ISSN 0003-6838, Applied Biochemistry and Microbiology, 2006, Vol. 42, No. 3, pp. 229–235. © MAIK “Nauka /Interperiodica” (Russia), 2006. Original Russian Text © E.A. Tsavkelova, S.Yu. Klimova, T.A. Cherdyntseva, A.I. Netrusov, 2006, published in Prikladnaya Biokhimiya i Mikrobiologiya, 2006, Vol. 42, No. 3, pp. 261–268. Hormones and Hormone-Like Substances of Microorganisms: A Review E. A. Tsavkelova, S. Yu. Klimova, T. A. Cherdyntseva, and A. I. Netrusov Faculty of Biology, Moscow State University, Moscow, 119992 Russia e-mail: tsavkelova@mail.ru Received January 19, 2005 Abstract—Data from the literature on the ability of microorganisms to form plant hormones have been reviewed. The substances covered include abscisic acid, ethylene and other compounds with phytohormonelike properties (brassinosteroids, oligosaccharines) and analogues of animal neurotransmitters (biogenic amines). Pathways whereby the substances are metabolized and their effects on the development and activity (physiological and biochemical) of the microorganisms are considered. The role of phytohormones and hormone-like substances in the formation of association (microorganism–host) interactions are analyzed. The potential utilities of microorganisms producing hormones and hormone-like substances are discussed. DOI: 10.1134/S000368380603001X The ability of microorganisms to synthesize phytohormones is widely known [1–3]. Producers with the highest activity enter into association interactions with plants, which may have pathogenetic or symbiotic consequences. Bacteria, micromycetes, and algae form phytohormones of auxin, cytokinin, or gibberellin nature [1]. On the other hand, microorganisms also synthesize other phytohormones and phytohormone-like substances, including ethylene and abscisic acid (ABA), brassinosteroids, oligosaccharines, salicylic acid, and jasmonic acid. In this review, we discuss the ability of microorganisms to synthesize these compounds, with an emphasis on their role in the formation of association interactions with plants and the potential utilities of such phytohormone producers. drastic increased in the level of ABA [9]. Several explanations for this phenomenon have been proposed, for example, plant stimulation of fungal ABA biosynthesis, stimulation of plant ABA biosynthesis by pathogenic fungi, and suppression of metabolic activity of the plant host [9]. The first variant seems to have the greatest likelihood, since many phytopathogenic fungi synthesize and excrete ABA into the medium, examples include B. cinerea, Cercospora rosicola and C. cruenta, Agrocybe praecox, Rhizoctonia solani, Ceratocystis coerulescens, Schizophyllum commune, Monilia sp., Fusarium culmorum [5, 11–16]. ABA formation has also been documented in Polyporus sp., Trametes versicolor, Aspergillus niger, Cladosporium cladosporioides [11], and micromycete Curvularia lunata, which was isolated from marine sponges [17]. ABA AND ETHYLENE ABA (figure) promotes phylloptosis, closure of stomata, and ageing; it maintains buds and seeds in the state of quiescence; it also inhibits the syntheses of DNA, RNA, and certain enzymes and suppresses plant growth, when tested in biological assays [4]. ABA is known to be involved in plant interactions with pathogenic fungi, as the level of ABA in the plant determines its susceptibility to phytopathogenic microorganisms [5]. Elevation of the level of exogenous ABA increases plant sensitivity to such pathogenic fungi as Phytophthora infestans and Cladosporium cucumerinum [6], P. megasperma (P. sojae) [7], Peronospora tabacina [8], and Botrytis cinerea [5, 9]. While inoculation of pea (Pisum sativum L.) roots with the symbiotic nodule bacterium Rhizobium leguminosarum does not affect the ABA content considerably [10], the infection of tomato (Lycopersicon esculentum Mill.) plants, caused by the pathogenic fungus Botrytis cinerea, produced a ABA has been identified in cyanobacteria and representatives of green (Ulva sp.), brown Fucus sp., Laminaria sp., Ascophyllum sp., Cystoseira sp. and red (Porphyra sp.) algae [18, 19]. ABA belongs to isoprenoid compounds of the sesquiterpene series (ë15). In plants ABA may be formed from mevalonic acid or during carotenoid oxidation [4]. However at present time, direct ABA biosynthesis (via mevalonate) is not believed to be characteristic