Abiotic stress tolerance in mangroves with a special reference to salinity

Srinivas Acharya; Madhusmita Pradhan; Gyanranjan  Mahalik; Ram Babu; Sangeeta Parida; Pradipta Kumar Mohapatra

doi:10.14719/pst.1925

Authors

Srinivas Acharya Department of Botany, Utkal University, Bhubaneswar, Odisha, India https://orcid.org/0000-0001-6095-4840
Madhusmita Pradhan Majhighariani Institute of Technology and Science, Rayagada, Odisha, India https://orcid.org/0000-0002-9328-3622
Gyanranjan Mahalik Department of Botany, School of Applied Sciences, Centurion University of Technology and Management, Odisha, India https://orcid.org/0000-0003-4953-9982
Ram Babu Department of Botany, Kirori Mal College, University of Delhi, Delhi, India
Sangeeta Parida Department of Botany, Kalinga Institute of Social Sciences, Bhubaneswar, Odisha, India
Pradipta Kumar Mohapatra Department of Botany, Ravenshaw University, Cuttack, Odisha, India https://orcid.org/0000-0001-7435-7983

DOI:

https://doi.org/10.14719/pst.1925

Keywords:

Abiotic stress, Environmental pollutant, Mangroves, Salinity tolerance

Abstract

Since mangroves are found near extremely transitional ecosystems, they face a lot of physico-chemical perturbations. As mangroves possess a unique ecotone, they experience many abiotic stressors viz. salinity, metal, oil, humidity temperature, nutrient and a wide range of biotic interactions. Amongst all, salinity is the most important factor affecting mangrove physiology and biochemistry, and thereby regulating the organic matter contribution to the consumers underneath. Exploitation by human, being a dominant biotic interference, is above the rate at which natural replacement of mangrove vegetation occur. Mal-nutrition is a limiting factor in growth and reproduction of many mangroves whereas nutrient replenishment reduces the phytotoxicity of heavy metals. Different environmental pollutants including heavy metals, recalcitrant, cosmetics, petroleum oil and endocrine disrupters have reported impact on various mangroves and associated biota. Stress tolerance in mangroves involves various mechanism including morphological and anatomical features, osmoregulation, water use efficiency, salt secretion, salt exclusion and salt accumulation and molecular regulations. Various aspects of salt tolerance strategies of mangroves related to their growth, biochemical anatomy and physiology were reported by many researchers.

Downloads

Download data is not yet available.

References

Gibbs HK, Brown S, Niles JO, Foley JA. Monitoring and estimating tropical forest carbon stocks, making REDD a reality. Environ Res Lett. 2007;2:045023. https://doi.org/0.1088/1748-9326/2/4/045023

Li DL, Li XM, Peng ZY, Wang BG. Flavanol derivatives from Rhizophora stylosa and their DPPH radical scavenging activity. Molecules. 2007;12:1163-69. https://doi.org/10.3390/12051163

Han L, Huang X, Dahse HM, Moellmann U, Fu H, Grabley S, Sattler I, Lin W. unusal napthoquinone derivatives from the twigs of Avicennia marina. J Nat Prod. 2007;70:923-27. https://doi.org/10.1021/np060587g

Patra JK, Panigrahi TK, Rath SK, Dhal NK, Thatoi HN. Phytochemical screening and antimicrobial assessment of leaf extracts of Bhitarkanika, Orissa, Indian Adv Nat Appl Sci. 2009;3:241-46.

Acharya S, Patra DK, Pradhan C, Mohapatra PK. Anti-bacterial, anti-fungal and anti-oxidative properties of different extracts of Bruguiera gymnorrhiza L. (Mangrove). Eur J Int Med. 2020;36:101140. https://doi.org/10.1016/j.eujim.2020.101140

Rodrigues CS, Souza SS, Rezende RP, Silva A, Andrioli JL, Costa H et al. Application of denaturing gradient gel electrophoresis for detection of bacterial and yeast communities along a salinity gradient in the estuary of the Cachoeira River in Brazil. Genet Mol Res. 2013;12:1752-60. http://dx.doi.org/10.4238/2013.May.21.6

Bastami A, Kazemzadeh KJ, Esmailian M. Bioaccumulation of heavy metals in sediment and crab, Portunus pelagicus from the Persian Gulf, Iran. Mid-East J Sci Res. 2012;12:886-92.

