Growth, yield, and metabolic responses of temperature-stressed tomato to grafting onto rootstocks differing in cold tolerance

Journal of the American Society for Horticultural Science

Volumn 139, Issue 2, 2014, Pages 230-243

  Ntatsi, Georgia ^a,b   Savvas, Dimitrios ^a   Kläring, Hans Peter ^b   Schwarz, Dietmar ^b  

^a AGRICULTURAL UNIVERSITY OF ATHENS   (Greece)

^b LEIBNIZ INSTITUTE OF VEGETABLE AND ORNAMENTAL CROPS   (Germany)

Author keywords

Antioxidants; ROS; Scion; Solanum habrochaites; Solanum lycopersicum; Suboptimal temperature

Indexed keywords

EID: 84896323484     PISSN: 00031062     EISSN: None     Source Type: Journal    
DOI: 10.21273/jashs.139.2.230     Document Type: Article

References (81)

1. Abbas, S.M. 2012. Effects of low temperature and selenium application on growth and the physiological changes in sorghum seedlings. J. Stress Physiol. Biochem. 8:268-286.
2. Adams, S.R., K.E. Cockshull, and C.R.J. Cave. 2001. Effect of temperature on the growth and development of tomato fruits. Ann. Bot. (Lond.) 88:869-877.
3. Ainsworth, E.A. and D.R. Bush. 2011. Carbohydrate export from the leaf: A highly regulated process and target to enhance photosynthesis and productivity. Plant Physiol. 155:64-69.
4. Apel, K. and H. Hirt. 2004. Reactive oxygen species: Metabolism, oxidative stress and signal transduction. Annu. Rev. Plant Biol. 55:373-399.
5. Arenas-Huertero, F., A. Arroyo, L. Zhou, J. Sheen, and P. Leon. 2000. Analysis of arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes Dev. 14:2085-2096.
6. Aroca, R., F. Tognoni, J.J. Irigoyen, M. Sánchez-Díaz, and A. Pardossi. 2001. Different root low temperature response of two maize genotypes differing in their chilling sensitivity. Plant Physiol. Biochem. 39:1067-1073.
7. Bloom, A.J., L.B. Randall, P.A. Meyerhof, and D.A. St. Clair. 1998. The chilling sensitivity of root ammonium influx in a cultivated and wild tomato. Plant Cell Environ. 21:191-199.
8. Bloom, A.J., M.A. Zwieniecki, J.B. Passioura, L.B. Randall, N.M. Holbrook, and D.A. St. Clair. 2004. Water relations under root chilling in a sensitive and a tolerant tomato species. Plant Cell Environ. 27:971-979.
9. Bogdanovic, J., M. Mojovic, N. Milosavic, A. Mitrovic, Z. Vucinic, and I. Spasojevic. 2008. Role of fructose in the adaptation of plants to cold induced oxidative stress. Eur. Biophys. J. 37:1241-1246.
10. Bradford, M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
11. Cakmak, I. and H. Marshner. 1992. Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol. 98:1222-1227.
12. Cheng, W.H., A. Endo, L. Zhou, J. Penney, H.C. Chen, A. Arroyo, P. Leon, E. Nambara, T. Asami, M. Seo, T. Koshiba, and J. Sheen. 2002. A unique short-chain dehydrogenase/reductase in arabidopsis abscisic acid biosynthesis and glucose signaling. Plant Cell 14:2723-2743.
13. Chinnusamy, V., J. Zhu, and J.K. Zhu. 2007. Cold stress regulation of gene expression in plants. Trends Plant Sci. 12:444-451.
14. Chiou, T.J. and D.R. Bush. 1998. Sucrose is a signal molecule in assimilate partitioning. Proc. Natl. Acad. Sci. USA 95:4784-4788.
15. Cook, D., S. Fowler, O. Fiehn, and M.F. Thomashow. 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.
16. De Kreij, C., W. Voogt, A.L. Van den Bos, and R. Baas. 1997. Voedingsoplossingen voor de teelt van tomaat in gesloten teeltsystemen. Brochure VG 2 Tomaat, Proefstation voor Bloemisterij en Glasgroente, Naaldwijk, The Netherlands.
17. Demiral, T. and I. Turkan. 2005. Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ. Exp. Bot. 53:247-257.
18. Domínguez, E., J. Cuartero, and R. Fernandez-Munoz. 2005. Breeding tomato for pollen tolerance to low temperatures by gametophytic selection. Euphytica 142:253-263.
19. Egley, G.H., R.N. Paul, K.C. Vaughn, and S.O. Duke. 1983. Role of peroxidase in the development of water impermeable seed coats in Sida spinosa L. Planta 157:224-232.
