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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Methyl jasmonate improves tolerance to high salt stress in the recretohalophyte Limonium bicolor

Fang Yuan A C , Xue Liang A C , Ying Li A , Shanshan Yin A and Baoshan Wang https://orcid.org/0000-0002-0991-9190 A B
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A Shandong Provincial Key Laboratory of Plant Stress, College of Life Sciences, Shandong Normal University, Ji’nan, Shandong, 250014, PR China.

B Corresponding author. Email: bswang@sdnu.edu.cn

C These authors equally contributed to this work.

Functional Plant Biology 46(1) 82-92 https://doi.org/10.1071/FP18120
Submitted: 2 November 2017  Accepted: 29 August 2018   Published: 15 October 2018

Abstract

Limonium bicolor is a typical recretohalophyte with salt glands in the epidermis, which shows maximal growth at moderate salt concentrations (100 mM NaCl) but reduced growth in the presence of excess salt (more than 200 mM). Jasmonic acid (JA) alleviates the reduced growth of L. bicolor under salt stress; however, the underlying mechanism is unknown. In this study we investigated the effects of exogenous methyl jasmonate (MeJA) application on L. bicolor growth at high NaCl concentrations. We found that treatment with 300 mM NaCl led to dramatic inhibition of seedling growth that was significantly alleviated by the application of 0.03 mM MeJA, resulting in a biomass close to that of plants not subjected to salt stress. To determine the parameters that correlate with MeJA-induced salt tolerance (assessed as the biomass production in saline and control conditions), we measured 14 physiological parameters relating to ion contents, plasma membrane permeability, photosynthetic parameters, salt gland density, and salt secretion. We identified a correlation between individual indicators and salt tolerance: the most positively correlated indicator was net photosynthetic rate, and the most negatively correlated one was relative electrical conductivity. These findings provide insights into a possible mechanism underlying MeJA-mediated salt stress alleviation.

Additional keywords: biomass, MeJA, net photosynthetic rate, relative electrical conductivity, salt alleviation, salt gland.


References

Ahmadi FI, Karimi K, Struik PC (2018) Effect of exogenous application of methyl jasmonate on physiological and biochemical characteristics of Brassica napus L. cv. Talaye under salinity stress. South African Journal of Botany 115, 5–11.
Effect of exogenous application of methyl jasmonate on physiological and biochemical characteristics of Brassica napus L. cv. Talaye under salinity stress.Crossref | GoogleScholarGoogle Scholar |

Arisz W, Camphuis I, Heikens H, van Tooren AJ (1955) The secretion of the salt glands of Limonium latifolium Ktze. Acta Botanica Neerlandica 4, 322–338.
The secretion of the salt glands of Limonium latifolium Ktze.Crossref | GoogleScholarGoogle Scholar |

Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant, Cell & Environment 32, 666–681.
Regulation and function of root exudates.Crossref | GoogleScholarGoogle Scholar |

Badri DV, Loyola-Vargas VM, Du J, Stermitz FR, Broeckling CD, Iglesias-Andreu L, Vivanco JM (2008) Transcriptome analysis of Arabidopsis roots treated with signaling compounds: a focus on signal transduction, metabolic regulation and secretion. New Phytologist 179, 209–223.
Transcriptome analysis of Arabidopsis roots treated with signaling compounds: a focus on signal transduction, metabolic regulation and secretion.Crossref | GoogleScholarGoogle Scholar |

Barkla BJ, Zingarelli L, Blumwald E, Smith JAC (1995) Tonoplast Na+/H+ antiport activity and its energization by the vacuolar H+-ATPase in the halophytic plant Mesembryanthemum crystallinum L. Plant Physiology 109, 549–556.
Tonoplast Na+/H+ antiport activity and its energization by the vacuolar H+-ATPase in the halophytic plant Mesembryanthemum crystallinum L.Crossref | GoogleScholarGoogle Scholar |

Chen J, Xiao Q, Wu F, Dong X, He J, Pei Z, Zheng H (2010) 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 Physiology 30, 1570–1585.
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.Crossref | GoogleScholarGoogle Scholar |

