Phytohormones in algae - Springer Link

ISSN 1021-4437, Russian Journal of Plant Physiology, 2007, Vol. 54, No. 2, pp. 163–170. © Pleiades Publishing, Ltd., 2007. Original Russian Text © E.R. Tarakhovskaya, Yu.I. Maslov, M.F. Shishova, 2007, published in Fiziologiya Rastenii, 2007, Vol. 54, No. 2, pp. 186–194.

REVIEWS

Phytohormones in Algae E. R. Tarakhovskaya, Yu. I. Maslov, and M. F. Shishova Institute of Biology, St. Petersburg State University, Oranienbaumskoe sh. 2, Staryi Peterhof, 198504 Russia; e-mail: [email protected] Received June 5, 2006

Abstract—In various algal taxa, essentially all known phytohormones were detected in concentrations comparable with their content in higher plants. The occurrence of diverse free and conjugated hormone forms substantiates the functioning of the complex system of metabolism and activity regulation of these compounds. In most cases, the spectrum of biological activities of algal hormones corresponds to the functions of higher plant hormones. Some physiological and biochemical processes in algal cells and tissues are under the control of several phytohormones. All these facts permit a consideration of the algal hormonal system as a full-value regulatory system. DOI: 10.1134/S1021443707020021 Key words: phytohormones - algae - IAA - cytokinins - ABA - polyamines - jasmonic acid

INTRODUCTION Several system control growth and development of the plant organism at cellular, tissue, and organismal levels [1, 2]. The life of a unicellular organism is controlled by the gene, membrane, and enzymatic systems. In more complex plant organisms, the regulation at the tissue level acquires an increasing significance, providing for the contacts between cells. Firstly, the trophic system evidently arises, which provides for the exchange of nutrients and energy-rich compounds. Trophic factors secreted by the cells (sugars, alcohols, fatty acids, and amino acids) gradually acquire a signal role and a capability of controlling the activity of intracellular regulatory systems, gene transcription in particular [3]. The cells could excrete not only low-molecular compounds but also some polymers (proteins, polysaccharides, etc.); their physiological role was reliably proven in experiments with higher plant callus and suspension cell cultures [4–6]. All these compounds combined were named “the factors of conditioning.” A disturbance in the mechanisms of excretion could substantially reduce cell viability and the rate of embryogenesis. Thus, the nutrient medium enriched in the cell excretes could be considered a peculiar extracellular compartment with a regulatory function. At present, some data accumulated indicating that not only higher plant cultured cells but also microalgae, unicellular plant organisms, are capable of excretion of some lowmolecular compounds into ambient medium, and these compounds could fulfill a protective function or the function of attractants required during fertilization (reviewed in [7]). It seems likely that due to excretion of physiologically active compounds, frequently derivAbbreviation: IPA—isopentenyladenine.

atives of basic metabolic pathways, the second regulatory system of metabolism, the hormonal one, arises. R. Starling introduced the term hormone in 1905 for secretin isolated from duodenum and stimulating secretion of the pancreatic juice via blood. All-round studying the structure, functions, and action mechanism of higher plant hormones attracted the attention of many researchers both earlier and now. At present, ten groups of hormonal type physiologically active compounds are identified in higher plants (Table 1) [1, 8]. It is evident that only two of them, auxins and cytokinins, meet all criteria assumed at present, i.e., hormone is a lowmolecular compound displaying its action at a distance and at very low concentrations. Some indirect evidence permits a supposition that just these phytohormones appeared at the earliest steps of evolution. IAA is a natural auxin; one of its primary effects is activation of the plasmalemmal ç+-ATPase involved in the process of growth by elongation. This process could be considered as aromorphosis providing for an economic and rapid usage of basic resources of nutrition (light energy and mineral nutrients) [1, 2]. In higher plants, IAA is synthesized in chloroplasts of young leaves and induces the process of root formation. In contrast, cytokinins are synthesized mainly in the root tips but affect substantially shoot development, primarily, the functioning of the photosynthetic apparatus. Recent data concerning the pathways of phytohormone biosynthesis permit a conclusion that, in most cases, it is connected with chloroplasts [8]. According to modern notions about the origin of the eukaryotic cell, the plastid apparatus is an evolutionary development of a prokaryotic photosynthesizing organism [9]. Thus, it is expected that phytohormones, which synthesis and functioning is

