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Plant Hormone Conjugation

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Plant Hormone Conjugation Plant Molecular Biology 26: 1459-1481, 1994. © 1994 Kluwer Academic Publishers. Printed in Belgium. 1459 Plant hormone conjugation Gtlnther Sembdner*, Rainer Atzorn and Gernot Schneider Institut far Pflanzenbiochemie, Weinberg 3, D-06018 Halle, Germany (* author for correspondence) Received and accepted 11 October 1994 Key words: plant hormone, conjugation, auxin, cytokinin, gibberellin, abscisic acid, jasmonate, brassinolide Introduction (including structural elucidation, synthesis etc.) and, more recently, their biochemistry (including Plant hormones are an unusual group of second- enzymes for conjugate formation or hydrolysis), ary plant constituents playing a regulatory role in and their genetical background. However, the plant growth and development. The regulating most important biological question concerning the properties appear in course of the biosynthetic physiological relevance of plant hormone conju- pathways and are followed by deactivation via gation can so far be answered in only a few cases catabolic processes. All these metabolic steps are (see Conjugation of auxins). There is evidence in principle irreversible, except for some processes that conjugates might act as reversible deactivated such as the formation of ester, glucoside and storage forms, important in hormone 'homeosta- amide conjugates, where the free parent com- sis' (i.e. regulation of physiologically active hor- pound can be liberated by enzymatic hydrolysis. mone levels). In other cases, conjugation might For each class of the plant hormones so-called accompany or introduce irreversible deactivation. 'bound' hormones have been found. In the early The difficulty in investigating these topics is, in literature this term was applied to hormones part, a consequence of inadequate analytical bound to other low-molecular-weight substances methodology. However, the advent of analytical or associated with macromolecules or cell struc- techniques such as HPLC-MS or capillary tures irrespective of whether structural elucida- electrophoresis-MS may help to resolve matters. tion had been achieved. After the characteriza- tion of the first gibberellin (GA) glucoside - GA8- 2-O-fl-D-glucoside from maturing fruit of Conjugation of auxins Phaseolus coccineus [175, 176] - the term GA conjugate was used for a GA covalently bound to It is the main intention in this section to review another low-molecular-weight compound [184]. the conjugation of naturally occurring auxins; the Subsequently, the term was extended to all other numerous data on conjugates of synthetic auxins groups of plant hormones [ 178], including their will not be discussed. In addition to biosynthesis, precursors and metabolites as well as to second- catabolism is another way to control the levels of ary plant constituents in general. free indole-3-acetic acid (IAA), and conjugation Plant hormone conjugates have been studied represents one important aspect of IAA catabo- intensively during the past decades and good lism. However, at least some IAA conjugates are progress was made concerning their chemistry not merely irreversibly deactivated end products [223] 1460 of metabolism but instead act as temporary stor- lic acid [3, 151]. It has been proposed that a spe- age forms, from which IAA can be released via cial 'IAA-oxidase' is responsible for these hydrolysis. Convincing data about IAA metabo- conversions [9, 50, 70]. However, there is a dis- lism in Zea mays suggest that in seedlings conju- crepancy between results of in vitro oxidation gate hydrolysis in the endosperm represents the under different conditions and the relatively low dominating source of free IAA in the coleoptile occurrence of these catabolites in plant tissues [5, 6, 7]. It is not known whether this mechanism [1431. is valid for higher plants in general. The main products of the non-decarboxylation After the first comprehensive review about pathway, which appears to operate in many plant 'bound auxins' in 1982 [27], the number of iden- species, are oxindole-3-acetic acid and dioxin- tified IAA catabolites increased, as documented dole-3-acetic acid [66, 141, 142]. In Zea mays, by several subsequent reviews [4, 8, 88, 143, 152]. 7-hydroxylation and subsequent glucosylation of Major catabolic routes (Fig. 1) are (1)oxidative oxindole-3-acetic acid have also been observed decarboxylation of IAA, (2) non-decarboxylative [126]. The concentrations of both substances ex- oxidative catabolism and (3) ester and amino acid ceeded the levels of free IAA about ten-fold, im- conjugation. The latter can be divided into for- plying that this is a major route for the inactiva- mation of conjugates from which IAA hydrolysis tion of IAA. In contrast, there are many data is still possible and into compounds where IAA indicating that the formation of both ester and was inactivated via oxidation after conjugate for- amino acid IAA conjugates is associated with a mation. transport function rather than modes