Skip to main content
SpringerLink
Log in

Role of abscisic acid (ABA) in activating antioxidant tolerance responses to desiccation stress in intertidal seaweed species

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

The hormone ABA regulates the oxidative stress state under desiccation in seaweed species; an environmental condition generated during daily tidal changes.

Desiccation is one of the most important factors that determine the distribution pattern of intertidal seaweeds. Among most tolerant seaweed is Pyropia orbicularis, which colonizes upper intertidal zones along the Chilean coast. P. orbicularis employs diverse mechanisms of desiccation tolerance (DT) (among others, e.g., antioxidant activation, photoinhibition, and osmo-compatible solute overproduction) such as those used by resurrection plants and bryophytes. In these organisms, the hormone abscisic acid (ABA) plays an important role in regulating responses to water deficit, including gene expression and the activity of antioxidant enzymes. The present study determined the effect of ABA on the activation of antioxidant responses during desiccation in P. orbicularis and in the sensitive species Mazzaella laminarioides and Lessonia spicata. Changes in endogenous free and conjugated ABA, water content during the hydration–desiccation cycle, enzymatic antioxidant activities [ascorbate peroxidase (AP), catalase (CAT) and peroxiredoxine (PRX)], and levels of lipid peroxidation and cell viability were evaluated. The results showed that P. orbicularis had free ABA levels 4–7 times higher than sensitive species, which was overproduced during water deficit. Using two ABA inhibitors (sodium tungstate and ancymidol), ABA was found to regulate the activation of the antioxidant enzymes activities during desiccation. In individuals exposed to exogenous ABA the enzyme activity increased, concomitant with low lipid peroxidation and high cell viability. These results demonstrate the participation of ABA in the regulation of DT in seaweeds, and suggest that regulatory mechanisms with ABA signaling could be of great importance for the adaptation of these organisms to dehydration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

AP:

Ascorbate peroxidase

CAT:

Catalase

DT:

Desiccation tolerance

MEP:

Methylerythritol phosphate

MVA:

Mevalonate

MTT:

(3-[4,5-Dimethylthiazol-2yl]-2,5-diphenyltetrazolium bromide)

PRX:

Peroxiredoxine

ROS:

Reactive oxygen species

References

  • Abe S, Kurashima A, Yokohama Y, Tanaka J (2001) The cellular ability of desiccation tolerance in Japanese intertidal seaweeds. Bot Mar 44:125–131

  • Alpert P (2000) The discovery, scope, and puzzle of desiccation tolerance in plants. Plant Ecol 151:5–17

    Article  Google Scholar 

  • Alpert P (2005) The limits and frontiers of desiccation-tolerant life. Integr Comp Biol 45:685–695

    Article  PubMed  Google Scholar 

  • Bajguz A (2009) Brassinosteroid enhanced the level of abscisic acid in Chlorella vulgaris subjected to short-term heat stress. J Plant Physiol 166:882–886

    Article  PubMed  CAS  Google Scholar 

  • Bartels D, Schneider K, Terstappen G, Piatkowski D, Salamini F (1990) Molecular cloning of ABA-modulated genes from the resurrection plant Craterostigma plantagineum which are induced during desiccation. Planta 181:27–34

    Article  PubMed  CAS  Google Scholar 

  • Bell EC (1993) Photosynthetic response to temperature and desiccation of the intertidal alga Mastocarpus papillatus. Mar Biol 117:337–346

    Article  Google Scholar 

  • Bray EA, Zeevaart JDA (1985) The compartmentation of abscisic acid and 8-D-glucopyranosyl abscisate in mesophyll cells. Plant Physiol 79:719–722

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Brown MT (1987) Effects of desiccation on photosynthesis of intertidal algae from a southern New Zealand shore. Bot Mar 30:121–127

  • Castro P, Huber M (2003) Between the tides. In: Castro P, Huber M (eds) Marine biology, 4th edn. McGraw-Hill Science, London, pp 235–258

    Google Scholar 

  • Chang WC, Chen MH, Lee TM (1999) 2,3,5-Triphenyltetrazolium reduction in the viability assay of Ulva fasciata (Chlorophyta) in response to salinity stress. Bot Bull Acad Sinica 40:207–212