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Table 1. Physiologically active substances of the hormonal type (after [1, 8]) Name

Biosynthetic pathway

Synthesis location

Basic physiological activity

Auxin

from tryptophan or indol leaf primordia, young induction of elongation growth; differentiation leaves, and developing fruits of phloem elements; apical dominance; tropisms; initiation of root formation; etc. Cytokinins biochemical modification root tips, young leaves, control of cell division; bud development; develof adenine and developing seeds opment of the leaf blade; senescence retardation; Gibberellins from glyceraldehydes-3- young shoot tissues stem elongation; initiation of seed germination phosphate and developing seeds Ethylene from methionine stressed tissues senescence induction; initiation of defensive and maturing fruits responses ABA from carotenoides roots and expanded leaves control of the stomatal apparatus function; growth inhibition; seed dormancy Polyamines by decarboxylation various tissues regulation of growth and development of arginine or ornithine at micromolar concentrations Brassinosteroids from mevalonic acid various tissues control of division, growth by elongation, differentiation of the vascular system Jasmonides from polyunsaturated various tissues development of defensive responses (oxilipins) fatty acids Salicylates from phenylalanine various tissues induction of the complex of defensive responses during pathogenesis Signal peptides from amino acids various tissues initiation of defensive responses; identification of self-imcompatibility

immediately connected with plastids, should display their regulatory activity in algae as well. At present, our knowledge of the algal hormonal system is still rather fragmentary. Until now, the presence of the full-value hormonal system in algae and the correspondence of their biological activities to those of higher plant hormones are debated [10, 11]. The information about the hormone metabolism and action mechanisms in algae is extremely scarce. In this review, we classify experimental data available concerning algal phytohormones. Algal phytohormone studying could be conventionally subdivided into the two periods. The boundary between them is primarily determined by the elaboration of methodological approaches, namely, the methods of algal hormone extraction and identification. In the 1960–1970s, an active search for phytohormones in various algal taxa was performed. During this period, a wide set of compounds with hormonal activity was found in Chlorophyta, Phaeophyta, and Rhodophyta. Among them are IAA, isopentenyladenine (IPA), GA, and lunularic acid [12–15]. Provasoli and Carlucci [14] reviewed these studies most comprehensively. However, later it turned out that some of the results obtained in the 1960–1970s were insignificant because the presence and concentrations of phytohormones were assessed after chromatographic separation of the extracts with subsequent quantification in bioassays [11]. A new surge of the interest to algal hormones arose approximately in the middle of the 1980s, and essentially all known phytohormones of higher plants

were found in algae. During this period, the spectra of algal hormone biological activity were thoroughly studied, the interaction between separate hormones and between the algal hormonal system with other regulatory system started to be analyzed [16–19]. These researches were reviewed by Bradley [10] and Sitnik et al. [20]. AUXINS In the 1960–1970s, it was found that auxins and their inactive analogs were present in brown (Macrocystis and Laminaria), red (Botryocladia), and green (Enteromorpha, Chlorella, and Cladophora) algae and also in cyanobacteria (Oscillatoria) ([21], for example). Further investigations confirmed these results but not all of them [22]. Nevertheless, using modern methodologies, it was demonstrated the presence of auxins (IAA in particular) in green and characean algae and in the extracts from brown algae (Fucus and Ascophyllum) [16, 18, 20, 23]. In zygotes and adult plants of Fucus distichus and F. vesiculosus, IAA was present at the concentrations only slightly lower than in higher plant tissues (2–9 ng/g fr wt) [24, 25]. The content of auxin in the algal thalli varied in dependence on the season and developmental stage. The highest concentration was observed in summer in vegetative tissues [20]. The data concerning the pathways of auxin synthesis and localization are very fragmentary. In the cyanobacterium Chlorogloea fritschii, some elements of the tryptophan-dependent pathway were found, tryptamine

