Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
EVOLUTIONARY REVIEW

The evolution of abscisic acid (ABA) and ABA function in lower plants, fungi and lichen

Wolfram Hartung

A Lehrstuhl Botanik I, der Universität Würzburg, Julius von Sachsplatz 2, D 97082 Würzburg, Germany. Email: hartung@botanik.uni-wuerzburg.de

This paper is part of an ongoing series: ‘The Evolution of Plant Functions’.

Functional Plant Biology 37(9) 806-812 http://dx.doi.org/10.1071/FP10058
Submitted: 16 March 2010  Accepted: 27 May 2010   Published: 24 August 2010

Abstract

Abscisic acid (ABA) – the universal stress hormone of cormophytes – was detected in very low concentrations in almost all organisms tested from a range of cyanobacteria, algae, bryophytes, fungi and lichens and higher plants (Fig. 1). There are a few reports only on stress-induced ABA biosynthesis in cyanobacteria and algae. This extra ABA is released to the external medium. Application of external ABA has been shown to produce weak and contradicting effects on development and metabolism of algae. In most studies, extremely high concentrations of external ABA have been applied, those being far beyond any physiological concentration range. It is, therefore, extremely difficult to discuss those data satisfactorily. When organisms start to colonise terrestrial habitats (e.g. aquatic liverworts, mosses), endogenous ABA is increased even under mild drought stress, then desiccation protecting mechanisms are stimulated and the formation of terrestrial organs is induced. The same can be observed in water ferns (Marsilea) and in a range of heterophyllous angiosperms. Sporophytes of hornwort and mosses that bear true stomata, have particularly high ABA levels and their stomata respond to ABA as is the case in cormophytes, although a significant regulatory function of these stomata does not exist. Fungi produce large amounts of ABA that are released into the external medium and do not seem to have a function for the fungus. Fungal ABA, however, may be significant in associations of fungi with cyanophytes and algae (lichens), in mycorrhizal associations and in the rhizosphere of higher plants.

Additional keywords: algae, bacteria, cyanophytes, desiccation, landform, rhizosphere, soil, stomata, stress.


References

Ahmad MR Saxena PM Amla DV Shyam R 1978 Effect of abscisic acid on the blue green algae Anacystis nidulans and Nostoc muscorum. Beiträge zur Biologie der Pflanzen 54 33 40

Assante G Merlini L Nasini G 1977 (+)-Abscisic acid, a metabolite in the fungus Cercospora rosicola. Experientia 33 1556 1557
doi:10.1007/BF01933993

Bajguz A 2009 Brassinosteroid enhanced the level of abscisic acid in Chlorella vulgaris subjected to short term heat stress. Journal of Plant Physiology 166 882 886 doi:10.1016/j.jplph.2008.10.004

Bopp-Buhler ML Wabra P Hartung W Gimmler H 1991 Evidence for direct ABA synthesis in Dunaliella (Volvocales). Cryptogamic Botany 2/3 192 200

Bresinski A , Kadereit W (2002) Systematik und Stammesgeschichte. In ‘Lehrbuch der Botanik für Hochschulen’. (Ed. E Strasburger) pp. 571–884. (Spektrum Akademischer Verlag: Berlin)

Cohen AC Travaglia CN Bottini R Piccoli PN 2009 Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botany 87 455 462
doi:10.1139/B09-023

Cowan AK Rose PD 1991 Abscisic acid metabolism in salt-stressed cells of Dunaliella salina. Plant Physiology 97 798 803 doi:10.1104/pp.97.2.798

Cowan AK Rose PD Horne LG 1992 Dunaliella salina: a model system for studying the response of plant cells to stress. Journal of Experimental Botany 43 1535 1547 doi:10.1093/jxb/43.12.1535

Danneberg G Latus C Zimmer W Hundshagen B Schneider-Poetsch JH Bothe H 1992 Influence of vesicular arbuscular mycorrhiza on phytohormone balances in maize (Zea mays L.). Journal of Plant Physiology 141 33 39

Darwin Ch (1880) ‘The power of movement in plants.’ (John Murray: London)

Dietz S Hartung W 1997 Regulation of the abscisic acid content in the two lichen species Hypogymnia physoides and Peltigera praetextata. Bibliotheca Lichenologica 20 119 126


Dietz S Hartung W 1998 Abscisic acid in lichens: variation, water relations and metabolism. New Phytologist 138 99 106
doi:10.1046/j.1469-8137.1998.00881.x

Dietz S Hartung W 1999 The effect of abscisic acid (ABA) on chlorphyll fluorescence in lichens under extreme water regimes. New Phytologist 143 495 501 doi:10.1046/j.1469-8137.1999.00473.x