20. Elings, A., F.L.K. Kempkes, R.C. Kaarsemaker, M.N.A. Ruijs, N.J. Van de Braak, and T.A. Dueck. 2005. The energy balance and energy-saving measures in greenhouse tomato cultivation. Acta Hort. 691:67-74.
21. Ensminger, I., N. Busch, and N.P.A. Huner. 2006. Photostasis and cold acclimation: Sensing low temperature through photosynthesis. Physiol. Plant. 126:28-44.
22. Equiza, M.A., J.P. Mirave, and J.A. Tognetti. 2001. Morphological, anatomical and physiological responses related to differential shoot vs. root growth inhibition at low temperature in spring and winter wheat. Ann. Bot. (Lond.) 87:67-76.
23. Fernández-Muñoz, R., J.J. González-Fernández, and J. Cuartero. 1995. Genetics of the viability of pollen grain produced at low temperatures in Lycopersicon Mill. Euphytica 84:139-144.
24. Foyer, C.H. and G. Noctor. 2005. Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. Plant Cell 17:1866-1875.
25. Gao, C., D. Xing, L. Li, and L. Zhang. 2008. Implication of reactive oxygen species and mitochondrial dysfunction in the early stages of plant programmed cell death induced by ultraviolet-C overexposure. Planta 227:755-767.
26. Garay-Arroyo, A., M. De La Paz Sánchez, B. García-Ponce, E. Azpeitia, and E.R. Álvarez-Buylla. 2012. Hormone symphony during root growth and development. Dev. Dyn. 241:1867-1885.
27. Geigenberger, P. and M. Stitt. 1993. Sucrose synthase catalyses a readily reversible reaction in vivo in developing potato tubers and other plant tissues. Planta 189:329-339.
28. Gill, S.S. and N. Tuteja. 2010. Polyamines and abiotic stress tolerance in plants. Plant Signal. Behav. 5:26-33.
29. Goulas, E., M. Schubert, T. Kieselbach, L.A. Kleczkowski, P. Gardestrom, and W.V. Schroder. 2006. The chloroplast lumen and stromal proteomes of Arabidopsis thaliana show differential sensitivity to shortand long-term exposure to low temperature. Plant J. 47:720-734.
30. Gupta, A.K. and N. Knaur. 2005. Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants. J. Biosci. 30:761-776.
31. He, Y., Z. Zhu, J. Yang, X. Ni, and B. Zhu. 2009. Grafting increases the salt tolerance of tomato by improvement of photosynthesis and enhancement of antioxidant enzymes activity. Environ. Exp. Bot. 66:270-278.
32. Ho, L.C. and P.J. White. 2005. A cellular hypothesis for the induction of blossom-end rot in tomato. Fruit Ann. Bot. 95:571-581.
33. Hodges, M.D., J.M. DeLong, C.F. Forney, and R.K. Prange. 1999. Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604-611.
34. Kasper, T.C. and W.L. Bland. 1992. Soil temperature and root growth. Soil Sci. 154:290-299.
35. Kiegle, E., C.A. Moore, J. Haseloff, M.A. Tester, and M.R. Knight. 2000. Cell-type-specific calcium responses to drought, salt and cold in the arabidopsis root. Plant J. 23:267-278.
36. Knight, H., A.J. Trewavas, and M.R. Knight. 1996. Cold calcium signalling in arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8:489-503.
37. Kodama, H., G. Horiguchi, T. Nishiuchi, M. Nishimura, and K. Iba. 1995. Fatty acid desaturation during chilling acclimation is one of the factors involved in conferring low-temperature tolerance to young tobacco leaves. Plant Physiol. 107:1177-1185.
38. Korkmaz, A. and R.J. Dufault. 2002. Short-term cyclic cold temperature stress on water melon yield. HortScience 37:487-489.
39. Kratsch, H.A. and R.R. Wise. 2000. The ultrastructure of chilling stress. Plant Cell Environ. 23:337-350.
40. Lee, J.M. 1994. Cultivation of grafted vegetables. I. Current status, grafting methods, and benefits. HortScience 29:235-239.
41. Liu, B.H., L. Cheng, F.W. Ma, D. Liang, and Y.J. Zou. 2012. Influence of rootstock on drought response in young 'Gale Gala' apple (Malus domestica Borkh.) trees. J. Sci. Food Agr. 92:2421-2427.