Gan WQ, McLean K, Brauer M. Modeling population exposure to comm https://doi.org/10.1016/j.envres.2012.04.001unity noise and air pollution in a large metropolitan area. Environ Res. 2012;116:11-16. https://doi.org/10.1016/j.envres.2012.04.001

Duke NC, Ball MC, Ellison JC. Factors influencing biodiversity and distributional gradients in mangroves. Globoal Ecol Biogeogr. 1998;7:27-47. https://doi.org/10.1111/j.1466-8238.1998.00269.x

Zhang K, Liu H, Li Y, Xu H, Shen J, Rhome J et al. The role of mangroves in attenuating storm surges, Estuar. Coast Shelf S. 2012;102:11-23. https://doi.org/10.1016/j.ecss.2012.02.021

Acharya S, Patra DK, Mahalik G, Mohapatra PK. Quantitative ecological study of Rhizophoraceae mangroves of Bhitarkanika Wildlife Sanctuary regions of Odisha coast, India. Proc Natl Acad Sci India Sect B Biol Sci. 2021;91(4):897-908. https://doi.org/10.1007/s40011-021-01295-2

Cui Y, Zhang LJ, Luo XX, Zhang X. Study on the water pollution and eutrophication in the Xiaoqing River Estuary. J Ocean U China. 2013;43:60-66.

Krauss KW, Ball MC. On the halophytic nature of mangroves. Tree. 2013;27:7-11. https://doi.org/10.1007/s00468-012-0767-7

Kathiresan K, Rajendran N. Coastal mangrove forests mitigated tsunami. Estuar Coast Shelf Sci. 2005;65(3):601-06. https://doi.org/10.1016/j.ecss.2005.06.022

Parida AK, Jha B. Salt tolerance mechanisms in mangroves: a review. Trees. 2010;24:199-217. https://doi.org/10.1007/s00468-010-0417-x

Hossain MD, Inafuku M, Iwasaki H, Taira N, Mostofa MG, Oku H. Differential enzymatic defense mechanisms in leaves and roots of two true mangrove species under long-term salt stress. Aquatic Botany. 2017;142:32-40. https://doi.org/10.1016/j.aquabot.2017.06.004

Murdiyarso D, Purbopuspito J, Kauffman JB, Warren MW, Sasmito SD, Donato DC, Manuri S, Krisnawati H, Taberima S, Kurnianto S. The potential of Indonesian mangrove forests for global climate change mitigation. Nat Clim Chang. 2015;5(12):1089-92. https://doi.org/10.1038/nclimate2734

Global Mangrove Alliance, 2018. Goals and Objectives. Global Mangrove Alliance, Washington DC. https://www.mangrovealliance.org/about/

Friess DA, Rogers K, Lovelock CE, Krauss KW, Hamilton SE, Lee SY et al. The State of the World’s Mangrove Forests: past, present and Future. Annu Rev Environ Resour. 2019;44(1):89-115. https://doi.org/10.1146/annurev-environ-101718-033302

Lewis RR. Ecological engineering for successful management and restoration of mangrove forests. Ecol Eng. 2005;24(4):403-18. https://doi.org/10.1016/j.ecoleng.2004.10.003

Friess DA, Krauss KW, Horstman EM, Balke T, Bouma TJ, Galli D, Webb EL. Are all intertidal wetlands naturally created equal? Bottlenecks, thresholds and knowledge gaps to mangrove and saltmarsh ecosystems. Biol Rev. 2012;87(2):346-66. https://doi.org/10.1111/j.1469-185X.2011.00198.x

Asaeda T, Barnuevo A. Oxidative stress as an indicator of niche-width preference of mangrove Rhizophora stylosa. Forest Ecology and Management. 2019;432:73-82. https://doi.org/10.1016/j.foreco.2018.09.015

Duke NC, Ying Lo, EY, Sun M. Global distribution and genetic discontinuities of mangroves ? emerging patterns in the evolution of Rhizophora. Trees. 2002;16:65-79. https://doi.org/10.1007/s00468-001-0141-7

Sakthivel K. Survey of molluscs in Killai backwaters of South India. Indian J Ecol. 2020;47:190-95.

