Peace talks and trade deals. Keys to long-term harmony in legume-microbe symbioses.

Terrestrial autotrophs such as higher plants are confronted with challenges largely unknown to their counterparts in the seas, including extreme patchiness of inorganic nutrients. Evolution of higher plants has yielded interesting and important solutions to the problem of nutrient acquisition on land. Some of the most intriguing of these involve mutually beneficial symbioses. In fact, evolution of a fungal-plant symbiosis around 450 million years ago may have been the key innovation that enabled plants to colonize the land (Pirozynski and Malloch, 1975; Remy et al., 1994). Related mycorrhizal associations continue to exist for more than 90% of land plants, a reflection of their ancient origin and importance. Mycorrhizal associations enhance the ability of plants to scavenge nutrients such as phosphate from the soil, by virtue of the greater volume of soil exploited by the filamentous fungal partner (Smith and Read, 1997; Smith et al., 2003). In return for its services, the fungus is provided with a carbon source, derived from plant photosynthesis, for biosynthesis and energy metabolism. To avoid exploitation, however, plants have evolved a series of checkpoints that help to discern friend from foe, which presumably switch off defense responses against robbers when a friend comes to visit. A different kind of beneficial plant-microbe interaction that provides a more restricted range of plants with the often-limiting macronutrient nitrogen is symbiotic nitrogen fixation (SNF). This type of symbiosis evolved more recently, some 60 million years ago, and is confined to legumes and a few nonlegumes (Doyle, 1998), which form intracellular symbioses with rhizobia or other nitrogen-fixing bacteria, respectively (Pawlowski and Bisseling, 1996). Once again, the plant provides its beneficial endosymbiont with photosynthate, together with other nutrients, in exchange for valuable fixed nitrogen, in the form of ammonium and amino acids (Udvardi and Day, 1997). Interestingly, some of the signaling pathways that mediate peace between legumes and mycorrhizal fungi also function in the rhizobial symbiosis, and stunning progress has been made recently in identifying a few of the genes involved. Significant progress has also been made in identifying changes in transport and metabolism during symbiosis development, which will contribute to a better understanding of the nature of trade between legumes and their microsymbionts. These breakthroughs largely stem from focused research on two model legumes, Lotus japonicus and Medicago truncatula, and the conjunction of genetics, genomics, and functional genomics. This Update focuses on recent discoveries in the areas of legume-microbe communication and trade, two essential aspects of stable mutualism.