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Transgenic tomatoes for abiotic stress tolerance: status and way ahead

Abstract

Tomato (Solanum lycopersicum) is one of the most important vegetable crops; its production, productivity and quality are adversely affected by abiotic stresses. Abiotic stresses such as drought, extreme temperature and high salinity affect almost every stage of tomato life cycle. Depending upon the plant stage and duration of the stress, abiotic stress causes about 70% yield loss. Several wild tomato species have the stress tolerance genes; however, it is very difficult to transfer them into cultivars due to high genetic distance and crossing barriers. Transgenic technology is an alternative potential tool for the improvement of tomato crop to cope with abiotic stress, as it allows gene transfer across species. In recent decades, many transgenic tomatoes have been developed, and many more are under progress against abiotic stress using transgenes such as DREBs, Osmotin, ZAT12 and BADH2. The altered expression of these transgenes under abiotic stresses are involved in every step of stress responses, such as signaling, control of transcription, proteins and membrane protection, compatible solute (betaines, sugars, polyols, and amino acids) synthesis, and free-radical and toxic-compound scavenging. The stress-tolerant transgenic tomato development is based on introgression of a gene with known function in stress response and putative tolerance. Transgenic tomato plants have been developed against drought, heat and salt stress with the help of various transgenes, expression of which manages the stress at the cellular level by modulating the expression of downstream genes to ultimately improve growth and yield of tomato plants and help in sustainable agricultural production. The transgenic technology could be a faster way towards tomato improvement against abiotic stress. This review provides comprehensive information about transgenic tomato development against abiotic stress such as drought, heat and salinity for researcher attention and a better understanding of transgenic technology used in tomato improvement and sustainable agricultural production.

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References

  1. Abdelmageed AHA, Gruda N (2009) Influence of high temperatures on gas exchange rate and growth of eight tomato cultivars under controlled heat stress conditions. Eur J Hortic Sci 74:152–159

    CAS  Google Scholar 

  2. Acquaah G (2009) Principles of plant genetics and breeding. Wiley, New York

    Google Scholar 

  3. Amooaghaie R, Nikzad K (2013) The role of nitric oxide in priming-induced low-temperature tolerance in two genotypes of tomato. Seed Sci Res 23:123–131. https://doi.org/10.1017/S0960258513000068

    CAS  Article  Google Scholar 

  4. Amudha J, Balasubramani G (2011) Recent molecular advances to combat abiotic stress tolerance in crop plants. Biotechnol Mol Biol Rev 6:31–58

    CAS  Google Scholar 

  5. Anderson EN (2005) Everyone eats: understanding food and culture. New York University Press, New York

    Google Scholar 

  6. Battilani A, Prieto MH, Argerich C et al (2012) Tomato. In: Steduto P, Hsiao TC, Fereres E, Raes D (eds) Crop yield response to water, irrigation and drainage Paper 66. pp 174–180

  7. Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273. https://doi.org/10.3389/fpls.2013.00273

    Article  PubMed  PubMed Central  Google Scholar 

  8. Bommarco R, Kleijn D, Potts SG (2013) Ecological intensification: Harnessing ecosystem services for food security. Trends Ecol Evol 28:230–238. https://doi.org/10.1016/j.tree.2012.10.012

    Article  PubMed  Google Scholar 

  9. Böndel KB, Nosenko T, Stephan W (2018) Signatures of natural selection in abiotic stress-responsive genes of Solanum chilense. R Soc Open Sci 5:171198. https://doi.org/10.1098/rsos.171198

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Boyer JS, Byrne P, Cassman KG et al (2013) The US drought of 2012 in perspective: a call to action. Glob Food Sec 2:139–143. https://doi.org/10.1016/j.gfs.2013.08.002

    Article  Google Scholar 

  11. Brown L (2012) World on the edge: how to prevent environmental and economic collapse. Routledge, New York

    Book  Google Scholar 

  12. Chai Q, Gan Y, Turner NC et al (2014) Water-saving innovations in Chinese agriculture. Adv Agron 126:149–201. https://doi.org/10.1016/B978-0-12-800132-5.00002-X

    Article  Google Scholar 

  13. Chai Q, Gan Y, Zhao C et al (2016) Regulated deficit irrigation for crop production under drought stress. A review. Agron Sustain Dev 36:1–21. https://doi.org/10.1007/s13593-015-0338-6