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in particular [26]. In the green alga Caulerpa paspaloides, IAA and the product of its catabolism, dioxyindole-3-acetic acid, were detected [27]. CYTOKININS It was repeatedly shown that the extracts from the marine phytoplankton exhibited cytokinin activity [14]. These hormones were found in the extracts of fucoid algae. Zeatin, zeatin riboside, IPA, and isopentenyladenosine were identified in these extracts [23, 28]. Euglena gracilis chloroplasts contain tRNA with cytokinin activity and a wide spectrum of cytokinins, such as IPA, 2-methylisopentenyladenine, and 2-methylisopentenyladenosine [15]. IPA was found in the cyanobacterium Arthronema africanum, IPA, isopentenyladenosine, zeatin, zeatin riboside, and aromatic cytokinins, topolin conjugates, were identified in characean and green micro- and macroalgae [19, 20–21]. Basic cytokinins in green microalgae (Protococcus, Chlorella, and Scenedesmus) are free IPA, zeatin (cis-isomer prevails), and riboside and ribotide conjugates [19]. A great diversity of cytokinin conjugates is evidently rather a property of higher plants but not algae. Trace amounts of O-glucosides were detected in some microalgae and brown macrophytes (Sargassum heterophyllum, Macrocystis pyrifera) [31]. Such cytokinin species as dihydrozeatin and N-glucosides were not found in algae. It is possible that functions of N-glucosides (inactive cytokinins) in the control of the phytohormone level in the cells are partially fulfilled by cis-zeatin, which prevails in algae and is much less active than trans-isomer. In various algal groups, aromatic cytokinins (topolins) were found as well. Microalgae and macrophytes differ considerably in the relative content of these hormones: the proportion of aromatic cytokinins in them are 28 and < 1%, respectively [19, 31]. Thus, at present, both isoprenoid and aromatic cytokinins and some their conjugates are found in algae tested, which indicates the presence in algae of the complex systems of hormonal metabolism and of the control of hormonal activity. It is supposed that the pathway of cytokinin biosynthesis in algae differs from that in higher plants [32]. However, this question is not well studied. It seems likely that algal cytokinins are mostly produced at tRNA degradation [31]. The dynamics of the endogenous cytokinin content in algae is not essentially studied. In the cyanobacterium Arthronema africanum, daily oscillations of cytokinin activity were demonstrated. Similar processes were observed in green microalgae [19]. These oscillations evidently reflect changes in the cell physiological state in the culture at various stages of the life cycle. GIBBERELLINS There is only few data indicating the presence of compounds with gibberellin activity in brown algae, RUSSIAN JOURNAL OF PLANT PHYSIOLOGY

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and all of them were obtained in bioassays. Active gibberellins, GA1 and GA3, and inactive GA6 were isolated chromatographically from the tissue extracts of F. vesiculosus and F. spiralis [12]. The substances with gibberellin activity were also isolated from the green alga Caulerpa paspaloides, but they were not precisely identified [27]. ABSCISIC AND LUNULARIC ACIDS In various groups of algae, some compounds were repeatedly detected, which suppressed plant growth in bioassays [13, 16]. At least one component of this inhibitory complex was isolated from the green alga Enteromorpha compressa and studied. This component was identified as dihydrostilben, lunularic acid [16]. The identification of this compound confirmed a theory of Pryce [13], who supposed that, as distinct from higher plants, algae and liverworts do not contain ABA and its functions are fulfilled by lunularic acid. However, the increasing body of information appears about the presence of ABA in the algae of various groups. This hormone was found in green microalgae (Chlorella sp., Dunaliella salina, and Haematococcus pluvialis) and also in the thalli of brown macrophytes from the genus Ascophyllum and some species of Laminaria [33–35]. It might be that the growth-inhibiting complex found in various algal groups comprises several components, including lunularic acid, ABA, and some other so far unidentified biologically active compounds. One of the possible candidates for this role is salicylic acid [16]. Lunularic acid is a growth inhibitor of liverworts; its structure, metabolism, and the range of activities really resemble those of ABA [36]. Exogenous lunularic acid could imitate many effects of ABA in higher plants, in particular, such specific function as the suppression of α-amylase activity in cereal kernels [36, 37]. Assuming the hypothesis that several biologically active compounds fulfilling similar functions could be simultaneously present in algae, we could suppose that, during evolution, plants were subdivided into the groups, where basic growth inhibitors became lunularic acid (liverworts) and ABA (other higher plants). JASMONIC ACID Nuumerous oxylipins, including jasmonic acid and its volatile methyl ester, are found in almost all algae. These hormones were detected in green (Dunaliella tertiolecta, D. salina, and Chlorella sp.), Euglenophyta (Euglena gracilis), and red (Gelidium latifolium) algae and also in cyanobacteria (Spirulina sp.). In Chlorella and Lithothamnion, some components of the octadecanoid pathway of jasmonic acid biosynthesis from linolenic acid were detected. Various oxilipins and corresponding lipoxygenases were found in brown algae [20, 38]. No. 2