42. Ma, Y., Y. Zhang, J. Lu, and H. Shao. 2009. Roles of plant soluble sugars and their responses to plant cold stress. Afr. J. Biotechnol. 8:2004-2010.
43. Macduff, J.H., A. Wild, M.J. Hopper, and M.S. Dhanoa. 1986. Effects of temperature on parameters of root growth relevant to nutrient uptake: Measurements on oilseed rape and barley grown in flowing nutrient solution. Plant Soil 94:321-332.
44. Mahajan, S. and N. Tuteja. 2005. Cold, salinity and drought stresses: An overview. Arch. Biochem. Biophys. 444:139-158.
45. Mitchell, D.E. and M.A. Madore. 1992. Patterns of assimilate production and translocation in muskmelon (Cucumis melo L.): II. Low temperature effects. Plant Physiol. 99:966-971.
46. Moore, S. and W.H. Stein. 1948. Photometric ninhydrin method for use in the chromatography of amino acids. J. Biol. Chem. 176:357-388.
47. Nishiyama, I. 1995. Damage due to extreme temperatures, p. 769-812. In: Matsuo, T., K. Kumazawa, R. Ishii, H. Ishihara, and H. Hirata (eds.). Science of the rice plant. Food Agr. Policy Res. Ctr., Tokyo, Japan.
48. Noctor, G. and C.H. Foyer. 1998. Ascorbate and glutathione: Keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49:249-279.
49. Ntatsi, G., D. Savvas, U. Druege, and D. Schwarz. 2013. Contribution of phytohormones in alleviating the impact of sub-optimal temperature stress on grafted tomato. Sci. Hort. 149:28-38.
50. Patterson, B.D., R. Paull, and R.M. Smillie. 1978. Chilling resistance in Lycopersicon hirsutum Humb. and Bonpl., a wild tomato with a wide altitudinal distribution. Aust. J. Plant Physiol. 5:609-617.
51. Paul, E.M.M., R.C. Hardwick, and P.F. Parker. 1984. Genotypic variation in the response to sub-optimal temperatures of growth in tomato (Lycopersicon esculentum Mill.). New Phytol. 98:221-230.
52. Rao, K.V.M. and T.V.S. Sresty. 2000. Antioxidant parameters in the seedlings of pigonpea [Cajanus cajan (L.) Millspaugh] in response to Zn and Ni stresses. Plant Sci. 157:113-128.
53. Rao, M.V., G. Paliyath, and D.P. Ormrod. 1996. Ultraviolet-Band ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiol. 110:125-136.
54. Rick, C.M., J.W. Uhlig, and A.D. Jones. 1994. High alpha-tomatine content in ripe fruit of Andean Lycopersicon esculentum var. cerasiforme-Developmental and genetic aspects. Proc. Natl. Acad. Sci. USA 91:12877-12881.
55. Rook, F., F. Corke, R. Card, G. Munz, C. Smith, and M.W. Bevan. 2001. Impaired sucrose-induction mutants reveal the modulation of sugar-induced starch biosynthetic gene expression by abscisic acid signaling. Plant J. 26:421-433.
56. Rosa, M., C. Prado, G. Podazza, R. Interdonato, J.A. González, M. Hilal, and F.E. Prado. 2009a. Soluble sugars-Metabolism, sensing and abiotic stress: A complex network in the life of plants. Plant Signal. Behav. 4:388-393.
57. Rosa, M., M. Hilal, J.A. González, and F.E. Prado. 2009b. Lowtemperature effect on enzyme activities involved in sucrose-starch partitioning in salt-stressed and salt-acclimated cotyledons of quinoa (Chenopodium quinoa Wild.) seedlings. Plant Physiol. Biochem. 47:300-307.
58. Ruelland, E., M.N. Vaultier, A. Zachowski, and V. Hurry. 2009. Cold signaling and cold acclimation in plants. Adv. Bot. Res. 49:35-150.
59. Salinas, J. 2002. Molecular mechanisms of signal transduction in cold acclimation, p. 116-139. In: Scheel, D. and C. Wasternack (eds.). Plant signal transduction. Oxford Univ. Press, London, UK.
60. Schwarz, D. and H.-P. Klaring. 2001. Allometry to estimate leaf area of tomato. J. Plant Nutr. 24:1291-1309.
61. Schwarz, D., Y. Rouphael, G. Colla, and J.H. Venema. 2010. Grafting as a tool to improve tolerance of vegetables to abiotic stress. Thermal stress, water stress and organic pollutants. Sci. Hort. 127:162-171.
62. Siddiqui, K.S. and R. Cavicchioli. 2006. Cold-adapted enzymes. Annu. Rev. Biochem. 75:403-433.
