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Secondary metabolites are essential for plant survival and reproduction. Wild undomesticated and tropical plants are expected to harbor highly diverse metabolomes. We investigated the metabolomic diversity of two morphologically similar trees of tropical Africa, Erythrophleum suaveolens and E. ivorense, known for particular secondary metabolites named the cassaine-type diterpenoids. To assess how the metabolome varies between and within species, we sampled leaves from individuals of different geographic origins but grown from seeds in a common garden in Cameroon. Metabolites were analyzed using reversed phase LC-HRMS(/MS). Data were interpreted by untargeted metabolomics and molecular networks based on MS/MS data. Multivariate analyses enabled us to cluster samples based on species but also on geographic origins. We identified the structures of 28 cassaine-type diterpenoids among which 19 were new, 10 were largely specific to E. ivorense and five to E. suaveolens. Our results showed that the metabolome allows an unequivocal distinction of morphologically-close species, suggesting the potential of metabolite fingerprinting for these species. Plant geographic origin had a significant influence on relative concentrations of metabolites with variations up to eight (suaveolens) and 30 times (ivorense) between origins of the same species. This shows that the metabolome is strongly influenced by the geographical origin of plants (i.e., genetic factors).

We report the first annotated chromosome-level reference genome assembly for pea, Gregor Mendel’s original genetic model. Phylogenetics and paleogenomics show genomic rearrangements across legumes and suggest a major role for repetitive elements in pea genome evolution. Compared to other sequenced Leguminosae genomes, the pea genome shows intense gene dynamics, most likely associated with genome size expansion when the Fabeae diverged from its sister tribes. During Pisum evolution, translocation and transposition differentially occurred across lineages. This reference sequence will accelerate our understanding of the molecular basis of agronomically important traits and support crop improvement. The first annotated chromosome-level reference genome assembly for pea, Gregor Mendel’s original genetic model, provides insights into legume genome evolution and the molecular basis of agricultural traits for pea improvement.

Phylogenomic analyses have helped resolve many recalcitrant relationships in the angiosperm tree of life, yet phylogenetic resolution of the backbone of the Leguminosae, one of the largest and most economically and ecologically important families, remains poor due to generally limited molecular data and incomplete taxon sampling of previous studies. Here, we resolve many of the Leguminosae’s thorniest nodes through comprehensive analysis of plastome-scale data using multiple modified coding and noncoding data sets of 187 species representing almost all major clades of the family. Additionally,we thoroughly characterize conflicting phylogenomic signal across the plastome in light of the family’s complex history of plastome evolution. Most analyses produced largely congruent topologies with strong statistical support and provided strong support for resolution of some long-controversial deep relationships among the early diverging lineages of the subfamilies Caesalpinioideae and Papilionoideae. The robust phylogenetic backbone reconstructed in this study establishes a framework for future studies on legume classification, evolution, and diversification. However, conflicting phylogenetic signal was detected and quantified at several key nodes that prevent the confident resolution of these nodes using plastome data alone.

A symbiosis between certain bacteria and their plant hosts delivers fixed nitrogen to the plants. Griesmann et al. sequenced several plant genomes to analyze why nitrogen-fixing symbiosis is irregularly scattered through the evolutionary tree (see the Perspective by Nagy). Various genomes carried traces of lost pathways that could have supported nitrogen-fixing symbiosis. It seems that this symbiosis, which relies on multiple pathways and complex interorganismal signaling, is susceptible to selection and prone to being lost over evolutionary time. Science , this issue p. eaat1743 ; see also p. 125 Genome-wide comparative analysis across species reveals the fragility of the plant-bacterial symbiosis needed for nitrogen fixation. The root nodule symbiosis of plants with nitrogen-fixing bacteria affects global nitrogen cycles and food production but is restricted to a subset of genera within a single clade of flowering plants. To explore the genetic basis for this scattered occurrence, we sequenced the genomes of 10 plant species covering the diversity of nodule morphotypes, bacterial symbionts, and infection strategies. In a genome-wide comparative analysis of a total of 37 plant species, we discovered signatures of multiple independent loss-of-function events in the indispensable symbiotic regulator NODULE INCEPTION in 10 of 13 genomes of nonnodulating species within this clade. The discovery that multiple independent losses shaped the present-day distribution of nitrogen-fixing root nodule symbiosis in plants reveals a phylogenetically wider distribution in evolutionary history and a so-far-underestimated selection pressure against this symbiosis.