    CAS  Google Scholar 

  • Contreras L, Moenne A, Correa JA (2005) Antioxidant responses in Scytosiphon lomentaria (Phaeophyceae) inhabiting copper enriched coastal environments. J Phycol 41:1184–1195

    Article  CAS  Google Scholar 

  • Contreras-Porcia L, Thomas D, Flores V, Correa JA (2011) Tolerance to oxidative stress induced by desiccation in Porphya columbina (Bangiales, Rhodophyta). J Exp Bot 62:1815–1829

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Contreras-Porcia L, Callejas S, Thomas D, Sordet C, Pohnert G, Contreras A, Lafuente A, Flores-Molina M, Correa JA (2012) Seaweeds early development: detrimental effects of desiccation and attenuation by algal extracts. Planta 235:337–348

    Article  PubMed  CAS  Google Scholar 

  • Contreras-Porcia L, López-Cristoffanini C, Lovazzano C et al (2013) Differential gene expression in Pyropia columbina (Plantae, Rhodophyta) under natural hydration and desiccation stress. Lat Am J Aquat Res 41:933–958

    Article  Google Scholar 

  • Coolbaugh R, Hamilton R (1976) Inhibition of ent-kaurene oxidation and growth by as cyclopropyl-a-(p-methoxyphenyl)-5-pyrimidine methyl alcohol. Plant Physiol 57:245–248

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Cowan A, Rose P (1991) Abscisic acid metabolism in salt-stressed cells of Dunaliella salina. Possible interrelationship with β-carotene accumulation. Plant Physiol 97:798–803

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Cruz De Carvalho RC, Branquinho C, da Silva JM (2011) Physiological consequences of desiccation in the aquatic bryophyte Fontinalis antipyretica. Planta 234:195–205

    Article  CAS  Google Scholar 

  • Cutler A, Krochko J (1999) Formation and breackdown of ABA. Trends Plant Sci 4:1360–1385

    Article  Google Scholar 

  • Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    Article  PubMed  CAS  Google Scholar 

  • Davison IR, Pearson GA (1996) Stress tolerance in intertidal seaweeds. J Phycol 32:197–211

    Article  Google Scholar 

  • Dring MJ, Brown FA (1982) Photosynthesis of intertidal brown algae during and after periods of emersion: a renewed search for physiological causes of zonation. Mar Ecol Prog Ser 8:301–308

    Article  Google Scholar 

  • Fierro C (2013) Cinética de expresión de genes de tolerancia identificados en la macroalga roja Pyropia columbina bajo el ciclo desecación-rehidratación natural: comparación funcional con especies sensibles. Universidad de Chile, p 65

  • Finkelstein R, Rock C (2002) Abscisic acid biosynthesis and response. The Arabidopsis Book, pp 1–52

  • Finkelstein R, Gampala S, Rock C (2002) Abscisic acid signaling in seeds and seedlings. The Plant Cell: S15–S45

  • Flores-Molina MR, Thomas D, Lovazzano C, Núñez A, Zapata J, Kumar M, Correa JA, Contreras-Porcia L (2014) Desiccation stress in intertidal seaweeds: effects on morphology, photosynthetic performance and antioxidant responses. Aquat Bot 113:90–99

    Article  CAS  Google Scholar 

  • Gao C, Zhang K, Yang G, Wang Y (2012) Expression analysis of four peroxiredoxin genes from Tamarix hispida in response to different abiotic stresses and exogenous abscisic acid (ABA). Int J Mol Sci 13:3751–3764

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Geiger D, Scherzer S, Mumm P et al (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci USA 106:21425–21430

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Grill E, Himmelbach A (1998) ABA signal transduction. Curr Opin Plant Biol 1:412–418

    Article  PubMed  CAS  Google Scholar 

  • Guillemin M-L, Contreras-Porcia L, Ramírez ME, Macaya EC, Bulboa C, Woods H, Wyatt CH, Brodie J (2016) The bladed Bangiales (Rhodophyta) of the South Eastern Pacific: molecular species delimitation reveals extensive diversity. Mol Phyl Evol 94:814–826

