Abstract
Pterocarpus officinalis (Fabaceae) dominates in the swamp forests of the Lesser Antilles, submitted to strong variations of soil salinity (30–445 mM). This study aimed to assess the effect of salinity on growth, nodulation, N2 fixation, water status and ions content in P. officinalis and to clarify the mechanisms involved. Seedlings inoculated or not with two strains from areas of contrasting salinity levels (< to 50 or 445 mM) were watered with 0, 171 and 342 mM solutions of NaCl in greenhouse conditions. Non-inoculated seedlings were tolerant to a salinity of 171 mM, with no significant effect on seedling biomass. Evapotranspiration per unit of leaf area (E/TLa) remained unchanged at 171 mM. Maintenance of a constant E/TLa and especially the control of ion transport to the upper parts of the plant could explain seedling salt tolerance up to intermediate salinity conditions (171 mM). The two strains have a 99.8% genetic identity in spite of differences in their original habitats, this explaining the similar response of the symbiosis to salinity. The higher salt sensitivity of inoculated seedlings was linked to the sensitivity of both Bradyrhizobium strains (reduction of free-living cells) and to that of the nodulation process (fewer nodules and inhibition of N2-fixation) to intermediate salinity.
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References
Anthraper A, Dubois JD (2003) The effect of NaCl on growth, N2 fixation (acetylene reduction), and percentage total nitrogen in Leucaena leucocephala (Leguminosae). Am J Bot 90:683–692
Azevedo Neto AD, Prisco JT, Enéas Filho J, Lacerda CF, Silva JV, Costa PHA, Gomes Filho E (2004) Effects of salt stress on plant growth, stomatal response and solute accumulation of different maize genotypes. Braz J Plant Physiol 16:31–38
Bâ AM, Samba R, Sylla SN, Le Roux C, Neyra M, Rousteau A, Imbert D, Toribio A (2004) Characterization of the diversity of symbiotic microorganisms in Pterocarpus officinalis in swamp forests of Guadeloupe and Martinique. Rev Ecol 59:163–170
Bolaños L, Martín M, El-Hamdaoui A, Rivilla R, Bonilla I (2006) Nitrogenase inhibition in nodules from Pea plants grown under salt stress occurs at the physiological level and can be alleviated by B and Ca. Plant Soil 280:135–142
Bonhême I, Imbert D, Rousteau A, Saur E (1998) La forêt marécageuse à Pterocarpus officinalis. Sa situation en Guadeloupe. Bois Forêt Trop 258:59–68
Cheeseman JM (1988) Mechanisms of Salinity Tolerance. Plant Physiol 87:547–550
Cintrón G, Lugo A, Pool D, Morris G (1978) Mangroves of Arid Environments in Puerto Rico and Adjacent Islands. Biotropica 10:110–121
Conner WH, McLeod KW, McCarron JK (1997) Flooding and salinity effects on growth and survival of four common forested wetland species. Wetl Ecol Manage 5:99–109
Craig GF, Atkins CA, Bell DT (1991) Effect of salinity on growth of four strains of Rhizobium and their infectivity and effectiveness on two species of Acacia. Plant Soil 133:253–262
Cramer GR (2003) Differential effects of salinity on leaf elongation kinetics of three grass species. Plant Soil 253:233–244
De Lacerda CF, Cambraia J, Oliva MA, Ruiz HA, Prisco JT (2003) Solute accumulation and distribution during shoot and leaf development in two sorghum genotypes under salt stress. Environ Exp Bot 49:107–120
Del Pilar Cordovilla M, Ligero F, Lluch C (1999) Effects of salinity on growth, nodulation and nitrogen assimilation in nodules of faba bean (Vicia faba L.). Appl Soil Ecol 11:1–7
Eusse AM, Aide TM (1999) Patterns of litter production across a salinity gradient in a Pterocarpus officinalis tropical wetland. Plant Ecol 145:307–315