Manson FJ, Loneragan NR, Skilleter GA, Phinn SR. An evaluation of the evidence for linkages between mangroves and fisheries: a synthesis of the literature and identification of research directions. Oceanogra Mar Biol Annu Rev. 2005;43:483-513. https://doi.org/10.1201/9781420037449

Selvam PP, Geevarghese GA, Ramachandran P, Ramachandran R. Spatial assessment of net canopy photosynthetic rate and species diversity in Pichavaram mangrove forest, Tamil Nadu. Indian J Ecol. 2018;45:717-23.

Alimov AF. Theory of ecosystem functioning: application to esturine ecology. Abstracts of the symposium ECSA42 “Estuarine ecosystem: structure, functional management.” Svetlogorsk, Russia. 2007; p. 8-9.

Pickens CN, Sloey TM, Hester MW. Influence of salt marsh canopy on black mangrove (Avicennia germinans) survival and establishment at its northern latitudinal limit. Hydrobiologia. 2019;826:195-208. https://doi.org/10.1007/s10750-018-3730-9

Björkman O, Demmig B, Andrews TJ. Mangrove photosynthesis: response to high-irradiance stress. Aust J Plant Physiol. 1988;15:43-61. https://doi.org/10.1071/PP9880043

Cheeseman JM, Clough BF, Carter DR, Lovelock CE, Eong OJ, Sim RG. The analysis of photosynthetic performance in leaves under field conditions: a case study using Bruguiera mangroves. Photosynthesis Research. 1991;29:11-22. https://doi.org/10.1007/BF00035202

Asaeda T, Barnuevo A. Oxidative stress as an indicator of niche-width preference of mangrove Rhizophora stylosa. Ecol Manag. 2019;432:73-82. https://doi.org/10.1016/j.foreco.2018.09.015

Rout P, Kumar Mohapatra P, Chand Basak U. Ex vitro multiple shoot regeneration potential of hypocotyls of four Rhizophoraceae mangroves. Sci Agr. 2016;14:210-15. https://doi.org/0.15192/PSCP.SA.2016.14.1.210215

Clarke LD, Hannon NJ. The mangrove swamp and salt marsh communities of the Sydney district III. Plant growth in relation to salinity and water logging. J Ecol. 1970;58:351-69. https://doi.org/10.2307/2258276

Naidoo G. Effects of nitrate, ammonium and salinity on growth of the mangrove Bruguiera gymnorrhiza (L.) Lam. Aquat Bot. 1990;38:209-19. https://doi.org/10.1016/0304-3770(90)90006-7

Werner A, Stelzer R. Physiological responses of the mangrove Rhizophora mangle grown in the absence and presence of NaCl. Plant Cell Environ. 1990;13:243-55. https://doi.org/10.1111/j.1365-3040.1990.tb01309.x

Khan MA, Aziz I. Salinity tolerance in some mangrove species from Pakistan. Wetl Ecol Manag. 2001;9:219-23. https://doi.org/10.1023/A:1011112908069

Ashraf M, Harris PJC. Photosynthesis under stressful environment. Photosynthetica. 2013;51:163-90. https://doi.org/10.1007/s11099-013-0021-6

McMillan C. Environmental factors affecting seedling establishment of the black mangrove on the central Texas Coast. Ecology. 1971;52:927-30. https://doi.org/10.2307/1936046

Chen Y, Ye Y. Effects of salinity and nutrient addition on mangrove Excoecaria agallocha. PLoS ONE. 2014;9. https://doi.org/10.1371/journal.pone.0093337

Aziz I, Khan MA. Physiological adaptations to seawater concentration in Avicennia marina from Indus delta, Pakistan. Pak J Bot. 2000;32:171-89.

