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Oligosaccharide Signalling for Defence Responses in Plant Physiological and Molecular Plant Pathology (2001) 59, 223±233 doi:10.1006/pmpp.2001.0364, available online at http://www.idealibrary.com on MINI-REVIEW Oligosaccharide signalling for defence responses in plant N. SHIBUYA and E. MINAMI Biochemistry Department, National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan (Accepted for publication October 2001) Keywords: elicitor; receptor; OGA; chitin; chitosan; beta-glucan; signal transduction; ion ¯ux; protein phosphorylation; defence response. INTRODUCTION transduction cascades and elicitor-responsive genes. Several reviews [5, 25, 34, 40] have already been Higher plants have the ability to initiate various defence published on these subjects and in this review the authors reactions such as the production of phytoalexins, try to focus mostly on recent progress. antimicrobial proteins, reactive oxygen species, and reinforcement of cell walls when they are infected by pathogens such as fungi, bacteria and viruses. If these reactions occur in a timely manner, the infection will not CHARACTERISTICS OF OLIGOSACCHARIDE proceed further. However, if the defence reactions occur ELICITORS too late or are suppressed, the infection process will proceed successfully [89]. Thus, it is critically important b-glucan oligosaccharides for plants to detect infecting pathogens eectively and Oligosaccharide elicitors derived from the b-glucans of deliver such information intracellularly/intercellularly to pathogenic Oomycetes, such as Phytophthora sojae,have activate their defence machinery. been very well characterized. A doubly-branched hepta- It is believed that the detection of pathogens is b-glucoside that was generated from P. sojae glucan by mediated by chemical substances secreted/generated by partial acid hydrolysis was shown to be a very active the pathogens. Various types of such compounds (elicitor elicitor for glyceollin biosynthesis in soybean cotyledon molecules) including oligosaccharides, (glyco)proteins, cells [86]. From detailed studies with a set of naturally (glyco)peptides and lipids, have been shown to induce obtained as well as synthetic oligosaccharides, it has been defence responses in plant cells and their involvement in shown that soybean cells recognize speci®c features of the the detection of (potential) pathogens in plant has been hepta-b-glucoside structure, including all three non- discussed [5, 24, 34]. Oligosaccharides derived from reducing terminal glucosyl residues and their spacing fungal and plant cell wall polysaccharides are one class of along the backbone of the molecule [10]. A partial well characterized elicitors that, in some cases, can induce hydrolysate of the P. sojae b-glucan also acts as an active defence responses at a very low concentration e.g. nM.In elicitor on various plant cells belonging to the family view of their well-de®ned chemical nature and the Fabaceae, indicating the presence of similar perception presence of highly sensitive perception systems in plants, systems in these plants [14]. In the case of tobacco cells, some of these elicitors have provided good model systems however, the hepta-b-glucoside did not act as an elicitor, to study how plant cells recognize such chemical signals but linear b-1,3-linked glucooligosaccharides (laminar- and transduce them for activation of the defence ioligosaccharides) were active elicitors [47]. Interestingly, machinery. These studies include structure±activity a cyclic 1,3- 1,6-linked b-glucan secreted by a symbiotic relationships of the elicitor molecules, characterization bacterium, Bradyrhizobioum japonicum, was reported to act of the corresponding receptors and analysis of signal as a suppressor for the induction of phytoalexin biosynthesis in soybean by b-glucan elicitor [62]. Abbreviations used in text: A9-C, anthracene 9-carboxylic acid; MBP, mannan binding protein; OGAs, oligogalacturo- There has been little information on the b-glucan nides; TLR, toll-like receptors; 2-D PAGE, two-dimensional gel fragment elicitor that acts on monocots. Inui et al.[38] electrophoresis. reported the induction of chitinase and PAL activity in 0885-5765/01/110223+11 $35.00/00 224 N. Shibuya and E. Minami cultured rice cells by laminarihexaose. Recently Yama- The requirements for the size and structure of active guchi et al.