Fougnies L, Renciot S, Muller F, Plenchette C, Prin Y, de Faria SM, Bouvet JM, Nd SS, Dreyfus B, Bâ A (2007) Arbuscular mycorrhizal colonization and nodulation improve flooding tolerance in Pterocarpus officinalis Jacq. seedlings. Mycorrhiza 17:159–66
Högberg P, Kvarnström M (1982) Nitrogen fixation by the woody legume Leucaena leucocephala in Tanzania. Plant Soil 66:21–28
Imbert D, Portecop J (1986) Etude de la production de litière dans la mangrove de Guadeloupe (Antilles Françaises). Oecol Plant 7:379–396
Imbert D, Bonhême I, Saur E, Bouchon C (2000) Floristics and structure of Pterocarpus officinalis swamp forest in Guadeloupe, Lesser Antilles. J Trop Ecol 16:55–68
Lemaire G (1997) Diagnosis of the nitrogen status in crops. Springler-Verlag, Heidelberg, Berlin
Liang S, Zhou R, Dong S, Shi S (2008) Adaptation to salinity in mangroves: Implication on the evolution of salt-tolerance. Chin Sci Bull 53:1708–1715
López-Hoffman L, Anten N, Martínez-Ramos M, Ackerly D (2007) Salinity and light interactively affect neotropical mangrove seedlings at the leaf and whole plant levels. Oecologia 150:545–556
Lugo AE (1990) Introduction. In: Lugo AE, Brinson M, Broxn S (eds) Forest wetland: Ecosystems of the world 15. Elsevier Science Publisher, Amsterdam, pp 1–14
Lugo AE, Medina E, Cuevas E, Cintron G, Laboy Nieves EN, Novelli YS (2007) Ecophysiology of a Mangrove Forest in Jobos Bay, Puerto Rico. Caribb J Sci 43:200–219
Medina E, Cuevas E, Lugo A (2007) Nutrient and salt relations of Pterocarpus officinalis L. in coastal wetlands of the Caribbean: assessment through leaf and soil analyses. Trees 21:321–327
Medina E, Francisco M, Quilice A (2008) Isotopic signatures and nutrient relations of plants inhabiting brackish wetlands in the north eastern coastal plain of Venezuela. Wetl Ecol Manage 16:51–64
Mendes MM, Gazariniet LC, Rodrigues ML (2001) Acclimation of Myrtus communis to contrasting Mediterranean light environments—effects on structure and chemical composition of foliage and plant water. Environ and Exp Bot 45:165–178
Muller F, Voccia M, Bâ A, Bouvet J-M (2009) Genetic diversity and gene flow in a Caribbean tree Pterocarpus officinalis Jacq.: a study based on chloroplast and nuclear microsatellites. Genetica 135:185–198
Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250
Munns R (2005) Genes and salt tolerance: bringing them together. New phytologist 167:45–663
Munns R, Husain S, Rivelli AR, James RA, Condon AG, Lindsay MP, Lagudah ES, Schachtma DP, Hare RA (2002) Avenues for increasing salt tolerance of crops, and the role of physiologically based selection traits. Plant Soil 247:93–105
Nicholls RJ, Hoozemans FMJ, Marchand M (1999) Increasing flood risk and wetland losses due to global sea-level rise: Regional and global analyses. Global Environ Change 9:69–87
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349
Parida AK, Das AB, Mittra B (2004) Effects of salt on growth, ion accumulation, photosynthesis and leaf anatomy of the mangrove, Bruguiera parviflora. Trees 18:167–174
Rao DLN, Giller KE, Yeo AR, Flowers TJ (2002) The effects of salinity and sodicity upon nodulation and nitrogen fixation in Chickpea (Cicer arietinum). Ann Bot 89:563–570
Ritchie GA, Hinckley TM (1975) The pressure chamber as an instrument for ecological research. Adv Ecol Res 9:165–254
Rivera-Ocasio E, Aide M, McMillan W (2002) Patterns of genetic diversity and biogeographical history of the tropical wetland tree, Pterocarpus officinalis (Jacq.), in the Caribbean basin. Mol Ecol 11:675–684
Rivera-Ocasio E, Aide M, Rios-Lopez N (2007) The effects of salinity on the dynamics of a Pterocarpus forest stand in Puerto Rico. J Trop Ecol 23:559–568