    Article  Google Scholar 

  14. Chen S, Liu A, Zhang S et al (2013) Overexpression of mitochondrial uncoupling protein conferred resistance to heat stress and Botrytis cinerea infection in tomato. Plant Physiol Biochem 73:245–253. https://doi.org/10.1016/j.plaphy.2013.10.002

    CAS  Article  PubMed  Google Scholar 

  15. Cheng L, Zou Y, Ding S et al (2009) Polyamine accumulation in transgenic tomato enhances the tolerance to high temperature stress. J Integr Plant Biol 51:489–499. https://doi.org/10.1111/j.1744-7909.2009.00816.x

    CAS  Article  PubMed  Google Scholar 

  16. Deinlein U, Stephan AB, Horie T et al (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379. https://doi.org/10.1016/j.tplants.2014.02.001

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environ Exp Bot 109:212–228. https://doi.org/10.1016/j.envexpbot.2014.06.021

    CAS  Article  Google Scholar 

  18. Dixit S (2008) Identification of plant genes for abiotic stress resistance. Doctoral thesis, Wageningen University

  19. Dixon GR, Aldous DE (2014) Horticulture: plants for people and places. Environ Hortic 2:1–949. https://doi.org/10.1007/978-94-017-8581-5

    Article  Google Scholar 

  20. FAO (2011) http://faostat.fao.org. Accessed 11 Feb 2018

  21. Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319. https://doi.org/10.1093/jxb/erh003

    CAS  Article  Google Scholar 

  22. Fragkostefanakis S, Simm S, Paul P et al (2015) Chaperone network composition in Solanum lycopersicum explored by transcriptome profiling and microarray meta-analysis. Plant Cell Environ 38:693–709. https://doi.org/10.1111/pce.12426

    CAS  Article  PubMed  Google Scholar 

  23. Frank G, Pressman E, Ophir R et al (2009) 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 60:3891–3908. https://doi.org/10.1093/jxb/erp234

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Gan Y, Siddique KHM, Turner NC et al (2013) Ridge-furrow mulching systems-an innovative technique for boosting crop productivity in semiarid rain-fed environments. Adv Agron 118:429–476. https://doi.org/10.1016/B978-0-12-405942-9.00007-4

    Article  Google Scholar 

  25. García-Abellan JO, Egea I, Pineda B et al (2014) Heterologous expression of the yeast HAL5 gene in tomato enhances salt tolerance by reducing shoot Na+ accumulation in the long term. Physiol Plant 152:700–713. https://doi.org/10.1111/ppl.12217

    CAS  Article  PubMed  Google Scholar 

  26. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. https://doi.org/10.1016/j.plaphy.2010.08.016

    CAS  Article  Google Scholar 

  27. Goel D, Singh AK, Yadav V et al (2010) Overexpression of osmotin gene confers tolerance to salt and drought stresses in transgenic tomato (Solanum lycopersicum L.). Protoplasma 245:133–141. https://doi.org/10.1007/s00709-010-0158-0

    CAS  Article  PubMed  Google Scholar 

  28. Gould WA (1992) Tomato production, processing, and technology. Elsevier, New York

    Book  Google Scholar 

  29. Gourdji SM, Sibley AM, Lobell DB (2013) Global crop exposure to critical high temperatures in the reproductive period: historical trends and future projections. Environ Res Lett 8:24041. https://doi.org/10.1088/1748-9326/8/2/024041

    Article  Google Scholar 

  30. Greco M, Chiappetta A, Bruno L, Bitonti MB (2012) In Posidonia oceanica cadmium induces changes in DNA methylation and chromatin patterning. J Exp Bot 63:695–709. https://doi.org/10.1093/jxb/err313

    CAS  Article  PubMed  Google Scholar 

  31. Grube R, Livingstone KD, Zamir D et al (1999) Comparative analysis of disease resistance within the Solanaceae. Plant Anim Genome VII Conf San Diego P350:873–887

    Google Scholar 

  32. Gujjar RS, Karkute SG, Rai A, Singh M, Singh B (2018) Proline-rich proteins may regulate free cellular proline levels during drought stress in tomato. Curr Sci. https://doi.org/10.18520/cs/v114/i04/915-920

    Article  Google Scholar 

  33. Hsieh T, Lee J, Yang P et al (2002) Heterology expression of the Arabidopsis C-repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. Plant Physiol 129:1086–1094. https://doi.org/10.1104/pp.003442.1086

