, Bendahmane A. The heat-shock protein/chaperone network and multiple stress resistance. Plant Biotechnol J. 2017;15:405–14. es_ES
dc.description.references Wang L, Ma K-B, Lu Z-G, Ren S-X, Jiang H-R, Cui J-W, et al. Differential physiological transcriptomic and metabolomic responses of Arabidopsis leaves under prolonged warming and heat shock. BMC Plant Biol. 2020;20:86. es_ES
dc.description.references Wang Y, Lin S, Song Q, Li K, Tao H, Huang J, et al. Genome-wide identification of heat shock proteins (Hsps) and Hsp interactors in rice: Hsp70s as a case study. BMC Genomics. 2014;15:344. es_ES
dc.description.references Kumar A, Sharma S, Chunduri V, Kaur A, Malhotra N, et al. Genome-wide identification and characterization of heat shock protein family reveals role in development and stress conditions in Triticum aestivum L. Sci Rep. 2020;10:7858. es_ES
dc.description.references Marko D, El-Shershaby A, Carriero F, Summerer S, Petrozza A, Iannacone R, et al. Identification and characterization of a thermotolerant TILLING allele of heat shock binding protein 1 in tomato. Genes. 2019;10:516. es_ES
dc.description.references Frank G, Pressman E, Ophir R, Althan L, Shaked R, Freedman M, et al. Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins ROS scavengers hormones and sugars in the heat stress response. J Exp Bot. 2009;60:3891–908. es_ES
dc.description.references Yoon Y, Seo DH, Shin H, Kim HJ, Kim CM, Jang G. The role of stress-responsive transcription factors in modulating abiotic stress tolerance in plants. Agronomy. 2020;10:788. es_ES
dc.description.references Baron KN, Schroeder DF, Stasolla C. Transcriptional response of abscisic acid (ABA) metabolism and transport to cold and heat stress applied at the reproductive stage of development in Arabidopsis thaliana. Plant Sci. 2012;188–189:48–50. es_ES
dc.description.references Yu W, Wang L, Zhao R, Sheng J, Zhang S, Li R, et al. Knockout of SlMAPK3 enhances tolerance to heat stress involving ROS homeostasis in tomato plants. BMC Plant Biol. 2019;19:354. es_ES
dc.description.references Gao H, Brandizzi F, Benning C, Larkin RM. A membrane-tethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana. Proc Natl Acad Sci USA. 2008;105:16398–403. es_ES
dc.description.references Hsieh TH, Li CW, Su RC, Cheng CP, Sanjaya Tsai YC, et al. A tomato bZIP transcription factor SlAREB is involved in water deficit and salt stress response. Planta. 2010;231:1459–73. es_ES
dc.description.references Rivero RM, Ruiz JM, Garcia PC, Lopez-Lefebre LR, Sanchez E, Romero L. Resistance to cold and heat stress: accumulation of phenolic compounds in tomato and watermelon plants. Plant Sci. 2001;160:315–21. es_ES
dc.description.references JMP® 12 JSL Syntax Reference. Cary: SAS Institute Inc. NC, 1989–2019. es_ES


Este ítem aparece en la(s) siguiente(s) colección(ones)

Mostrar el registro sencillo del ítem