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Protoplasma

, Volume 256, Issue 1, pp 181–191 | Cite as

Insight into salt tolerance mechanisms of the halophyte Achras sapota: an important fruit tree for agriculture in coastal areas

  • Md. Mezanur Rahman
  • Mohammad Golam MostofaEmail author
  • Md. Abiar Rahman
  • Md. Giashuddin Miah
  • Satya Ranjan Saha
  • M. Abdul Karim
  • Sanjida Sultana Keya
  • Munny Akter
  • Mohidul Islam
  • Lam-Son Phan TranEmail author
Original Article

Abstract

Sapota (Achras sapota), a fruit tree with nutritional and medicinal properties, is known to thrive in salt-affected areas. However, the underlying mechanisms that allow sapota to adapt to saline environment are yet to be explored. Here, we examined various morphological, physiological, and biochemical features of sapota under a gradient of seawater (0, 4, 8, and 12 dS m–1) to study its adaptive responses against salinity. Our results showed that seawater-induced salinity negatively impacted on growth-related attributes, such as plant height, root length, leaf area, and dry biomass in a dose-dependent manner. This growth reduction was positively correlated with reductions in relative water content, stomatal conductance, xylem exudation rate, and chlorophyll, carbohydrate, and protein contents. However, the salt tolerance index did not decline in proportional to the increasing doses of seawater, indicating a salt tolerance capacity of sapota. Under salt stress, ion analysis revealed that Na+ mainly retained in roots, whereas K+ and Ca2+ were more highly accumulated in leaves than in roots, suggesting a potential mechanism in restricting transport of excessive Na+ to leaves to facilitate the uptake of other essential minerals. Sapota plants also maintained an improved leaf succulence with increasing levels of seawater. Furthermore, increased accumulations of proline, total amino acids, soluble sugars, and reducing sugars suggested an enhanced osmoprotective capacity of sapota to overcome salinity-induced osmotic stress. Our results demonstrate that the salt adaptation strategy of sapota is attributed to increased leaf succulence, selective transport of minerals, efficient Na+ retention in roots, and accumulation of compatible solutes.