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. Hu D-G, Ma Q-J, Sun C-H et al (2016) Overexpression of MdSOS2L1, a CIPK protein kinase, increases the antioxidant metabolites to enhance salt tolerance in apple and tomato. Physiol Plant 156:201–214. https://doi.org/10.1111/ppl.12354

    CAS  Article  PubMed  Google Scholar 

  35. Huertas R, Olías R, Eljakaoui Z et al (2012) Overexpression of SlSOS2 (SlCIPK24) confers salt tolerance to transgenic tomato. Plant, Cell Environ 35:1467–1482. https://doi.org/10.1111/j.1365-3040.2012.02504.x

    CAS  Article  Google Scholar 

  36. Ingram J (2011) A food systems approach to researching food security and its interactions with global environmental change. Food Secur 3:417–431. https://doi.org/10.1007/s12571-011-0149-9

    Article  Google Scholar 

  37. Julkowska MM, Testerink C (2015) Tuning plant signaling and growth to survive salt. Trends Plant Sci 20:586–594. https://doi.org/10.1016/j.tplants.2015.06.008

    CAS  Article  PubMed  Google Scholar 

  38. Karapanos IC, Akoumianakis KA, Olympios CM, Passam HC (2010) Tomato pollen respiration in relation to in vitro germination and pollen tube growth under favourable and stress-inducing temperatures. Sex Plant Reprod 23:219–224. https://doi.org/10.1007/s00497-009-0132-1

    CAS  Article  PubMed  Google Scholar 

  39. Karkute SG, Krishna R, Ansari WA, Singh B, Singh PM, Singh M, Singh AK (2019) Heterologous expression of the AtDREB1A gene in tomato confers tolerance to chilling stress. Biol Plant. https://doi.org/10.32615/bp.2019.031

    Article  Google Scholar 

  40. Khan AL, Waqas M, Asaf S et al (2017) Plant growth-promoting endophyte Sphingomonas sp. LK11 alleviates salinity stress in Solanum pimpinellifolium. Environ Exp Bot 133:58–69. https://doi.org/10.1016/j.envexpbot.2016.09.009

    CAS  Article  Google Scholar 

  41. Kong F, Deng Y, Wang G et al (2014) LeCDJ1, a chloroplast DnaJ protein, facilitates heat tolerance in transgenic tomatoes. J Integr Plant Biol 56:63–74. https://doi.org/10.1111/jipb.12119

    CAS  Article  PubMed  Google Scholar 

  42. Kotak S, Larkindale J, Lee U et al (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316. https://doi.org/10.1016/j.pbi.2007.04.011

    CAS  Article  PubMed  Google Scholar 

  43. Krasensky J, Jonak C (2012) Drought, salt, and temperature stress induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608

    CAS  Article  Google Scholar 

  44. Kumar A, Verma JP (2018) Does plant—microbe interaction confer stress tolerance in plants: a review? Microbiol Res 207:41–52. https://doi.org/10.1016/j.micres.2017.11.004

    CAS  Article  PubMed  Google Scholar 

  45. Kumar K, Aggarwal C, Sapna B et al (2018) Microbial genes in crop improvement. In: Crop improvement through microbial biotechnology. Elsevier, Amsterdam, Netherlands, pp 39–56. https://doi.org/10.1016/B978-0-444-63987-5.00003-7

    Chapter  Google Scholar 

  46. Laloi C, Apel K, Danton A (2004) Reactive oxygen signalling: the latest news. Curr Opin Plant Biol 7:323e326

    Article  Google Scholar 

  47. Larkindale J (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 138:882–897. https://doi.org/10.1104/pp.105.062257

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62:4731–4748. https://doi.org/10.1093/jxb/err210

    CAS  Article  PubMed  Google Scholar 

  49. Lee JT, Prasad V, Yang PT et al (2003) Expression of Arabidopsis CBF1 regulated by an ABA/stress inducible promoter in transgenic tomato confers stress tolerance without affecting yield. Plant Cell Environ 26:1181–1190. https://doi.org/10.1046/j.1365-3040.2003.01048.x

    CAS  Article  Google Scholar 

  50. Li Z, Peng Y, Zhang XQ et al (2014) Exogenous spermidine improves water stress tolerance of white clover (Trifolium repens L.) involved in antioxidant defence, gene expression and proline metabolism. Plant Omics 7:517–526. https://doi.org/10.3390/molecules191118003

