The evolution of abscisic acid (ABA) and ABA function in lower plants, fungi and lichen
Wolfram HartungA 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 https://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.
Acknowledgements
The constructive comments of Professor Hermann Heilmeier (Technical University, Freiberg, Germany) and the help of Dr Jiang Fan (Beijing Normal University, Beijing) with the figures are gratefully acknowledged.
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bopp-Buhler ML,
Wabra P,
Hartung W, Gimmler H
(1991) Evidence for direct ABA synthesis in Dunaliella (Volvocales). Cryptogamic Botany 2/3, 192–200.
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.
| Crossref | GoogleScholarGoogle Scholar |
Cowan AK, Rose PD
(1991) Abscisic acid metabolism in salt-stressed cells of Dunaliella salina. Plant Physiology 97, 798–803.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Garner LB, Paolillo DJ
(1973) On the function of the stomata in Funaria. The Bryologist 76, 423–427.
| Crossref | GoogleScholarGoogle Scholar |
Gee D, Anderson LWJ
(1998) Influence of leaf age on responsiveness of Potamogeton nodosus to ABA induced heterophylly. Plant Growth Regulation 24, 119–125.
| Crossref | GoogleScholarGoogle Scholar |
Goliber TE
(1989) Endogenous ABA content correlates with photon fluence rate and induced leaf morphology in Hippuris vulgaris. Plant Physiology 89, 732–734.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
Ishiura M
(1976) Gametogenesis of Chlamydomonas in the dark. Plant & Cell Physiology 17, 1141–1151.
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kane ME, Albert LS
(1982) Environmental and growth regulator effects on heterophylly and growth of Proserpinaca intermedia Haloragaceae. Aquatic Botany 13, 73–85.
| Crossref | GoogleScholarGoogle Scholar |
Kentzer T, Mazur H
(1991) Abscisic acid as endogenous inhibitor of the marine diatom Coscinodiscus granii. Acta Physiologiae Plantarum 13, 153–157.
Kettner J, Dörffling K
(1987) Abscisic acid metabolism in Ceratocystis coerulescens. Physiologia Plantarum 69, 278–282.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Marsalek B,
Zahradnickova H, Hronkova M
(1992a) Extracellular abscisic acid produced by cyanobacteria under salt stress. Journal of Plant Physiology 139, 506–508.
Marsalek B,
Zahradnickova H, Hronkova M
(1992b) 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
(1992c) 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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
Ullrich WR, Kunz G
(1984) Effect of abscisic acid on nitrate uptake respiration and photosynthesis in green algae. Plant Science Letters 37, 9–14.
| Crossref | GoogleScholarGoogle Scholar |
Vanden Driessche T,
Petiau-de Vries GM, Guisset JL
(1997) Differentiation, growth and morphogenesis: Acetabularia as a model system. New Phytologist 135, 1–20.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
Werner O,
Ros Espín RM,
Bopp M, Atzorn R
(1991) Abscisic-acid-induced drought tolerance in Funaria hygrometrica Hedw. Planta 186, 99–103.
| Crossref |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
Zhang W,
Yamane H, Chapman DJ
(1993) The phytohormone profile in the red alga Porphyra perforata. Botanica Marina 36, 257–266.
| Crossref | GoogleScholarGoogle Scholar |
1 1The results seem to imply the presence of ‘some matter’ in the upper part which is acted on by light and which transmits its effect to the lower part.