Keywords

Halophytes Salinity Ion homeostasis Photosynthesis Proline 

Notes

Acknowledgements

The authors sincerely acknowledge the constructive suggestions of Prof. Dr. Qazi Abdul Khaliq, Department of Agronomy, BSMRAU during manuscript preparation. The authors are also grateful to the Department of Agronomy, BSMRAU for providing the LI-6400XT portable photosynthesis system.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abideen Z, Koyro HW, Huchzermeyer B, Ahmed MZ, Gul B, Khan MA (2014) Moderate salinity stimulates growth and photosynthesis of Phragmites karka by water relations and tissue specific ion regulation. Environ Exp Bot 105:70–76CrossRefGoogle Scholar
  2. Acosta-Motos JR, Ortuño MF, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA (2017) Plant responses to salt stress: adaptive mechanisms. Agronomy 7:1–38CrossRefGoogle Scholar
  3. Akhter N, Hossainn F, Karim A (2013) Influence of calcium on water relation of two cultivars of wheat under salt stress. Int J Env 2:1–8CrossRefGoogle Scholar
  4. Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190CrossRefGoogle Scholar
  5. Bağci SA, Ekiz H, Yilmaz A (2003) Determination of the salt tolerance of some barley genotypes and the characteristics affecting tolerance. Turk J Agric For 27:253–260Google Scholar
  6. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  7. Bazzaz MM, Hossain MA (2015) Plant water relations and proline accumulations in soybean under salt and water stress environment. J Plant Sci 3:272–278Google Scholar
  8. Bhusan D, Das DK, Hossain M, Murata Y, Hoque MA (2016) Improvement of salt tolerance in rice (Oryza sativa L.) by increasing antioxidant defense systems using exogenous application of proline. Aus J Crop Sci 10:50Google Scholar
  9. Borah KD, Bhuyan J (2017) Magnesium porphyrins with relevance to chlorophylls. Dalton Trans 46:6497–6509CrossRefGoogle Scholar
  10. Dawood MG, Taie HAA, Nassar RMA, Abdelhamid MT, Schmidhalter U (2014) The changes induced in the physiological, biochemical and anatomical characteristics of Vicia faba by the exogenous application of proline under seawater stress. S Afr J Bot 93:54–63CrossRefGoogle Scholar
  11. Demidchik V, Straltsova D, Medvedev SS, Pozhvanov GA, Sokolik A, Yurin V (2014) Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment. J Exp Bot 65:1259–1270CrossRefGoogle Scholar
  12. Delf EM (1912) Transpiration in succulent plants. Ann Bot 26:409–440CrossRefGoogle Scholar
  13. Duarte B, Sleimi N, Caçador I (2014) Biophysical and biochemical constraints imposed by salt stress: learning from halophytes. Front Plant Sci 5:746CrossRefGoogle Scholar
  14. DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356CrossRefGoogle Scholar
  15. Flowers TJ, Colmer TD (2015) Plant salt tolerance: adaptations in halophytes. Ann Bot 115:327–331CrossRefGoogle Scholar
  16. Flowers TJ, Munns R, Colmer TD (2015) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Ann Bot 115:419–431CrossRefGoogle Scholar
  17. Gengmao Z, Quanmei S, Yu H, Shihui L, Changhai W (2014) The physiological and biochemical responses of a medicinal plant (Salvia miltiorrhiza L.) to stress caused by various concentrations of NaCl. PloS One 9:e89624CrossRefGoogle Scholar
  18. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefGoogle Scholar
  19. Gururani MA, Venkatesh J, Tran LSP (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant 8:1304–1320CrossRefGoogle Scholar
  20. Hanin M, Ebel C, Ngom M, Laplaze L, Masmoudi K (2016) New insights on plant salt tolerance mechanisms and their potential use for breeding. Front Plant Sci 7:1787CrossRefGoogle Scholar
  21. Hasegawa M (2013) Sodium (Na+) homeostasis and salt tolerance of plants. Environ Exp Bot 92:19–31CrossRefGoogle Scholar
  22. Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Sig Behav 7(11):1456–1466CrossRefGoogle Scholar
  23. Hossain MM, Paul DK, Rahim MA (2016) Physico-chemical changes during growth and development of sapota fruit (Manilkara achras mill.). Turkish J Agric Natural Sci 3:58–63Google Scholar