Ma D, Song S, Wei L, Ding Q, Zheng HL. Comparative transcriptome analysis on the mangrove Acanthus ilicifolius and its two terrestrial relatives provides insights into adaptation to intertidal habitats. Gene. 2022;839:146730. https://doi.org/10.1016/j.gene.2022.146730

Meera SP, Augustine A. De novo transcriptome analysis of Rhizophora mucronata Lam. furnishes evidence for the existence of glyoxalase system correlated to glutathione metabolic enzymes and glutathione regulated transporter in salt tolerant mangroves. Plant Physiol Biochem. 2020;155:683-96. https://doi.org/10.1016/j.plaphy.2020.08.008

Patel NT, Gupta A, Pandey AN. Salinity tolerance of Avicennia marina (Forssk.) Vierh. from Gujarat coasts of India. Aquat Bot. 2010;93:9-16. https://doi.org/10.1016/j.aquabot.2010.02.002

Manikandan T, Neelkandan T, Usha Rani. Effect of salinity on the growth, photosynthesis and mineral constituents of the mangrove Rhizophora apiculata L. seedlings, Recent Res Sci Technol. 2009;1:134-41.

Reef R, Feller IC, Lovelock CE. Nutrition in mangroves, Tree Physiol. 2010;30:1148-60. https://doi.org/10.1093/treephys/tpq048

Cheng H, Wang YS, Ye ZH, Chen DT, Wang YT et al. Influence of N deficiency and salinity on metal (Pb, Zn and Cu) accumulation and tolerance by Rhizophora stylosa in relation to root anatomy and permeability. Environ Pollut. 2012;164:110-17. https://doi.org/10.1016/j.envpol.2012.01.034

Yates EJ, Ashwath N, Midmore DJ. Responses to nitrogen, phosphorus, potassium and sodium chloride by three mangrove species in pot culture. Trees. 2002;16:120-25. https://doi.org/10.1007/s00468-001-0145-3

Kao WY, Tsai HC, Tsai TT. Effect of NaCl and nitrogen availability on growth and photosynthesis of seedlings of a mangrove species, Kandelia candel (L.) Druce. J Plant Physiol. 2001;158:841-46. https://doi.org/10.1078/0176-1617-00248

Shi GR, Cai QS, Liu CF, Wu L. Silicon alleviates cadmium toxicity in peanut plants in relation to cadmium distribution and stimulation of antioxidative enzymes. J Plant Growth Regul. 2010;61:45-52. https://doi.org/10.1007/s10725-010-9447-z

Ye Y, Tam NF, Wong YS, Lu CY. Growth and physiological responses of two mangrove species (Bruguiera gymnorrhiza and Kandelia candel) to waterlogging. Environ Exp Bot. 2003;49(3):209-21. https://doi.org/10.1016/S0098-8472(02)00071-0

Youssef T, Saenger P. Anatomical adaptive strategies and rhizosphere oxidation in mangrove seedlings. Aust J Bot. 1996;44:297-313. https://doi.org/10.1071/BT9960297

Ashraf M, Yasmin H. Differential waterlogging tolerance in three grasses of contrasting habitats: Aeluropus lagopoides (L.) Trin., Cynodon dactylon (L.) Pers. and Leptochloa fusca (L.) Kunth. Environ Exp Bot. 1991;31:437-46. https://doi.org/10.1016/0098-8472(91)90042-M

McKevlin MR, Hook DD, McKee JWH. Growth and nutrient use efficiency of water tupelo seedlings in flooded and well-drained soil. Tree Physiol. 1995;15:753-58.

