Grafting improves tomato drought tolerance through enhancing photosynthetic capacity and reducing ROS accumulation


Drought is the main meteorological threat to plants and limits plant growth, development, and adaptation to environmental changes. However, root-shoot communication plays a vital role in improving tomato plant drought tolerance, especially when cultivars are grafted onto drought-tolerant rootstock. In this study, the relationship between photosynthetic capacity and reactive oxygen species (ROS) in response to drought stress was studied in tomato grafted with different drought-resistant tomato seedlings. To determine the drought-relieving effect of drought-tolerant rootstocks, we measured the effects of grafting on plant growth, net photosynthetic rate (Pn), ROS accumulation, and antioxidant enzyme activities in tomato leaves and roots under drought stress. Plant growth and Pn were significantly inhibited by drought, but ROS accumulation and antioxidant enzyme activities were significantly increased. Treatment with drought-tolerant tomato seedlings significantly increased plant growth and increased Pn under water-deficit conditions compared with those grafted with drought-susceptible rootstock. In addition, the plants grafted with drought-tolerant seedlings had increased activities of partial antioxidant enzymes, leading to decreased ROS production. Our results indicate that tomato grafted with drought-tolerant seedlings alleviated the phytotoxicity and oxidative damage caused by drought by regulating antioxidant enzymes under drought stress.

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Ascorbate peroxidase



H2O2 :

Hydrogen peroxide


maximal photochemical efficiency


Effective quantum use efficiency of (photosystem II) PSII in the light-adapted state


Malic acid



O :

Superoxide anion


Net photosynthetic rate




Photosystem II


Relative electrolyte leakage


Reactive oxygen species


Superoxide dismutase


Transpiration rate


  1. Ahmedi CB, Rouina BB, Sensoy S, Boukhris M, Abdallah FB (2009) Changes in gas exchange, proline accumulation and antioxidative enzyme activities in three olive cultivars under contrasting water availability regimes. Environ Exp Bot 67:345–352

    Article  CAS  Google Scholar 

  2. Alan Ö, Özdemir N, Günen Y (2007) Effect of grafting on watermelon plant growth, yield and quality. J Agron 6:362–365

    Article  Google Scholar 

  3. Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bacon MA (2004) Water use efficiency in plant biology. Water Use Effic Plant Biol 45:329

    Google Scholar 

  5. Calatayud A, Barreno E (2004) Response to ozone in two lettuce varieties on chlorophyll a, fluorescence, photosynthetic pigments and lipid peroxidation. Plant Physiol Biochem 42:549–555

    Article  CAS  PubMed  Google Scholar 

  6. Chaitanya KV, Jutur PP, Sundar D, Reddy AR (2003) Water stress effects on photosynthesis in different mulberry cultivars. Plant Growth Regul 40:75–80

    Article  CAS  Google Scholar 

  7. Colla G, Rouphael Y, Cardarelli M, Salerno A, Rea E (2010) The effectiveness of grafting to improve alkalinity tolerance in watermelon. Environ Exp Bot 68:283–291

    Article  CAS  Google Scholar 

  8. Dias MC, Correia S, Serôdio J, Silva AMS, Freitas H, Santos C (2018) Chlorophyll fluorescence and oxidative stress endpoints to discriminate olive cultivars tolerance to drought and heat episodes. Sci Hortic 231:31–35

    Article  CAS  Google Scholar 

  9. Gambetta GA, Manuck CM, Drucker ST, Shaghasi T, Fort K, Matthews MA, Walker MA, Mc E, A.J. (2012) The relationship between root hydraulics andscion vigour across Vitis rootstocks: what role do root aquaporins play? J Exp Bot 63:6445–6455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Huang Y, Li J, Hua B, Liu Z, Fan M, Bie Z (2013) Grafting onto different rootstocks as a means to improve watermelon tolerance to low potassium stress. Sci Hortic 149:80–85

    Article  CAS  Google Scholar 

  11. Iersel MWV, Weaver G, Martin MT, Ferrarezi RS, Mattos E, Haidekker M (2016) A chlorophyll fluorescence-based biofeedback system to control photosynthetic lighting in controlled environment agriculture. J Am Soc Hortic Sci 141:169–176