  24. Kishor K, Polavarapu B, Sreenivasulu N (2014) Is proline accumulation per se correlated with stress tolerance or is proline homeostasis a more critical issue? Plant Cell Environ 37:300–311CrossRefGoogle Scholar
  25. Koyro HW, Hussain T, Huchzermeyer B, Khan MA (2013) Photosynthetic and growth responses of a perennial halophytic grass Panicum turgidum to increasing NaCl concentrations. Environ Exper Bot 91:22–29CrossRefGoogle Scholar
  26. Kumari AD, Parida AK, Agarwal K (2015) Proteomics metabolomics and ionomics perspectives of salinity tolerance in halophytes. Front Plant Sci 6:537CrossRefGoogle Scholar
  27. Lal R (2016) Feeding 11 billion on 0.5 billion hectare of area under cereal crops. Food Energy Secur 5:239–251CrossRefGoogle Scholar
  28. Lee YP, Takahashi T (1966) An improved colorimetric determination of amino acids with the use of ninhydrin. Anal Biochem 14:71–77CrossRefGoogle Scholar
  29. Liu Y, He C (2017) A review of redox signaling and the control of MAP kinase pathway in plants. Redox Biol 11:192–204CrossRefGoogle Scholar
  30. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275Google Scholar
  31. Lu Y, Lei J, Zeng F (2016) NaCl salinity-induced changes in growth, photosynthetic properties, water status and enzymatic antioxidant system of Nitraria roborowskii Kom. Pak J Bot 48:843–851Google Scholar
  32. Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 78:389–398CrossRefGoogle Scholar
  33. Mansour MMF, Ali EF (2017) Evaluation of proline functions in saline conditions. Phytochemistry 140:52–68CrossRefGoogle Scholar
  34. Meng N, Yu BJ, Guo JS (2016) Ameliorative effects of inoculation with Bradyrhizobium japonicum on Glycine max and Glycine soja plants under salt stress. Plant Growth Regul 80:137–147CrossRefGoogle Scholar
  35. Misratia KM, Ismail MR, Hakim MA, Musa MH, Puteh A (2013) Effect of salinity and alleviating role of gibberellic acid (GA3) for improving the morphological, physiological and yield traits of rice varieties. Aus J Crop Sci 7:1682Google Scholar
  36. Mostofa MG, Saegusa D, Fujita M, Tran L-SP (2015) Hydrogen sulfide regulates salt tolerance in rice by maintaining Na+/K+ balance, mineral homeostasis and oxidative metabolism under excessive salt stress. Front Plant Sci 6:1055CrossRefGoogle Scholar
  37. Muchate NS, Nikalje GC, Rajurkar NS, Suprasanna P, Nikam TD (2016) Physiological responses of the halophyte Sesuvium portulacastrum to salt stress and their relevance for saline soil bio-reclamation. Flora 224:96–105CrossRefGoogle Scholar
  38. Murty KS, Majumder SK (1962) Modifications of the technique for determination of chlorophyll stability index in relation to studies of drought resistance in rice. Curr Sci 31:470–471Google Scholar
  39. Nedjimi B (2011) Is salinity tolerance related to osmolytes accumulation in Lygeum spartum L. seedlings? J Saudi Soc Agril Sci 10:81–87Google Scholar
  40. Nishida K, Khan NM, Shiozawa S (2009) Effects of salt accumulation on the leaf water potential and transpiration rate of pot-grown wheat with a controlled saline groundwater table. Soil Sci Plant Nutr 55:375–384CrossRefGoogle Scholar
  41. Neelam S, Subramanyam R (2013) Alteration of photochemistry and protein degradation of photosystem II from Chlamydomonas reinhardtii under high salt grown cells. J Photochem Photobiol 124:63–70CrossRefGoogle Scholar
  42. Osman MA, Rashid MM, Aziz MA, Habib MR (2011) Inhibition of Ehrlich ascites carcinoma by Manilkara zapota L. stem bark in Swiss albino mice. Asian Pac J Trop Biomed 1:448–451CrossRefGoogle Scholar
  43. Pan YQ, Guo H, Wang SM, Zhao B, Zhang JL, Ma Q, Yin HJ, Bao AK (2016) The photosynthesis, Na+/K+ homeostasis and osmotic adjustment of Atriplex canescens in response to salinity. Front Plant Sci 7:848Google Scholar
  44. Panta S, Flowers T, Lane P, Doyle R, Haros G, Shabala S (2014) Halophyte agriculture: success stories. Environ Exp Bot 107:71–83CrossRefGoogle Scholar