Xiao Y, Wang W, Chen L. Stem anatomical variations in seedlings of the mangrove Bruguiera gymnorrhiza grown under periodical waterlogging. Flora: Morphol Distrib Funct Ecol Plants. 2010;205(8):499-505. https://doi.org/10.1016/j.flora.2009.12.004

Xiao Y, Jie Z, Wang M, Lin G, Wang W. Leaf and stem anatomical responses to periodical waterlogging in simulated tidal floods in mangrove Avicennia marina seedlings. Aqa Bot. 2009;91(3):231-37. https://doi.org/10.1016/j.aquabot.2009.07.001

Chen Y, Ye Y. Effects of salinity and nutrient addition on mangrove Excoecaria agallocha. PLoS ONE 2014;9. https://doi.org/10.1371/journal.pone.0093337

Lovelock CE, Ball MC, Choat B, Engelbrecht BMJ, Holbrook NM, Feller IC. Linking physiological processes with mangrove forest structure: phosphorus deficiency limits canopy development, hydraulic conductivity and photosynthetic carbon gain in dwarf Rhizophora mangle. Plant Cell Environ. 2006;29:793-802. https://doi.org/10.1111/j.1365-3040.2005.01446.x

Xin K, Huang X, Hu JL, Li C, Yang XB, Arndt SK. Land use change impacts on heavy metal sedimentation in mangrove wetlands-a case study in Dongzhai Harbor of Hainan, China. Wetlands. 2014;34:1-8. https://doi.org/10.1007/s13157-013-0472-3

Naser HA. Assessment and management of heavy metal pollution in the marine environment of the Arabian Gulf: a review. Mar Pollut Bull. 2013;72:6-13. https://doi.org/10.1016/j.marpolbul.2013.04.030

Sari I, Din ZB. Effects of salinity on the uptake of lead and cadmium by two mangrove species Rhizophora apiculata Bl. and Avicennia alba Bl. Chem Ecol. 2012;28:365-74. https://doi.org/10.1080/02757540.2012.666526

Zan Q, Wang Y, Wang B. Accumulation and cycle of heavy metals in Sonneratia apetala and S. caseolaris mangrove community at Futian of Shenzhen, China. Env Sci. 2002;23:81-88.

Dai M, Lu H, Liu W, Jia H, Hong H, Liu J, Yan C. Phosphorus mediation of cadmium stress in two mangrove seedlings Avicennia marina and Kandelia obovata differing in cadmium accumulation, Ecotoxicol Environ Saf. 2017;139:272-79. https://doi.org/10.1016/j.ecoenv.2017.01.017

Chauhan R, Ramanathan AL. Evaluation of water quality of Bhitarkanika mangrove system, Orissa. Indian J Mar Sci. 2008;37:153-58.

Panda SP, Subudhi H, Patra HK. Mangrove forest of river estuaries of Odisha. India Int J Biodivers Conserv. 2013;5:446-54. https://doi.org/10.5897/IJBC12.004

Page DS, Gilfillan ES, Foster JC, Hotham JR, Gonzalez L. Mangrove leaf tissue sodium and potassium ion concentrations as sublethal indicators of oil stress in mangrove trees. In: Proceedings of the 1985 International Oil Spill Conference. Los Angeles, California, American Petroleum Institute, Washington, DC; 1985. p. 391-93. https://doi.org/10.7901/2169-3358-1985-1-391

Paliyavuth C, Clough B, Patanaponpaiboon P. Salt uptake and shoot water relations in mangroves. Aquat Bot. 2004;78:349-60. https://doi.org/10.1016/j.aquabot.2004.01.002

Mills MA, Bonner JS, Page CA, Autenrieth RL. Evaluation of bioremediation strategies of a controlled oil release in a wetland. Mar Pollut Bull. 2004;49:425-35. https://doi.org/10.1016/j.marpolbul.2004.02.027

Ke L, Zhang C, Wong YS, Tam NFY. Dose and accumulative effects of spent lubricating oil on four common mangrove plants in South China. Eco Toxol Environ Saf. 2011;74:55-66. https://doi.org/10.1016/j.ecoenv.2010.09.011

Tian Y, Liu HJ, Zheng TL, Kwon KK, Kim SJ, Yan C. PAHs contamination and bacterial communities in mangrove surface sediments of the Jiulong River Estuary, China. Mar Pollut Bull. 2008;57:707-15. https://doi.org/10.1016/j.ecoenv.2010.09.011

Tomlinson PB. Responses of two mangrove species, Aegiceras corniculatm and Avicennia marina, to long term salinity and humidity conditions. Plant Physiol. 1986;74:1-6.

