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

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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.

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References

  • 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 105:70–76

    Article  CAS  Google Scholar 

  • 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 7:1–38

    Article  CAS  Google Scholar 

  • Akhter N, Hossainn F, Karim A (2013) Influence of calcium on water relation of two cultivars of wheat under salt stress. Int J Env 2:1–8

    Article  Google Scholar 

  • Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190

    Article  CAS  Google Scholar 

  • 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 27:253–260

    Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bazzaz MM, Hossain MA (2015) Plant water relations and proline accumulations in soybean under salt and water stress environment. J Plant Sci 3:272–278

    Google Scholar 

  • 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 10:50

    CAS  Google Scholar 

  • Borah KD, Bhuyan J (2017) Magnesium porphyrins with relevance to chlorophylls. Dalton Trans 46:6497–6509

    Article  CAS  PubMed  Google Scholar 

  • 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 93:54–63

    Article  CAS  Google Scholar 

  • 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 65:1259–1270

    Article  CAS  PubMed  Google Scholar 

  • Delf EM (1912) Transpiration in succulent plants. Ann Bot 26:409–440

    Article  Google Scholar 

  • Duarte B, Sleimi N, Caçador I (2014) Biophysical and biochemical constraints imposed by salt stress: learning from halophytes. Front Plant Sci 5:746

    Article  PubMed  PubMed Central  Google Scholar 

  • DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Flowers TJ, Colmer TD (2015) Plant salt tolerance: adaptations in halophytes. Ann Bot 115:327–331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flowers TJ, Munns R, Colmer TD (2015) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Ann Bot 115:419–431

    Article  CAS  PubMed  Google Scholar 

  • 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:e89624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Gururani MA, Venkatesh J, Tran LSP (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant 8:1304–1320

    Article  CAS  PubMed  Google Scholar 

  • 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 7:1787

    Article  PubMed  PubMed Central  Google Scholar 

  • Hasegawa M (2013) Sodium (Na+) homeostasis and salt tolerance of plants. Environ Exp Bot 92:19–31

    Article  CAS  Google Scholar 

  • 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):1456–1466

    Article  CAS  Google Scholar 

  • 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 3:58–63

    Google Scholar 

  • 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 37:300–311

    Article  CAS  Google Scholar 

  • 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 91:22–29

    Article  CAS  Google Scholar 

  • Kumari AD, Parida AK, Agarwal K (2015) Proteomics metabolomics and ionomics perspectives of salinity tolerance in halophytes. Front Plant Sci 6:537

    Article  PubMed  PubMed Central  Google Scholar 

  • Lal R (2016) Feeding 11 billion on 0.5 billion hectare of area under cereal crops. Food Energy Secur 5:239–251

    Article  Google Scholar 

  • Lee YP, Takahashi T (1966) An improved colorimetric determination of amino acids with the use of ninhydrin. Anal Biochem 14:71–77

    Article  CAS  Google Scholar 

  • Liu Y, He C (2017) A review of redox signaling and the control of MAP kinase pathway in plants. Redox Biol 11:192–204

    Article  CAS  PubMed  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • 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 48:843–851

    CAS  Google Scholar 

  • Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 78:389–398

    Article  CAS  Google Scholar 

  • Mansour MMF, Ali EF (2017) Evaluation of proline functions in saline conditions. Phytochemistry 140:52–68

    Article  CAS  PubMed  Google Scholar 

  • 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 80:137–147

    Article  CAS  Google Scholar 

  • 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 7:1682

    Google Scholar 

  • 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 6:1055

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 224:96–105

    Article  Google Scholar 

  • 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 31:470–471

    Google Scholar 

  • Nedjimi B (2011) Is salinity tolerance related to osmolytes accumulation in Lygeum spartum L. seedlings? J Saudi Soc Agril Sci 10:81–87

    CAS  Google Scholar 

  • 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 55:375–384

    Article  Google Scholar 

  • 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 124:63–70

    Article  CAS  Google Scholar 

  • 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 1:448–451

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 7:848

    PubMed  PubMed Central  Google Scholar 

  • Panta S, Flowers T, Lane P, Doyle R, Haros G, Shabala S (2014) Halophyte agriculture: success stories. Environ Exp Bot 107:71–83

