The radiation of nodulated Chamaecrista species from the rainforest into more diverse habitats has been accompanied by a reduction in growth form and a shift from fixation threads to symbiosomes

Abstract

All non-mimosoid nodulated genera in the legume subfamily Caesalpinioideae confine their rhizobial symbionts within cell wall-bound “fixation threads” (FTs). The exception is the large genus Chamaecrista in which shrubs and subshrubs house their rhizobial bacteroids more intimately within symbiosomes, whereas large trees have FTs. This study aimed to unravel the evolutionary relationships between Chamaecrista growth habit, habitat, nodule bacteroid type, and rhizobial genotype. The growth habit, bacteroid anatomy, and rhizobial symbionts of 30 nodulated Chamaecrista species native to different biomes in the Brazilian state of Bahia, a major centre of diversity for the genus, was plotted onto an ITS-TrnL-F-derived phylogeny of Chamaecrista. The bacteroids from most of the Chamaecrista species examined were enclosed in symbiosomes (SYM-type nodules), but those in arborescent species in the section Apoucouita, at the base of the genus, were enclosed in cell wall material containing homogalacturonan (HG) and cellulose (FT-type nodules). Most symbionts were Bradyrhizobium genotypes grouped according to the growth habits of their hosts, but the tree, C. eitenorum, was nodulated by Paraburkholderia. Chamaecrista has a range of growth habits that allow it to occupy several different biomes and to co-evolve with a wide range of (mainly) bradyrhizobial symbionts. FTs represent a less intimate symbiosis linked with nodulation losses, so the evolution of SYM-type nodules by most Chamaecrista species may have (a) aided the genus-wide retention of nodulation, and (b) assisted in its rapid speciation and radiation out of the rainforest into more diverse and challenging habitats.

Mimosaspecies endemic to acidic soils in central Brazil are nodulated by a high diversity ofParaburkholderiagenotypes, but widespread species are nodulated byParaburkholderia,CupriavidusorRhizobiumdepending on soil characteristics

“…also nodulate these hosts (Taulé et al 2012; Bournaud et al 2013, Silva et al 2018; Zilli et al 2021). The recent discovery that the non-mimosoid Caesalpinioideae species, Chamaecrista eitenorum , is nodulated effectively by P. nodosa -like strains (Casaes et al 2024) further indicates that it is likely that we are only scratching the surface of the actual diversity of neotropical and sub-neotropical Beta-rhizobial-legume interactions. Indeed, given the propensity of South American Paraburkholderia and Cupriavidus strains to nodulate effectively with papilionoids like common bean and Siratro ( Macroptilium atropurpureum ) (da Silva et al 2012; Dall-Agnol et al 2016, 2017) it is highly probable that Beta-rhizobia will be isolated from more crop legumes, as well as from their diverse native neotropical relatives.…”