of plants; this is largely encountered in phytopathogenic fungi [20]. In higher plants ABA may be viewed as the product of specific degradation of carotenoids, particularly violoxanthine, which is cleaved into two unequal fragments, ë15 (xanthoxin) and ë25; the latter undergoes rapid degradation [4]. The final stages of ABA biosynthesis remain obscure. Being an unstable compound, xanthoxin presumably undergoes spontaneous conversion into ABA-aldehyde, further oxidation of which results in the formation of ABA. The formation 229 230 TSAVKELOVA et al. OH COOH O 1 OH OH HO HO O H O 2 COOH O OH COOH 4 3 HO OH O OH OH O H C (CH2)5 C H C H (CH2)5 CH3 O NHAc NHAc NHAc NH CO C H CH2OSO3H+ O OH OH CH2OH O CH2OH O CH2OR O 5 HO CH2COOH CH2CH2NH2 N H N H 6 7 Structural formulae of hormones and hormone-like substances: 1, abscisic acid; 2, brassinolide; 3, salicylic acid; 4, jasmonic acid; 5, oligosaccharine [nodulation factor of Rhizobium melliotii (R = H)]; 6, serotonin (5-hydroxytryptamine); 7, indole-3-acetic acid [4, 5, 45]. APPLIED BIOCHEMISTRY AND MICROBIOLOGY Vol. 42 No. 3 2006 HORMONES AND HORMONE-LIKE SUBSTANCES of an ester with glucose, a biological activity of which is considerably lower than that of ABA, serves as a means of transportation and detoxification of the phytohormone [21]. Using phytopathogenic fungi of the genus Cercospora as an exemplary case, direct ABA biosynthesis (via mevalonic acid oxidation) was shown to involve ionylidene acetate as an immediate precursor (in C. rosicola and C. cruenta) [16]. The operation of the mevalonate pathway of ABA formation in certain phytopathogenic fungi was confirmed by other researchers [20]. Direct ABA biosynthesis (via the terpenoid pathway) also takes place in the green alga Dunaliella sp. [18]. Exogenous ABA is known to stimulate in vitro the growth and development of several phytopathogenic and saprophytic fungi (Aspergillus niger, Fusarium culmorum, Cylindrocarpon destructans, Schizophyllum commune, Monilia laxa, Gloeosporium album, Botrytis cinerea, and Monilia fructigena [11, 22]. There are researchers who believe that the ability of phytopathogens to synthesize ABA (which, in turn, stimulates the growth of its producers) may be viewed as a factor of pathogenicity in plant infections [11]. Other researchers view ABA as a signal molecule that controls metabolic processes taking place in symbiotic nitrogen-fixing nodules of leguminous plants. Exogenous ABA decreased the content of leghemoglobin, which is required for protecting nitrogenases from oxygen during the fixation of atmospheric oxygen, and the rate of nitrogen fixation in pea nodules; in both cases the net effect appeared as a decrease in the content of organic nitrogen in the plant host [23]. Other researchers, however, detected a considerable increase in the activity of the nitrogenase complex in Azotobacter chroococcum and the diazotrophic cyanobacterium Nostoc muscorum [24]. Ethylene is another inhibitor of plant growth. Ethylene slows down growth and cell extension, disrupts geotropism, promotes phylloptosis, and accelerates fruit maturation and ageing [4]. Ethylene production is activated in plants under stress conditions. Being a gaseous compound, ethylene may be transported throughout the plant only by diffusion (i.e., within short distances); its immediate precursor, aminocyclopropane carboxylic acid (ACA) is capable of migrating throughout the whole plant [4]. Microorganisms are also capable of synthesizing ethylene. The producers include heterotrophic bacteria (Escherichia coli [25, 26], Cryptococcus albidus, Pseudomonas syringae [27–29], Chromobacterium violaceum [26], and Ralstonia solanacearum [30]), phototrophic cyanobacteria (of the genera Synechococcus, Anabaena, Nostoc, Calothrix, Scytonema, and Cylindrospermum [18]), mycorrhizal fungi (Cenococcum geophilum, Hebeloma crustuliniforme, and Laccaria laccata [31]), phytopathogens (Botrytis cinerea [29] and Fusarium oxysporum [31]), and other microAPPLIED BIOCHEMISTRY AND MICROBIOLOGY 231 mycetes (Acremonium falciforme [32] and Penicillium digitatum [33]). Using Pseudomonas syringae it was shown that strains within the same species may widely vary in ability to form ethylene (ranging from an absence of this trait to a formation of considerable amounts) [28]. Ethylene was also detected in