of auxin The formation and physiological significance of inactivation [5, 12, 90]. IAA conjugation is of primary importance in this article, but from a regulatory point of view it is necessary to discuss briefly alternative routes of Ester conjugates IAA degradation. The oxidative decarboxylation pathway is catalysed by peroxidases, leading in Most of the available information on synthesis several plant species to products such as indole- and hydrolysis of IAA esters (see Fig. 2) comes 3-methanol [16, 149, 194] and indole-3-carboxy- from experiments with Zea mays [4, 5, 7, 8, 27], Oxidative [ decarboxylation 14 / I Am~oadd conjugafiom I Oy~n: / ~ Dioxindoles Fig. 1. Main routes of IAA metabolism in higher plants. [2241 1461 indole-3-acetyl-myo-inositol-galactoside myo-inositol was converted, which contrasts with the first glucosylation steps where there was al- (-arabinoside) most always complete conversion of the substrate [4, 29, 30]. The conjugating enzymes are soluble and can be separated from each other by Sepha- dex G 150 chromatography [4]. However, further characterization of IAA ester-forming enzymes is still lacking. Interesting information on IAA metabolism as indole-3-acetyl-myo-inositol ox an important regulative element has come from experiments with genetically manipulated plants I where the auxin biosynthesis genes from the Ti plasmid of Agrobacterium were expressed to ob- tain auxin overproducing plants [e.g. 68, 186, 187, x 189]. Quantitative determinations of bound and mdole-3-acetylglue~e free IAA showed an increase of both forms, but often conjugates accumulated to a higher extent. i In most cases the identity of the IAA conjugates was not determined, but there is some evidence [188] that they consist at least partly of ester H compounds, although IAA amino acid conjugates were the main products. Experiments of this kind indole-3-acetic acid are a powerful way to show how plant cells can Fig. 2. Formation of IAA ester conjugates. regulate the levels of active auxins and how they deal with excess production of IAA. It also opens possibilities for a better access to the metabo- although IAA esters have been found in many lizing enzymes. other plant species [8, 21,143]. The first evidence The release of IAA from ester conjugates has for an IAA-glucoside in plants was presented by been studied extensively in the maize coleoptile Zenk in 1961 [233]. In Zea mays kernels, 1-O- [7, 8]. A combination of quantification and turn- (indole-3-acetyl)-/3-D-glucose [43 ] and 2-O-(in- over studies revealed that most of the free IAA in dole-3-acetyl)-myo-inositol have been detected as the copeoptile tips of growing shoots did not well as 5-0-/3-1-arabinopyranosyl-2-O-(indole-3- originate from de novo synthesis but from ester acetyl)-myo-inositol and 5-galactopyranosyl-2-O- hydrolysis in the endosperm. Similar studies with (indole-3-acetyl)-myo-inositol [25, 203, 204]. In other species are not known, so whether this addition, a high-molecular-weight IAA ester of a source of IAA is widespread in young seedlings cellulosic glucan has been detected in extracts remains to be determined. from maize [ 139]. Numerous feeding experiments in combination The enzymology of IAA ester formation was with biological activity determinations and sub- studied by Michalczuk and Bandurski [ 104, 105], sequent analysis of metabolites [8, 28, 46, 125] using crude cell-free preparations from immature indicate that the high physiological activity of IAA kernels of sweet maize which converted (1)2- esters is indirect, resulting from release of free 14C-IAA and UDPG to IAA-/3-D-glucopyrano- IAA. The state of knowledge about enzymes side and IAA-myo-inositol, and (2)UDP-galac- which can hydrolyse IAA from esters is once tose and IAA-myo-inositol to IAA-myo-inositol- again confined to maize, and apart from studies galactose and IAA-myo-inositol-arabinose [4, 6, using more or less crude enzyme preparations, 30]. Typically not more than 20~/o of the IAA- not much information is available. [2251 1462 Amide conjugates Cohen [ 11 ] detected an IAA peptide with a mo- lecular weight of about 5 kDa in Phaseolus, and There are two types of amide conjugates formed the presence of an IAA glycoprotein conjugate with IAA in which either the indole ring of the has also been reported [137]. IAA remains unchanged or oxindole or dioxin- The function of amide conjugates is not fully dole derivatives are synthesized after formation understood. The peptide bond-forming enzymes of the peptide bond (Fig. 3). IAA-aspartate from are not, as yet, well-characterized, and it has not seeds of soybean was the first amino acid conju- been possible to produce these conjugates in vitro. gate to be identified conclusively [26]. This form There is evidence from many experiments mostly of IAA conjugation occurs in legume seeds [4], confined to plant tissue cultures [e.g. 90] or seeds but has been observed in other species too, for [e.g. 12] that hydrolysis of IAA-aspartate takes example in shoots ofPinus silvestris [ 1] and fruits place to a high extent.
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