    Article  Google Scholar 

  12. IPCC (2007) Contribution of working groups I, II and III to the fourth assessment report of the intergovernmental panel on climate change Climate Change 2007: Synthesis report104 (Geneva, Switzerland)

  13. Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889–905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Ke D, Saltveit ME (1988) Plant hormone interaction and phenolic metabolism in the regulation of russet spotting in iceberg lettuce. Plant Physiol 88:1136–1140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Łabędzki LŁ, Bąk B (2017) Impact of meteorological drought on crop water deficit and crop yield reduction in polish agriculture. J Water Land Dev 34:181–190

    Article  Google Scholar 

  16. Lee JM, Kubota C, Tsao SJ, Bie Z, Hoyos Echevarria P, Morra L, Oda M (2010) Current status of vegetable grafting: diffusion grafting techniques, automation. Sci Hortic 127:93–105

    Article  Google Scholar 

  17. Li H, Liu SS, Yi CY, Wang F, Zhou J, Xia XJ, Shi K, Zhou YH, Yu JQ (2014a) Hydrogen peroxide mediates abscisic acid-induced hsp70 accumulation and heat tolerance in grafted cucumber plants. Plant Cell Environ 37:2768–2780

    Article  CAS  Google Scholar 

  18. Li H, Wang F, Chen XJ, Shi K, Xia XJ, Considine MJ, Yu JQ, Zhou YH (2014b) The sub/supra-optimal temperature-induced inhibition of photosynthesis and oxidative damage in cucumber leaves are alleviated by grafting onto figleaf gourd/luffa rootstocks. Physiol Plant 152:571–584

    Article  CAS  PubMed  Google Scholar 

  19. Liu YF, Qi HY, Bai CM, Qi MF, Xu CQ, Hao JH, Li Y, Li TL (2011) Grafting helps improve photosynthesis and carbohydrate metabolism in leaves of muskmelon. Int J Biol Sci 7:1161–1170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Liu B, Li M, Cheng L, Liang D, Zou Y, Ma F (2012) Influence of rootstock on antioxidant system in leaves and roots of young apple trees in response to drought stress. Plant Growth Regul 67:247–256

    Article  CAS  Google Scholar 

  21. Liu J, Li J, Su X, Xia Z (2014) Grafting improves drought tolerance by regulating antioxidant enzyme activities and stress-responsive gene expression in tobacco. Environ Exp Bot 107:173–179

    Article  CAS  Google Scholar 

  22. Liu S, Li H, Lv X, Ahammed GJ, Xia X, Zhou J, Shi K, Asami T, Yu J, Zhou Y (2016) Grafting cucumber onto luffa improves drought tolerance by increasing ABA biosynthesis and sensitivity. Sci Rep 6:20212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Lucas WJ, Groover A, Lichtenberger R, Furuta K, Yadav SR, Helariutta Y, He XQ, Fukuda H, Kang J, Brady SM, Patrick JW, Sperry J, Yoshida A, López-Millán AF, Grusak MA, Kachroo P (2013) The plant vascular system: evolution, development and functions. J Integr Plant Biol 55:294–388

    Article  CAS  PubMed  Google Scholar 

  24. Marguerit E, Brendel O, Lebon E, Van Leeuwen C, Ollat N (2012) Rootstock control of scion transpiration and its acclimation to water deficit are controlled by different genes. New Phytol 194:416–429

    Article  CAS  Google Scholar 

  25. Martinez-Rodriguez MM, Estan MT, Moyano E, Garcia-Abellan JO, Flores FB, Campos JF, Al-Azzawi MJ, Flowers TJ, Bolarin MC (2008) The effectiveness of grafting to improve salt tolerance in tomato when an ‘excluder’ genotype is used as scion. Environ Exp Bot 63:392–401