    Article  Google Scholar 

  • 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 35:2821–2832

    Article  CAS  Google Scholar 

  • 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 7:351

    Article  PubMed  PubMed Central  Google Scholar 

  • Pottosin I, Shabala S (2014) Polyamines control of cation transport across plant membranes: implications for ion homeostasis and abiotic stress signaling. Front Plant Sci 5:154

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 38:282–295

    Article  Google Scholar 

  • 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:e071

    Google Scholar 

  • 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 8:155

    PubMed  PubMed Central  Google Scholar 

  • 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 36:497–503

    Article  Google Scholar 

  • 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 7:50

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 79:39–47

    Article  CAS  Google Scholar 

  • Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell 14:S185–S205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 39:491–504

    Article  Google Scholar 

  • Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571

    Article  PubMed  PubMed Central  Google Scholar 

  • Santos CV (2004) Regulation of chlorophyll biosynthesis and degradation by salt stress in sunflower leaves. Sci Hort 103:93–99

    Article  CAS  Google Scholar 

  • 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):e10

    Article  CAS  PubMed  Google Scholar 

  • 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 146:26–38

    Article  CAS  PubMed  Google Scholar 

  • Shabala S (2013) Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Ann Bot 112:1209–1221

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 8:85–96

    Article  CAS  Google Scholar 

  • 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 187:385–394

    Article  CAS  PubMed  Google Scholar 

  • 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 115:433–447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Somogyi M (1952) Notes on sugar determination. J Biol Chem 195:19–23

    CAS  Google Scholar 

  • Song J, Wang B (2015) Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Ann Bot 115:541–553

    Article  CAS  PubMed  Google Scholar 

  • 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 4:6147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suárez N, Sobrado MA (2000) Adjustments in leaf water relations of mangrove (Avicennia germinans) seedlings grown in a salinity gradient. Tree Physiol 20:277–282

    Article  PubMed  Google Scholar 

  • Sumathi M, Shivashankar S (2017) Metabolic profiling of sapota fruit cv. Cricket ball grown under foliar nutrition, irrigation and water deficit stress. Sci Hort 215:1–8

    Article  CAS  Google Scholar 

  • 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 105:306–312

    Article  CAS  Google Scholar 

  • 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 35:425–437

    Article  CAS  PubMed  Google Scholar 

  • 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 10:371–374

    CAS  Google Scholar 

  • 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 6:630

    Article  PubMed  PubMed Central  Google Scholar 

  • Vasantha S, Venkataramana S, Rao PNG, Gomathi R (2010) Long-term salinity effect on growth, photosynthesis and osmotic characteristics in sugarcane. Sugar Tech 12:5–8

    Article  CAS  Google Scholar 

  • 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 32:486–496

    Article  CAS  PubMed  Google Scholar 

  • 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 38:655–669

    Article  CAS  PubMed  Google Scholar 

  • 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 82:69–78

    Article  CAS  Google Scholar 

  • 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 10:3852–3870

    Article  CAS  PubMed  Google Scholar 

  • 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 7:977

    PubMed  PubMed Central  Google Scholar 

  • 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 38:713–723

    Article  CAS  Google Scholar 

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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.

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Authors and Affiliations

  1. Department of Agroforestry and Environment, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, 1706, Bangladesh

    Md. Mezanur Rahman, Md. Abiar Rahman, Md. Giashuddin Miah, Satya Ranjan Saha & Sanjida Sultana Keya

  2. Department of Biochemistry and Molecular Biology, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, 1706, Bangladesh

    Mohammad Golam Mostofa

  3. Department of Agronomy, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, 1706, Bangladesh

    M. Abdul Karim & Munny Akter

  4. Hill Agricultural Research Station, Raikhali, Rangamati Hill District, Bangladesh

    Mohidul Islam

  5. Plant Stress Research Group & Faculty of Applied Sciences, Ton Duc Thang University, Ho Chi Minh City, Vietnam

    Lam-Son Phan Tran

  6. Stress Adaptation Research Unit, RIKEN Center for Sustainable Resource Science, Yokohama, Japan

    Lam-Son Phan Tran

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  1. Md. Mezanur Rahman
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  2. Mohammad Golam Mostofa
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Correspondence to Mohammad Golam Mostofa or Lam-Son Phan Tran.

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Rahman, M.M., Mostofa, M.G., Rahman, M.A. et al. Insight into salt tolerance mechanisms of the halophyte Achras sapota: an important fruit tree for agriculture in coastal areas. Protoplasma 256, 181–191 (2019). https://doi.org/10.1007/s00709-018-1289-y

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