Salt stress differently affects growth, water status and antioxidant enzyme activities in Solanum lycopersicum and its wild relative Solanum chilense
Juan Pablo Martínez A E H , Alejandro Antúnez B , Héctor Araya C , Ricardo Pertuzé D , Lida Fuentes E , X. Carolina Lizana F and Stanley Lutts GA Instituto de Investigaciones Agropecuarias (INIA-La Cruz), Chorrillos 86, La Cruz, Casilla 3, Región de Valparaíso, Chile.
B Instituto de Investigaciones Agropecuarias (INIA-La Platina), Santa Rosa 11610, La Pintana, Casilla 3, Santiago, Chile.
C Facultad de Medicina, Universidad de Chile, Santiago, Avenida Independencia 1027, Santiago, Chile.
D Facultad de Ciencias Agrarias, Universidad de Chile, Avenida Santa Rosa 11315, Santiago, Chile.
E Centro Regional de Estudios en Alimentos Saludables (CREAS), Conicyt Regional, Gore Región de Valparaíso, R12C1001, Avenida Universidad 330, sector Curauma, Valparaíso, Chile.
F Instituto de Producción y Sanidad Vegetal, Facultad de Ciencias Agrarias. Universidad Austral de Chile, Campus Isla Teja, Valdivia, Chile.
G Groupe de Recherche en Physiologie Végétale, Université catholique de Louvain (UCL), Croix du Sud 5, Boîte 13, B-138 Louvain-la-Neuve, Belgium.
H Corresponding author. Email: jpmartinez@inia.cl
Australian Journal of Botany 62(5) 359-368 https://doi.org/10.1071/BT14102
Submitted: 27 November 2013 Accepted: 21 June 2014 Published: 9 September 2014
Abstract
The effect of saline stress (NaCl, 40, 80 and 160 mmol L−1 of NaCl) on growth, plant water status and leaf antioxidant enzyme activities was investigated in a commercial cultivar of cherry tomato (Solanum lycopersicum var. cerasiforme L.) and in a wild-related species collected in a salt-affected area of North Chile (Solanum chilense Dun.). Salt stress was applied in a nutrient solution at the vegetative stage during 40 days. The highest NaCl concentration reduced shoot relative growth, fresh and dry weight and leaf area in the cultivated S. lycopersicum but had less impact on S. chilense. Both species were able to efficiently perform osmotic adjustment but S. chilense also exhibited an increase in leaf succulence. The oxidative stress estimated through malondialdehyde quantification was always higher in the cultivated S. lycopersicum, both in the absence and in the presence of salt. Total superoxide dismutase activity (EC 1.15.1.1) increased in response to the highest dose of NaCl in S. chilense but remained constant in S. lycopersicum. Salinity induced an increase in ascorbate peroxidase (EC 1.11.1.11) in S. chilense but reduced it in S. lycopersicum. It is concluded that S. chilense displays efficient strategies to cope with high NaCl doses and that management of the oxidative status is a key mechanism allowing this species to tolerate salinity.
Additional keywords: halophyte, salinity, tomato.
References
Albacete A, Martínez-Andújar C, Ghanem ME, Acosta M, Sánchez-Bravo J, Asins MJ, Cuartero J, Lutts S, Dodd IC, Pérez-Alfocea F (2009) Rootstock-mediated changes in xylem ionic and hormonal status are correlated with delayed leaf senescence, and increased leaf area and crop productivity in salinized tomato. Plant, Cell & Environment 32, 928–938.| Rootstock-mediated changes in xylem ionic and hormonal status are correlated with delayed leaf senescence, and increased leaf area and crop productivity in salinized tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosl2jsb0%3D&md5=7b726de7abc31986348a59a4fd0b5f35CAS |
Asins MJ, Bolarín MC, Pérez-Alfocea F, Estañ MT, Martínez-Andújar C, Albacete A, Villalta I, Bernet GP, Dodd IC, Carbonell EA (2010) Genetic analysis of physiological components of salt tolerance conferred by Solanum rootstocks. What is the rootstock doing for the scion? Theoretical and Applied Genetics 121, 105–115.