Adaptive changes in plant phenology are often considered to be a feature of the so-called ‘domestication syndrome’ that distinguishes modern crops from their wild progenitors, but little detailed evidence supports this idea. In soybean, a major legume crop, flowering time variation is well characterized within domesticated germplasm and is critical for modern production, but its importance during domestication is unclear. Here, we identify sequential contributions of two homeologous pseudo-response-regulator genes, Tof12 and Tof11 , to ancient flowering time adaptation, and demonstrate that they act via LHY homologs to promote expression of the legume-specific E1 gene and delay flowering under long photoperiods. We show that Tof12 -dependent acceleration of maturity accompanied a reduction in dormancy and seed dispersal during soybean domestication, possibly predisposing the incipient crop to latitudinal expansion. Better understanding of this early phase of crop evolution will help to identify functional variation lost during domestication and exploit its potential for future crop improvement. Whole-genome resequencing and association analyses in 424 soybean accessions identify two homeologous genes that contributed to flowering time adaptation during soybean domestication.

Among legumes (Fabaceae) capable of nitrogen-fixing nodulation, several Aeschynomene spp. use a unique symbiotic process that is independent of Nod factors and infection threads. They are also distinctive in developing root and stem nodules with photosynthetic bradyrhizobia. Despite the significance of these symbiotic features, their understanding remains limited. To overcome such limitations, we conduct genetic studies of nodulation in Aeschynomene evenia , supported by the development of a genome sequence for A. evenia and transcriptomic resources for 10 additional Aeschynomene spp. Comparative analysis of symbiotic genes substantiates singular mechanisms in the early and late nodulation steps. A forward genetic screen also shows that AeCRK, coding a receptor-like kinase, and the symbiotic signaling genes AePOLLUX, AeCCamK, AeCYCLOPS, AeNSP2, and AeNIN are required to trigger both root and stem nodulation. This work demonstrates the utility of the A. evenia model and provides a cornerstone to unravel mechanisms underlying the rhizobium–legume symbiosis. The establishment of symbiotic interaction between Aeschynomene evenia and photosynthetic bradyrhizobia doesn’t involve the canonical Nod factors and infection threads. Here, the authors assemble the draft genome of A. evenia and identify a receptor-like kinase in mediating the symbiotic interaction.

Drought and its interaction with high temperature are the major abiotic stress factors affecting soybean yield and production stability. Ongoing climate changes are anticipated to intensify drought events, which will further impact crop production and food security. However, excessive water also limits soybean production. The success of soybean breeding programmes for crop improvement is dependent on the extent of genetic variation present in the germplasm base. Screening for natural genetic variation in drought– and flooding tolerance-related traits, including root system architecture, water and nitrogen-fixation efficiency, and yield performance indices, has helped to identify the best resources for genetic studies in soybean. Genomic resources, including whole-genome sequences of diverse germplasms, millions of single-nucleotide polymorphisms, and high-throughput marker genotyping platforms, have expedited gene and marker discovery for translational genomics in soybean. This review highlights the current knowledge of the genetic diversity and quantitative trait loci associated with root system architecture, canopy wilting, nitrogen-fixation ability, and flooding tolerance that contributes to the understanding of drought– and flooding-tolerance mechanisms in soybean. Next-generation mapping approaches and high-throughput phenotyping will facilitate a better understanding of phenotype–genotype associations and help to formulate genomic-assisted breeding strategies, including genomic selection, in soybean for tolerance to drought and flooding stress.