many algal species; the most active producers belong to the genera Porphyra, Acetabularia, Codium, and Dunaliella [18]. Plants synthesize ethylene primarily from methionine, via the ACA pathway. However, ethionine, β alanine, and linolenic acid may also undergo a conversion into ethylene. Methionine reacts with ATP in the formation of S-adenosylmethionine, which is further converted into ACA by ACA synthase. Thereafter, ACA oxidase catalyzes ACA oxidation by oxygen, with the formation of ethylene [4, 21]. The presence of ACA was also demonstrated in red alga Porphyra perforata [18]. Two pathways of ethylene biosynthesis are known to operate in microorganisms, which involve 2-oxo-4methylthiobutyrate (OMTB) or 2-oxoglutarate [29]. The first pathway was detected in bacteria of the genera Escherichia, Cryptococcus, Ralstonia, Chromobacterium, Aeromonas, Rhizobium, and Corynebacterium [25, 26, 29, 34]. The OMTB pathway presumably operates in Pseudomonas syringae, the yeast Saccharomyces cerevisiae, and the fungi Penicillium digitatum and Botrytis cinerea [29, 30, 34, 35]. The genes responsible for the synthesis of ethyleneforming enzymes in phytopathogenic Pseudomonas spp. (efe) are structurally similar in various strains and localize to plasmid(s) [30, 35]. It is hypothesized that efe genes undergo a horizontal transfer among various pathogenic strains of Pseudomonas syringae [30]. However, these genes may not be universal, because neither efe activity nor genes that would be homologous to efe could be identified in the other pathogenic bacterium, R. solanacearum [30]. The activity of efe genes depends on the presence in the medium of methionine [29, 31, 34], the nitrogen and carbon source [26]. For example, in the absence of NADPH, the formation of OMTB in cell-free extracts of E. coli was stimulated by supplementation with glucose [25]. The amount of ethylene in plants increases when they are infected with pathogenic microorganisms [29]. This is viewed as a defense reaction against pathogen invasion, even though ethylene itself may a have a certain role in disease development. Many phytopathogens form ethylene in vitro, as well as in vivo in the tissues of infected plants. Thus, the biosynthesis of ethylene in vivo was recorded in B. cinerea [29] and P. syringae [28]. It is believe that the increase of ethylene in plants results from its production by microorganisms [28]. Inoculation of gnotobiotic spruce (Picea abies) seedlings with mycorrhizal fungi (Cenococcum sp., Hebeloma sp., and Laccaria sp.) demonstrated that the Vol. 42 No. 3 2006 232 TSAVKELOVA et al. appearance of ethylene coincides with the formation of mycorrhyza [31]. On the other hand, the infection caused in these seedlings by the phytopathogen Fusarium oxysporum was associated with excretion of considerably higher amounts of ethylene than in the seedlings with mycorrhyza; this observation may indicate that the role of ethylene in the development of symbiotic and pathogenetic fungus–plant interactions is ambiguous [31]. Inoculation with RGPR strains of rhizobacteria is used for improving the growth and development characteristics of plants. These strains decrease the level of excreted ethylene by forming ACA deaminase (ACAD), an enzyme that cleaves ACA (ethylene precursor) [36]. The enzyme was found in many rhizospheric bacteria of the genera Pseudomonas, Alcaligenes, Rhodococcus, and Rhizobium [37, 38]. Moreover, certain bacteria (e.g., Rhizobium japonicum and Streptomyces spp.) synthesize phytotoxic antibiotics that inhibit ethylene formation in plants (aminoethoxyvinylglycine and rhizobitoxin) [4]. A decrease in the amount of ethylene synthesized by the plant is of particular importance for nodule bacteria, because ethylene suppresses nodule formation [38]. The authors of this report believe that bacterial ACAD may, in spite of its low affinity for ACA, efficiently compete with the plant enzyme ACA oxidase, the affinity of which is higher. This may likely be accounted for by the differences in the content of the enzymes, because the amount of ACAD exceeds by two or three orders of magnitude that of the plant ACA oxidase. HORMONE-LIKE COMPOUNDS Phytohormone-like compounds (brassinosteroids, oligosaccharines, salicylic acid, and jasmonic acid) were only discovered at the end of the 20th century, this