| Genetic analysis of physiological components of salt tolerance conferred by Solanum rootstocks. What is the rootstock doing for the scion?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3czjsF2lsQ%3D%3D&md5=a4c578e087345e3ff2f1a9b78ccba07dCAS | 20180091PubMed |
Beyer WF, Fridovitch I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Analytical Biochemistry 161, 559–566.
| Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXktVaqtb8%3D&md5=3063a7f4b9d93bf6d7fc6f07223db85eCAS | 3034103PubMed |
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry 72, 248–254.
| A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=13d639c8b62b7bfb06f33c4b9935e7eaCAS | 942051PubMed |
Bretó MP, Asíns MJ, Carbonell EA (1994) Salt tolerance in Lycopersicon species. III. Detection of QTLs by means of molecular markers. Theoretical and Applied Genetics 88, 395–401.
| Salt tolerance in Lycopersicon species. III. Detection of QTLs by means of molecular markers.Crossref | GoogleScholarGoogle Scholar | 24186024PubMed |
Chang CCC, Slesak I, Jordá L, Sotnikov A, Melzer M, Miszalski Z, Mullineaux PM, Parker JE, Karpinska B, Karpinski S (2009) Arabidopsis chloroplastic glutathine peroxidases play a role in cross talk between photooxidative stress and immune responses. Plant Physiology 150, 670–683.
| Arabidopsis chloroplastic glutathine peroxidases play a role in cross talk between photooxidative stress and immune responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsleit7Y%3D&md5=c8863971cce9f0907ee1839407738405CAS |
Chetelat RT, Pertuze RA, Faundez L, Graham EB, Jones CM (2009) Distribution, ecology and reproductive biology of wild tomatoes and related nightshades from the Atacama Desert region of northern Chile. Euphytica 167, 77–93.
| Distribution, ecology and reproductive biology of wild tomatoes and related nightshades from the Atacama Desert region of northern Chile.Crossref | GoogleScholarGoogle Scholar |
Colmer TD, Flowers TJ, Munns R (2006) Use of wild relatives to improve salt tolerance in wheat. Journal of Experimental Botany 57, 1059–1078.
| Use of wild relatives to improve salt tolerance in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1Gls7s%3D&md5=b15d65388e8311d02b7245023c015de2CAS | 16513812PubMed |
Cuartero J, Fernández-Muñoz R (1998) Tomato and salinity. Scientia Horticulturae 78, 83–125.
| Tomato and salinity.Crossref | GoogleScholarGoogle Scholar |
Cuartero J, Bolarín MC, Asíns MJ, Moreno V (2006) Increasing salt tolerance in the tomato. Journal of Experimental Botany 57, 1045–1058.
| Increasing salt tolerance in the tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1Glsrc%3D&md5=a3654d8b5ffc24bb565cc880740bff6fCAS | 16520333PubMed |
de Azevedo Neto AD, Prisco JT, Enéas-Filho J, Braga de Abreu CE, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environmental and Experimental Botany 56, 87–94.
| Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes.Crossref | GoogleScholarGoogle Scholar |
del Rio LA, Corpas FJ, Sandalio LM, Palma JM, Gomez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. Journal of Experimental Botany 53, 1255–1272.
| Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFSls7s%3D&md5=802fa41c001c8afecb7f84028ec74026CAS | 11997374PubMed |
Delpérée C, Kinet JM, Lutts S (2003) Low irradiance modifies the effect of wáter stress on survival and growth-related parameters during the early developmental stages of buckwheat (Fagopyrum esculentum). Physiologia Plantarum 119, 211–220.
| Low irradiance modifies the effect of wáter stress on survival and growth-related parameters during the early developmental stages of buckwheat (Fagopyrum esculentum).Crossref | GoogleScholarGoogle Scholar |
Dianese EC, Fonseca MEN, Inoue-Nagata AK, Resende RO, Boiteux LS (2011) Search in Solanum (section Lycopersicon) gerplasm for sources of broad-spectrum resistance to four Tospovirus species. Euphytica 180, 307–319.