  45. Parida AK, Jha B (2013) Inductive responses of some organic metabolites for osmotic homeostasis in peanut (Arachis hypogaea L.) plants during salt stress. Acta Physiol Plant 35:2821–2832CrossRefGoogle Scholar
  46. Parida AK, Veerabathini SK, Kumari A, Agarwal PK (2016) Physiological, anatomical and metabolic implications of salt tolerance in the halophyte Salvadora persica under hydroponic culture condition. Front Plant Sci 7:351CrossRefGoogle Scholar
  47. Pottosin I, Shabala S (2014) Polyamines control of cation transport across plant membranes: implications for ion homeostasis and abiotic stress signaling. Front Plant Sci 5:154CrossRefGoogle Scholar
  48. Qadir M, Quillérou E, Nangia V, Murtaza G, Singh M, Thomas RJ, Drechsel P, Noble AD (2014) Economics of salt–induced land degradation and restoration. Nat Resour Forum 38:282–295CrossRefGoogle Scholar
  49. Rahman MM, Haque MA, Nihad SAI, Akand MMH, Howlader MRA (2016) Morpho-physiological response of Acacia auriculiformis as influenced by seawater induced salinity stress. For Syst 25:e071Google Scholar
  50. Rahman MM, Rahman MA, Miah MG, Saha SR, Karim MA, Mostofa MG (2017) Mechanistic insight into salt tolerance of Acacia auriculiformis: the importance of ion selectivity, osmoprotection, tissue tolerance, and Na+ exclusion. Front Plant Sci 8:155Google Scholar
  51. Rajput VD, Minkina T, Yaning C, Sushkova S, Chapligin VA, Mandzhieva S (2016) A review on salinity adaptation mechanism and characteristics of Populus euphratica, a boon for arid ecosystems. Acta Ecol Sin 36:497–503CrossRefGoogle Scholar
  52. Rangani J, Parida AK, Panda A, Kumari A (2016) Coordinated changes in antioxidative enzymes protect the photosynthetic machinery from salinity induced oxidative damage and confer salt tolerance in an extreme halophyte Salvadora persica L. Front Plant Sci 7:50CrossRefGoogle Scholar
  53. Rabhi M, Castagna A, Remorini D, Scattino C, Smaoui A, Ranieri A, Abdelly C (2012) Photosynthetic responses to salinity in two obligate halophytes: Sesuvium portulacastrum and Tecticornia indica. S Afr J Bot 79:39–47CrossRefGoogle Scholar
  54. Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell 14:S185–S205CrossRefGoogle Scholar
  55. Roni MS, Zakaria M, Hossain MM, Siddiqui MN (2014) Effect of plant spacing and nitrogen levels on nutritional quality of broccoli (Brassica oleracea L.). Bangladesh J Agril Res 39:491–504CrossRefGoogle Scholar
  56. Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571CrossRefGoogle Scholar
  57. Santos CV (2004) Regulation of chlorophyll biosynthesis and degradation by salt stress in sunflower leaves. Sci Hort 103:93–99CrossRefGoogle Scholar
  58. Santos J, Al-Azzawi M, Aronson J, Flowers TJ (2016) eHALOPH a database of salt–tolerant plants: helping put halophytes to work. Plant Cell Physiol 57(1):e10CrossRefGoogle Scholar
  59. Shabala L, Mackay A, Tian Y, Jacobsen SE, Zhou D, Shabala S (2012) Oxidative stress protection and stomatal patterning as components of salinity tolerance mechanism in quinoa (Chenopodium quinoa). Physiol Plant 146:26–38CrossRefGoogle Scholar
  60. Shabala S (2013) Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Ann Bot 112:1209–1221CrossRefGoogle Scholar
  61. Shaheen S, Naseer S, Ashraf M, Akram NA (2013) Salt stress affects water relations, photosynthesis, and oxidative defense mechanisms in Solanum melongena L. J Plant Interact 8:85–96CrossRefGoogle Scholar
  62. Siddiqui MN, Mostofa MG, Akter MM, Srivastava AK, Sayed MA, Hasan MS, Tran LSP (2017) Impact of salt-induced toxicity on growth and yield-potential of local wheat cultivars: oxidative stress and ion toxicity are among the major determinants of salt-tolerant capacity. Chemosphere 187:385–394CrossRefGoogle Scholar
  63. Slama I, Abdelly C, Bouchereau A, Flowers T, Savouré A (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann Bot 115:433–447CrossRefGoogle Scholar
  64. Somogyi M (1952) Notes on sugar determination. J Biol Chem 195:19–23Google Scholar