Davies PJ (1995) The plant hormone concept: concentration, sensitivity and transport. In ‘Plant hormones’. (Ed. PJ Davies) pp. 13–38. (Springer: Dordrecht, The Netherlands)

Ding F, Song J, Ruan Y, Wang BS (2009) Comparison of the effects of NaCl and KCl at the roots on seedling growth, cell death and the size, frequency and secretion rate of salt glands in leaves of Limonium sinense. Acta Physiologiae Plantarum 31, 343–350.
Comparison of the effects of NaCl and KCl at the roots on seedling growth, cell death and the size, frequency and secretion rate of salt glands in leaves of Limonium sinense.Crossref | GoogleScholarGoogle Scholar |

Ding F, Chen M, Sui N, Wang BS (2010) Ca2+ significantly enhanced development and salt-secretion rate of salt glands of Limonium bicolor under NaCl treatment. South African Journal of Botany 76, 95–101.
Ca2+ significantly enhanced development and salt-secretion rate of salt glands of Limonium bicolor under NaCl treatment.Crossref | GoogleScholarGoogle Scholar |

Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Methods in Enzymology 186, 421–431.
Malondialdehyde determination as index of lipid peroxidation.Crossref | GoogleScholarGoogle Scholar |

Dschida W, Platt-Aloia K, Thomson W (1992) Epidermal peels of Avicennia germinans (L.) Stearn: a useful system to study the function of salt glands. Annals of Botany 70, 501–509.
Epidermal peels of Avicennia germinans (L.) Stearn: a useful system to study the function of salt glands.Crossref | GoogleScholarGoogle Scholar |

Faraday CD, Quinton PM, Thomson WW (1986) Ion fluxes across the transfusion zone of secreting Limonium salt glands determined from secretion rates, transfusion zone areas and plasmodesmatal frequencies. Journal of Experimental Botany 37, 482–494.
Ion fluxes across the transfusion zone of secreting Limonium salt glands determined from secretion rates, transfusion zone areas and plasmodesmatal frequencies.Crossref | GoogleScholarGoogle Scholar |

Fedina IS, Tsonev TD (1997) Effect of pretreatment with methyl jasmonate on the response of Pisum sativum to salt stress. Journal of Plant Physiology 151, 735–740.
Effect of pretreatment with methyl jasmonate on the response of Pisum sativum to salt stress.Crossref | GoogleScholarGoogle Scholar |

Feng Z, Sun Q, Deng Y, Sun S, Zhang J, Wang B (2014) Study on pathway and characteristics of ion secretion of salt glands of Limonium bicolor. Acta Physiologiae Plantarum 36, 2729–2741.
Study on pathway and characteristics of ion secretion of salt glands of Limonium bicolor.Crossref | GoogleScholarGoogle Scholar |

Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytologist 179, 945–963.
Salinity tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar |

Fung RW, Wang CY, Smith DL, Gross KC, Tian M (2004) MeSA and MeJA increase steady-state transcript levels of alternative oxidase and resistance against chilling injury in sweet peppers (Capsicum annuum L.). Plant Science 166, 711–719.
MeSA and MeJA increase steady-state transcript levels of alternative oxidase and resistance against chilling injury in sweet peppers (Capsicum annuum L.).Crossref | GoogleScholarGoogle Scholar |

Iqbal N, Masood A, Khan NA (2012) Phytohormones in salinity tolerance: ethylene and gibberellins cross talk. In ‘Phytohormones and abiotic stress tolerance in plants’. (Eds NA Khan, R Nazar, N Iqbal, NA Anjum) pp. 77–98. (Springer: Berlin)

Kuwabara A, Nagata T (2006) Cellular basis of developmental plasticity observed in heterophyllous leaf formation of Ludwigia arcuata (Onagraceae). Planta 224, 761–770.
Cellular basis of developmental plasticity observed in heterophyllous leaf formation of Ludwigia arcuata (Onagraceae).Crossref | GoogleScholarGoogle Scholar |