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POLYAMINES In red (Cyanidium caldarium, Gelidium canariensis, and Grateloupia doryphora) and brown (Dyctiota dichotoma) macrophytes and also in green (Ulva rigida and Chlorella sp.) and euglenacean (Euglena gracilis) algae, the compounds from the putrescine group (putrescine, spermine, and spermidine) are present [39– 41]. The content of polyamines in algae does not differ from that in higher plants (50–150 µg/g fr wt); the pathways of their biosynthesis are evidently similar as well. The activities of enzymes catalyzing some stages of polyamine synthesis were shown in algae [42]. The content of endogenous polyamines in macrophytes changes considerably in dependence on the season and the developmental stage of the alga [39, 42]. In G. doryphora, the content of all polyamines in tissues of the female gametophyte reduced with the developing of reproductive structures [42]. The algae secrete polyamines in the ambient medium [40]. BRASSINOSTEROIDS So far, we found only a single evidence for the presence of brassinosteroids in algal cells. 24-epicastasterone and 28-homocastasterone were identified in the green alga Hydrodictyon reticulatum. The concentrations of these hormones in the cell of this alga were 0.3 and 4.0 µg/kg fr wt, respectively, which corresponds to the brassinosteroid content in higher plants [43, 44]. RHODOMORPHIN This regulator was first found in the red filamentous alga Griffithsia pacifica [45]. It was demonstrated its following morphogenetic effect: when one of intercalar cells is removed, the basal cell of one of fragments obtained starts to secrete rhodomorphin, which induces the formation of a specific “reparatory” cell by the apical cell of the second fragment, and this cell provides for fusion of both fragments and restoration of filament integrity. Further investigations showed that rhodomorphin is a glycopeptide with a mol wt of about 14 kD [45, 46]. Glycoproteins of similar structure were found in other organisms as well, in the green alga Volvox in particular. In this case, they function as pheromones, possibly providing for gamete adhesion and fusion [10]. Thus, the functions of glycoproteins, the analogs of higher plant peptide hormones, in algae could be defined as follows: providing for cell adhesion and fusion during reparatory processes and attraction and fusion of gametes during algal sexual propagation. Thus, by now the following phytohormones were detected in algae: auxins, cytokinins, gibberellins, ABA, lunularic acid, jasmonic acid, polyamines, and brassinisteroids (Table 2). Regretfully, information obtained is rather fragmentary and does not permit to elucidate the correlation between the frequency of phytohormone occurrence and algal taxa. At present, green,

