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A Simple Model Based on Known Plant Defence Reactions Is Sufficient to Explain Most Aspects of Nodulation

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A Simple Model Based on Known Plant Defence Reactions Is Sufficient to Explain Most Aspects of Nodulation Journal of Journal of Experimental Botany, Vol. 46, No. 282, pp. 1-18, January 1995 Experimental Botany HYPOTHESIS PAPER A simple model based on known plant defence reactions is sufficient to explain most aspects of nodulation Robert B. Mellor12'3 and David B. Collinge1 1 Department of Plant Biology, Royal Veterinary and Agricultural University, Thorvaldsensvej 40, DK-1871 Frederiksberg C, Denmark 2 Botanical Institute, University of Basel, Basel, Switzerland Received 23 May 1994; Accepted 15 September 1994 Abstract all plants exhibit the ability to distinguish between patho- genic and symbiotic contacts, since they readily enter into We present the following hypothesis; that lipo- symbiotic associations (for example, over 95% of all oligochitin Nod-factors can act in an elicitor-like fash- vascular plants can enter into intimate symbioses with ion inducing, amongst other effects, a plant chitolytic enzyme, capable of hydrolysing the oligochitin chain fungi, Newman and Reddell, 1987), but are simultan- of the Nod-factor. Decorative groups on the oligochitin eously able actively to rebuff pathogenic challenges chain, e.g. sulphate, may confer partial resistance (Collinge et ai, 1994). There may be similarities between to hydrolysis upon particular Nod-factors. After entry pathogenic and symbiotic modes of infection and at least into the plant, Nod-factor synthesis must be down- some elements of the molecular recognition mechanisms regulated in order to avoid further, unwanted, eli- may be common to both cases. The end results of citation and the consequent abortion of the symbiosis. the recognition sequences are, however, very different. The plant-derived compounds inhibiting the synthesis Pathogenic attack leads to cell necrosis and cell death, of bacterial Nod-factors are limiting in root tissue, whereby, for example, symbiotic nodule formation results leading to residual elicitation and the abortion of infec- in nitrogen-fixing bacteroids encapsulated in apparently tion thread formation. Nod-gene anti-induction is, fur- healthy leghaemoglobin-containing plant tissue (Staehelin thermore, inactivated by both light and nitrate, thus etal., 1992a). contributing to the inhibition of nodulation under these In the following sections, we examine the phenomenon conditions. In nitrogen-fixing nodules, the bacteroids of the nitrogen-fixing root nodule symbiosis (between are exposed to both nod-gene inducing and repressing rhizobia and legume plants) in the light of known plant compounds. The slow accumulation of Nod-factors responses to antagonistic microorganisms generally. This within the peribacteroid space eventually results in includes the production of phytoalexins and their (often the elicitation of phytoalexin synthesis and nodule bio-active) precursors, the anti-microbial hydrolases senescence. glucanase and chitinase, and the action of these upon bacterial components, especially the action of plant chi- Key words: Chitinase, elicitors, Leguminosae, Nod-factors, tinase (s) on Nod-factors. We also analyse the methods Rhizobium, symbiosis. whereby the plant can influence the bacterial synthesis of Nod-factors and factors affecting these control mechan- isms. The result is a model which explains almost all Introduction facets of nodulation. By virtue of their immobility, terrestrial plants have had to develop an extraordinary genetic and metabolic plasti- Terms and definitions city enabling them to deal with diverse environmental stresses. Such stresses include their habitual encounters Whilst not wanting to introduce new expressions into the with soil, water, or air-borne microbes. Apparently almost literature, the following terms will be used in specific 'To whom correspondence should be addressed in Denmark. Fax; +45 35 28 33 10. 6 Oxford University Press 1995 2 Mellor and Collinge ways for the purposes of this paper. Nod-on; any low the automatic consequence of elicitation (Jakobek and molecular weight substance, usually plant-derived, cap- Lindgren, 1993). able of inducing expression of the rhizobial common nod- genes when present at low concentrations. Nod-off; as above, but capable of inhibiting or reversing the above Plant defence reactions in nodulation process (for further explanation, see Section 7). Chitinase; (1) Properties of Nod-factors an enzymic activity capable of hydrolysing oligochitin chains of length equal to, or greater than, 3 JV-acetyl- The molecular structure of a typical Nod-factor was first glucosamine units. Elicitors; products, often of microbial presented by Lerouge et al. (1990) and has recently been origin, capable of inducing one or several responses in reviewed by Vijn et al. (1993). The molecule consists of plants, all of which are associated with the 'defence a backbone of saccharide residues attached to a lipid tail. response' (sometimes called 'resistance response' or This has led to the term 'lipo-oligosaccharides' to describe 'pathogenesis response', e.g. Lucas et al., 1985; Collinge Nod-factors. The