| Search in Solanum (section Lycopersicon) gerplasm for sources of broad-spectrum resistance to four Tospovirus species.Crossref | GoogleScholarGoogle Scholar |
Ding S, Lu Q, Zhan Y, Yang Z, Wen X, Zhang L, Lu C (2009) Enhanced sensitivity to oxidative stress in transgenic tobacco plants with decreased glutathione reductase activity leads to a decrease in ascorbate pool and ascorbate redox state. Plant Molecular Biology 69, 577–592.
| Enhanced sensitivity to oxidative stress in transgenic tobacco plants with decreased glutathione reductase activity leads to a decrease in ascorbate pool and ascorbate redox state.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvFehtL4%3D&md5=b0b193757ef6c94e615c26cd31fbd812CAS | 19043665PubMed |
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytologist 179, 945–963.
| Salinity tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWqur%2FE&md5=ce74aed5431022dad136c81c3e416cb9CAS | 18565144PubMed |
Flowers TJ, Yeo AR (1995) Breeding for salinity resistance in crop plants: where next? Australian Journal of Plant Physiology 22, 875–884.
| Breeding for salinity resistance in crop plants: where next?Crossref | GoogleScholarGoogle Scholar |
Gálvez FJ, Baghour M, Hao G, Cagnac O, Rodríguez-Rosales MP, Venema K (2012) Expression of LeNHX isoforms in response to salt stress in salt sensitive and salt tolerant tomato species. Plant Physiology and Biochemistry 51, 109–115.
| Expression of LeNHX isoforms in response to salt stress in salt sensitive and salt tolerant tomato species.Crossref | GoogleScholarGoogle Scholar | 22153246PubMed |
Ghanem ME, Albacete A, Martínez-Andújar C, Acosta M, Romero-Aranda R, Dodd IC, Lutts S, Pérez-Alfocea F (2008) Hormonal changes during salinity-induced leaf senescence in tomato (Solanum lycopersicum L.). Journal of Experimental Botany 59, 3039–3050.
| Hormonal changes during salinity-induced leaf senescence in tomato (Solanum lycopersicum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpslalsb4%3D&md5=b5c30717f1135bda219e650ed6013ad6CAS | 18573798PubMed |
Harinasut P, Poonsopa D, Roengmongkol K, Charoensataporn R (2003) Salinity effects on antioxidant enzymes in mulberry cultivar. Science Asia 29, 109–113.
| Salinity effects on antioxidant enzymes in mulberry cultivar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotl2is70%3D&md5=654a49522e61d825c8b027a76c804ad7CAS |
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125, 189–198.
| Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1cXhtFWgtLw%3D&md5=a53bacf3bdbdc452759cc016712af6f8CAS | 5655425PubMed |
Igic B, Smith WA, Robertson KA, Schaal BA, Kohn JR (2007) Studies of self-incompatibility in wild tomatoes: I. S-allele diversity in Solanum chilense Dun. (Solanaceae). Heredity 99, 553–561.
| Studies of self-incompatibility in wild tomatoes: I. S-allele diversity in Solanum chilense Dun. (Solanaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1Wgtr7M&md5=db72869cf172e9eca59d995d11204b66CAS | 17700636PubMed |
Kuzniak E, Sklodowska M (2005) Compartment-specific role of the ascorbate-glutathione cycle in the response of tomato leaf cells to Botrytis cinerea infection. Journal of Experimental Botany 56, 921–933.
| Compartment-specific role of the ascorbate-glutathione cycle in the response of tomato leaf cells to Botrytis cinerea infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXit1Knurw%3D&md5=28fd444ab69ee50cec7f84abad442aa1CAS | 15668222PubMed |
M’rah S, Ouerhi Z, Emery F, Rey P, Hajji M, Grignon C, Lachaal M (2007) Efficiency of biochemical protection against toxic effects of accumulated salt differentiate Thelungiella halophila from Arabidopsis thaliana. Journal of Plant Physiology 164, 375–384.
| Efficiency of biochemical protection against toxic effects of accumulated salt differentiate Thelungiella halophila from Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvFSqtrk%3D&md5=279e1080d9999061595467cd42027631CAS | 17074409PubMed |
Malecka A, Jarmuszkiewicz W, Tomaszewska B (2001) Antioxidative defense to lead stress in subcellular compartments of pea root cells. Acta Biochimica Polonica 48, 687–698.