brown, red, and blue-green (cyanobacteria) algae are most studied. Nevertheless, only identification of the compound in the tissue could not witness its physiological role. Therefore, referring to the data concerning the physiological role of higher plant phytohormones presented in Table 1, we now attempt to classify similar data obtained for algal phytohormones. PHYSIOLOGICAL ROLE OF PHYTOHORMONES IN ALGAE Auxin was shown to stimulate rhizoid formation in the green alga Bryopsis plumosa and activate the growth of some cultured microalgae and cyanobacteria [14, 47]. In red macrophytes, treatment with natural or synthetic auxins accelerated tissue growth in the culture and callus development [48–50]. On the other hand, auxin did not stimulate growth of cultured unicellular algae, such as Euglena gracilis and Chlorella sp. Only IAA but not its synthetic analogs affected growth of the green alga Codium fragile [51]. The herbicides of the auxin row (fluroxipir, ethylbenzoline) are known to affect Chlorella growth only slightly [52]. Ambiguous data obtained could indicate that, like in higher plants, only low hormone concentrations (below 1 mg/l) exerted a beneficial effect. The high auxin concentrations (10 mg/l) suppressed growth of cultured tissues considerably. In addition, ethylene was not detected in algae until now, and just accelerated ethylene synthesis underlies some auxin-depended responses (for example, the effects of auxin herbicides) [1]. Some data indicate that auxin controls thallus branching of red and brown macrophytes on the principle of apical dominance [48, 53]. Treatment with IAA or naphthylacetic acid reduced the number of branches produced by F. vesiculosus, and the removal of the apical cell or treatment with the inhibitor of auxin transport (triiodbenzoic acid) had an opposite effect [53]. It was also supposed (Moss (1967), cited after [54]) that auxin plays an important role in the formation of Fucus reproductive structures. In particular, treatment with NAA retarded gamete release. Exogenous IAA stimulated zygote polarization and germination in fucacean [24, 25, 55–57]. The aforementioned data about the action of endogenous and exogenous auxins on algal growth (thallus branching, rhizogenesis, polarization) and development (induction of division, the formation of reproductive structures) indicate that its functions correspond to those fulfilled by this phytohormone in higher plants. The data concerning the effects of exogenous cytokinins on algal growth and development were obtained mainly on the members of the division Rhodophyta. Cytokinins (alone or in combination with auxins) were shown to accelerate red alga growth in the culture and, in some cases, facilitate callus formation [50]. In the tissue culture of Grateloupia doryphora, cytokinins suppressed morphogenetic processes [49]. Alga treatment with cytokinins activated cell division and protein


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Table 2. Phytohormones in the algae of various taxonomic groups Division

Phytohormones found

Source

Chlorophyta

IAA (genera Enteromorpha, Chlorella, Cladophora, Caulerpa) cytokinins (genera Protococcus, Chlorella, Scenedesmus, Chlamydomonas) gibberellins (genus Caulerpa) ABA (genera Chlorella, Dunaliella, Haematococcus) lunularic acid (genus Enteromorpha) jasmonic acid (genera Dunaliella, Chlorella) polyamines (genera Ulva, Chlorella) brassinosteroids (genus Hydrodictyon) Phaeophyta IAA (genera Macrocystis, Laminaria, Fucus, Ascophyllum) cytokinins (genera Fucus, Ascophyllum, Sargassum, Macrocystis) gibberellins (genus Fucus) ABA (genera Ascophyllum, Laminaria) polyamines (genus Dyctiota) Rhodophyta IAA (genera Botryocladia, Porphyra) cytokinins (genus Porphyra) jasmonic acid (genus Gelidium) polyamines (genera Cyanidium, Gelidium, Grateloupia) rhodomorphin (genus Griffithsia) Charophyta cytokinins (genus Chara) Euglenophyta cytokinins (genus Euglena) jasmonic acid (genus Euglena) polyamines (genus Euglena) Cyanophyta IAA (genera Oscillatoria, Chlorogloea) cytokinins (genera Arthronema, Calothrix) jasmonic acid (genus Spirulina)

