Abstract
A future rise in sea level will expand areas of salt-affected acid sulfate soil, calling for studies on plant tolerance to combined aluminum (Al) and salt (NaCl) stress. We investigated random amplified polymorphic DNA (RAPD) profiles and tolerance to Al and NaCl alone and in combination in 14 Melaleuca cajuputi Powell provenances. Two-month-old seedlings were grown with or without 10 mM Al and/or 50 mM NaCl at pH 3.8 for 3 months. Plant growth was reduced mostly by combined Al and NaCl stress and then by NaCl and least by Al. Moreover, Al enhanced the effect of NaCl on growth and vice versa. There were significant differences in plant growth among provenances under all treatments; however, positive relationships were found among Al tolerance, NaCl tolerance, and combined Al and NaCl tolerance. Provenance variation in stress tolerance increases with the increasing levels of stress effect. Furthermore, NaCl tolerance tended to have a positive relationship with osmotic potential. Leaf sap K concentration was decreased by NaCl and increased by Al; however, provenances that were more tolerant to NaCl tended to have lower K concentrations. RAPD analysis also revealed genetic variation among provenances. These results suggest that the low tolerance to combined Al and NaCl stress in M. cajuputi is largely due to low tolerance to NaCl and the effect of interaction between Al and NaCl. Provenance variation in stress tolerance was significant and could be partly explained by the variation in genetic material and the ability of plants to reduce ion excess stress in their shoots.
Similar content being viewed by others
References
Asian Development Bank (1994) Climate change in Asia: Vietnam country report. Asian Development Bank, Manila
Bell DT (1999) Australian trees for the rehabilitation of waterlogged and salinity-damaged landscapes. Aust J Bot 47:697–716. doi:10.1071/BT96110
Blamey RPC, Asher CJ, Edwards DC, Kerven GL (1993) In vitro evidence of aluminum effects on solution movement through root cell walls. J Plant Nutr 16:555–562. doi:10.1080/01904169309364556
Blancaflor EB, Jones DL, Gilroy S (1998) Alterations in the cytoskeleton accompanies aluminum-induced growth inhibition and morphological changes in primary roots of maize. Plant Physiol 118:159–172. doi:10.1104/pp.118.1.159
Carter JL, Colmer TD, Veneklaas EJ (2005) Variable tolerance of wetland tree species to combined salinity and waterlogging is related to regulation of ion uptake and production of organic solutes. New Phytol 169:123–134. doi:10.1111/j.1469-8137.2005.01552.x
Chen THH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–275. doi:10.1016/S1369-5266(02)00255-8
Doran JC, Gunn BV (1994) Exploring the genetic resources of tropical melaleucas. Forest Genetic Resources No 22 FAO, Rome
Ezaki B, Gardner RC, Ezaki Y, Matsumoto H (2000) Expression of aluminum-induced genes in transgenic Arabidopsis plants can ameliorate aluminum stress and/or oxidative stress. Plant Physiol 122:657–665. doi:10.1104/pp.122.3.657
Flower TJ, Troke PF, Yeo AJ (1977) The mechanisms of salt tolerance in halophytes. Annu Rev Plant Physiol 28:89–121. doi:10.1146/annurev.pp.28.060177.000513
Godbold DL, Jentschke G (1998) Aluminium accumulation in root cell walls coincides with inhibition of root growth but not with inhibition of magnesium uptake in Norway spruce. Physiol Plant 102:553–560. doi:10.1034/j.1399-3054.1998.1020410.x
Hussain TM, Chandrasekhar T, Hazara M, Sultan Z, Saleh BK, Gopal GR (2008) Recent advances in salt stress biology—a review. Biotechnol Mol Biol Rev 3:8–13
Kinraide TB, Parker DR (1990) Apparent phytotoxicity of mononuclear hydroxyl aluminum to four dicotyledonous species. Plant Physiol 79:283–288. doi:10.1111/j.1399-3054.1990.tb06743.x
Kinraide TB, Ryan PR, Kochain LV (1992) Interactive effects of Al3+, H+, and other cations on root elongation considered in terms of cell-surface electrical potential. Plant Physiol 99:1461–1468
Krauss KW, Chambers JL, Allen JA, Soileau DM Jr, DeBosier AS (2000) Growth and nutrition of bald cypress families planted under varying salinity regimes in Louisiana, USA. J Coast Res 16:153–163
McCann MC, Shi J, Roberts K, Carpita NC (1994) Changes in pectin structure and localization during the growth of unadapted and NaCl-adapted tobacco cells. Plant J 5:773–785. doi:10.1046/j.1365-313X.1994.5060773.x
Naidu BP, Paleg LG, Jones GP (2000) Accumulation of proline analogues and adaptation of Melaleuca species to diverse environments in Australia. Aust J Bot 48:611–620. doi:10.1071/BT99059
Neumann PM, van Volkenburgh E, Clelamd RE (1988) Salinity stress inhibits bean leaf expansion by reducing turgor, not wall extensibility. Plant Physiol 88:233–237
Nguyen NT (1999) The results from Melaleuca provenance trials in Mekong delta, Vietnam. Inform Sci Technol Econ Agric Rural Dev 7:20–24 (in Vietnamese)
Nguyen NT, Nakabayashi K, Thompson J, Fujita K (2003a) Role of exudation of organic acids and phosphate in aluminum tolerance of four tropical woody species. Tree Physiol 23:1041–1050
Nguyen TN, Mohapatra PK, Fujita K (2003b) Leaf necrosis is a visual symptom of the shift from growth stimulation to inhibition effect of Al in Eucalyptus camaldulensis. Plant Sci 165:147–157. doi:10.1016/S0168-9452(03)00153-5
