Genisteae

Abstract: The papilionoid legume genus Lupinus comprises ca. 275 species of annual and perennial herbs and shrubs with an amphi-Atlantic distribution. The majority of species are distributed in the New World, with ca. 100 species in the western part of North America and ca. 85 species in the Andes. Only 15 species are found in the Old World, mainly surrounding the Mediterranean (15). Lupines, in part due to their highly effective nitrogen-fixing symbiosis with root nodule bacteria, have been grown since antiquity as a green manure and are an important pulse crop. Their adaptation to nutrient-poor, often acid soils and arid climates means that lupines can be grown in areas where cultivation of more demanding crops, such as soybeans, is problematic (12). Lupines constitute an isolated lineage within the tribe Genisteae sensu stricto (2). The remaining Genisteae form two assemblages, one comprising the genera Anarthrophyllum, Argyrolobium, Dichilus, and Melolobium, which diversified predominantly in the Southern Hemisphere, and the other (called Genistinae) comprising Cytisus, Chamaecytisus, Genista, Retama, Spartium, Teline, Ulex, and several other small genera that have their centers of diversity in the Mediterranean basin. The geographic origin of the genus Lupinus remains unclear. However, phylogenetic analyses reveal four robustly supported clades that are congruent with lupine geography and chromosome number (1, 2, 3, 15). Notably, all the Old World species are placed in a single clade, here labeled OW, while the New World species comprise three strongly supported lineages; a large western New World (WNW) group distributed in western North America, Mexico, and the Andes; a small group centered in the southeast United States; and a predominately lowland eastern New World (ENW) group distributed mainly in the south-central United States and eastern South America (Fig. ​(Fig.1).1). The two large WNW and ENW lineages have largely allopatric distributions, but species from both clades are sympatric in limited areas, notably, in the south-central Andes in Bolivia. The Andean species (81 out of 85), which are nested in a strongly supported subclade within the WNW clade, provide one of the most spectacular examples of recent explosive plant species diversification driven by the recent uplift of the Andes (15). FIG. 1. Schematic Lupinus phylogeny showing major clades, which are robustly supported in individual and combined parsimony and Bayesian analyses of the nuclear DNA sequence loci internal transcribed spacer and LEGCYC1A that include up to 140 accession numbers ... Cross-inoculation studies have shown that lupines share a common rhizobial pool with other legumes in the tribe Genisteae, including the genera Cytisus, Genista, Retama, and Teline (18, 19, 37, 38, 47). Additionally, lupines are effectively nodulated by rhizobia isolated from serradella (Ornithopus, a genus that belongs to the more distantly related tribe Loteae) and are ineffectively nodulated by rhizobia isolated from the genera Lotus, Anthyllis, and Phaseolus (8, 9, 25). Lupines are nodulated by fast-growing rhizobia (that are poorly characterized), as well as by slow-growing strains of the genus Bradyrhizobium (8, 25). Phylogenetic studies based on nonsymbiotic genes revealed significant heterogeneity among lupine bradyrhizobia, which group with several additional distinct lineages, including Bradyrhizobium japonicum and Bradyrhizobium canariense. Fewer lupine bradyrhizobia grouped with Bradyrhizobium elkanii in housekeeping gene studies (5, 17, 23, 28, 41, 42, 48). In contrast to the housekeeping gene phylogenies, most lupine isolates form a single cluster, referred to as clade II, in nodA nodulation gene trees. Notably, nodA clade II comprises bradyrhizobia isolated from other Genisteae species and from serradella species, which corroborates cross-inoculation data (19, 28, 42). Similar grouping was observed in phylogenies of nodC and nifH genes (17, 48, 49), giving rise to the new biovar genistearum for Bradyrhizobium strains nodulating Genisteae legumes, which presumably correspond to clade II Bradyrhizobium strains. So far, most research has focused on Bradyrhizobium isolates from native Old World lupines growing in the Mediterranean (2) or from Old World species introduced into continental Europe, Australia, and South Africa. Considering that the four major lupine lineages occupy largely isolated present-day geographic distributions, the presumption is that they may be nodulated by rhizobia differing from European clade II strains. Our objective was to address this issue by searching for possible biogeographic patterns preserved in nod gene phylogenies. For this purpose, we selected Bradyrhizobium strains isolated mainly from lupine nodules collected from native Andean and lowland South American lupines (15).