    CAS  Article  Google Scholar 

  51. Lim MY, Jeong BR, Jung M, Harn CH (2016) Transgenic tomato plants expressing strawberry d-galacturonic acid reductase gene display enhanced tolerance to abiotic stresses. Plant Biotechnol Rep 10:105–116. https://doi.org/10.1007/s11816-016-0392-9

    Article  Google Scholar 

  52. Lin D, Xia J, Wan S (2010) Climate warming and biomass accumulation of terrestrial plants: a meta-analysis. New Phytol 188:187–198. https://doi.org/10.1111/j.1469-8137.2010.03347.x

    Article  PubMed  Google Scholar 

  53. Liu H, Zhou Y, Li H et al (2018) Molecular and functional characterization of ShNAC1, an NAC transcription factor from Solanum habrochaites. Plant Sci 271:9–19. https://doi.org/10.1016/J.PLANTSCI.2018.03.005

    CAS  Article  PubMed  Google Scholar 

  54. Lobell DB, Roberts MJ, Schlenker W et al (2014) Greater sensitivity to drought accompanies maize yield increase in the US Midwest. Science (80-) 344:516–519. https://doi.org/10.1126/science.1251423

    CAS  Article  Google Scholar 

  55. Lu SW, Qi F, Li TL (2012) Effects of salt stress on sugar content and sucrose metabolism in tomato fruit. China Veg 20:56–61

    CAS  Google Scholar 

  56. Masle J, Gilmore SR, Farquhar GD (2005) The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 436:866–870. https://doi.org/10.1038/nature03835

    CAS  Article  PubMed  Google Scholar 

  57. McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155:1051–1059. https://doi.org/10.1104/pp.110.170704

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  58. Moghaieb REA, Tanaka N, Saneoka H et al (2000) Expression of betaine aldehyde dehydrogenase gene in transgenic tomato hairy roots leads to the accumulation of glycine betaine and contributes to the maintenance of the osmotic potential under salt stress. Soil Sci Plant Nutr 46:873–883. https://doi.org/10.1080/00380768.2000.10409153

    CAS  Article  Google Scholar 

  59. Moghaieb REA, Nakamura A, Saneoka H, Fujita K (2011) Evaluation of salt tolerance in ectoine-transgenic tomato plants (Lycopersicon esculentum) in terms of photosynthesis, osmotic adjustment, and carbon partitioning. GM Crops 2:58–65. https://doi.org/10.4161/gmcr.2.1.15831

    Article  PubMed  Google Scholar 

  60. Mohanty A, Kathuria H, Ferjani A et al (2002) Transgenics of an elite indica rice variety Pusa Basmati 1 harbouring the coda gene are highly tolerant to salt stress. Theor Appl Genet 106:51–57. https://doi.org/10.1007/s00122-002-1063-5

    CAS  Article  PubMed  Google Scholar 

  61. Morrow G, Tanguay RM (2012) Small heat shock protein expression and functions during development. Int J Biochem Cell Biol 44:1613–1621. https://doi.org/10.1016/j.biocel.2012.03.009

    CAS  Article  PubMed  Google Scholar 

  62. Nautiyal PC, Shono M, Egawa Y (2005) Enhanced thermotolerance of the vegetative part of MT-sHSP transgenic tomato line. Sci Hortic (Amsterdam) 105:393–409. https://doi.org/10.1016/j.scienta.2005.02.001

    Article  Google Scholar 

  63. Nebauer S, Sánchez M, Martínez L et al (2013) Differences in photosynthetic performance and its correlation with growth among tomato cultivars in response to different salts. Plant Physiol Biochem 63:61–69. https://doi.org/10.1016/j.plaphy.2012.11.006 PMID: 23232248

    CAS  Article  PubMed  Google Scholar 

  64. Neta-Sharir I (2005) Dual role for tomato heat shock protein 21: protecting photosystem II from oxidative stress and promoting color changes during fruit maturation. Plant Cell Online 17:1829–1838. https://doi.org/10.1105/tpc.105.031914

    CAS  Article  Google Scholar 

  65. Nieto-Sotelo J (2002) Maize HSP101 plays important roles in both induced and basal thermotolerance and primary root growth. Plant Cell Online 14:1621–1633. https://doi.org/10.1105/tpc.010487