Lan WZ, Wang W, Wang SM, Li LG, Buchanan BB, Lin HX, Gao JP, Luan S (2010) A rice high-affinity potassium transporter (HKT) conceals a calcium-permeable cation channel. Proceedings of the National Academy of Sciences of the United States of America 107, 7089–7094.
A rice high-affinity potassium transporter (HKT) conceals a calcium-permeable cation channel.Crossref | GoogleScholarGoogle Scholar |

Leng BY, Yuan F, Dong XX, Wang J, Wang BS (2018) Distribution pattern and salt excretion rate of salt glands in two recretohalophyte species of Limonium (Plumbaginaceae). South African Journal of Botany 115, 74–80.
Distribution pattern and salt excretion rate of salt glands in two recretohalophyte species of Limonium (Plumbaginaceae).Crossref | GoogleScholarGoogle Scholar |

Levering CA, Thomson WW (1971) The ultrastructure of the salt gland of Spartina foliosa. Planta 97, 183–196.
The ultrastructure of the salt gland of Spartina foliosa.Crossref | GoogleScholarGoogle Scholar |

Li X, Schuler MA, Berenbaum MR (2002) Jasmonate and salicylate induce expression of herbivore cytochrome P450 genes. Nature 419, 712–715.
Jasmonate and salicylate induce expression of herbivore cytochrome P450 genes.Crossref | GoogleScholarGoogle Scholar |

Lin J, Li J, Yuan F, Yang Z, Wang B, Chen M (2018) Transcriptome profiling of genes involved in photosynthesis in Elaeagnus angustifolia L. under salt stress. Photosynthetica 56, 998–1009.
Transcriptome profiling of genes involved in photosynthesis in Elaeagnus angustifolia L. under salt stress.Crossref | GoogleScholarGoogle Scholar |

Meinke DW (1994) Seed development in Arabidopsis thaliana. Cold Spring Harbor Monograph Archive 27, 253–295.

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar |

O’Neal ME, Landis DA, Isaacs R (2002) An inexpensive, accurate method for measuring leaf area and defoliation through digital image analysis. Journal of Economic Entomology 95, 1190–1194.
An inexpensive, accurate method for measuring leaf area and defoliation through digital image analysis.Crossref | GoogleScholarGoogle Scholar |

Praxedes SC, Lacerda CFD, Damatta FM, Prisco JT, Gomes-Filho E (2010) Salt tolerance is associated with differences in ion accumulation, biomass allocation and photosynthesis in cowpea cultivars. Journal Agronomy & Crop Science 196, 193–204.
Salt tolerance is associated with differences in ion accumulation, biomass allocation and photosynthesis in cowpea cultivars.Crossref | GoogleScholarGoogle Scholar |

Qi T, Song S, Ren Q, Wu D, Huang H, Chen Y, Fan M, Peng W, Ren C, Xie D (2011) The jasmonate-ZIM-domain proteins interact with the WD-repeat/bHLH/MYB complexes to regulate jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana. Plant Cell Online 23, 1795–1814.
The jasmonate-ZIM-domain proteins interact with the WD-repeat/bHLH/MYB complexes to regulate jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Qiu ZB, Guo JL, Zhu AJ, Zhang L, Zhang MM (2014) Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotoxicology and Environmental Safety 104, 202–208.
Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress.Crossref | GoogleScholarGoogle Scholar |

Rozema J, Flowers T (2008) Crops for a salinized world. Science 322, 1478–1480.
Crops for a salinized world.Crossref | GoogleScholarGoogle Scholar |

Rozema J, Riphagen I (1977) Physiology and ecologic relevance of salt secretion by the salt gland of Glaux maritima L. Oecologia 29, 349–357.
Physiology and ecologic relevance of salt secretion by the salt gland of Glaux maritima L.Crossref | GoogleScholarGoogle Scholar |

Ryu H, Cho YG (2015) Plant hormones in salt stress tolerance. Journal of Plant Biology 58, 147–155.
Plant hormones in salt stress tolerance.Crossref | GoogleScholarGoogle Scholar |