63. Sirova, J., M. Sedlarova, J. Piterkova, L. Luhova, and M. Petrivalsky. 2011. The role of nitric oxide in the germination of plant seeds and pollen. Plant Sci. 181:560-572.
64. Sonnewald, U. 1992. Expression of E. coli inorganic pyrophosphatase in transgenic plants alters photoassimilate partitioning. Plant J. 2:571-581
65. Spooner, D.M., I.E. Peralta, and S. Knapp. 2005. Comparison of AFLPs with other markers for phylogenetic inference in wild tomatoes [Solanum L. section Lycopersicon (Mill.) Wettst.]. Taxonomy 54:43-61.
66. Strand, A., C.H. Foyer, P. Gustafsson, and V. Hurry. 2003. Increased expression of sucrose phosphate synthase in transgenic Arabidopsis thaliana results in improved photosynthetic performance and increased freezing tolerance al low temperatures. Plant Cell Environ. 26:523-535.
67. Sundar, D., K.V. Chaitanya, P.P. Jutur, and A.R. Reddy. 2004. Low temperature-induced changes in antioxidative metabolism in rubber-producing shrub, guayule (Parthenium argentatum Gray). Plant Growth Regulat. 44:175-181.
68. Tahtiharju, S., V. Sangwan, A.F. Monroy, R.S. Dhindsa, and M. Borg. 1997. The induction of kin genes in cold-acclimating Arabidopsis thaliana. Evidence of a role for calcium. Planta 203:442-447.
69. Theocharis, A., C. Clement, and E.A. Barka. 2012. Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091-1105.
70. Tucker, D.E. and D.R. Ort. 2002. Low temperature induces expression of nitrate reductase in tomato that temporarily overrides circadian regulation of activity. Photosynth. Res. 72:285-293.
71. Tuteja, N. 2009. Cold, Salinity and drought stress, p. 137-159. In: Hirt, H. (ed.). Plant stress biology: From genomics to systems biology. Wiley VHC Verlag, Weinheim, Germany.
72. Van der Ploeg, A. and E. Heuvelink. 2005. Influence of sub-optimal temperature on tomato growth and yield: A review. J. Hort. Sci. Biotechnol. 80:652-659.
73. Venema, J.H., B.E. Dijk, J.M. Bax, P.R. Van Hasselt, and J.T.M. Elzenga. 2008. Grafting tomato (Solanum lycopersicum) onto the rootstock of a high-altitude accession of Solanum habroachites improves suboptimal-temperature tolerance. Environ. Exp. Bot. 63:359-367.
74. Venema, J.H., P. Linger, A.W. Van Heusden, P.R. Van Hasselt, and W. Bruggemann. 2005. The inheritance of chilling tolerance in tomato (Lycopersicon ssp.). Plant Biol. 7:118-130.
75. Venema, J.H., F. Posthumus, and P.R. Van Hasselt. 1999. Impact of suboptimal temperature on growth, photosynthesis, leaf pigments and carbohydrates of domestic and high-altitude wild Lycopersicon species. J. Plant Physiol. 155:711-718.
76. Walter, A., R. Feil, and U. Schurr. 2009. Environmental effects on spatial and temporal patterns of leaf and root growth. Annu. Rev. Plant Biol. 60:279-304.
77. Wilkinson, S., A.L. Clephan, and W.J. Davies. 2001. Rapid low temperature-induced stomatal closure occurs in cold-tolerant Commelina communis leaves but not in cold-sensitive tobacco leaves, via a mechanism that involves apoplastic calcium but not abscisic acid. Plant Physiol. 126:1566-1578.
78. Yadav, S.K. 2010. Cold stress tolerance mechanisms in plants. A review. Agron. Sustainainable Dev. 30:515-527.
79. Zhang, Y., Y. Zhang, Y. Zhou, and J. Yu. 2007. Adaptation of cucurbit species to changes in substrate temperature: Root growth, antioxidants, and peroxidation. J. Plant Biol. 50:527-532.
80. Zhang, Z.K., S.Q. Liu, S.Q. Hao, and S.H. Liu. 2010. Grafting increases the copper tolerance of cucumber seedlings by improvement of polyamine contents and enhancement of antioxidant enzymes activity. Agr. Sci. China 9:985-994.
81. Zhou, Y.H., L.F. Huang, Y. Zhang, K. Shi, J.Q. Yu, and S. Nogues. 2007. Chill-induced decrease in capacity of RuBP carboxylation and associated H2O2 accumulation in cucumber leaves are alleviated by grafting onto figleaf gourd. Ann. Bot. (Lond.) 100:839-845.