accumulation and stimulated photosynthetic processes (accumulation of photosynthetic pigments and Rubisco, activation of photosystems I and II) [58, 59]. These functions correspond completely to cytokinin functions in higher plants. In the presence of exogenous gibberellin, heterotrophic growth of Westiellopsis prolifica was accelerated [60]. In these experiments, the effect of the hormone depended on the organic substrate used, which indicates a possibility that gibberellins are involved in the control of the assimilation of the exogenous sources of organic carbon by the cells. Gibberellic acid suppressed callus formation and organogenesis in the tissue culture of the red alga G. doryphora [49]. It was also supposed that gibberellins could be involved in the control of brown macrophyte branching [61]. In brown and red macrophytes, exogenous gibberellins accelerated growth and increased the thallus length [62]. Thus, it seems likely that, like in higher plants, gibberellins control growth of axial structures. Exogenous ABA suppressed growth of disks cut out from the cultured Laminaria thallus and facilitated the RUSSIAN JOURNAL OF PLANT PHYSIOLOGY

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[14, 16, 18, 20, 21, 27] [14, 19, 29–31] [27] [33, 34] [13, 16] [20, 38] [40, 41] [43] [14, 20, 23–25] [23, 28, 31] [12] [35] [41] [14, 20, 21] [31] [38] [39, 41, 42] [45, 46] [19] [15] [38] [41] [14, 26] [19, 30] [20]

development of reproductive tissues at the same concentrations (10–6 to 10–4 M), which are usually used for higher plant treatments [35]. The hormone exerted a morphogenetic effect on the cells of H. pluvialis, stimulating their transition to cyst formation. In some cases, ABA stimulated the synthesis and accumulation of carotenoids in the cells of microalgae [34, 63]. In sporophytes of Laminaria, a seasonal increase in the endogenous ABA content was described, which was correlated with the development of reproductive tissues [35]. It might be that one of the functions of ABA in this alga is a control of sporophyte transition from the stage of growth to the state of propagation. In some microalgae, the content of endogenous ABA increased under stress conditions, namely, after the increase in the salt content in water or under lowered moisture content [33, 34]. ABA is one of phytohormones providing for a higher plant vital activity under stress conditions [1]. It seems likely that it could fulfill similar function in algae as well. Treatment with methyl jasmonate activated metabolism of polyphenols in F. vesiculosus [38, 64]. This No. 2

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effect was especially bright in apices. It is likely that, in F. vesiculosus, like in higher plants, jasmonic acid and its methyl ester are important components of the signaling pathway resulting in the development of defensive responses after plant damage with phytophages [38, 65]. This mechanism evidently is of especially great importance in the case of ryons and young plants, which are most frequent targets of phytophages [64]. Essentially all algae could uptake great amounts of polyamines passively and transport them in other parts of the thallus [40]. The only discussed hormonal function of polyamines in algae is stimulation of macrophyte growth and morphogenesis. Most of these studies were performed with the tissue culture of G. doryphora [41, 49]. Spermine was most efficient in these experiments. In addition, spermine stimulated sporulation in mature algal thalli [42]. Exogenous brassinosteroids (brassinolide, 24-epibrassinolide, castasterone) at the concentrations of 10–15 to 10–8 M accelerated growth of the cultured green microalga Chlorella vulgaris, increased the content of protein and nucleic acids in the cells, and stimulated photosynthetic processes [17]. These hormones also activate medium acidification by the cultured cells (evidently, due to the activation of the plasmalemmal proton pump) [66]. To sum up, we can state the following points. Undoubtedly, phytohormones play an important role in the life of algae. The analysis of modern notions about phytohormone diversity in algae permits a conclusion that the greatest number of phytohormones are characterized in the divisions Chlorophyta, Phaeophyta, and Rhodophyta (Table 2). Just these algal taxa are considered most evolutionarily advanced. Nevertheless, we cannot conclude that there is no developed hormonal system in such divisions as the Charophyta, Euglenophyta, and Cyanobacteria. It might be that these algae were less attractive for researchers as compared, for example, with Chlorophyta, an ancestor of contemporary higher plants. In most cases, the observed spectrum of biological activities of algal phytohormones corresponded to those of higher plant phytohormones. Nevertheless, a great effort is required for a further identification of hormone physiological action and diverse functions in dependence on the evolution of various algal taxonomic groups.

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