Shou H, Bordallo P, Fan JB, Yeakley JM, Bibikova M, Sheen J, Wang K (2004) Expression of an active tobacco mitogen-activated protein kinase kinase kinase enhances freezing tolerance in transgenic maize. Proceedings of the National Academy of Sciences of the United States of America 101, 3298
Expression of an active tobacco mitogen-activated protein kinase kinase kinase enhances freezing tolerance in transgenic maize.Crossref | GoogleScholarGoogle Scholar |

Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. The Plant Cell 14, S153
The jasmonate signal pathway.Crossref | GoogleScholarGoogle Scholar |

Volkov V, Beilby M (2017) Editorial: salinity tolerance in plants: mechanisms and regulation of ion transport. Frontiers in Plant Science 8, 1795

Waisel Y (1972) ‘Biology of halophytes.’ (Academic Press: New York)

Yamamoto N, Takano T, Tanaka K, Ishige T, Terashima S, Endo C, Kurusu T, Yajima S, Yano K, Tada Y (2015) Comprehensive analysis of transcriptome response to salinity stress in the halophytic turf grass Sporobolus virginicus. Frontiers in Plant Science 6, 241
Comprehensive analysis of transcriptome response to salinity stress in the halophytic turf grass Sporobolus virginicus.Crossref | GoogleScholarGoogle Scholar |

Yoon JMH, Lee S, Lee I (2009) Methyl jasmonate alleviated salinity stress in soybean. Journal of Crop Science and Biotechnology 12, 63–68.
Methyl jasmonate alleviated salinity stress in soybean.Crossref | GoogleScholarGoogle Scholar |

Yuan F, Chen M, Leng BY, Wang B (2013) An efficient autofluorescence method for screening Limonium bicolor mutants for abnormal salt gland density and salt secretion. South African Journal of Botany 88, 110–117.
An efficient autofluorescence method for screening Limonium bicolor mutants for abnormal salt gland density and salt secretion.Crossref | GoogleScholarGoogle Scholar |

Yuan F, Chen M, Yang JC, Leng BY, Wang BS (2014) A system for the transformation and regeneration of the recretohalophyte Limonium bicolor. In Vitro Cellular & Developmental Biology. Plant 50, 610–617.
A system for the transformation and regeneration of the recretohalophyte Limonium bicolor.Crossref | GoogleScholarGoogle Scholar |

Yuan F, Leng BY, Wang BS (2016a) Progress in studying salt secretion from the salt glands in recretohalophytes: how do plants secrete salt? Frontiers in Plant Science 7, 977
Progress in studying salt secretion from the salt glands in recretohalophytes: how do plants secrete salt?Crossref | GoogleScholarGoogle Scholar |

Yuan F, Lyu MJA, Leng BY, Zhu XG, Wang BS (2016b) The transcriptome of NaCl-treated Limonium bicolor leaves reveals the genes controlling salt secretion of salt gland. Plant Molecular Biology 91, 241–256.
The transcriptome of NaCl-treated Limonium bicolor leaves reveals the genes controlling salt secretion of salt gland.Crossref | GoogleScholarGoogle Scholar |

Zhang H, Huang Z, Xie B, Chen Q, Tian X, Zhang X, Zhang H, Lu X, Huang D, Huang R (2004) The ethylene-, jasmonate-, abscisic acid- and NaCl-responsive tomato transcription factor JERF1 modulates expression of GCC box-containing genes and salt tolerance in tobacco. Planta 220, 262–270.
The ethylene-, jasmonate-, abscisic acid- and NaCl-responsive tomato transcription factor JERF1 modulates expression of GCC box-containing genes and salt tolerance in tobacco.Crossref | GoogleScholarGoogle Scholar |

Zhang Y, Chen JM, Miller JR, Noland TL (2008) Leaf chlorophyll content retrieval from airborne hyperspectral remote sensing imagery. Remote Sensing of Environment 112, 3234–3247.
Leaf chlorophyll content retrieval from airborne hyperspectral remote sensing imagery.Crossref | GoogleScholarGoogle Scholar |

Zhu JK (2002) Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53, 247
Salt and drought stress signal transduction in plants.Crossref | GoogleScholarGoogle Scholar |