    CAS  Article  Google Scholar 

  66. Nir I, Moshelion M, Weiss D (2014) The Arabidopsis gibberellin methyl transferase 1 suppresses gibberellin activity, reduces whole-plant transpiration and promotes drought tolerance in transgenic tomato. Plant Cell Environ 37:113–123. https://doi.org/10.1111/pce.12135

    CAS  Article  PubMed  Google Scholar 

  67. Parfitt J, Barthel M, MacNaughton S (2010) Food waste within food supply chains: quantification and potential for change to 2050. Philos Trans R Soc B Biol Sci 365:3065–3081. https://doi.org/10.1098/rstb.2010.0126

    Article  Google Scholar 

  68. Park S, Li J, Pittman JK et al (2005) Up-regulation of a H+-pyrophosphatase (H+-PPase) as a strategy to engineer drought-resistant crop plants. Proc Natl Acad Sci 102:18830–18835. https://doi.org/10.1073/pnas.0509512102

    CAS  Article  PubMed  Google Scholar 

  69. Park EJ, Jeknić Z, Pino MT et al (2007) Glycinebetaine accumulation is more effective in chloroplasts than in the cytosol for protecting transgenic tomato plants against abiotic stress. Plant Cell Environ 30:994–1005. https://doi.org/10.1111/j.1365-3040.2007.01694.x

    CAS  Article  PubMed  Google Scholar 

  70. Parmar N, Singh KH, Sharma D, Singh L, Kumar P, Nanjundan J, Khan YJ, Chauhan DK, Thakur AK (2017) Genetic engineering strategies for biotic and abiotic stress tolerance and quality enhancement in horticultural crops: a comprehensive review. 3 Biotech 7(4):239. https://doi.org/10.1007/s13205-017-0870-y

    Article  PubMed  PubMed Central  Google Scholar 

  71. Peleman JD, Van Der Voort JR (2003) Breeding by design. Trends Plant Sci 8:330–334. https://doi.org/10.1016/S1360-1385(03)00134-1

    CAS  Article  PubMed  Google Scholar 

  72. Popp HW (1951) An introduction to plant physiology. Science Publishers, New York

    Book  Google Scholar 

  73. Prasanna HC, Sinha DP, Rai GK, Krishna R, Kashyap SP, Singh NK, Singh M, Malathi VG (2015) Pyramiding T y-2 and T y-3 genes for resistance to monopartite and bipartite tomato leaf curl viruses of India. Plant Pathol 64(2):256–264. https://doi.org/10.1111/ppa.12267

    CAS  Article  Google Scholar 

  74. Rai GK, Rai NP, Kumar S et al (2012) Effects of explant age, germination medium, pre-culture parameters, inoculation medium, pH, washing medium, and selection regime on Agrobacterium-mediated transformation of tomato. Vitr Cell Dev Biol Plant 48:565–578. https://doi.org/10.1007/s11627-012-9442-3

    CAS  Article  Google Scholar 

  75. Rai AC, Singh M, Shah K (2013a) Engineering drought tolerant tomato plants over-expressing BcZAT12 gene encoding a C2H2 zinc finger transcription factor. Phytochemistry 85:44–50. https://doi.org/10.1016/j.phytochem.2012.09.007

    CAS  Article  PubMed  Google Scholar 

  76. Rai GK, Rai NP, Rathaur S et al (2013b) Expression of rd29A:: AtDREB1A/CBF3 in tomato alleviates drought-induced oxidative stress by regulating key enzymatic and non-enzymatic antioxidants. Plant Physiol Biochem 69:90–100. https://doi.org/10.1016/j.plaphy.2013.05.002

    CAS  Article  PubMed  Google Scholar 

  77. Rivero RM, Kojima M, Gepstein A et al (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci 104:19631–19636. https://doi.org/10.1073/pnas.0709453104

    Article  PubMed  Google Scholar 

  78. Roy R, Purty RS, Agrawal V, Gupta SC (2006) Transformation of tomato cultivar “Pusa Ruby” with bspA gene from Populus tremula for drought tolerance. Plant Cell Tissue Organ Cult 84:55–67. https://doi.org/10.1016/j.ctrv.2005.12.002

    CAS  Article  Google Scholar 

  79. Rosenzweig C, Elliott J, Deryng D et al (2014) Assessing agricultural risks of climate change in the 21st century in a global gridded crop model intercomparison. Proc Natl Acad Sci 111:3268–3273. https://doi.org/10.1073/pnas.1222463110