Martínez JP, Araya H (2010) Ascorbate-glutation cycle: enzymatic and non-enzymatic integrated mechanisms and its biomolecular regulation. In ‘Ascorbate-glutathion pathway and stress tolerance in plants’. (Eds NA Anjum, MT Chan, S Umar) pp. 303–322. (Springer: Amsterdam)
Martìnez JP, Ledent JF, Bajji M, Kinet JM, Lutts S (2003) Effect of water stress on growth, Na+ and K+ accumulation and water use efficiency in relation to osmotic adjustment in two populations of Atriplex halimus L. Plant Growth Regulation 41, 63–73.
| Effect of water stress on growth, Na+ and K+ accumulation and water use efficiency in relation to osmotic adjustment in two populations of Atriplex halimus L.Crossref | GoogleScholarGoogle Scholar |
Martìnez JP, Lutts S, Schanck A, Bajji M, Kinet JM (2004) Is osmotic adjustment required for water stress resistance in the Mediterranean shrub Atriplex halimus L.? Journal of Plant Physiology 161, 1041–1051.
| Is osmotic adjustment required for water stress resistance in the Mediterranean shrub Atriplex halimus L.?Crossref | GoogleScholarGoogle Scholar | 15499906PubMed |
Martínez JP, Kinet JM, Bajji M, Lutts S (2005) NaCl alleviates PEG-induced water stress in the halophyte species Atriplex halimus L. Journal of Experimental Botany 34, 795–810.
Martínez JP, Antúnez A, Pertuze R, Acosta MP, Palma X, Fuentes L, Ayala A, Araya H, Lutts S (2012) Effects of saline water on water status, yield and fruit quality of wild (Solanum chilense) and domesticated (Solanum lycopersicum var. cerasiforme) tomatoes. Experimental Agriculture 48, 573–586.
| Effects of saline water on water status, yield and fruit quality of wild (Solanum chilense) and domesticated (Solanum lycopersicum var. cerasiforme) tomatoes.Crossref | GoogleScholarGoogle Scholar |
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405–410.
| Oxidative stress, antioxidants and stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntVWnu7Y%3D&md5=b830ac267f048ddaa66451f74b84bb0bCAS | 12234732PubMed |
Mittova V, Tal M, Volokita M, Guy M (2002) Salt stress induces up-regulation of an efficient chloroplast antioxidant system in the salt-tolerant wild tomato species Lycopersicon pennellii but not in the cultivated species. Physiologia Plantarum 115, 393–400.
| Salt stress induces up-regulation of an efficient chloroplast antioxidant system in the salt-tolerant wild tomato species Lycopersicon pennellii but not in the cultivated species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVGitL4%3D&md5=773761b9fd64a05faefbc06962ef2fcdCAS | 12081532PubMed |
Monforte A, Asíns MJ, Carbonnell EA (1997) Salt tolerance in Lycopersicon species. VI. Genotype by salinity interaction in quantitative trait loci detection. Constitutive and response QTs. Theoretical and Applied Genetics 95, 706–713.
| Salt tolerance in Lycopersicon species. VI. Genotype by salinity interaction in quantitative trait loci detection. Constitutive and response QTs.Crossref | GoogleScholarGoogle Scholar |
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 31, 1565–1574.
Munns R, Schachtman DP, Condon AG (1995) The significance of a two-phase growth response to salinity in wheat and barley. Australian Journal of Plant Physiology 22, 561–569.
| The significance of a two-phase growth response to salinity in wheat and barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXos1erur0%3D&md5=d73f75a7de2023ac4c5389dc83724e58CAS |
Nakano Y, Asada K (1981) Hydrogen peroxide scavenged by ascorbate specific peroxidase in spinach chloroplast. Plant & Cell Physiology 22, 867–880.