    Article  Google Scholar 

  • Hansen H, Grossmann K (2000) Auxin-induced ethylene triggers abscisic acid biosynthesis and growth inhibition. Plant Physiol 124:1437–1448

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hartung W (2010) The evolution of abscisic acid (ABA) and ABA function in lower plants, fungi and lichen. Funct Plant Biol 37:806–812

    Article  CAS  Google Scholar 

  • He T, Cramer GR (1996) Abscisic acid concentrations are correlated with leaf area reductions in two salt-stressed rapid-cycling Brassica species. Plant Soil 179:25–33

    Article  CAS  Google Scholar 

  • Hu X, Jiang M, Zhang A, Lu J (2005) Abscisic acid-induced apoplastic H2O2 accumulation up-regulates the activities of chloroplastic and cytosolic antioxidant enzymes in maize leaves. Planta 223:57–68

    Article  PubMed  CAS  Google Scholar 

  • Hurd CL, Harrison PJ, Bischof K, Lobban CH (2014) Seaweed ecology and physiology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Ikegami K, Okamoto M, Seo M, Koshiba T (2009) Activation of abscisic acid biosynthesis in the leaves of Arabidopsis thaliana in response to water deficit. J Plant Res 122:235–243

    Article  PubMed  CAS  Google Scholar 

  • Jiang M, Zhang J (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53:2401–2410

    Article  PubMed  CAS  Google Scholar 

  • Karadeniz A, Topcuoglu SF, Inan S (2006) Auxin, gibberellin, cytokinin and abscisic acid production in some bacteria. World J Microb Biot 22:1061–1064

    Article  CAS  Google Scholar 

  • Kobayashi M, Hirai N, Kurimura Y, Ohigashi H, Tsuji Y (1997) Abscisic acid-dependent algal morphogenesis in the unicellular green alga Haematococcus pluvialis. Plant Growth Regul 22:79–85

    Article  CAS  Google Scholar 

  • López-Cristoffanini C, Tellier F, Otaíza R, Correa JA, Contreras-Porcia L (2013) Tolerance to air exposure: a feature driving the latitudinal distribution of two sibling kelp species. Bot Mar 56:431–440

  • López-Cristoffanini C, Zapata J, Gaillard F, Potin P, Correa JA, Contreras-Porcia L (2015) Identification of proteins involved in the tolerance responses to desiccation stress in the red seaweed Pyropia orbicularis (Rhodophyta. Bangiales). Proteomics. doi:10.1002/pmic.201400625

    Google Scholar 

  • Lovazzano C, Serrano C, Correa JA, Contreras-Porcia L (2013) Comparative analysis of peroxiredoxin activation in the brown macroalgae Scytosiphon gracilis and Lessonia nigrescens (Phaeophyceae) under copper stress. Physiol Plant 149:378–388

    PubMed  CAS  Google Scholar 

  • Milborrow BV (2001) The pathway of biosynthesis of abscisic acid in the vascular plants: a review of the present state of knowledge of ABA biosynthesis. J Exp Bot 52:1145–1164

    Article  PubMed  CAS  Google Scholar 

  • Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Physiol 56:165–185

    CAS  Google Scholar 

  • Nimura K, Mizuta H (2002) Inducible effects of abscisic acid on sporophyte discs from Laminaria japonica Areschoug (Laminariales, Phaeophyceae). J Appl Phycol 14:159–163

    Article  CAS  Google Scholar 

  • Norman SM, Poling SM, Maier VP, Orme ED (1983) Inhibition of abscisic acid biosynthesis in Cercospora rosicola by inhibitors of gibberellin biosynthesis and plant growth retardants. Plant Physiol 71:15–18

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Pierce M, Raschke K (1980) Correlation between loss of turgor and accumulation of abscisic acid in detached leaves. Planta 148:174–182

    Article  PubMed  CAS  Google Scholar 

  • Popisilova J (2003) Participation of the phytohormones in the stomatal regulation of gas exchange during water stress. Biol Plant 46:491–506

