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

Differential responses of the mangrove Avicennia marina to salinity and abscisic acid

Ruth Reef A D , Nele Schmitz B , Britt A. Rogers A , Marilyn C. Ball C and Catherine E. Lovelock A
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, The University of Queensland, St Lucia, Qld 4072, Australia.

B Laboratory for Plant Biology and Nature Management, Vrije Universiteit Brussel, 1050 Brussels, Belgium.

C Research School of Biology, The Australian National University, Canberra, ACT 0200, Australia.

D Corresponding author. Email: r.reef@uq.edu.au

Functional Plant Biology 39(12) 1038-1046 https://doi.org/10.1071/FP12178
Submitted: 20 June 2012  Accepted: 25 August 2012   Published: 24 September 2012

Abstract

Salinisation of the soil can cause plant water deficits, ion and nutrient imbalances and toxic reactions. The halophyte, Avicennia marina (Forssk.) Vierh., is a mangrove that tolerates a wide range of soil salinities. In order to understand how salinity affects plant growth and functioning and how salinity responses are influenced by the water deficit signalling hormone abscisic acid (ABA) we grew A. marina seedlings under two non-growth limiting salinities: 60% seawater and 90% seawater and with and without exogenously supplied ABA. We measured growth, photosynthesis, sap flow, aquaporin gene expression, hydraulic anatomy and nutrient status as well as sap ABA concentrations. ABA addition resulted in a drought phenotype (reduced sap flow, transpiration rates and photosynthesis and increased water use efficiency and aquaporin expression). In contrast, growth in high salinity did not lead to responses that are typical for water deficits, but rather, could be characterised as drought avoidance strategies (no reduction in sap flow, transpiration rates and photosynthesis and reduced aquaporin expression). Tissue nutrient concentrations were higher in seedlings grown at high salinities. We did not find evidence for a role for ABA in the mangrove salinity response, suggesting ABA is not produced directly in response to high concentrations of NaCl ions.

Additional keywords: ABA, aquaporins, halophytes, salinity tolerance, sap flow, stomata.


References

Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y, Galili G (2003) Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. The Plant Cell 15, 439–447.
Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress.CrossRef | 1:CAS:528:DC%2BD3sXhtlOmtbg%3D&md5=8fa5b8937acb289af6993e5ea61062e9CAS |

Albacete A, Ghanem ME, Martínez-Andújar C, Acosta M, Sánchez-Bravo J, Martínez V, Lutts S, Dodd IC, Pérez-Alfocea F (2008) Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants. Journal of Experimental Botany 59, 4119–4131.
Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants.CrossRef | 1:CAS:528:DC%2BD1cXhsVCgt73M&md5=36554fe34084cd213ff622362a3b7332CAS |

Ball MC (1988) Salinity tolerance in mangroves Aegiceras corniculatum and Avicennia marina. I. Water use in relation to growth, carbon partitioning, and salt balance. Australian Journal of Plant Physiology 15, 447–464.
Salinity tolerance in mangroves Aegiceras corniculatum and Avicennia marina. I. Water use in relation to growth, carbon partitioning, and salt balance.CrossRef |

Ball MC (2002) Interactive effects of salinity and irradiance on growth: implications for mangrove forest structure along salinity gradients. Trees Structure and Function 16, 126–139.
Interactive effects of salinity and irradiance on growth: implications for mangrove forest structure along salinity gradients.CrossRef |

Carvajal M, Martinez V, Alcarez CF (1999) Physiological function of water channels as affected by salinity in roots of paprika pepper. Physiologia Plantarum 105, 95–101.
Physiological function of water channels as affected by salinity in roots of paprika pepper.CrossRef | 1:CAS:528:DyaK1MXitFCktbs%3D&md5=01715bb0620f522dc11cc827690986cfCAS |

Chen S, Li J, Wang T, Wang S, Polle A, Hüttermann A (2002) Osmotic stress and ion-specific effects on xylem abscisic acid and the relevance to salinity tolerance in poplar. Journal of Plant Growth Regulation 21, 224–233.
Osmotic stress and ion-specific effects on xylem abscisic acid and the relevance to salinity tolerance in poplar.CrossRef | 1:CAS:528:DC%2BD3sXjt1akt7o%3D&md5=2add66a91adf87f1155c6d86b04dcd16CAS |

Clipson NJW, Lachno DR, Flowers TJ (1988) Salt tolerance in the halophyte Suaeda maritima L.Dum.: abscisic acid concentrations in response to constant and altered salinity. Journal of Experimental Botany 39, 1381–1388.
Salt tolerance in the halophyte Suaeda maritima L.Dum.: abscisic acid concentrations in response to constant and altered salinity.CrossRef |