    Article  CAS  Google Scholar 

  26. Mathobo R, Marais D, Steyn JM (2017) The effect of drought stress on yield, leaf gaseous exchange and chlorophyll fluorescence of dry beans (Phaseolus vulgaris, l). Agric Water Manag 180:118–125

    Article  Google Scholar 

  27. Menconi M, Sgherri CLM, Pinzino C, Navari-Izzo F (1995) Activated oxygen production and detoxification in wheat plants subjected to a water deficit programme. J Exp Bot 46:1123–1130

    Article  CAS  Google Scholar 

  28. Mittler R, Vanderauwera S, Gollery M, Van BF (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  Google Scholar 

  29. Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Suzuki T, Fujita M (2016) Polyamine and nitric oxide crosstalk: antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicol Environ Saf 126:245–255

    Article  CAS  Google Scholar 

  30. Ntatsi G, Savvas D, Kläring HP, Schwarz D (2014) Growth, yield, and metabolic responses of temperature-stressed tomato to grafting onto rootstocks differing in cold tolerance. J Am Soc Hortic Sci 139:230–243

    Article  CAS  Google Scholar 

  31. Ozbahce A, Tari AF (2010) Effects of different emitter space and water stress on yield and quality of processing tomato under semi-arid climate conditions. Agric Water Manag 97:1405–1410

    Article  Google Scholar 

  32. Pagliarani C, Vitali M, Ferrero M, Vitulo N, Incarbone M, Lovisolo C, Valle G, Schubert A (2017) Accumulation of microRNAs differentially modulated by drought is affected by grafting in grapevine. Plant Physiol 173:2180–2195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Rauckman EJ, Rosen GM, Kitchell BB (1979) Superoxide radical as anointer mediate in the oxidation of hydroxylamines by mixed function amine oxidase. Mol Pharmacol 15:131–137

    CAS  PubMed  Google Scholar 

  34. Ray RL, Fares A, Risch E (2018) Effects of drought on crop production and cropping areas in Texas. Agric Environ L 3(1)

  35. Rivero RM, Ruiz JM, Romero L (2003) Role of grafting in horticultural plants. J Food Agric Environ 1:70–74

    Google Scholar 

  36. Rouphael Y, Cardarelli M, Rea E, Colla G (2008) Grafting of cucumber as a means to minimize copper toxicity. Environ Exp Bot 63:49–58

    Article  CAS  Google Scholar 

  37. Ruiz JM, Blasco B, Rivero RM, Romero L (2010) Nicotine-free and salt-tolerant tobacco plants obtained by grafting to salinity-resistant rootstocks of tomato. Physiol Plant 124:465–475

    Article  CAS  Google Scholar 

  38. Sánchez-Rodríguez E, Rubio-Wilhelmi MM, Blasco B, Leyva R, Romero L, Ruiz JM (2012) Antioxidant response resides in the shoot in reciprocal grafts of drought-tolerant and drought-susceptible cultivars in tomato under water stress. Plant Sci 188:89–96

    Article  CAS  PubMed  Google Scholar 

  39. Savvas D, Papastavrou D, Ntatsi G, Ropokis A, Olympios C, Hartmann H, Schwarz D (2009) Interactive effects of grafting and manganese supply on growth yield, and nutrient uptake by tomato. Hortic Science 44:1978–1982

    Google Scholar 

  40. Schwarz D, Rouphael Y, Colla G, Venema JH (2010) Grafting as a tool to improve tolerance of vegetables to abiotic stresses: thermal stress, water stress and organic pollutants. Sci Hortic 127:162–171

    Article  CAS  Google Scholar 

  41. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    Article  CAS  Google Scholar 

  42. Silva VA, Prado FM, Antunes WC, Paiva RMC, Ferrão MAG, Andrade AC, Mascio PD, Loureiro ME, DaMatta FM, Almeida AM (2018) Reciprocal grafting between clones with contrasting drought tolerance suggests a key role of abscisic acid in coffee acclimation to drought stress. Plant Growth Regul:1–9

  43. Tramontini S, Vitali M, Centioni L, Schubert A, Lovisolo C (2013) Rootstock control of scion response to water stress in grapevine. Environ Exp Bot 93:20–26

