Legume–rhizobial symbiosis: an anorexic model?

In order to elucidate the detailed interactions between host legume and rhizobial symbiont, two model legumes are being widely studied. These are Medicago truncatula and Lotus japonicus, which have been chosen because of their small genome and seed sizes and the sequencing of their rhizobia. They represent different types of nodule morphology and anatomy, having indeterminate and determinate nodules respectively (Fig. 1a,b). They have already yielded significant information on the processes of initial root hair infection and early nodulation events (see Jones et al., 2007 for Medicago and Oldroyd & Downie, 2008 for a more general discussion). Later stages in the development of nodules are less well understood and, unfortunately, it now emerges that the symbiosis between M. truncatula and the preferred symbiont Sinorhizobium meliloti Sm1021 is not very good at fixing nitrogen (Terpolilli et al., this issue pp. 62–66), leaving plants nitrogen deficient compared with those grown on combined nitrogen. Workers with L. japonicus are using a variety of endophytes, but those most commonly used are Mesorhizobium loti strains R7A, Tono, NZP2235 and MAFF303099. There is no information as to how good these are in fixing nitrogen, although M. loti NZP2235 has a reputation in the L. japonicus community for good nodulating ability (Kanamori et al., 2006; T. Ott, pers. comm.). However, the genome of M. loti MAFF303099 has been sequenced since 2000 by Kaneko et al., and therefore it is inevitably the strain of choice for many L. japonicus researchers (Ooki et al., 2005). It would certainly be very interesting to compare these M. loti strains for their ability to fix nitrogen in symbiosis with L. japonicus. However, even if they are very efficient, they are not typical of determinate nodules in general. Lotus is one of a small group of temperate legume genera having determinate ‘desmodioid’ nodules similar in appearance and general internal structure to those of the large clade of tropical-subtropical legumes such as soybean Glycine max and beans (species of Phaseolus and Vigna). Whereas Lotus nodules, in common with all tested temperate counterparts, export amides as a product of fixation, all tropical desmodioid legumes (but not other tropical legumes tested) export the ureides allantoin and allantoic acid (Sprent, 2001). This requires a completely different suite of enzymes as Ramirez et al (2005) have shown. (a) Sections of nodules on roots of Medicago truncatula inoculated with Sinorhizobium (Ensifer) meliloti Sm1021. (b) Lotus japonicus inoculated with Mesorhizobium loti NZP2235 and (c) on Aeschynomene sensitiva. The nitrogen-fixing zone is marked with an asterisk in each case, and the meristems in (a) and (c) are indicated by an arrow. In (a) the nodule appears normal, but appearances can obviously be deceptive. Bar, 200 µm. Are there other species that could be used as models? To some extent this depends on the questions being asked. M. truncatula and L. japonicus both have a root hair infection pathway, in common with most, but not all crop legumes. One of the alternative modes of infection is the so-called ‘crack entry’ where bacteria invade through breaks in the epidermis where lateral or adventitious roots emerge and where infected tissue contains no uninfected cells (Fig. 1c). Nonhair infection may occur in 25% of legumes and has been suggested to be the basal type (Sprent, 2007). It is thus also of interest to those who want to try to extend the range of nodulated plants. Recent work with photosynthetic bradyrhizobia and certain stem nodulating species of Aeschynomene, support the idea of the basal nature of this type of symbiosis, since the bacteria lack the common nod genes, nodABC, essential for hair infection (Giraud et al., 2007). ‘... in the real world, especially in the tropics, ineffective symbioses are common.’ Because of its importance in the diet of many of the poorest peoples in the world, the common bean (Phaseolus vulgaris) is being targeted in an international programme called ‘Phaseomics’ (Broughton et al., 2003, Ramirez et al., 2005). Despite its wide use for food, P. vulgaris is an unreliable nodulator, possibly because of the range of rhizobia with which it can associate. This is one of the many problems being tackled by the Phaseomics programme; others include disease control and yield improvement. Phaseomics is the most advanced of a number of legume projects discussed at a meeting on legumes as a model plant family – Genomics for Food and Feed (Gepts et al., 2005). Pea (Pisum sativum) remains popular for studies on nodulation as well as all the traits originally identified by Mendel. Lodwig et al. (2003) published a very detailed study using mutants of both pea and its symbiont Rhizobium leguminosarum in which they established that a very specific exchange of metabolites is necessary for the symbiosis to be fully effective. However, in the real world, especially in the tropics, ineffective symbioses are common (Sprent, 2003). In their paper on Medicago truncatula Terpolilli et al. (2008) suggest an alternative sequenced strain, Sinorhizobium medicae WSM 419, which is fully effective with this host. Comparison of the nodulation processes using this strain with those of the less effective Sinorhizobium meliloti Sm1021, could be an ideal way to find out more about what makes ineffective nodules. We thank Jason Terpolilli for providing the section shown in Fig. 1a and Allan Downie for providing us with a copy of Oldroyd and Downie in advance of publication.