Saintilan N. Above and below ground biomasses of two patterns of biomass and ANPP in a mangrove ecosystem species of mangrove on the Hawkesbury River estuary, New South Wales. Mar Fresh water Res. 1997;48:147-52. https://doi.org/10.1071/MF96079

Krauss KW, Lovelock CE, McKee KL, Hoffman LL, Ewe SML. Sousa, W.P., Environmental drivers in mangrove establishment and early development: A review. Aquat Bot. 2008;89:105-27. https://doi.org/10.1016/j.aquabot.2007.12.014

Biebl R, Kinzel H. Blattbau and Salzhaushalt von Laguncularia racemosa (L.) Gaertn. under Mangroven Blume auf Puerto Rico. Oesterreichische Botanische Zeitschrift. 1965;112:56-93. https://www.jstor.org/stable/43339272 https://doi.org/10.1007/BF01372978

Kemis JR. Petiolar glands in Combretaceae: new observations and an anatomical description of the extra-floral nectar of buttonwood (Conocarpus erectus). Am J Bot. 1984;71:34.

Yan L, Guizhu C. Physiological adaptability of three mangrove species to salt stress. Acta Ecologica Sinica. 2007;27:2208-14. https://doi.org/10.1016/S1872-2032(07)60052-3

Lv X, Li D, Yang X, Zhang M, Deng Q. Leaf enzyme and plant productivity responses to environmental stress associated with sea level rise in two Asian mangrove species. Forests. 2019;10:250. https://doi.org/10.3390/f10030250

Munns R, Tester M. Mechanisms of salinity tolerance. Annu Rev Plant Physiol. 2008;59:651-81. https://doi.org/10.1146/annurev.arplant.59.032607.092911

Munns R. Plant adaptations to salt and water stress: differences and commonalities. In: Turkan, I. (ed) Plant Responses to Drought and Salinity Stress: Developments in a Post-Genomic Era. Advances in Botanical Research; 2011;57; Academic, London; p. 1-32. https://doi.org/10.1016/B978-0-12-387692-8.00001-1

Kefu Z, Munns R, King RW. Abscisic acid levels in NaCl-treated barley, cotton and salt bush. Aust J Plant Physiol. 1991;18:17-24. https://doi.org/10.1071/PP9910017

Krishnamurthy P, Mohanty B, Wijaya E, Lee DY, Lim TM et al. Transcriptomics analysis of salt stress tolerance in the roots of the mangrove Avicennia officinalis. Sci Rep. 2017;7:10031. https://doi.org/10.1038/s41598-017-10730-2

Su W, Ye C, Zhang Y, Hao S, Li QQ. Identification of putative key genes for coastal environments and cold adaptation in mangrove Kandelia obovata through transcriptome analysis. Sci Total Environ. 2019;681:191-201. https://doi.org/10.1016/j.scitotenv.2019.05.127

Wang WQ, Ke L, Tam NFY, Wong YS. Changes in the main osmotica during the development of Kandelia candel hypocotyls and after mature hypocotyls were transplanted in solutions with different salinities. Mar Biol. 2002;141:1029-34. https://doi.org/10.1007/s00227-002-0951-1

Li LQ, Ding ZH, Liu JL, Lin HN, Wu H. Distribution of heavy metals in surficial sediments from main mangrove wetlands of China and their influence factors. Acta Oceanologica Sinica. 2008;30:159-64.