Ergün N Topcuoglu SF Yildiz A 2002 Auxin (indole-3-acetic acid) gibberellic acid (GA3), abscisic acid (ABA) and cytokinin (zeatin) production in some species of mosses and lichens. Turkish Journal of Botany 26 13 18

Forchetti G Masciarelli O Alemano S Alvarez D Abdala G 2007 Endophytic bacteria in sunflower (Helianthus annuus L.): isolation, characterization, and production of jasmonates and abscisic acid in culture medium. Applied Microbiology and Biotechnology 76 1145 1152
doi:10.1007/s00253-007-1077-7

Garner LB Paolillo DJ 1973 On the function of the stomata in Funaria. The Bryologist 76 423 427 doi:10.2307/3241726

Gee D Anderson LWJ 1998 Influence of leaf age on responsiveness of Potamogeton nodosus to ABA induced heterophylly. Plant Growth Regulation 24 119 125 doi:10.1023/A:1005912727159

Goliber TE 1989 Endogenous ABA content correlates with photon fluence rate and induced leaf morphology in Hippuris vulgaris. Plant Physiology 89 732 734 doi:10.1104/pp.89.3.732

Hartung W , Eggeling S (1984) ‘Untersuchungen zur Biosynthese, zum Metabolismus und zum Transport von Abscisinsäure (ABA) bei Cercospora cruenta unter osmotischem Stress. Mitteilungsband. Kurzfassungen der Beiträge’ Botanikertagung in Wien 1984, (Ed. F Ehrendorfer) p. 43. (Deutsche Botanische Gesellschaft: Wien)

Hartung W Gimmler H 1994 A stress physiological role for abscisic acid (ABA) in lower plants. Progress in Botany 55 157 173

Hartung W Weiler EW Volk OH 1987 Immunochemical evidence that abscisic acid is produced by several species of Anthocerotae and Marchantiales. The Bryologist 90 393 400
doi:10.2307/3243104

Hartung W Sauter A Turner NC Fillery I Heilmeier H 1996 Abscisic acid in soils: what is its function and which factors influence its concentration? Plant and Soil 184 105 110 doi:10.1007/BF00029279

Hellwege EM Hartung W 1997 Synthesis, metabolism and compartmentation of abscisic acid in Riccia fluitans L. Journal of Plant Physiology 150 287 291

Hellwege E Volk OH Hartung W 1992 A physiological role of abscisic acid in the liverwort Riccia fluitans. Journal of Plant Physiology 140 553 556


Hellwege E Dietz KJ Volk OH Hartung W 1994 Abscisic acid and the induction of desiccation resistance in the extremely xerophilic liverwort Exormotheca holstii. Planta 194 525 531
doi:10.1007/BF00714466

Hellwege E Dietz KJ Hartung W 1996 Abscisic acid causes changes in gene expression involved in the induction of the landform in the liverwort Riccia fluitans L. Planta 198 423 432 doi:10.1007/BF00620059

Hirsch R Hartung W Gimmler H 1989 Abscisic acid content of algae under stress. Botanica Acta 102 326 334

Huang CY 1991 Regulation of ionic fluxes and protein release from Anabaena HA101 by exogenous abscisic acid. Botanical Bulletin Academia Sinica 32 265 270


Hussain A Boney AD 1973 Hydrophilic growth inhibitors from Laminaria digitata and Ascophyllum nodosum. New Phytologist 72 403 410
doi:10.1111/j.1469-8137.1973.tb02048.x

Ishiura M 1976 Gametogenesis of Chlamydomonas in the dark. Plant & Cell Physiology 17 1141 1151

Jacobs WP (1985) Are angiosperm hormones present in, and used as hormones in algae? In ‘Plant growth substances’. (Ed. M Bopp) pp. 249–256. (Springer: Berlin)

Jameson PE (1993) Plant hormones in the algae. In ‘Progress in phycological research’. (Eds E Round, DJ Chapman) pp. 240–279. (Biopress Ltd: Bristol, UK)

Jiang F Hartung W 2008 Long-distance signalling of abscisic acid (ABA): the factors regulating the intensity of the ABA signal. Journal of Experimental Botany 59 37 43
doi:10.1093/jxb/erm127

Kane ME Albert LS 1982 Environmental and growth regulator effects on heterophylly and growth of Proserpinaca intermedia Haloragaceae. Aquatic Botany 13 73 85 doi:10.1016/0304-3770(82)90042-0

Kentzer T Mazur H 1991 Abscisic acid as endogenous inhibitor of the marine diatom Coscinodiscus granii. Acta Physiologiae Plantarum 13 153 157

Kettner J (1991) Untersuchungen zur Biosynthese von Abscisinsäure bei der Interaktion des pflanzenpathogenen Pilzes Botrytis cinerea Pers. mit der Kulturtomate Lycopersicon esculentum Mill. PhD Thesis. Universität Hamburg, Germany.