being the reason for the insufficient information on their structure, mechanisms of biosynthesis, and properties. Nevertheless, there is increasing evidence that microorganisms are also capable of producing these substances [4]. Brassinosteroids. The first brassinosteroid was isolated in 1979 from the pollen of rape (Brassica napus L.) and thus got the name brassinolide (figure). More than 60 compounds of a related structure have been identified thus far. In plants brassinosteroids increase the content of chlorophyll, stimulate protein synthesis, activate certain enzymes, and regulate processes of cellular differentiation. An addition of exogenous brassinolide increases plant resistance to adverse external factors and phytopathogen-induced diseases [4, 39]. This was demonstrated for rice (Oryza sativa L.) and tobacco (Nicotiana tabacum L.) plants grown in vitro, which exhibited increased resistance to tobacco mosaic virus, phytopathogens (P. syringae and Xanthomonas oryzae), and fungi (Oidium sp. and Magnoporthe grisea) [39]. The causative agent of peanut cercosporosis (the fungus Cercospora arachidicola) is itself a brassinosteroid producer [4]. The unicellular green alga Chlorella vulgaris L. is also capable of synthesizing these phytohormone-like compounds [40]. In plants brassinosteroids are synthesized via the mevalonate pathway (as other terpenoids), with the formation of a variety of intermediates (isopentenyl pyrophosphate, geranyl pyrophosphate, farnesyl pyrophosphate, and squalene). No mevalonate pathway of isopentenyl pyrophosphate formation has been identified in C. vulgaris [40]. It is believed that endogenous brassinosteroids are required for the normal development of C. vulgaris in the light; this conclusion was made based on two observations: (1) brassinozole, an inhibitor of brassinosteroid biosynthesis, suppressed the growth of this microorganism; and (2) suppression was prevented by the addition into the medium of brassinosteroids [40]. On the other hand, brassinosteroids are known to inhibit the growth of certain phytopathogenic fungi [4]. Salicylic and jasmonic acids. These compounds are endogenous inhibitors of plant growth and seed germination. Salicylate (figure) is also known to prolong the life of flowers, inhibit ethylene biosynthesis, and facilitate (via thermogenesis) pollination of certain plants. Jasmonate (figure) activates processes of ageing, phylloptosis, tuber formation, fruit ripening, and pigment formation [4]. Both compounds stimulate the synthesis of several factors that protect plants from the effects of pathogens (e.g., tobacco mosaic virus and phytopathogenic fungi of the genera Botrytis and Fusarium) [41, 42]. Jasmonic acid facilitates the development of symbiotic bacteria. Jasmonate activates the expression of nod genes in Bradyrhizobium japonicum and Rhizobium leguminosum; the genes are responsible for the formation of nodules at a stage when these nitrogen-fixing microorganisms have formed associations with plant hosts [43, 44]. Conversely, salicylic acid, which is a phenolic compound, inhibits the expression of nod genes in R. leguminosarum [43]. Jasmonic acid was detected in cyanobacteria (Spirulina sp.) and green algae (Chlorella sp.) [18]. Oligosaccharines. These biologically active oligosaccharides (represented by fragments of β-D-glucan, chitin and chitosan of cell walls of phytopathogenic fungi, fragments of polygalacturonic acid and xyloglucan of plant-cell walls, and lipooligosaccharides synthesized by symbiont bacteria) perform signaling functions in plants [45]. In certain cases oligosaccharines are found to contain inositol (a polyhydric alcohol), the residue of which originates in membrane glycolipids [1]. Oligosaccharines are formed during partial cleavage of cell-wall polysaccharides (of plants or phytopathogenic micromycetes); the lytic enzymes catalyzing the cleavage may originate either in the plant itself or in microorganisms (bacteria or fungi). Oligosaccharines are actively involved in regulating growth and differentiation of plant tissues (processes APPLIED BIOCHEMISTRY AND MICROBIOLOGY Vol. 42 No. 3 2006 HORMONES AND HORMONE-LIKE SUBSTANCES associated with partial cleavage of polysaccharide polymers of cell walls). The oligosaccharine XG9 (a nonasaccharide fragment of xyloglucan) exhibits antiauxin