Ottow EA, Brinker M, Teichmann T, Fritz E, Kaiser W, Brosché M, Kangasjärvi J, Jiang X, Polle A (2005) Populus euphratica displays apoplastic sodium accumulation, omotic adjustment by decreases in calcium and soluble carbohydrates and develops leaf succulence under salt stress. Plant Physiology 139, 1762–1772.
| Populus euphratica displays apoplastic sodium accumulation, omotic adjustment by decreases in calcium and soluble carbohydrates and develops leaf succulence under salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlGmsb7N&md5=27966497ebfde57adf9e123a8c05c3eaCAS | 16299175PubMed |
Qi CH, Chen M, Song J, Wang BS (2009) Increase in aquaporin activity is involved in leaf succulence of the euhalophyte Suaeda salsa, under salinity. Plant Science 176, 200–205.
| Increase in aquaporin activity is involved in leaf succulence of the euhalophyte Suaeda salsa, under salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFagtbrL&md5=01b55209c80b19d48384857ea4bafcdcCAS |
Rao MV, Paliyath G, Ormrod DP (1996) Ultraviolet-B radiation and ozone-induced biochemical changes in the antioxidant enzymes of Arabidopsis thaliana. Plant Physiology 110, 125–136.
| Ultraviolet-B radiation and ozone-induced biochemical changes in the antioxidant enzymes of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltFGnuw%3D%3D&md5=f05da0160b6f988cba9af8810452def9CAS | 8587977PubMed |
Salazar M, Gonzalez E, Casaretto JA, Casacuberta JM, Ruis-Lara S (2007) The promoter of the TLC1.1 retroptransposon from Solanum chilense is activated by multiple stress-related signalling molecules. Plant Cell Reports 26, 1861–1868.
| The promoter of the TLC1.1 retroptransposon from Solanum chilense is activated by multiple stress-related signalling molecules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVaksbjF&md5=4ca5081236f913bfc93854b664616ba6CAS | 17583815PubMed |
(a) SAS (2014) ‘SAS 9.2 – SAS/STAT users guide.’ (SAS Institute Inc.: Cary, NC)
Städler T, Arunyawat U, Stephan W (2008) Population genetics of speciation in two closely related wild tomatoes (Solanum section Lycopersicon). Genetics 178, 339–350.
| Population genetics of speciation in two closely related wild tomatoes (Solanum section Lycopersicon).Crossref | GoogleScholarGoogle Scholar |
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144, 307–313.
| The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmsFShsbY%3D&md5=0688a988ec82f9b93dcebb83ccf14d09CAS |
Xia H, Camus-Kulandaivelu L, Stephan W, Tellier A, Zhang Z (2010) Nucleotide diversity patterns of local adaptation at drought-related candidate genes in wild tomatoes. Molecular Ecology 19, 4144–4154.
| Nucleotide diversity patterns of local adaptation at drought-related candidate genes in wild tomatoes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVagtrfF&md5=3af6e29ee155bc1b2384e3843ca9fa83CAS | 20831645PubMed |
Yu Q, Osborne L, Rengel Z (1998) Micronutrient deficiency changes activities of superoxide dismutase and ascorbate peroxidase in tobacco plants. Journal of Plant Nutrition 21, 1427–1437.
| Micronutrient deficiency changes activities of superoxide dismutase and ascorbate peroxidase in tobacco plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXksVOmtrg%3D&md5=fab90be4fab31ae529c9b01e3d04481dCAS |
Zhou SP, Sauve RJ, Liu Z, Reddy S, Bhatti S, Hucko SD, Fish T, Thannhauser TW (2011) Identification of salt-induced changes in leaf and root proteomes of the wild tomato Solanum chilense. American Society for Horticultural Science 136, 288–302.
Zhu GY, Kinet JM, Lutts S (2001) Characterization of rice (Oryza sativa L.) F3 populations selected for salt resistance. I. Physiological behaviour during vegetative growth. Euphytica 121, 251–263.
| Characterization of rice (Oryza sativa L.) F3 populations selected for salt resistance. I. Physiological behaviour during vegetative growth.Crossref | GoogleScholarGoogle Scholar |