Kettner J Dörffling K 1987 Abscisic acid metabolism in Ceratocystis coerulescens. Physiologia Plantarum 69 278 282
doi:10.1111/j.1399-3054.1987.tb04287.x

Kitagawa Y Yamamoto H Oritani T 1995 Biosynthesis of abscisic acid in the fungus Cercospora cruenta: stimulation of biosynthesis by water stress and isolation of a transgenic mutant with reduced biosynthetic capacity. Plant & Cell Physiology 36 557 564

Kobayashi M Hirai N Kurimura Y Ohigashi H Tsuji Y 1997 Abscisic acid dependent morphogenesis in the unicellular green alga Haematococcus pluvialis. Plant Growth Regulation 22 79 85
doi:10.1023/A:1005862809711

Kobayashi M Todoroki Y Hirai N Kurimura Y Ohigashi H Tsuji Y 1998 Biological activities of abscisic acid analogs in the morphological change of the green alga Haematococcus pluvialis. Journal of Fermentation and Bioengineering 85 529 531 doi:10.1016/S0922-338X(98)80076-7

Kuwabara A Ikegami K Koshiba T Nagata T 2003 Effects of ethylene and abscisic acid upon heterophylly in Ludwigia arcuata (Onagraceae). Planta 217 880 887 doi:10.1007/s00425-003-1062-z

Lin BL Wang HJ Wang JS Zaharia LI Abrams SR 2005 Abscisic acid regulation of heterophylly in Marsilea quadrifolia L.: effects of R-(–) an S-(+) isomers. Journal of Experimental Botany 56 2935 2948 doi:10.1093/jxb/eri290

Manickavelu A Nadarajan N Ganesh SK Ramalingam R Raguraman S Gnanamalar RP 2006 Organogenesis induction in rice callus by cyanobacterial extracellular product. African Journal of Biotechnology 5 437 439

Marsalek B Simek M 1992 Abscisic acid and its synthetic analog in relation to growth and nitrogenase activity of Azotobacter chroococcum and Nostoc muscorum. Folia Microbiologica 37 159 160
doi:10.1007/BF02836623

Marsalek B Zahradnickova H Hronkova M 1992 a Extracellular abscisic acid produced by cyanobacteria under salt stress. Journal of Plant Physiology 139 506 508

Marsalek B Zahradnickova H Hronkova M 1992 b Extracellular production of abscisic acid by soil algae under salt, acid or drought stress. Zeitschrift für Naturforschung 47c 701 704


Marsalek B Simek M Lukesova A 1992 c The effect of abscisic and gibberellic acids on nitrogenase activity and growth of the cyanobacterium Nostoc muscorum AGARDH. Algological Studies 66 119 127


Müller M Deigele C Ziegler H 1989 Hormonal interaction in the rhizosphere of maize (Zea mays L.) and their effects on plant development. Zeitschrift für Pflanzenernährung und Bodenkunde 152 247 254
doi:10.1002/jpln.19891520217

Murakami-Mizukami Y Yamamoto Y Yamaki S 1991 Analyses of IAA and abscisic acid contents in nodules of soy bean plants bearing VA mycorrhizas. Soil Science and Plant Nutrition 37 291 298

Niemann DI Dörffling K 1980 Growth inhibitors and growth promoters in Enteromorpha compressa (Chlorophyta). Journal of Phycology 16 383 389
doi:10.1111/j.1529-8817.1980.tb03049.x

Norman SM Maier VP Echols SLC 1981 Influence of nitrogen source, thiamine and light on biosynthesis of abscisic acid by Cercospora rosicola. Applied and Environmental Microbiology 41 981 985

Ord GNSG Cameron IF Fensom DS 1977 The effect of pH and ABA on hydraulic conductivity of Nitella membranes. Canadian Journal of Botany 55 1 4
doi:10.1139/b77-001

Ott S Krieg T Spanier U Schieleit P 2000 Phytohormones in lichens with emphasis on ethylene biosynthesis and functional aspects on lichen symbiosis. Phyton 40 83 94

Pence VC Dunford SS Redella S 2005 Differential effects of abscisic acid on desiccation tolerance and carbohydrates in three species of liverworts. Journal of Plant Physiology 162 1331 1337
doi:10.1016/j.jplph.2005.02.002

Saradhi PP Suzuki I Katoh A Sakamoto A Sharmila P Shi DJ Murata N 2000 Protection against the photoinduced inactivation of the photosystem II complex by abscisic acid. Plant, Cell & Environment 23 711 718 doi:10.1046/j.1365-3040.2000.00579.x