activity [45]. Oligosaccharines stimulate fruit ripening in vivo and cell division in vitro; they are involved in plant defenses (from pathogenic fungi and bacteria) and in regulating plant interactions with bacterial symbionts. Certain oligosaccharide fragments formed during enzymatic hydrolysis of cell walls (of plants or pathogenic fungi, such as Phytophthora) act as elicitors, i.e., inducers of specific plant immune responses. Such oligosaccharide elicitors stimulate the lignification of plant cell walls and the formation of enzymes that cleave cell walls of pathogens; they also increase synthesis of protease inhibitors in plants, which halts the degradation of host proteins at infection sites and facilitates the production of phytoalexins (low-molecularweight substances toxic to microorganisms) [45]. Extracellular β-D-glucan, which is formed by the phytopathogen Botrytis cinerea in the form of a capsule or film, may be used by the fungus itself as an extracellular source of energy and carbon (after the pool of nutrients in the medium has been exhausted) [46]. The role of oligosaccharines in the differentiation of plant tissues makes itself most evident during the formation process of symbioses between leguminous plants and rhizobia (symbiotic nitrogen-fixing bacteria). These specific oligosaccharines involved in this process (known as Nod factors) do not result from cellwall degradation; rather, they are products of targeted biosynthesis taking place within the bacteria [45]. Nod factors are produced in response to the appearance in the medium of flavones and isoflavones (synthesized by plant roots). Each Nod factor is a glucosamine, the reducing and nonreducing ends of which carry, respectively, a strongly polar substituent in the form of a sulfate residue and an unsaturated fatty acid with two double bonds (figure). Lipochitinoligosaccharides of similar structure were found in Bradyrhizobium japonicum and other rhizobia. Nod factors cause deformation of the root hair of the plant host, facilitate nodule formation, and act as substances that determine the specificity of the interaction taking place between a particular plant host and its symbiont [45]. It was found that Bacillus circulans forms a lipochitinoligosaccharide similar to that of B. japonicum, which deforms root hair in leguminous plants [47]. Nod factors may affect the hormonal status of a plant: within 24 h, the lipochitinoligosaccharide of Rhizobium leguminosarum bv. viciae decreases the polar transport of auxins (from the leaves and the apex of a shoot to its base, and from the base to the roots) in its plant host, Vicia sativa subsp nigra [48]. Oligosaccharines resemble “classic phytohormones” in that they lack species-specificity and multiplicity of effects; nevertheless, unlike typical phytohorAPPLIED BIOCHEMISTRY AND MICROBIOLOGY 233 mones, oligosaccharines are active at considerably lower concentrations. Bioamines. In addition to phytohormones, microorganisms also synthesize other signal molecules conserved in evolution (e.g., animal hormones). Microorganisms are capable of synthesizing acetylcholine, biogenic amines (dopamine, serotonin, norepinephrine), and metabolites thereof. These substances, which act as neurotransmitters in animals, are also found in certain plants, where they are involved in the regulation of growth and development [49]. Serotonin, which is a major neuromediator, is a structural analogue of auxins (figure) found in Enterococcus faecalis [50], Rhodospirillum rubrum [51], Bacillus cereus, and Staphylococcus aureus [52]. Norepinephrine is detected in representatives of the genus Bacillus, Proteus vulgaris, Serratia marcescens, the yeast Saccharomyces cereviseae and the microscopic fungus Penicillium chrysogenum [52]. Moreover, the quantitative content of biogenic amines is species-specific, differing in dissociants of the same bacterium (R- and M-dissociants of B. subtilis; R- and S-dissociants of P. aeruginosa) [52]. When added into the culture medium, exogenous bioamines affect microorganism development. Serotonin stimulates the growth of both the yeast Candida guilliermondii and the bacteria S. faecalis [50], Escherichia coli, and R. rubrum [51]. Serotonin facilitates cell aggregation and myxospore formation in myxobacteria (Polyangium sp.) and inhibits the formation