Diédhiou CJ, Popova OV, Golldack D (2009) Transcript profiling of the salt-tolerant Festuca rubra ssp. litoralis reveals a regulatory network controlling salt acclimatization. Journal of Plant Physiology 166, 697–711.
Transcript profiling of the salt-tolerant Festuca rubra ssp. litoralis reveals a regulatory network controlling salt acclimatization.CrossRef |

Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytologist 179, 945–963.
Salinity tolerance in halophytes.CrossRef | 1:CAS:528:DC%2BD1cXhtFWqur%2FE&md5=72b4deb297e7aba3822bd35460a0cbe9CAS |

Franks PJ, Drake PL, Beerling DJ (2009) Plasticity in maximum stomatal conductance constrained by negative correlation between stomatal size and density: an analysis using Eucalyptus globulus. Plant, Cell & Environment 32, 1737–1748.
Plasticity in maximum stomatal conductance constrained by negative correlation between stomatal size and density: an analysis using Eucalyptus globulus.CrossRef |

Friend AD (1991) Use of a model of photosynthesis and leaf microenvironment to predict optimal stomatal conductance and leaf nitrogen partitioning. Plant, Cell & Environment 14, 895–905.
Use of a model of photosynthesis and leaf microenvironment to predict optimal stomatal conductance and leaf nitrogen partitioning.CrossRef | 1:CAS:528:DyaK38Xitlais74%3D&md5=4d471f6b69daccfc37472e10dfcceb1aCAS |

Gómez-Cadenas A, Tadeo FR, Primo-Millo E, Talon M (1998) Involvement of abscisic acid and ethylene in the responses of citrus seedlings to salt shock. Physiologia Plantarum 103, 475–484.
Involvement of abscisic acid and ethylene in the responses of citrus seedlings to salt shock.CrossRef |

Gu R, Fonseca S, Puskas LG, Hackler LJ, Zvara A, Dudits D, Pais MS (2004) Transcript identification and profiling during salt stress and recovery of Populus euphratica. Tree Physiology 24, 265–276.
Transcript identification and profiling during salt stress and recovery of Populus euphratica.CrossRef | 1:CAS:528:DC%2BD2cXislyiurg%3D&md5=648681c981b64d6cd9e6463ad2de0bc0CAS |

Hutchings P, Saenger P (1987) ‘Ecology of mangroves.’ (University of Queensland Press St Lucia, Qld)

Jang JY, Kim DG, Kim YO, Kim JS, Kang H (2004) An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Molecular Biology 54, 713–725.
An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana.CrossRef | 1:CAS:528:DC%2BD2cXptlCrtLg%3D&md5=e32945034fa29aa9ec728f6021939ea5CAS |

Jeschke WD, Peuke AD, Pate JS, Hartung W (1997) Transport, synthesis and catabolism of abscisic acid (ABA) in intact plants of castor bean (Ricinus communis L.) under phosphate deficiency and moderate salinity. Journal of Experimental Botany 48, 1737–1747.
Transport, synthesis and catabolism of abscisic acid (ABA) in intact plants of castor bean (Ricinus communis L.) under phosphate deficiency and moderate salinity.CrossRef | 1:CAS:528:DyaK2sXnt1Onurg%3D&md5=1e0c7227b249d8bd948715a157046349CAS |

Johansson I, Larsson C, Ek B, Kjellbom P (1996) The major integral proteins of spinach leaf plasma membranes are putative aquaporins and are phosphorylated in response to Ca2+ and apoplastic water potential. The Plant Cell 8, 1181–1191.

Katsuhara M, Koshio K, Shibasaka M, Hayashi Y, Hayakawa T, Kasamo K (2003) Over-expression of a barley aquaporin increased the shoot/root ratio and raised salt sensitivity in transgenic rice plants. Plant & Cell Physiology 44, 1378–1383.
Over-expression of a barley aquaporin increased the shoot/root ratio and raised salt sensitivity in transgenic rice plants.CrossRef | 1:CAS:528:DC%2BD2cXhsFOjsA%3D%3D&md5=ee178f722c7d5ac73e296bc120c9f385CAS |

Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. The Plant Cell 13, 889–906.

Kefu Z, Munns R, King R (1991) Abscisic acid levels in NaCl-treated barley, cotton and saltbush. Functional Plant Biology 18, 17–24.