    Article  Google Scholar 

  44. Venema JH, Dijk BE, Bax JM, Hasselt PRV, Elzenga JTM (2008) Grafting tomato (Solanum lycopersicum) onto the rootstock of a high-altitude accession of Solanum habrochaites improves suboptimal-temperature tolerance. Environ Exp Bot 63:359–367

    Article  Google Scholar 

  45. Wang WB, Kim YH, Lee HS, Kim KY, Deng XP, Kwak SS (2009) Analysis of antioxidant enzyme activity during germination of alfalfa under salt and drought stresses. Plant Physiol Biochem 47:570–577

    Article  CAS  Google Scholar 

  46. Wang S, Liang D, Li C, Hao Y, Ma F, Shu H (2012) Influence of drought stress on the cellular ultrastructure and antioxidant system in leaves of drought-tolerant and drought- susceptible apple rootstocks. Plant Physiol Biochem 51:81–89

    Article  CAS  Google Scholar 

  47. Weerasinghe OR, De Costa WAJM, Perera ALT (2003) Evaluation of different genotypes of tomato under well watered and water stressed conditions on the basis of yield and some selected physiological parameters. Tropical Agricultural Research Vol, 144–156

  48. Wiese C, Shi LB, Heber U (1998) Oxygen reduction in the Mehler reaction is insufficient to protect photosystems I and II of leaves against photoinactivation. Physiol Plant 102:437–446

    Article  CAS  Google Scholar 

  49. Xing XH, Fang CW, Long LI, Jiang HQ, Qin Z, Jiang HD, Wang SH (2016) Improved drought tolerance by α-naphthaleneacetic acid-induced ROS accumulation in two soybean cultivars. J Integr Agric 15:1770–1784

    Article  CAS  Google Scholar 

  50. Xu J, Zhu Y, Ge Q, Li Y, Sun J, Zhang Y, Liu X (2012) Comparative physiological responses of Solanum nigrum and Solanum torvum to cadmium stress. New Phytol 196:125–138

    Article  CAS  PubMed  Google Scholar 

  51. Yao X, Yang R, Zhao F, Wang S, Li C, Zhao W (2016) An analysis of physiological index of differences in drought tolerance of tomato rootstock seedlings. J Plant Biol 59:311–321  

    Article  CAS  Google Scholar 

  52. Yi X, Burgess P, Zhang X, Huang B (2016) Enhancing cytokinin synthesis by overexpressing ipt alleviated drought inhibition of root growth through activating ROS-scavenging systems in Agrostis stolonifera. J Exp Bot 67:1979–1992

    Article  CAS  Google Scholar 

  53. Zhang ZH, Han M, Zhang Y, Wang Y, Xu K (2016) Identification and evaluation of tomato rootstock seedlings for drought tolerance. Chin J Ecol 35:719–725 (in Chinese)

    Google Scholar 

  54. Zhang ZH, Han M, Zhang Y, Wang Y, Liu CY, Cao BL, Xu K (2017) Effect of water stress on development and H2O and CO2 exchange in leaves of tomato grafted with different drought resistant rootstocks. Sci Agric Sin 50:391–398 (in Chinese)

    Google Scholar 

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This work was supported by the Special Foundation for Modern Agricultural Industry Technology System of Shandong Province (no. SDAIT-05-05) and the Double First-Class Discipline Construction Project of Shandong Province (no. SYL2017YSTD06).

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Zhihuan Zhang and Kun Xu designed the experiments; Zhihuan Zhang, Bili Cao, and Song Gao performed the experiments; and Zhihuan Zhang and Kun Xu wrote the manuscript.

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Correspondence to Kun Xu.

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Zhang, Z., Cao, B., Gao, S. et al. Grafting improves tomato drought tolerance through enhancing photosynthetic capacity and reducing ROS accumulation. Protoplasma 256, 1013–1024 (2019).

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  • Tomato
  • Grafting
  • Drought tolerance
  • Photosynthetic
  • ROS accumulation
  • Antioxidant