    Article  Google Scholar 

  • Raghavendra A, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401

    Article  PubMed  CAS  Google Scholar 

  • Ramírez ME, Contreras-Porcia L, Guillemin ML, Brodie J, Valdivia C, Flores-Molina MR, Núñez A, Bulboa-Contador C, Lovazzano C (2014) Pyropia orbicularis sp. nov. (Rhodophyta, Bangiaceae) based on a population previously known as Porphyra columbina from the central coast of Chile. Phytotaxa 158:133–153

    Article  Google Scholar 

  • Ratkevicius N, Correa JA, Moenne A (2003) Copper accumulation, synthesis of ascorbate and activation of ascorbate peroxidase in Enteromorpha compressa (L.) Grev. (Chlorophyta) from heavy metal-enriched environments in northern Chile. Plant Cell Environ 26:1599–1608

    Article  CAS  Google Scholar 

  • Ritter A, Ubertini M, Romac S et al (2010) Copper stress proteomics highlights local adaptation of two strains of the model brown alga Ectocarpus siliculosus. Proteomics 10:2074–2088

    Article  PubMed  CAS  Google Scholar 

  • Saradhi P, Suzuki I, Katoh A, Sakamoto A, Sharmila P, Shi D, Murata N (2000) Protection against the photo-induced inactivation of the photosystem II complex by abscisic acid. Plant Cell Environ 23:711–718

    Article  CAS  Google Scholar 

  • Schiller P, Heilmeier H, Hartung W (1997) Abscisic acid (ABA) relations in the aquatic resurrection plant Chamaegigas intrepidus under naturally fluctuating environmental conditions. New Phytol 136:603–611

    Article  CAS  Google Scholar 

  • Seo M, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends Plant Sci 1:1360–1385

    Google Scholar 

  • Shafer D, Sherman T, Wyllie-Echeverria S (2007) Do desiccation tolerances control the vertical distribution of intertidal seagrasses? Aquat Bot 87:161–166

    Article  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene Expression and signal transduction in water-stress response. Plant Physiol 115:327–334

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: difference and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223

    Article  PubMed  CAS  Google Scholar 

  • Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85 [Erratum en: Anal Biochem (1987). 163:279]

    Article  PubMed  CAS  Google Scholar 

  • Steadman J, Sequeira L (1970) Abscisic acid in tobacco plants. Plant Physiol 45:691–697

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Stephenson TA, Stephenson A (1949) The universal features of zonation between tide-marks on rocky coasts. J Ecol 37:289–305

    Article  Google Scholar 

  • Stirk W, Novák O, Hradecka V, Pencík A, Rolcík J, Strnad M, Van Staden J (2009) Endogenous cytokinins, auxins and abscisic acid in Ulva fasciata (Chlorophyta) and Dictyota humifusa (Phaeophyta): towards understanding their biosynthesis and homoeostasis. Eur J Phycol 44:231–240

    Article  CAS  Google Scholar 

  • Thurman RG, Ley HG, Scholz R (1972) Hepatic microsomal ethanol oxidation. Hydrogen peroxide formation and the role of catalase. Eur J Biochem 25:420–430

    Article  PubMed  CAS  Google Scholar 

  • Tietz A, Ruttkowski U, Köhler R, Kasprik W (1989) Further investigations on the occurrence and the effects of abscisic acid in algae. Biochem Physiol Pfl 184:259–266

    Article  CAS  Google Scholar 

  • Tominaga N, Takahata M, Tominaga H (1993) Effects of NaCl and KNO3 concentrations on the abscisic acid content of Dunaliella sp. (Chlorophyta). Hydrobiologia 267:163–168

    Article  CAS  Google Scholar 

  • Towill LE, Mazur P (1975) Studies on the reduction of 2,3,5-triphenyltretrazolium chloride as a viability assay for plant tissue cultures. Can J Bot 53:1097–1102