of thymine dimers in the DNA of C. guilliermondii (by forming an intercalated-type complex with nucleotides) [53]. Norepinephrine is also capable of accelerating the growth if bacteria (e.g., representatives of Enterobacteriaceae and Pseudomonadoceae [54], Actinomyces naeslundii, Actinomyces gerenscseriae, Eikenella corrodens, and Campylobacter gracilisi [55]). Norepinephrine inhibits insignificantly the development of Porphyromonas gingivalis and Bacteroides forsythus [55]. Norepinephrine causes the formation of adhesin and shiga-like toxins in pathogenic strains of E. coli and Yersinia enterocolitica. Pathways of the biosynthesis and metabolism of serotonin (which is an indole derivative) in microorganisms remain to be clarified. In mammals serotonin is formed from tryptophan, by hydroxylation into 5-hydroxytryptophan (by tryptophan hydroxylase) and its decarboxylation into 5-hydroxytryptamine (serotonin) [56]. Monoamine oxidase converts serotonin into 5-hydroxy-indoleacetic acid. In plants tryptophan is first decarboxylated into tryptamine, which is then hydroxylated into serotonin [49]. Plant metabolism of serotonin leads to the formation of indoleacetic acid (IAA). Certain bacteria were found to contain 5-hydroxyindoleacetic acid [52]. Experiments with the yeast C. guilliermondii demonstrated that p-chlorophenylalanine, an inhibitor of tryptophan hydroxylase, suppresses serotonin formation, which is indicative of the Vol. 42 No. 3 2006 234 TSAVKELOVA et al. operation in microorganisms of the animal-type biosynthetic pathway [53]. However, p-chlorophenylalanine did not affect the growth dynamics of E. coli, seeming to suggest that a plant-type biosynthetic pathway, which does not require tryptophan hydroxylase, operates in this bacterium [51]. Biogenic amines are found primarily in the extracellular matrix of bacteria [52]. The matrix is responsible for cell–cell communications; it serves to assemble cells into colonies (unified populations) and concentrates nutrients, regulators, ions, and signaling molecules [57]. Phytohormones and hormone-like substances of a bacterial origin may also accumulate in the matrix, thereby increasing their concentrations and availability (e.g., to macroorganism hosts, with which the bacteria are associated). The role of hormones and hormone-like substances is not limited to intracellular signaling in plants and animals; they also mediate interactions between macrooganisms (of plant or animal origin) and microorganisms. Stimulators and inhibitors of plant growth, formed by phytopathogenic fungi and bacteria, govern early stages of pathogenesis and thereby determine the success or failure of a pathogen invasion [1, 2, 58, 59]. Moreover, phytohormones and hormone-like compounds play an important role in the development of symbiotic relations between plants on one hand, and mycorrhyzal fungi and association-forming microorganisms (such as nodule bacteria) on the other. Such relations may be critical for successful seed germination or normal growth of mature plants [1–3]. Microorganisms that form ACAD, the enzyme that decreases the level of endogenous plant ethylene, exert beneficial effects on plant growth. There is evidence that bacterization of a cabbage seed by ACAD-positive strains decreases the level of ACA and stimulates the growth of the plant roots [36]. A European orchid seed requires mycorrhyzal fungi for the successful germination and cessation of quiescence (induced by ABA at the onset of winter) [60]. Industrial microbiology and medicine use not only phytohormone-producing microorganisms, but also phytohormone degraders. Thus, this ability of certain mycobacteria to cleave and modify steroids (including compounds with brassinosteroid substituents) is used in the production of human steroid hormones [61]. In conclusion, the foregoing data reflect the increasing interest in studies of microorganisms producing phytohormones and hormone-like substances, which determine the formation and development of relationships within natural communities. Studies of the biosynthetic pathways of these substances and their effects on pro- and eukaryotes may identify regulators of interactions between macroorganisms (animals or plants) and their associated microorganisms. REFERENCES 1. 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