Schmidt K Pflugmacher M Klages S Mäser A Mock A Stahl DJ 2008 Accumulation of the hormone abscisic acid (ABA) at the infection site of the fungus Cercospora beticola supports the role of ABA as a repressor of plant defence in sugar beet. Molecular Plant Pathology 9 661 673 doi:10.1111/j.1364-3703.2008.00491.x

Schroeter B Schlensog M Hartung W 2000 Abscisic acid in antarctic lichens. Bibliotheca Lichenologica 75 93 98

Simek M Marsalek B 1992 Evidence for abscisic acid caused enhancement of nitrogenase activity in Trichormus variabilis. Algological Studies 67 91 102


Simek M Marsalek B 1993 Response of the cyanobacterium Nostoc muscorum to abscisic acid and its analog LAB. Algological Studies 71 75 79


Stirk WA Drimalova D Strnad M van Staden J Oerdoeg V Balint P 2005 Diurnal fluctuations in the phytohormones of Chlorella minutissima. Phycologia 44 Suppl. S 98 99


Stopinska J Michniewicz M 1988 Control of growth and development of Ceratocystis fimbriata Ell. et Halst. by plant growth regulators. II. Abscisic acid. Bulletin of the Polish Academy of Sciences Biological Sciences 36 253 258


Takaichi S Mimuro M 1998 Distribution and geometric isomerism of neoxanthin in oxygenic phototrophs: 9′-cis, a sole molecular form. Plant & Cell Physiology 39 968 977


Tanaka S Ikeda K Miyasaka H 2004 Isolation of a new member of group 3 late embryogenesis abundant protein gene from a halotolerant gree alga by a functional expressiom screening with cyanobacterial cells. FEMS Microbiology Letters 236 41 45
doi:10.1111/j.1574-6968.2004.tb09624.x

Tietz A Kasprik W 1986 Identification of abscisic acid in green alga. Biochemie und Physiologie der Pflanzen 181 259 266

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
doi:10.1007/BF00018798

Tudzynski B , Sharon A (2002) Biosynthesis, biological role and application of fungal phytohormones. In ‘The Mycota X. Industrial applications’. (Ed. HD Osiewacx) pp. 183–224. (Springer-Verlag: Berlin)

Ullrich WR Kunz G 1984 Effect of abscisic acid on nitrate uptake respiration and photosynthesis in green algae. Plant Science Letters 37 9 14 doi:10.1016/0304-4211(84)90195-0

Vanden Driessche T Petiau-de Vries GM Guisset JL 1997 Differentiation, growth and morphogenesis: Acetabularia as a model system. New Phytologist 135 1 20 doi:10.1046/j.1469-8137.1997.00575.x

Wanless IR Bryniak N Fensom DS 1973 The effect of some growth regulating compounds upon electroosmotic measurements, transcellular water flow, and Na, K and Cl influx in Nitella flexilis. Canadian Journal of Botany 51 1055 1070 doi:10.1139/b73-130

Werner O Ros Espín RM Bopp M Atzorn R 1991 Abscisic-acid-induced drought tolerance in Funaria hygrometrica Hedw. Planta 186 99 103

Yokoya NS Stirk W Strnad M van Staden J 2009 Endogenous cytokinins, auxin and abscisic acid in Brazilian red algae. Phycologia 48 4, Suppl. S 147 148


Yoshida K 2005 Evolutionary process of stress response systems controlled by abscisic acid in photosynthetic organisms. Yakugaku Zasshi 125 927 936
doi:10.1248/yakushi.125.927

Yoshida K Igarashi E Mukai M Hirata K Miyamato K 2003 Induction of tolerance to oxidative stress in green alga, Chlamydomonas reinhardtii, by abscisic acid. Plant, Cell & Environment 26 451 457 doi:10.1046/j.1365-3040.2003.00976.x

Yoshida K Igarashi E Wakatsugi E Myamoto K Hirata K 2004 Mitigation of osmotic and salt stresses by abscisic acid through reduction of stress derived oxidative damage in Chlamydomonas reinhardtii. Plant Science 167 1335 1341 doi:10.1016/j.plantsci.2004.07.002

Young JP Dengler NG Horton RF 1987 Heterophylly in Ranunculus flabellaris. The effect of abscisic acid on leaf anatomy. Annals of Botany 60 117 126

Zahradnickova H Marsalek B Polisenska M 1991 High performance thin layer chromatographic and high performance liquid chromatographic determination of abscisic acid produced by cyanobacteria. Journal of Chromatography. A 555 239 245
doi:10.1016/S0021-9673(01)87184-3

Zhang W Yamane H Chapman DJ 1993 The phytohormone profile in the red alga Porphyra perforata. Botanica Marina 36 257 266 doi:10.1515/botm.1993.36.3.257


Full Text PDF (248 KB) Export Citation Cited By (31)