  65. Song J, Wang B (2015) Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Ann Bot 115:541–553CrossRefGoogle Scholar
  66. Srivastava M, Hegde M, Chiruvella KK, Koroth J, Bhattacharya S, Choudhary B, Raghavan SC (2014) Sapodilla plum (Achras sapota) induces apoptosis in cancer cell lines and inhibits tumor progression in mice. Sci Rep 4:6147CrossRefGoogle Scholar
  67. Suárez N, Sobrado MA (2000) Adjustments in leaf water relations of mangrove (Avicennia germinans) seedlings grown in a salinity gradient. Tree Physiol 20:277–282CrossRefGoogle Scholar
  68. Sumathi M, Shivashankar S (2017) Metabolic profiling of sapota fruit cv. Cricket ball grown under foliar nutrition, irrigation and water deficit stress. Sci Hort 215:1–8CrossRefGoogle Scholar
  69. Taïbi K, Taïbi F, Abderrahim LA, Ennajah A, Belkhodja M, Mulet JM (2016) Effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidant defence systems in Phaseolus vulgaris L. S Afr J Bot 105:306–312CrossRefGoogle Scholar
  70. Tang X, Mu X, Shao H, Wang H, Brestic M (2015) Global plant-responding mechanisms to salt stress: physiological and molecular levels and implications in biotechnology. Crit Rev Biotechnol 35:425–437CrossRefGoogle Scholar
  71. Tayebimeigooni A, Awang Y, Mahmood M, Selamat A, Wahab Z (2012) Leaf water status, proline content, lipid peroxidation and accumulation of hydrogen peroxide in salinized Chinese kale (Brassica alboglabra). J Food Agric Environ 10:371–374Google Scholar
  72. Theerawitaya C, Tisarum R, Samphumphuang T, Singh HP, Cha-Um S, Kirdmanee C (2015) Physio-biochemical and morphological characters of halophyte legume shrub, Acacia ampliceps plants in response to salt stress under greenhouse. Front Plant Sci 6:630CrossRefGoogle Scholar
  73. Vasantha S, Venkataramana S, Rao PNG, Gomathi R (2010) Long-term salinity effect on growth, photosynthesis and osmotic characteristics in sugarcane. Sugar Tech 12:5–8CrossRefGoogle Scholar
  74. Wang CM, Zhang JL, Liu XS, Li Z, Wu GQ, Cai JY, Flowers TJ, Wang SM (2009) Puccinellia tenuiflora maintains a low Na+ level under salinity by limiting unidirectional Na+ influx resulting in a high selectivity for K+ over Na+. Plant Cell Environ 32:486–496CrossRefGoogle Scholar
  75. Wang J, Meng Y, Li B, Ma X, Lai Y, Si E, Yang K, Xu X, Shang X, Wang H, Wang D (2015) Physiological and proteomic analyses of salt stress response in the halophyte Halogeton glomeratus. Plant Cell Environ 38:655–669CrossRefGoogle Scholar
  76. Wang T, Yang W, Xie Y, Shi D, Ma Y, Sun X (2017) Effects of exogenous nitric oxide on the photosynthetic characteristics of bamboo (Indocalamus barbatus McClure) plants under acid rain stress. Plant Growth Regul 82:69–78CrossRefGoogle Scholar
  77. Yu J, Chen S, Zhao Q, Wang T, Yang C, Diaz C, Sun G, Dai S (2011) Physiological and proteomic analysis of salinity tolerance in Puccinellia tenuiflora. J Proteome Res 10:3852–3870CrossRefGoogle Scholar
  78. Yuan F, Leng B, Wang B (2016) Progress in studying salt secretion from the salt glands in Recretohalophytes: how do plants secrete salt? Front Plant Sci 7:977Google Scholar
  79. Zhang L, Gao M, Shengxiu L, Ashok AL, Ashraf M (2014) Potassium fertilization mitigates the adverse effects of drought on selected Zea mays cultivars. Turk J Bot 38:713–723CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Agroforestry and EnvironmentBangabandhu Sheikh Mujibur Rahman Agricultural UniversityGazipurBangladesh
  2. 2.Department of Biochemistry and Molecular BiologyBangabandhu Sheikh Mujibur Rahman Agricultural UniversityGazipurBangladesh
  3. 3.Department of AgronomyBangabandhu Sheikh Mujibur Rahman Agricultural UniversityGazipurBangladesh
  4. 4.Hill Agricultural Research StationRangamati Hill DistrictBangladesh
  5. 5.Plant Stress Research Group & Faculty of Applied SciencesTon Duc Thang UniversityHo Chi Minh CityVietnam
  6. 6.Stress Adaptation Research UnitRIKEN Center for Sustainable Resource ScienceYokohamaJapan

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