    Article  Google Scholar 

  • Ünyayar S, Topcuoglu F, Ünyayar A (1996) A modified method for extraction and identification of indole-3-acetic acid (IAA), gibberellic acid (GA3), abscisic acid (ABA) and zeatin produced by Phanerochate chrysosporium. Bulg J Plant Physiol 22:105–110

    Google Scholar 

  • Werner O, Ros Espin RM, Bopp M, Atzorn R (1991) Abscisic-acid-induced drought tolerance in Funaria hygrometrica Hedw. Planta 186:99–103

    Article  PubMed  CAS  Google Scholar 

  • Yokoya N, Stirk W, van Staden J, Novák O, Turecková V, Pencík A, Strnad M (2010) Endogenous cytokinins, auxins, and abscisic acid in red algae from Brazil. J Phycol 46:1198–1205

    Article  CAS  Google Scholar 

  • Yoshida K, Igarashi E, Mukai M, Hirata K, Miyamoto K (2003) Induction of tolerance to oxidative stress in the green alga, Chlamydomonas reinhardtii, by abscisic acid. Plant Cell Environ 26:451–457

    Article  CAS  Google Scholar 

  • Yoshida K, Igarashi E, Wakatsuki E, Miyamoto K, Hirata K (2004) Mitigation of osmotic and salt stresses by abscisic acid through reduction of stress-derived oxidative damage in Chlamydomonas reinhardtii. Plant Sci 167:1335–1341

    Article  CAS  Google Scholar 

  • Zar JH (2010) Multisample hypotheses and the analysis of variance. In: Zar JH (ed) Biostatistical analysis, 5th edn. Pearson Prentince Hall, New Jersey, pp 189–224

    Google Scholar 

  • Zardi GI, Nicastro KR, Ferreira Costa J, Serrao EA, Pearson GA (2013) Broad scale agreement between intertidal habitats and adaptive traits on a basis of contrasting population genetic structure. Estuar Coast Shelf S 131:140–148

    Article  Google Scholar 

  • Zeevaart JA, Creelman RA (1988) Metabolism and physiology of abscisic acid. Ann Rev Plant Physiol Plant Mol Biol 39:439–473

    Article  CAS  Google Scholar 

  • Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crop Res 97:111–119

    Article  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Ann Rev Plant Biol 53:247–273

    Article  CAS  Google Scholar 

  • Zörb C, Schmitt S, Mühling KH (2010) Proteomic changes in maize roots after short-term adjustment to saline growth conditions. Proteomics 10:4441–4449

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by FONDECYT 1120117 and DI-501-14/R (Universidad Andrés Bello, Proyectos Regulares Internos) to LC-P. We are especially grateful to C. Fierro, D. Thomas, A. Núñez, C. López-Cristoffanini, J. Zapata and C. Lovazzano for field assistance. The comments and suggestions of anonymous reviewers helped to improve the final version of the manuscript, and their assistance is deeply appreciated.

Author information

Authors and Affiliations

  1. Departamento de Ecología y Biodiversidad, Facultad de Ecología y Recursos Naturales, Universidad Andres Bello, República 440, Santiago, Chile

    Eduardo Guajardo & Loretto Contreras-Porcia

  2. Departamento de Ecología, and Center of Applied Ecology and Sustainability (CAPES), Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile

    Juan A. Correa

  3. UMI 3614, Evolutionary Biology and Ecology of Algae, Station Biologique de Roscoff, Roscoff, France

    Juan A. Correa

  4. Center of Applied Ecology and Sustainability (CAPES), Pontificia Universidad Católica de Chile, Santiago, Chile

    Loretto Contreras-Porcia

Authors
  1. Eduardo Guajardo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juan A. Correa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Loretto Contreras-Porcia
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Loretto Contreras-Porcia.

Ethics declarations

Conflict of interest

The authors have declared no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 82 kb)

Supplementary material 2 (DOCX 33 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guajardo, E., Correa, J.A. & Contreras-Porcia, L. Role of abscisic acid (ABA) in activating antioxidant tolerance responses to desiccation stress in intertidal seaweed species. Planta 243, 767–781 (2016). https://doi.org/10.1007/s00425-015-2438-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-015-2438-6

Keywords

Search

Navigation