Kuiper PJC (1984) Functioning of plant cell membranes under saline conditions: membrane lipid composition and ATPases. In ‘Salinity tolerance in plants. Strategies for crop improvement’. (Eds RC Staples, GH Toenniessen) pp. 77–91. (John Wiley & Sons: New York)

Lewis AM (1992) Measuring the hydraulic diameter of a pore or conduit. American Journal of Botany 79, 1158–1161.
Measuring the hydraulic diameter of a pore or conduit.CrossRef |

Lin G, Sternberg L (1992) Effect of growth form, salinity, nutrient and sulfide on photosynthesis, carbon isotope discrimination and growth of red mangrove (Rhizophora mangle L.). Functional Plant Biology 19, 509–517.

Liu C, Li C, Liang D, Wei Z, Zhou S, Wang R, Ma F (2012) Differential expression of ion transporters and aquaporins in leaves may contribute to different salt tolerance in Malus species. Plant Physiology and Biochemistry 58, 159–165.
Differential expression of ion transporters and aquaporins in leaves may contribute to different salt tolerance in Malus species.CrossRef | 1:CAS:528:DC%2BC38Xht1emsrvM&md5=66688a4f59c41f62277a732be206e561CAS |

Lovelock CE, Ball MC, Feller IC, Engelbrecht BMJ, Ewe ML (2006a) Variation in hydraulic conductivity of mangroves: influence of species, salinity, and nitrogen and phosphorus availability. Physiologia Plantarum 127, 457–464.
Variation in hydraulic conductivity of mangroves: influence of species, salinity, and nitrogen and phosphorus availability.CrossRef | 1:CAS:528:DC%2BD28XosVKgsrs%3D&md5=610da3ba93841ea07d89e5495310dc2bCAS |

Lovelock CE, Feller IC, Ball MC, Engelbrecht BMJ, Ewe ML (2006b) Differences in plant function in phosphorus and nitrogen limited mangrove ecosystems. New Phytologist 172, 514–522.
Differences in plant function in phosphorus and nitrogen limited mangrove ecosystems.CrossRef | 1:CAS:528:DC%2BD28Xht1GntbrL&md5=56fd25b18a74a35694708e983406cfdcCAS |

Maathuis FJM, Filatov V, Herzyk P, Krijger GC, Axelsen KB, Chen S, Green BJ, Li Y, Madagan KL, Sánchez-Fernández R, Forde BG, Palmgren MG, Rea PA, Williams LE, Sanders D, Amtmann A (2003) Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress. The Plant Journal 35, 675–692.
Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress.CrossRef | 1:CAS:528:DC%2BD3sXot1OqtbY%3D&md5=bf437440240f2f4b6ab0bb36edde2703CAS |

Maurel C, Chrispeels MJ (2001) Aquaporins. A molecular entry into plant water relations. Plant Physiology 125, 135–138.
Aquaporins. A molecular entry into plant water relations.CrossRef | 1:CAS:528:DC%2BD3MXjslymur4%3D&md5=e5fc5618a13adb725e876b658fe107f3CAS |

Montero E, Cabot C, Poschenrieder CH, Barcelo J (1998) Relative importance of osmotic-stress and ion-specific effects on ABA-mediated inhibition of leaf expansion growth in Phaseolus vulgaris. Plant, Cell & Environment 21, 54–62.
Relative importance of osmotic-stress and ion-specific effects on ABA-mediated inhibition of leaf expansion growth in Phaseolus vulgaris.CrossRef | 1:CAS:528:DyaK1cXitlCgsLg%3D&md5=080cc86f33ccba0a2201e6107845d6f3CAS |

Moon G, Clough B, Peterson C, Allaway W (1986) Apoplastic and symplastic pathways in Avicennia marina (Forsk.) Vierh. roots revealed by fluorescent tracer dyes. Functional Plant Biology 13, 637–648.

Morrisey DJ, Swales A, Dittmann S, Morrison MA, Lovelock CE, Beard CM (2010) The ecology and management of temperate mangroves. In ‘Oceanography and marine biology: an annual review’. (Eds RN Gibson, RJA Atkinson, JDM Gordon) pp. 43–160. (CRC Press: Boca Raton, FL)

Munns R (2005) Genes and salt tolerance: bringing them together. New Phytologist 167, 645–663.
Genes and salt tolerance: bringing them together.CrossRef | 1:CAS:528:DC%2BD2MXhtVGisbfP&md5=881055c3bb6e020524525efdcc73821eCAS |

Oku H, Baba S, Koga H, Takara K, Iwasaki H (2003) Lipid composition of mangrove and its relevance to salt tolerance. Journal of Plant Research 116, 37–45.