Saint-Etienne S, Paul S, Imbert D, Dulormne M, Muller F, Toribio A, Plenchette C, Bâ AM (2006) Arbuscular mycorrhizal soil infectivity in a stand of the wetland tree Pterocarpus officinalis along a salinity gradient. Forest Ecol Manag 232:86–89
Salter J, Morris K, Bailey P, Boon P (2007) Interactive effects of salinity and water depth on the growth of Melaleuca ericifolia Sm (Swamp paperbark) seedlings. Aquat Bot 86:213–222
Saur E, Bohême I, Nygren P, Imbert D (1998) Nodulation of Pterocarpus officinalis in the swamp forest of Guadeloupe (Lesser Antilles). J Trop Ecol 14:761–770
Saur E, Carcelle S, Guezennec S, Rousteau A (2000) Nodulation of legume species in Wetlands of Guadeloupe (Lesser Antilles). Wetlands 20:730–734
Singleton PW, Bohlool BB (1984) Effect of Salinity on Nodule Formation by Soybean. Plant Physiol 74:72–76
Sobrado M (2005) Leaf characteristics and gas exchange of the mangrove Laguncularia racemosa as affected by salinity. Photosynthetica 43:217–221
Suárez N, Medina E (2006) Influence of salinity on Na+ and K+ accumulation, and gas exchange in Avicennia germinans. Photosynthetica 44:268–274
Sylla SN, Samba RT, Neyra M, Ndoye I, Giraud E, Willems A, deLajudie P, Dreyfus B (2002) Phenotypic and genotypic diversity of rhizobia nodulating Pterocarpus erinaceus and P. lucens in Senegal. Syst Appl Microbiol 25:572–583
Teakle NL, Flowers TJ, Real D, Colmer TD (2007) Lotus tenuis tolerates the interactive effects of salinity and waterlogging by ‘excluding’ Na+ and Cl– from the xylem. J exp bot 58:2169–2180
Vincent JM (1970) A manual for the practical study of root nodule bacteria, vol 15. Blackwell, Oxford
Walinga I, Van der Lee JJ, Houba VJG, Van Vark W, Novozamsky I (1995) Plant Analysis Manual. Kluwer Academic, Dordrecht
Wang Y, Nil N (2000) Changes in chlorophyll, ribulose biphosphate carboxylase oxygenase, glycine betaïne content, photosynthesis and transpiration in Amaranthus tricolor leaves during salt stress. J Horticult Sci Biotechnol 75:623–627
Willems A, Munive A, de Lajudie P, Gillis M (2003) In most bradyrhizobium groups sequence comparison of 16S–23S rDNA internal transcribed spacer regions corroborates DNA-DNA hybridizations. Syst Appl Microbiol 26:203–210
Zahran HH, Sprent JI (1986) Effects of sodium chloride and polyethylene glycol on root-hair infection and nodulation of Vicia faba L. plants by Rhizobium leguminosarum. Planta 167:303–309
Acknowledgments
We thank GIS ECOFOR, the Ministère de l’Ecologie et du Développement Durable (grant n° 020000118), and the Conseil Général de la Guadeloupe for financially supporting the postdoctoral fellowship of M. Dulormne. The authors are also grateful to Sandrine Durimel and Lydia Saint-Etienne for their technical help as well as to INRA Guadeloupe, in particular its Caribbean Zone Agropedoclimatic Unit (INRA Guadeloupe), for generously providing the equipment. The authors are greatly indebted to Dr. Marc Chillet (CIRAD FLHOR, Guadeloupe) for providing access to gas chromatography facilities and to Dr. Alain Rousteau (UAG) for his help in the field and his comments on the manuscript. We gratefully thank Anya Cockle-Bétian for improving the English and the anonymous reviewers for her relevant comments.
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Dulormne, M., Musseau, O., Muller, F. et al. Effects of NaCl on growth, water status, N2 fixation, and ion distribution in Pterocarpus officinalis seedlings. Plant Soil 327, 23–34 (2010). https://doi.org/10.1007/s11104-009-0066-2
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DOI: https://doi.org/10.1007/s11104-009-0066-2