Update on Symbiosis

With one notable exception, namely the genus Parasponia in the elm family, the ability to form nitrogen-fixing symbiosis with gram-negative soil bacteria known as rhizobia is restricted to the legume family, Leguminosae. It has been well established that initiation of successful nodular symbiosis requires strict compatibility between rhizobial-secreted Nod factors and a perception machinery of the plant host roots (Albrecht et al., 1999). Nod factors comprise a heterogeneous group of morphogenic lipochitooligosaccharides with a major role as determinants of host specificity (Spaink, 2000). Nanomolar concentrations of purified Nod factors can mimic bacterial infections to a certain extent by inducing several root cellular responses that are characteristic of compatible interaction between the host plant and symbiotic bacteria. Early plant responses to Nod factors, including activation of a subset of plant specific genes called early nodulins (ENODs), calcium spiking, root hair curling, pre-infection thread formation, and induction and organogenesis of nodule primordia (NP), have been extensively studied and constitute the subject of several recent reviews (for example, Geurts and Bisseling, 2002). Curiously, while the biology of nitrogen-fixing root nodules has been broadly investigated, we still do not understand what unique evolutionary event predisposed legume plants and Parasponia to form nodular symbiosis with rhizobia. In an attempt to address this question, we analyze here three specific examples demonstrating that this symbiosis may have recruited existing plant regulatory programs during its evolution. The fact that there are homologs of ENOD genes in non-legumes suggests that development of nodular symbiosis involved the harnessing of genetic functions from existing developmental pathways. Albrecht et al. (1999) discussed genetic and corroborating molecular observations that support the notion that legume-Rhizobium symbiosis may have evolved, in part, from a pre-existing pathway(s) that regulates the more widespread (pertaining to more than 80% of extant plant species) and ancient phosphate-acquiring symbiosis of plant roots with fungi, termed arbuscular mycorrhiza (AM). In the first section of this Update, we discuss recently characterized genes that may represent “footprints” of such a pathway(s). That a number of nodulin genes are also expressed in non-symbiotic plant tissues suggests that genes involved in nonsymbiotic pathways may also have been recruited during the evolution of nodular symbiosis. We highlight this point in the second section of the Update by discussing similarities between early rhizobial infections and events occurring during flower pollination. The final section addresses early nodulation events on a broader, organismal, level. Here, we consider a longrange signaling mechanism, termed autoregulation of nodulation, and its relationship with other regulatory pathways that coordinate plant growth and development. While these three examples refer to a broad spectrum of early developmental events during legume-Rhizobium interactions, they emphasize that the evolution of nodular symbiosis probably involved the recruitment of several different plant developmental programs.