Keys to Symbiotic Harmony

W. J. Broughton, S. Jabbouri, X. Perret
2000 Journal of Bacteriology  
At least three different sets of symbiotic signals (here, they are compared to locks and keys) are exchanged between legumes and rhizobia during nodule development. Flavonoids, the first of these, emanate from the plant and interact with rhizobial NodD proteins that serve as both environmental sensors and activators of transcription. A second set of signals is synthesized when NodD-flavonoid complexes activate transcription from nod boxes. Most of the genes immediately downstream of these
more » ... ers are involved in the synthesis of lipooligosaccharidic Nod factors that provoke deformation of root hairs and allow rhizobia to enter the root through infection threads. Fine-tuning of transcription of nodulation (nod) genes is probably related to sequence variations in individual nod boxes (there are 19 on the symbiotic plasmid of the broad-hostrange Rhizobium sp. strain NGR234). Other rhizobial products seem to be necessary for continued infection thread development, and these represent a third set of signals. Among them are extracellular polysaccharides (EPS) and related compounds, as well as proteins exported by the type three secretion system (TTSS). In the latter case, flavonoids also activate protein secretion, suggesting that the same keys can unlock different doors. Symbioses are nearly ubiquitous, and many are also persistent (56). Mutualistic, nitrogen-fixing associations between members of the plant family Leguminosae, and the soil bacteria Azorhizobium, Bradyrhizobium, Mesorhizobium, and Rhizobium (collectively called rhizobia) contribute substantially to plant productivity (111). Legume-Rhizobium symbioses are marriages between two vastly different genomes. In rhizobia, these include a chromosome plus zero to many plasmids, totalling 6 to 9 Mbp (71). In contrast, genomes of legumes are much larger, some comprising more than 20 chromosomes with total DNA contents that range from about 450 to 4,500 Mbp per haploid genome (1C) (1). As examples, the model legumes Lotus japonicus and Medicago truncatula have six or eight chromosomes totalling 450 and 500 Mbp/1C (14) , respectively. Common beans (Phaseolus vulgaris) and related species (e.g., Vigna unguiculata) (both genera belong to the tribe Phaseoleae) have 11 chromosomes each (24) with DNA contents of 637 (1) and 540 Mbp/1C (50). Furthermore, several widely cultivated legumes such as Arachis hypogaea, Glycine max, and Medicago sativa are effectively polyploid, although in G. max most loci segregate as if they were diploid. Legume genomes are thus at least 50 times larger than those of their microsymbionts. Given this disparity, it is difficult to imagine that theirs is a marriage of equals. Nevertheless, their respective contributions are probably not vastly different (see reference 48). LEGUME BOWERS ARE DECORATED WITH FLAVONOIDS Which partner initiates contact? Since plants are nonmotile, it is tempting to think that courtship begins when bacteria advance into the legume rhizosphere. Yet chemotaxis and motility among rhizobia are clearly not essential for nodulation (see reference 30). Rather than "love at first sight" other, more subtle factors help the partners match each other. Foremost among these are phenolic substances, especially flavonoids. Although small quantities are excreted continuously, flavonoid concentrations in the rhizosphere increase in response to compatible rhizobia (82, 94, 117) . In turn, rhizobia use these plant products for their own ends. Some flavonoids induce the expression of nodulation (nod, noe, and nol) and related genes (see reference 12), while others are catabolized (15, 79, 80) . Degradation leads first to the appearance of chalcones, which can be more efficient inducers of nod genes than the flavonoids themselves (41). Plant "attractiveness" probably correlates with the spectrum of phenolic compounds (especially flavonoids) that it secretes. Rhizobia respond to these advances through NodD and related proteins which act as both sensors of the environment and activators of transcription (93). Once derepressed, nodulation and other genes direct the synthesis and release of substances that profoundly affect legume roots (see below). It is as if plants construct elaborate "bowers," replete with flavonoids and other attractants, to entice rhizobia towards them. If this bower analogy reflects reality, then the various types of bower should mirror legume host range. This poses two questions. Do bowers exist? And if yes, are their decorations unique? Although it is impossible, given the limited information available to definitively answer these questions, a tentative yes seems to be the most likely answer to the first for the following reasons. (i) Legumes support considerably larger rhizosphere populations than nonlegumes do (see reference 3). (ii) These larger populations are enriched in rhizobia (see reference 10). (iii) The roots of M. sativa are surrounded by a coarse, granular, mucilaginous material contained within a membranous layer of greater electron density (17). Rhizobia penetrate this outer "membrane" and form an almost continuous layer five to ten cells deep. (iv) Rhizobia rapidly proliferate around the roots of developing legumes (see reference 10). (v) Although the evidence is not completely consistent, there are indications that production of nod gene-inducing flavonoids is restricted to the elongating root hair zone from which most nodules later develop (117). It is as if niches in the legume rhizosphere are tailored to rhizobia, but the question remains-are these niches especially
doi:10.1128/jb.182.20.5641-5652.2000 pmid:11004160 pmcid:PMC94683 fatcat:33cltssuyzb3znup3dt4dxfkse