    CAS  Article  PubMed  Google Scholar 

  80. Ruiz-Vera UM, Siebers MH, Drag DW et al (2015) Canopy warming caused photosynthetic acclimation and reduced seed yield in maize grown at ambient and elevated [CO2]. Glob Chang Biol 21:4237–4249. https://doi.org/10.1111/gcb.13013

    Article  PubMed  Google Scholar 

  81. Ryu H, Cho Y-G (2015) Plant hormones in salt stress tolerance. J Plant Biol 58:147–155. https://doi.org/10.1007/s12374-015-0103-z

    CAS  Article  Google Scholar 

  82. Saadi S, Todorovic M, Pereira LS (2010) Climate change and Mediterranean agriculture: 2. Impacts on wheat and tomato yields and water productivity. Elsevier 147:1–14

    Google Scholar 

  83. Sahi C, Singh A, Blumwald E, Grover A (2006) Beyond osmolytes and transporters: novel plant salt-stress tolerance-related genes from transcriptional profiling data. Physiol Plant 127:1–9. https://doi.org/10.1111/j.1399-3054.2005.00610.x

    CAS  Article  Google Scholar 

  84. Sakuma Y (2006) Functional analysis of an Arabidopsis transcription factor. DREB2A, involved in drought-responsive gene expression. Plant Cell Online 18:1292–1309. https://doi.org/10.1105/tpc.105.035881

    CAS  Article  Google Scholar 

  85. Sánchez-Rodríguez E, Rubio-Wilhelmi MM, Cervilla LM et al (2010) Genotypic differences in some physiological parameters symptomatic for oxidative stress under moderate drought in tomato plants. Plant Sci 178:30–40. https://doi.org/10.1016/j.plantsci.2009.10.001

    CAS  Article  Google Scholar 

  86. Sanmiya K, Suzuki K, Egawa Y, Shono M (2004) Mitochondrial small heat-shock protein enhances thermotolerance in tobacco plants. FEBS Lett 557:265–268

    CAS  Article  Google Scholar 

  87. Schramm F, Larkindale J, Kiehlmann E et al (2008) A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis. Plant J 53:264–274. https://doi.org/10.1111/j.1365-313X.2007.03334.x

    CAS  Article  PubMed  Google Scholar 

  88. Scippa GS, Griffiths A, Chiatante D, Bray EA (2000) The H1 histone variant of tomato, H1-S, is targeted to the nucleus and accumulates in chromatin in response to water-deficit stress. Planta 211:173–181. https://doi.org/10.1007/s004250000278

    CAS  Article  PubMed  Google Scholar 

  89. Seki M, Narusaka M, Abe H et al (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13:61. https://doi.org/10.2307/3871153

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  90. Seong ES, Cho HS, Choi D, Joung YH, Lim CK, Hur JH, Wang MH (2007) Tomato plants overexpressing CaKR1 enhanced tolerance to salt and oxidative stress. Biochem Biophys Res Commun 363:983–988. https://doi.org/10.1016/j.bbrc.2007.09.104

    CAS  Article  PubMed  Google Scholar 

  91. Shah K, Singh M, Rai AC (2013) Effect of heat-shock induced oxidative stress is suppressed in BcZAT12 expressing drought tolerant tomato. Phytochemistry 95:109–117. https://doi.org/10.1016/j.phytochem.2013.07.026

    CAS  Article  PubMed  Google Scholar 

  92. Silva Dias J, Ryder EJ (2011) World vegetable industry: production, breeding, trends. Hortic Rev 38:299–356

    Google Scholar 

  93. Tung SA, Smeeton R, White CA et al (2008) Over-expression of LeNCED1 in tomato (Solanum lycopersicum L.) with the rbcS3C promoter allows recovery of lines that accumulate very high levels of abscisic acid and exhibit severe phenotypes. Plant Cell Environ 31:968–981. https://doi.org/10.1111/j.1365-3040.2008.01812.x

    CAS  Article  PubMed  Google Scholar 

  94. Turk H, Erdal S, Genisel M et al (2014) The regulatory effect of melatonin on physiological, biochemical and molecular parameters in cold-stressed wheat seedlings. Plant Growth Regul 74:139–152. https://doi.org/10.1007/s10725-014-9905-0

    CAS  Article  Google Scholar 

  95. Verslues PE, Agarwal M, Katiyar-Agarwal S et al (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45:523–539. https://doi.org/10.1111/j.1365-313X.2005.02593.x