Parida AK, Mittra B, Das AB, Das TK, Mohanty P. High salinity reduces the content of a highly abundant 23-kDa protein of the mangrove Bruguiera parviflora. Planta. 2005;221:135-40. https://doi.org/10.1007/s00425-004-1415-2

Akram NA, Ashraf M. Improvement in growth, chlorophyll pigments and photosynthetic performance in salt-stressed plants of sunflower (Helianthus annuus L.) by foliar application of 5-aminolevulinic acid. Agrochemica. 2011;55:94-104.

Vovides AG, Juliane V, Armin K, Uta B, Uwe G, Peters R et al. Morphological plasticity in mangrove trees: salinity-related changes in the allometry of Avicennia germinans. Trees. 2014;28:1413-25. https://doi.org/10.1007/s00468-014-1044-8

Sugihar K, Hanagata N, Dubinsky Z, Baba S, Karube I. Molecular characterization of cDNA encoding oxygen evolving enhancer protein 1 increased by salt treatment in the mangrove Bruguiera gymnorrhiza. Plant Cell Physiol. 2000;41:1279-85. https://doi.org/10.1093/pcp/pcd061

Yamada A, Saitoh T, Mimura T, Ozeki Y. Expression of mangrove allene oxide cyclase enhances salt tolerance in Escherichia coli, yeast and tobacco cells. Plant Cell Physiol. 2002;43:903-10. https://doi.org/10.1093/pcp/pcf108

Parida AK, Das AB, Mittra B. Effects of salt on growth, ion accumulation, photosynthesis and leaf anatomy of the mangrove Bruguiera parviflora. Trees-Struct Funct. 2004;18:167-74. https://doi.org/10.1007/s00468-003-0293-8

Patra DK, Pradhan C, Patra HK. Chromium bioaccumulation, oxidative stress metabolism and oil content in lemon grass Cymbopogon flexuosus (Nees ex Steud.) W. Watson grown in chromium rich over burden soil of Sukinda chromite mine, India. Chemosphere.2019;218:1082-88. https://doi.org/10.1016/j.chemosphere.2018.11.211

Feng X, Xu S, Li J, Yang Y, Chen Q, Lyu H, Zhong C, He Z, Shi S. Molecular adaptation to salinity fluctuation in tropical intertidal environments of a mangrove tree Sonneratia alba. BMC Plant Biol. 2020;20:178. https://doi.org/10.1186/s12870-020-02395-3

He Z, Xu S, Zhang Z, Guo W, Lyu H, Zhong C et al. The International Mangrove Consortium and Shi, S. Convergent adaptation of the genomes of woody plants at the land–sea interface. Natl Sci Rev. 2020;7:978-93. https://doi.org/10.1093/nsr/nwaa027

Lyu H, He Z, Wu CI, Shi S. Convergent adaptive evolution in marginal environments: unloading transposable elements as a common strategy among mangrove genomes. New Phytol. 2018;217:428-38. https://doi.org/10.1111/nph.14784

Xu S, Wang J, Guo Z, He Z, Shi S. Genomic convergence in the adaptation to extreme environments. Plant Comm. 2020;1:100117. https://doi.org/10.1016/j.xplc.2020.100117

Hayyan M, Hashim MA, AlNashef IM. Superoxide ion: generation and chemical implications. Chem Rev. 2016;116:3029-85. https://doi.org/10.1021/acs.chemrev.5b00407

Prashanth SR, Sadhasivam V, Parida A. Overexpression of cytosolic copper/zinc superoxide dismutase from a mangrove plant Avicennia marina in indica rice var Pusa Basmati-1 confers abiotic stress tolerance. Transgenic Res. 2008;17:281-91. https://doi.org/10.1007/s11248-007-9099-6

Wang L, Pan D, Lv X, Cheng C-L, Li J, Liang W et al. A multilevel investigation to discover why Kandelia candel thrives in high salinity. Plant Cell Environ. 2016;39:2486-97. https://doi.org/10.1111/pce.12804