[104] reported that a pentasaccharide (in the chitin fragments are dierent depending on the experi- reduced form) puri®ed from an enzymatic digest of the b- mental systems. In the case of rice and wheat, larger glucan from the rice blast fungus, Magnaporthe grisea oligosaccharides such as heptamer or octamer are (Pyricularia oryzae), shows potent elicitor activity to induce preferentially recognized and showed detectable activity phytoalexin biosynthesis in suspension-cultured rice cells. even at nM concentrations [3, 103]. On the other hand, in The elicitor-active glucopentaose induced phytoalexin the case of tomato cells, the elicitor activity was almost the biosynthesis in rice cells at 10 nM concentrations. Struc- same for oligosaccharides larger than tetramer [27]. Such tural elucidation of the elicitor-active glucopentaose dierences in the speci®city probably re¯ect the charac- showed a quite contrasting structure compared to the teristics of the corresponding receptors and will be hepta-b-glucoside that is active on soybean. In the case of explained in future studies of the interaction of these the hepta-b-glucoside elicitor from P. sojae, the backbone oligosaccharides with these receptor molecules. In these is a 1,6-linked b-glucooligosaccharide with branches at plant cells, deacetylated oligosaccharides, chitosan frag- the 3-position of two 6-linked glucosyl residues. In the case ments, did not show elicitor activity. of the elicitor-active b-glucopentaose from M. grisea, the Chitosan or its fragments can induce defence responses backbone oligosaccharide is 1,3-linked and branched at in several plant systems, mostly dicots. Chitosan induces the 6-position of a 3-linked residue. Two related callose formation in soybean and parsley cells [13, 49], glucopentaoses that dier only in the position of the proteinase inhibitors in tomato leaves [102] and phyto- glucosyl stub showed little elicitor activity, indicating a alexin biosynthesis in pea [31]. However, the concentra- strict recognition of the active oligosaccharide in rice cells. tions required for these responses are usually much higher Comparison of the elicitor activity of the b-glucan than those necessary for activity of chitin oligosaccharides fragments from M. grisea and synthetic hexa-b-glucoside, in other plant systems. The eects of the degree of the minimum structural unit for activity of the hepta-b- acetylation as well as the molecular size of chitosan and its glucoside in soybean, using both suspension-cultured rice oligosaccharides were examined with respect to callose cells and soybean cotyledons, indicated that each glucan formation, phytoalexin induction and ligni®cation [2, 43, fragment can only be recognized by the corresponding 99]. The elicitor activity of chitosan seems to be mediated host plants [104]. Although the structural requirement for through the interaction of this polycationic molecule with the recognition by the rice cells must be examined in more negatively charged phospholipids, rather than a speci®c detail, these results indicate clear dierences in the speci- interaction with a receptor-like molecule [43]. ®city of the corresponding receptors in rice and soybean. It will be interesting from an evolutionary viewpoint to see Oligogalacturonides whether various plants can be grouped depending on their abilities to recognize dierent b-glucan elicitors. Oligogalacturonides (OGAs) derived from pectic poly- saccharides of plant cell walls have also been known to act as elicitor molecules. OGAs have been shown to induce biosynthesis of phytoalexins in the cotyledons of soybean Chitin and chitosan oligosaccharides [70] and kidney bean [23], proteinase inhibitors in Chitin (b-1,4-linked polymer of N-acetylglucosamine) is tomato leaves [26], and ligni®cation of cucumber a common component of fungal cell walls and its cotyledons [78] and cultured castor bean cells [7]. So fragments, N-acetylchitooligosaccharides, have been far, there has been no report of elicitor activity of OGAs shown to act as potent elicitor signals in several plant in monocot plants, which might be reasonable in the light systems. These include the induction of ligni®cation in of the much lower content of pectic polysaccharides in wheat [3], ion ¯ux and protein phosphorylation in monocot cell walls. OGAs can be generated from pectic cultured tomato cells [27], chitinase activity in melon polysaccharides by partial acid hydrolysis or by the [79], and gene expression of glucanase in cultured barley action of pectinase or pectate lyase. Regardless of the cells [42]. In suspension-cultured rice cells, the action of method of generation, OGAs of DP 10±12 appear to be chitin fragments has been extensively studied. These the most active component. However, Reymond et al. studies showed the induction by chitin fragments of [77] showed that the ability of OGAs to induce protein enzyme activities involved in the biosynthesis of terpenoid phosphorylation in vitro in tomato increased with the size phytoalexins [75, 103], membrane depolarization [45, of the OGAs even to a DP more than 20. This result 50], Cl and K eux, cytoplasmic acidi®cation [52], indicates that the optimum size of OGAs for elicitor generation of reactive
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