saccharide backbone may be further and Slusarenko, 1987; Collinge et al., 1994). The defence decorated with additional groups, e.g. sulphate (for response can include the accumulation of phytoalexins reviews see Verma, 1992; Vijn et al., 1993). A closer (Ouchi, 1983; Dixon, 1986; Nicholson and Hammer- inspection of the sugar residues involved reveals that they schmidt, 1992; Collinge et al., 1994), peroxidase activity are iV-acetyl-glucosamine. Thus the Nod-factor molecule (Svalheim and Robertsen, 1990), glucanase activity could more correctly be called a 'lipochitosan'. (Mauch et al., 1988), chitinase activity (Collinge et al., It is central to our hypothesis that the oligochitin 1993) and may be associated with the production of the portion of Nod-factor molecules behaves as oligochitins stress hormone ethylene which, in turn, can provoke are known to do in other systems, that is, they can be certain of the above effects (Boiler, 1988). Elicitors can perceived by plant cells in an elicitor-like fashion and be either of exogenous (i.e. microbial), or endogenous that they are also substrates for plant hydrolases. The origin (i.e. derived from the plant, for example, its own contention that Nod-factors may be described as elicitors cell wall). Elicitors are fortuitously recognized by a host comes from the following considerations; they cause receptor; thus any elicitor may be of limited host range alkalinization of the medium in tomato cell-culture sys- (Collinge et al., 1994; Ebel and Cosio, 1994). Salicylic tems in a fashion similar to that caused by known elicitors, acid and jasmonic acid, which are often treated as eli- and this effect can be blocked by pre-treatment of the citors, are not considered as such here, but rather as cells with elicitor, exactly as the effect of oligochitin hormones. Hypersensitive response ('HR'); here the elicitor can also be blocked by Nod-factor (Staehelin definition of Klement (1982) is used, with the following et al., 1994a); they cause phytoalexin (capsidiol) accumu- comments; firstly, it is almost impossible to prove that a lation in green peppers (W.J. Bell and R.B. Mellor, localized response, for example, as noted recently in front unpublished observations) and phytoalexin response in of several growing infection threads (Vasse et al., 1993), homologous legume suspension cultures (Savoure et al., is a hypersensitive response because the increased enzyme 1994); they induce peroxidase activity on host legume or product levels are diluted out by surrounding, non- roots (Salzwedel and Dazzo, 1993); they induce chitinase reacting, tissue. Secondly, as shown in Table 1, even in activity after being applied to host and non-host roots those Fix" nodules accumulating higher levels of defence (Staehelin et al., 19946; Schultze et al., 1993) and non- response-associated activities, the absolute amounts of host leaves (Nielsen et al., 19946). It should, however, be phytoalexin and chitinase accumulated are far less than noted that the results from the tomato cell assay system those recorded for classical hypersensitive responses. In reveal Nod-factors to have a milder action (i.e. less short, caution should be exercised when using this expres- alkalinization per mole substance) than many classical elicitors (compare Staehelin et al., 1994a with Felix et al., sion, especially in connection with nodules. It should 1993). The second contention, that Nod-factors are sub- also be noted that the hypersensitive response is not strates for chitinases, has been proven using a variety of host and non-host derived chitinases both in vitro Table 1. Levels of some plant defence reactions in control and (Staehelin et al., 19926, 1994a) and in vivo (Staehelin infected soybean tissue et al., 19946; Schultze et al., 1993). Roots Fix + nodules Fix" nodules Pathogen/HR Recourt et al. (1992) state that 'Rhizobial signal molec- ules are only recognized by a host plant, whereas elicitors Phytoalexin 0.6±0.2' 5±3' 50-2001 c. 100O2 (^g/gFW) are recognized by various non-host plants'. Nod-factors, Chitinase 0.43 1.5-2.53 3-43 c. 5504 however, are perceived by such diverse tissues as tomato (nkat/g FW) (Staehelin et al., 19946), carrot (De Jong et al., 1992) Data collated from: 1, Werner et al. (1985). 2, Osman and Fett and both host and non-host legume roots (Staehelin et al., (1983). 3, Staehelin et al. (1992a). 4, Metraux and Boiler (1986). 1994a, 6). The difference between host and non-host Nodulation explained? 3 response lies in the timing of the elicitation response (see natant and pellet. If the majority of the Nod-factor Section 2, Fig. 1, Staehelin et al., 1994a). Thus the state- is associated with the bacterium, then this implies that ment of Recourt et al. (1992) should be modified to the plant reactions associated with nodulation could be 'Rhizobial signal molecules can be perceived by a wide extremely localized, an aspect discussed further below range of plants, and elicit their own rapid hydrolysis. In (Section 5 on the specificity of nodulation). those cases (host plants) where elicitation is delayed, the Nod-factor has a long enough half-life for the plant to (2) The autoregulation of nodulation experience other biological effects, including root-hair- curling ...'.
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