Nguyen TN, Morhaieb REA, Saneoka H, Fujita K (2004) RAPD markers associated with salt tolerance in Acacia auriculiformis and Acacia mangium. Plant Sci 167:797–805. doi:10.1016/j.plantsci.2004.05.016
Nguyen TN, Dudzinski MJ, Mohapatra PK, Fujita K (2005a) Distribution of accumulated aluminum and changes in cell wall polysaccharides in Eucalyptus camaldulensis and Melaleuca cajuputi under aluminum stress. Soil Sci Plant Nutr 51:737–740. doi:10.1111/j.1747-0765.2005.tb00103.x
Nguyen TN, Ngo DH, Fujita K (2005b) Iron enhances aluminum-induced leaf necrosis and plant growth inhibition in Eucalyptus camaldulensis. Plant Soil 277:139–152. doi:10.1007/s11104-005-6516-6
Nicholls RJ, Wong PP, Burkett VR, Codignotto JO, Hay JE, McLean RF, Ragoonaden S, Woodroffe CD (2007) Coastal systems and low-lying areas. In: Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (eds) Climate change 2007: impacts. Adaptation and vulnerability. Contribution of Working Group II to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 315–356
Niknam SR, McComb J (2000) Salt tolerance screening of selected Australian woody species—a review. For Ecol Manage 139:1–19
Okubo S, Takeuchi K, Chakranon B, Jongskul A (2003) Land characteristics and plant resources in relation to agricultural land-use planning in a humid tropical strand plain, southeastern Thailand. Landsc Urban Plan 65:133–148. doi:10.1016/S0169-2046(03)00011-2
Osaki M, Watanabe T, Ishizawa T, Nilnond C, Nuyim T, Shinano T, Urayama M, Tuah SJ (2003) Nutritional characteristics of the leaves of native plants growing in adverse soils of humid tropical lowlands. Plant Foods Hum Nutr 58:93–115. doi:10.1023/A:1024415203690
Pang CH, Wang BS (2008) Oxidative stress and salt tolerance in plants. In: Lüttge U, Beyschlag W, Murata J (eds) Progress in Botany, vol 69. Springer, Berlin, pp 231–245
Pengnoo A, Hashidoko Y, Onthong J, Gimsanguan S, Sae-ong M, Shinano T, Watanabe T, Osaki M (2007) Screening of phosphate-solubilizing microorganisms in rhizosphere and rhizoplane of adverse soil-adapting plants in Southern Thailand. Tropics 16:1–7. doi:10.3759/tropics.16.1
Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 116:409–418. doi:10.1104/pp.116.1.409
Sam DD, Binh NN (1999) Evaluation of potential use of forest land in the Mekong river delta. Agriculture publishing house, Hanoi
Scheepers D, Eloy MD, Briquet M (1997) Use of RAPD patterns for clone verification and in studying provenance relationships in Norway spruce (Picea abies). Theor Appl Genet 94:480–485. doi:10.1007/s001220050440
Schiliro E, Predieri S, Bertaccini AC (2001) Use of Random Amplified Polymorphic DNA analysis to detect genetic variation in Pyrus species. Plant Mol Biol Rep 19:271a–271h. doi:10.1007/BF02772900
Schmohl N, Horst WJ (2000) Cell wall pectin content modulates aluminium sensitivity of Zea mays (L.) cells grown in suspension culture. Plant Cell Environ 23:735–742. doi:10.1046/j.1365-3040.2000.00591.x
Schmohl N, Pilling J, Fisahn J, Horst WJ (2000) Pectin methylesterase modulates aluminium sensitivity in Zea mays and Solanum tuberosum. Physiol Plant 109:419–427. doi:10.1034/j.1399-3054.2000.100408.x
Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Asako K, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi S, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292. doi:10.1046/j.1365-313X.2002.01359.x
Shedletzky E, Shmuel M, Trainin T, Kalman S, Delmer D (1992) Cell wall structure in cells adapted to growth on the cellulose-synthesis inhibitor 2, 6-dichlorobenzonitile. Plant Physiol 100:120–130
Sivaguru M, Balu_ka F, Volkmann D, Felle HH, Horst WJ (1999) Impacts of aluminium on the cytoskeleton of the maize root apex. Short-term effects on the distal part of the transition zone. Plant Physiol 119:1073–1082. doi:10.1104/pp.119.3.1073
van der Moezel PG, Pearce-Pinto GVN, Bell DT (1991) Screening for salt and waterlogging tolerance in Eucalyptus and Melaleuca species. For Ecol Manage 40:27–37
White I (2002) Water management in the Mekong delta: changes, conflicts and opportunities, technical documents in hydrology, no. 61. UNESCO, Paris
Williams ER, Matheson AC (1994) Experimental design and analysis for use in tree improvement. CSIRO-ACIAR, Melbourne
Yamamoto Y, Hachiya A, Matsumoto H (1997) Oxidative damage to membranes by a combination of aluminum and iron in suspension-cultured tobacco cells. Plant Cell Physiol 38:1333–1339
Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H (2002) Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiol 128:63–72. doi:10.1104/pp.010417
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273. doi:10.1146/annurev.arplant.53.091401.143329
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S. Linder.
Rights and permissions
About this article
Cite this article
Nguyen, N.T., Saneoka, H., Suwa, R. et al. Provenance variation in tolerance of Melaleuca cajuputi trees to interactive effects of aluminum and salt. Trees 23, 649–664 (2009). https://doi.org/10.1007/s00468-008-0309-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-008-0309-5