Biology subjects

James, E. K.

Publications and source records attributed to James, E. K..

7 recordsLinked to original sources

bioRxiv2024

Mimosa species endemic to acidic soils in central Brazil are nodulated by a high diversity of Paraburkholderia genotypes, but widespread species are nodulated by Paraburkholderia, Cupriavidus or Rhizobium depending on soil characteristics

Neotropical Beta-rhizobia have a particular affinity to the large legume (Fabaceae) genus Mimosa and some of its relatives in the tribe Mimosae of the Caesalpinioideae subfamily. However, little is still known about the ecology of this interaction, especially the relationship between the rhizobia of "widespread" pan-tropical Mimosa species like M. pudica and the rhizobia that nodulate endemic Mimosa species that are very restricted in their habitats. The objective of this study was to examine the microsymbionts of Mimosa spp. and some other mimosoids in climates ranging from tropical to subtropical, humid to semi-arid, with varied soil characteristics and altitudes, with the aim of testing the hypothesis that widespread species have more cosmopolitan symbiont preferences than endemic ones. Nodules were sampled from more than 40 Mimosa spp. and related taxa in eleven Brazilian states, many endemics or biome-restricted, but particular attention was paid to sample nodules from the widespread species M. pudica at all locations. The Mimosa symbionts comprised 19 potential 16S rRNA and recA groups at the species level, with 16 belonging to the genus Paraburkholderia, including six lineages that may represent new species. The remaining genotypes consisted of 14 strains in two lineages of Cupriavidus that were mainly isolated from M. pudica growing at low altitudes, plus a single lineage of Rhizobium also from M. pudica. It is concluded that a high diversity of Paraburkholderia strains dominate as symbionts of Mimosa in the acidic soils of its main center of radiation in Central Brazil but that Cupriavidus and Rhizobium comprise a significant minority of symbionts of widespread Mimosa spp., especially M. pudica, in lowland or disturbed areas with less acidic soils. Mimosa symbiont diversity is thus driven either by edapho-climatic characteristics for widespread species and/or by co-evolution of the symbiotic partners for endemic species.

plant biology↗

bioRxiv2023

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

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.

plant biology↗

bioRxiv2022

Aromatic amino acid biosynthesis by a Lotus Aldolase impacts root hair development and symbiotic associations

O_LILegume roots can be symbiotically colonized by arbuscular mycorrhizal (AM) fungi and nitrogen-fixing bacteria. In Lotus japonicus, the latter occurs intracellularly by the cognate rhizobial partner Mesorhizobium loti or intercellularly with the Agrobacterium pusense IRBG74 strain. Although these symbiotic programs show distinctive cellular and transcriptome signatures, some molecular components are shared. C_LIO_LIIn this study, we demonstrate that Aldolase1, the first enzyme in the biosynthetic pathway of aromatic amino acids (AAA), plays a critical role in root hair development and for AM and rhizobial symbioses in Lotus. C_LIO_LITwo homozygous mutants affected in Aldolase1 (ald1-1 and ald1-2) show drastic alterations in the root hair morphology, associated with a progressive disruption of the actin cytoskeleton. The altered root hair structure was prevented by chemical and genetic complementation. C_LIO_LIBoth ald1-1 and ald1-2 show significant reductions in rhizobial infection (intracellular and intercellular), nodule organogenesis and AM colonization. RNAseq analysis of ald1-2 roots suggested that these phenotypes are associated with downregulation of several cell wall related genes, and with an attenuated symbiotic signalling. This work provides robust evidence that links AAA metabolism to root hair development and successful symbiotic associations. C_LI

plant biology↗

bioRxiv2022

Two shifts in evolutionary lability underlie independent gains and losses of root-nodule symbiosis in a single clade of plants

Root nodule symbiosis (RNS) allows plants to access atmospheric nitrogen converted into usable forms through a mutualistic relationship with soil bacteria. RNS is a complex trait requiring coordination from both the plant host and the bacterial symbiont, and pinpointing the evolutionary origins of root nodules is critical for understanding the genetic basis of RNS. This endeavor is complicated by data limitations and the intermittent presence of RNS in a single clade of ca. 30,000 species of flowering plants, i.e., the nitrogen-fixing clade (NFC). We developed the most extensive de novo phylogeny for all major lineages of the NFC and an enhanced root nodule trait database to reconstruct the evolution of RNS. Through identification of the evolutionary pathway to RNS gain, we show that shifts among heterogeneous evolutionary rates can explain how a complex trait such as RNS can arise many times across a large phylogeny. Our analysis identifies a two-step process in which an ancestral precursor state gave rise to a more labile state from which RNS was quickly gained at specific points in the NFC. Our rigorous reconstruction of ancestral states illustrates how a two-step pathway could have led to multiple independent gains and losses of RNS, contrary to recent hypotheses invoking just a single gain and numerous losses. RNS may be an example of multi-level convergent evolution, thus requiring a broader phylogenetic and genetic scope for genome-phenome mapping to elucidate mechanisms enabling fully functional RNS.