Ouziad F, Wilde P, Schmelzer E, Hildebrandt U, Bothe H (2006) Analysis of expression of aquaporins and Na+/H+ transporters in tomato colonized by arbuscular mycorrhizal fungi and affected by salt stress. Environmental and Experimental Botany 57, 177–186.
Analysis of expression of aquaporins and Na+/H+ transporters in tomato colonized by arbuscular mycorrhizal fungi and affected by salt stress.CrossRef | 1:CAS:528:DC%2BD28XkslSksrk%3D&md5=6ad9159ca8b0aea9c2a130bb10633210CAS |

Parida A, Jha B (2010) Salt tolerance mechanisms in mangroves: a review. Trees – Structure and Function 24, 199–217.
Salt tolerance mechanisms in mangroves: a review.CrossRef |

Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta 975, 384–394.
Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy.CrossRef | 1:CAS:528:DyaL1MXkvFehtL4%3D&md5=61552bb6b1288bbccc74fc2ed3898209CAS |

R Development Core Team (2011) R: A language and environment for statistical computing. (R Foundation for Statistical Computing: Vienna, Austria). Available at http://www.R-project.org/

Rada F, Goldstein G, Orozco A, Montilla M, Zabala O, Azócar A (1989) Osmotic and turgor relations of three mangrove ecosystem species. Australian Journal of Plant Physiology 16, 477–486.
Osmotic and turgor relations of three mangrove ecosystem species.CrossRef |

Rasband WS (1997) ‘Image J.’ (US National Institutes of Health: Bethesda, MD)

Reef R, Ball MC, Feller IC, Lovelock CE (2010) Relationships among RNA : DNA ratio, growth and elemental stoichiometry in mangrove trees. Functional Ecology 24, 1064–1072.
Relationships among RNA : DNA ratio, growth and elemental stoichiometry in mangrove trees.CrossRef |

Salisbury EJ (1928) On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora. Philosophical Transactions of the Royal Society of London. Series B, Containing Papers of a Biological Character 216, 1–65.
On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora.CrossRef |

Sobrado MA (1999) Drought effects on photosynthesis of the mangrove, Avicennia germinans, under contrasting salinities. Trees – Structure and Function 13, 125–130.

Sobrado MA (2000) Leaf photosynthesis of the mangrove Avicennia germinans as affected by NaCl. Photosynthetica 36, 547–555.
Leaf photosynthesis of the mangrove Avicennia germinans as affected by NaCl.CrossRef |

Spickett CM, Smirnoff N, Ratcliffe RG (1992) Metabolic response of maize roots to hyperosmotic shock. Plant Physiology 99, 856–863.
Metabolic response of maize roots to hyperosmotic shock.CrossRef | 1:CAS:528:DyaK38XlsVOhtLc%3D&md5=e40a5c541a62ebd72d012074ca1cfb0fCAS |

Suga S, Komatsu S, Maeshima M (2002) Aquaporin isoforms responsive to salt and water stresses and phytohormones in radish seedlings. Plant & Cell Physiology 43, 1229–1237.
Aquaporin isoforms responsive to salt and water stresses and phytohormones in radish seedlings.CrossRef | 1:CAS:528:DC%2BD38Xot12htbY%3D&md5=702eb57055aabf5492138c5290d0ad22CAS |

Tyerman SD, Niemietz CM, Bramley H (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant, Cell & Environment 25, 173–194.
Plant aquaporins: multifunctional water and solute channels with expanding roles.CrossRef | 1:CAS:528:DC%2BD38Xhslaktbk%3D&md5=2fdcce3231683752976e666afc2cdcb5CAS |

Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, research0034–research0034.11.
Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.CrossRef |

Wolf O, Jeschke WD, Hartung W (1990) Long distance transport of abscisic acid in NaCl-treated intact plants of Lupinus albus. Journal of Experimental Botany 41, 593–600.
Long distance transport of abscisic acid in NaCl-treated intact plants of Lupinus albus.CrossRef | 1:CAS:528:DyaK3cXkvFCqur4%3D&md5=85b58bda3339fb4cd9da7dba64da9956CAS |

Yamada S, Katsuhara M, Kelly WB, Michlowski CB, Bohnert HJ (1995) A family of transcripts encoding water channel proteins: tissue specific expression in the common ice plant. The Plant Cell 7, 1129–1142.

Zhu C, Schraut D, Hartung W, Schäffner AR (2005) Differential responses of maize MIP genes to salt stress and ABA. Journal of Experimental Botany 56, 2971–2981.
Differential responses of maize MIP genes to salt stress and ABA.CrossRef | 1:CAS:528:DC%2BD2MXhtFCjt7nN&md5=12b93cbb0791867957882ca09cf6f8b9CAS |



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