Yang Y, Li J, Yang S, Li X, Fang L, Zhong C et al. Effects of Pleistocene sea-level fluctuations on mangrove population dynamics: a lesson from Sonneratia alba. BMC Evol Biol. 2017;17:22. https://doi.org/10.1186/s12862-016-0849-z

Kumar S, Trivedi PK. Glutathione S Transferases: role in combating abiotic stresses including arsenic detoxification in plants. Front Plant Sci. 2018;9:751. https://doi.org/10.3389/fpls.2018.00751

Janicka-Russak M, Kaba?a K. The role of plasma membrane H+-ATPase in salinity stress of plants. In: Progress in Botany, U. Luttge and W. Beyschlag, (eds.) (Springer International Publishing); p. 2015. 77-92. https://doi.org/10.1007/978-3-319-08807-5_3

Mimura T, Kura-Hotta M, Tsujimura T, Ohnishi M, et al. Rapid increase of vacuolar volume in response to salt stress. Planta. 2003;216:397-402. https://doi.org/10.1007/s00425-002-0878-2

Hibino T, Meng YL, Kawamitsu Y, Uehara N, et al. Molecular cloning and functional characterization of two kinds of betaine-aldehyde dehydrogenase in betaine-accumulating mangrove Avicennia marina (Forsk.)Vierh. Plant Mol Biol. 2001;45:353-63. https://doi.org/10.1023/A:1006497113323

Fu X, Huang Y, Deng S, Zhou R, Yang G, Ni X et al. Construction of a SSH library of Aegiceras corniculatum under salt stress and expression analysis of four transcripts. Plant Sci. 2005;169:147-54. https://doi.org/10.1016/j.plantsci.2005.03.009

Xiao X, Hong Y, Xia W, Feng S et al. Transcriptome analysis of Ceriops tagal in saline environments using RNA-sequencing. PLoS One. 2016;11:e0167551. https://doi.org/10.1371/journal.pone.0167551

Wong YY, Ho CL, Nguyen PD, Teo SS et al. Isolation of salinity tolerant genes from the mangrove plant, Bruguiera cylindrica by using suppression subtractive hybridization (SSH) and bacterial functional screening. Aquat Bot. 2007;86:117-22. https://doi.org/10.1016/j.aquabot.2006.09.009

Krishnamurthy P, Jyothi-Prakash PA, Qin L, He J et al. Role of root hydrophobic barriers in salt exclusion of a mangrove plant Avicennia officinalis. Plant Cell Environ. 2014;37:1656-71. https://doi.org/10.1111/pce.12272

Evans DE. Aerenchyma formation. New Phytol. 2004;161:35-49. https://doi.org/10.1046/j.1469-8137.2003.00907.x

Hao S, Su W, Li QQ. Adaptive roots of mangrove Avicennia marina: structure and gene expressions analyses of pneumatophores. Sci Total Environ. 2021;757:143994. https://doi.org/10.1016/j.scitotenv.2020.143994

Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E. Regulator of PP2C phosphatase activity function as abscisic acid sensors. Science. 2009;324:1064-68. https://doi.org/10.1126/science.1172408

Wang F, Wu Q, Zhang Z, Chen S, Zhou R. Cloning, expression and characterization of iron superoxide dismutase in Sonneratia alba, a highly salt tolerant mangrove tree. Protein J. 2013;32:259-65. https://doi.org/10.1007/s10930-013-9482-5

Chen J, Xiao Q, Wu F, Dong X et al. Nitric oxide enhances salt secretion and Na+ sequestration in a mangrove plant, Avicennia marina, through increasing the expression of H+-ATPase and Na+/H+ antiporter under high salinity. Tree Physiol. 2010;30:1570-85. https://doi.org/10.1093/treephys/tpq086

Hong L, Su W, Zhang Y, Ye C, Shen Y, Li QQ. Transcriptome profiling during mangrove viviparity in response to abscisic acid. Sci Rep. 2018;8:770. https://doi.org/10.1038/s41598-018-19236-x