evolutionary biology↗

bioRxiv2022

The innovation of the symbiosome has enhanced the evolutionary stability of nitrogen fixation in legumes

O_LINitrogen-fixing symbiosis is globally important in ecosystem functioning and agriculture, yet the evolutionary history of nodulation remains the focus of considerable debate. Recent evidence suggesting a single origin of nodulation followed by massive parallel evolutionary losses raises questions about why a few lineages in the N2-fixing clade retained nodulation and diversified as stable nodulators while most did not. Within legumes, nodulation is restricted to the two most diverse subfamilies, Papilionoideae and Caesalpinioideae, which show stable retention of nodulation across their core clades. C_LIO_LIWe characterize two nodule anatomy types across 128 species in 56 of the 150 genera of the legume subfamily Caesalpinioideae: 1) fixation thread nodules (FTs), where nitrogen-fixing bacteroids are retained within the apoplast in modified infection threads and 2) symbiosomes, where rhizobia are symplastically internalized in the host cell cytoplasm within membrane-bound symbiosomes. C_LIO_LIUsing a robust phylogenomic tree based on 997 genes from 146 caesalpinioid genera, we show that losses of nodulation are more prevalent in lineages with FTs. C_LIO_LIWe propose that evolution of the symbiosome allows for a more intimate and enduring symbiosis through greater compartmentalisation of their rhizobial microsymbionts, resulting in greater evolutionary stability of nodulation across this species-rich pantropical clade of legumes. C_LI

evolutionary biology↗

bioRxiv2021

A promiscuity locus confers Lotus burttii nodulation with rhizobia from five different genera

Legumes acquire access to atmospheric nitrogen through nitrogen fixation by rhizobia in root nodules. Rhizobia are soil dwelling organisms and there is a tremendous diversity of rhizobial species in different habitats. From the legume perspective, host range is a compromise between the ability to colonize new habitats, where the preferred symbiotic partner may be absent, and guarding against infection by suboptimal nitrogen fixers. Here, we investigate natural variation in rhizobial host range across Lotus species. We find that Lotus burttii is considerably more promiscuous than Lotus japonicus, represented by the Gifu accession, in its interactions with rhizobia. This promiscuity allows Lotus burttii to form nodules with Mesorhizobium, Rhizobium, Sinorhizobium, Bradyrhizobium, and Allorhizobium species that represent five distinct genera. Using recombinant inbred lines, we have mapped the Gifu/burttii promiscuity QTL to the same genetic locus regardless of rhizobial genus, suggesting a general genetic mechanism for host-range expansion. The Gifu/burttii QTL now provides an opportunity for genetic and mechanistic understanding of promiscuous legume-rhizobia interactions.

plant biology↗

bioRxiv2020

Distinct signalling routes mediates intercellular and intracellular rhizobial infection in Lotus japonicus

Rhizobial infection of legume roots during development of nitrogen fixing root nodules occurs either intracellularly though plant derived infection threads traversing the epidermal and cortical cell layers to deliver the bacteria or intercellularly via bacterial entry between epidermal plant cells. Although, around 25% of all legume genera are postulated to be intercellularly infected, the pathways and mechanisms supporting this process has remained virtually unexplored due to lack of genetically amenable legumes that have this infection mode. In this study, we report that the model legume Lotus japonicus is infected intercellularly by Rhizobium sp. IRBG74 and demonstrate that the resources available in Lotus enable insight into the genetic requirements and the fine-tuning of the pathway governing intercellular infection. Inoculation of Lotus mutants shows that Ern1 and RinRK1 are dispensable for intercellular infection in contrast to intracellular infection. Other symbiotic genes, including Nfr5, SymRK, CCaMK, Epr3, Cyclops, Nin, Nsp1, Nsp2, Cbs and Vpy1 are equally important for both entry modes. Comparative RNAseq analysis of roots inoculated with IRBG74 revealed a distinctive transcriptome response compared to intracellular colonization. In particular, a number of cytokinin-related genes were differentially regulated. Corroborating this observation cyp735A and ipt4 cytokinin biosynthesis mutants were significantly affected in their nodulation with IRBG74 while lhk1 cytokinin receptor mutants did not form any nodules. These results indicate that a differential requirement for cytokinin signalling conditions intercellular rhizobial entry and highlight the distinct modalities of the inter- and intra-cellular infection mechanisms.

plant biology↗