• Phylogenomics is increasingly used to infer deep-branching relationships while revealing the complexity of evolutionary processes such as incomplete lineage sorting, hybridization/introgression and polyploidization. We investigate the deep-branching relationships among subfamilies of the Leguminosae (or Fabaceae), the third largest angiosperm family. Despite their ecological and economic importance, a robust phylogenetic framework for legumes based on genome-scale sequence data is lacking. • We generated alignments of 72 chloroplast genes and 7621 homologous nuclear-encoded proteins, for 157 and 76 taxa, respectively. We analysed these with maximum likelihood, Bayesian inference, and a multispecies coalescent summary method, and evaluated support for alternative topologies across gene trees. • We resolve the deepest divergences in the legume phylogeny despite lack of phylogenetic signal across all chloroplast genes and the majority of nuclear genes. Strongly supported conflict in the remainder of nuclear genes is suggestive of incomplete lineage sorting. • All six subfamilies originated nearly simultaneously, suggesting that the prevailing view of some subfamilies as ‘basal’ or ‘early-diverging’ with respect to others should be abandoned, which has important implications for understanding the evolution of legume diversity and traits. Our study highlights the limits of phylogenetic resolution in relation to rapid successive speciation.

Coevolutionary models suggest that herbivores drive diversification and community composition in plants. For herbivores, many questions remain regarding how plant defenses shape host choice and community structure. We addressed these questions using the tree genus Inga and its lepidopteran herbivores in the Amazon. We constructed phylogenies for both plants and insects and quantified host associations and plant defenses. We found that similarity in herbivore assemblages between Inga species was correlated with similarity in defenses. There was no correlation with phylogeny, a result consistent with our observations that the expression of defenses in Inga is independent of phylogeny. Furthermore, host defensive traits explained 40% of herbivore community similarity. Analyses at finer taxonomic scales showed that different lepidopteran clades select hosts based on different defenses, suggesting taxon-specific histories of herbivore–host plant interactions. Finally, we compared the phylogeny and defenses of Inga to phylogenies for the major lepidopteran clades. We found that closely related herbivores fed on Inga with similar defenses rather than on closely related plants. Together, these results suggest that plant defenses might be more evolutionarily labile than the herbivore traits related to host association. Hence, there is an apparent asymmetry in the evolutionary interactions between Inga and its herbivores. Although plants may evolve under selection by herbivores, we hypothesize that herbivores may not show coevolutionary adaptations, but instead “chase” hosts based on the herbivore’s own traits at the time that they encounter a new host, a pattern more consistent with resource tracking than with the arms race model of coevolution.

Mainly due to their economic importance, genomes of 10 legumes, including soybean (Glycine max), wild peanut (Arachis duranensis and Arachis ipaensis), and barrel medic (Medicago truncatula), have been sequenced. However, a family-level comparative genomics analysis has been unavailable. With grape (Vitis vinifera) and selected legume genomes as outgroups, we managed to perform a hierarchical and event-related alignment of these genomes and deconvoluted layers of homologous regions produced by ancestral polyploidizations or speciations. Consequently, we illustrated genomic fractionation characterized by widespread gene losses after the polyploidizations. Notably, high similarity in gene retention between recently duplicated chromosomes in soybean supported the likely autopolyploidy nature of its tetraploid ancestor. Moreover, although most gene losses were nearly random, largely but not fully described by geometric distribution, we showed that polyploidization contributed divergently to the copy number variation of important gene families. Besides, we showed significantly divergent evolutionary levels among legumes and, by performing synonymous nucleotide substitutions at synonymous sites correction, redated major evolutionary events during their expansion. This effort laid a solid foundation for further genomics exploration in the legume research community and beyond. We describe only a tiny fraction of legume comparative genomics analysis that we performed; more information was stored in the newly constructed Legume Comparative Genomics Research Platform (www.legumegrp.org).