    CAS  Article  PubMed  Google Scholar 

  96. Wang Y, Frei M (2011) Stressed food—the impact of abiotic environmental stresses on crop quality. Agric Ecosyst Environ 141:271–286. https://doi.org/10.1016/j.agee.2011.03.017

    Article  Google Scholar 

  97. Wang Y, Wisniewski M, Meilan R et al (2005) Overexpression of cytosolic ascorbate peroxidase in tomato confers tolerance to chilling and salt stress. J Am Soc Hortic Sci 130:167–173

    CAS  Article  Google Scholar 

  98. Wang BQ, Zhang QF, Liu JH, Li GH (2011) Overexpression of PtADC confers enhanced dehydration and drought tolerance in transgenic tobacco and tomato: Effect on ROS elimination. Biochem Biophys Res Commun 413:10–16. https://doi.org/10.1016/j.bbrc.2011.08.015

    CAS  Article  PubMed  Google Scholar 

  99. Wang JY, Lai L di, Tong SM, Li QL (2013) Constitutive and salt-inducible expression of SlBADH gene in transgenic tomato (Solanum lycopersicum L. cv. Micro-Tom) enhances salt tolerance. Biochem Biophys Res Commun 432:262–267. https://doi.org/10.1016/j.bbrc.2013.02.001

    CAS  Article  PubMed  Google Scholar 

  100. Wang G, Kong F, Zhang S et al (2015) A tomato chloroplast-targeted DnaJ protein protects Rubisco activity under heat stress. J Exp Bot 66:3027–3040. https://doi.org/10.1093/jxb/erv102

    CAS  Article  PubMed  Google Scholar 

  101. Waters ER (2013) The evolution, function, structure, and expression of the plant sHSPs. J Exp Bot 64:391–403. https://doi.org/10.1093/jxb/ers355

    CAS  Article  PubMed  Google Scholar 

  102. Wei D, Zhang W, Wang C et al (2017) Genetic engineering of the biosynthesis of glycinebetaine leads to alleviate salt-induced potassium efflux and enhances salt tolerance in tomato plants. Plant Sci 257:74–83. https://doi.org/10.1016/j.plantsci.2017.01.012

    CAS  Article  PubMed  Google Scholar 

  103. Yarra R, He SJ, Abbagani S et al (2012) Overexpression of a wheat Na+/H+ antiporter gene (TaNHX2) enhances tolerance to salt stress in transgenic tomato plants (Solanum lycopersicum L.). Plant Cell Tissue Organ Cult 111:49–57. https://doi.org/10.1007/s11240-012-0169-y

    CAS  Article  Google Scholar 

  104. Zhai Y, Yang Q, Hou M (2015) The effects of saline water drip irrigation on tomato yield, quality, and blossom-end rot incidence—a 3a case study in the South of China. PLoS One 10:e0142204. https://doi.org/10.1371/journal.pone.0142204

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  105. Zhao C, Shono M, Sun A et al (2007) Constitutive expression of an endoplasmic reticulum small heat shock protein alleviates endoplasmic reticulum stress in transgenic tomato. J Plant Physiol 164:835–841. https://doi.org/10.1016/j.jplph.2006.06.004

    CAS  Article  PubMed  Google Scholar 

  106. Zhang HX, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol 19:765–768. https://doi.org/10.1038/90824

    CAS  Article  PubMed  Google Scholar 

  107. Zhang X, Fowler SG, Cheng H et al (2004) Freezing-sensitive tomato has a functional CBF cold responsive pathway, but a CBF regulon that differs from that of freezing tolerant Arabidopsis. Plant J 39:905–919

    CAS  Article  Google Scholar 

  108. Zhu M, Chen G, Zhang J et al (2014) The abiotic stress-responsive NAC-type transcription factor SlNAC4 regulates salt and drought tolerance and stress-related genes in tomato (Solanum lycopersicum). Plant Cell Rep 33:1851–1863. https://doi.org/10.1007/s00299-014-1662-z

    CAS  Article  PubMed  Google Scholar 

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Correspondence to Jay Prakash Verma.

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Krishna, R., Karkute, S.G., Ansari, W.A. et al. Transgenic tomatoes for abiotic stress tolerance: status and way ahead. 3 Biotech 9, 143 (2019). https://doi.org/10.1007/s13205-019-1665-0

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Keywords

  • Tomato
  • Solanum lycopersicum
  • Genetic engineering
  • Abiotic stress
  • Sustainable agriculture