Incorporating evolutionary and threat processes into crop wild relatives conservation.

Crop wild relatives (CWR) intra- and interspecific diversity is essential for crop breeding and food security. However, intraspecific genetic diversity, which is central given the idiosyncratic threats to species in landscapes, is usually not considered in planning frameworks. Here, we introduce an approach to develop proxies of genetic differentiation to identify conservation areas, applying systematic conservation planning tools that produce hierarchical prioritizations of the landscape. It accounts for: (i) evolutionary processes, including historical and environmental drivers of genetic diversity, and (ii) threat processes, considering taxa-specific tolerance to human-modified habitats, and their extinction risk status. Our analyses can be used as inputs for developing national action plans for the conservation and use of CWR. Our results also inform public policy to mitigate threat processes to CWR (like crops living modified organisms or agriculture subsidies), and could advise future research (e.g. for potential germplasm collecting). Although we focus on Mesoamerican CWR within Mexico, our methodology offers opportunities to effectively guide conservation and monitoring strategies to safeguard the evolutionary resilience of any taxa, including in regions of complex evolutionary histories and mosaic landscapes.

Patterns of chromosomal variation in Mexican species of Aeschynomene (Fabaceae, Papilionoideae) and their evolutionary and taxonomic implications.

A cytogenetic analysis of sixteen taxa of the genus Aeschynomene Linnaeus, 1753, which includes species belonging to both subgenera Aeschynomene (Léonard, 1954) and Ochopodium (Vogel, 1838) J. Léonard, 1954, was performed. All studied species had the same chromosome number (2n = 20) but exhibited karyotype diversity originating in different combinations of metacentric, submetacentric and subtelocentric chromosomes, chromosome size and number of SAT chromosomes. The plasticity of the genomes included the observation in a taxon belonging to the subgenus Aeschynomene of an isolated spherical structure similar in appearance to the extra chromosomal circular DNA observed in other plant genera. By superimposing the karyotypes in a recent phylogenetic tree, a correspondence between morphology, phylogeny and cytogenetic characteristics of the taxa included in the subgenus Aeschynomene is observed. Unlike subgenus Aeschynomene, the species of Ochopodium exhibit notable karyotype heterogeneity. However the limited cytogenetic information recorded prevents us from supporting the proposal of their taxonomic separation and raise it to the genus category. It is shown that karyotype information is useful in the taxonomic delimitation of Aeschynomene and that the diversity in the diploid level preceded the hybridization/polyploidization demonstrated in the genus. The systematic implications of our results and their value can be extended to other Dalbergieae genera as knowledge about the chromosomal structure and its evolution increases.

Domestication Genomics of the Open-Pollinated Scarlet Runner Bean (Phaseolus coccineus L.).

The runner bean is a legume species from Mesoamerica closely related to common bean (Phaseolus vulgaris). It is a perennial species, but it is usually cultivated in small-scale agriculture as an annual crop for its dry seeds and edible immature pods. Unlike the common bean, P. coccineus has received little attention from a genetic standpoint. In this work we aim to (1) provide information about the domestication history and domestication events of P. coccineus; (2) examine the distribution and level of genetic diversity in wild and cultivated Mexican populations of this species; and, (3) identify candidate loci to natural and artificial selection. For this, we generated genotyping by sequencing data (42,548 SNPs) from 242 individuals of P. coccineus and the domesticated forms of the closely related species P. vulgaris (20) and P. dumosus (35). Eight genetic clusters were detected, of which half corresponds to wild populations and the rest to domesticated plants. The cultivated populations conform a monophyletic clade, suggesting that only one domestication event occurred in Mexico, and that it took place around populations of the Trans-Mexican Volcanic Belt. No difference between wild and domesticated levels of genetic diversity was detected and effective population sizes are relatively high, supporting a weak genetic bottleneck during domestication. Most populations presented an excess of heterozygotes, probably due to inbreeding depression. One population of P. coccineus subsp. striatus had the greatest excess and seems to be genetically isolated despite being geographically close to other wild populations. Contrasting with previous studies, we did not find evidence of recent gene flow between wild and cultivated populations. Based on outlier detection methods, we identified 24 domestication-related SNPs, 13 related to cultivar diversification and eight under natural selection. Few of these SNPs fell within annotated loci, but the annotated domestication-related SNPs are highly expressed in flowers and pods. Our results contribute to the understanding of the domestication history of P. coccineus, and highlight how the genetic signatures of domestication can be substantially different between closely related species.

Genomic history of the origin and domestication of common bean unveils its closest sister species.

BACKGROUND: Modern civilization depends on only a few plant species for its nourishment. These crops were derived via several thousands of years of human selection that transformed wild ancestors into high-yielding domesticated descendants. Among cultivated plants, common bean (Phaseolus vulgaris L.) is the most important grain legume. Yet, our understanding of the origins and concurrent shaping of the genome of this crop plant is limited. RESULTS: We sequenced the genomes of 29 accessions representing 12 Phaseolus species. Single nucleotide polymorphism-based phylogenomic analyses, using both the nuclear and chloroplast genomes, allowed us to detect a speciation event, a finding further supported by metabolite profiling. In addition, we identified ~1200 protein coding genes (PCGs) and ~100 long non-coding RNAs with domestication-associated haplotypes. Finally, we describe asymmetric introgression events occurring among common bean subpopulations in Mesoamerica and across hemispheres. CONCLUSIONS: We uncover an unpredicted speciation event in the tropical Andes that gave rise to a sibling species, formerly considered the "wild ancestor" of P. vulgaris, which diverged before the split of the Mesoamerican and Andean P. vulgaris gene pools. Further, we identify haplotypes strongly associated with genes underlying the emergence of domestication traits. Our findings also reveal the capacity of a predominantly autogamous plant to outcross and fix loci from different populations, even from distant species, which led to the acquisition by domesticated beans of adaptive traits from wild relatives. The occurrence of such adaptive introgressions should be exploited to accelerate breeding programs in the near future.

A molecular phylogeny reveals the Cuban enigmatic genus Behaimia as a new piece in the Brongniartieae puzzle of papilionoid legumes.

The papilionoid legume tribe Brongniartieae comprises a collection of 15 genera with disparate morphologies that were previously positioned in at least four remotely related tribes. The Brongniartieae displays a wide geographical disjunction between Australia and the New World and previous phylogenetic studies had provided conflicting results about the relationships between the American and Australian genera. We carry out phylogenetic analyses of (1) a plastid matK dataset extensively sampled across legumes to solve the enigmatic relationship of the Cuban-endemic monospecific genus Behaimia; and (2) multilocus datasets with focus on all genera ever referred to Brongniartieae. These analyses resulted in a well-resolved and strongly-supported phylogenetic tree of the Brongniartieae. The monophyly of all American genera of Brongniartieae is strongly supported. The doubtful position of the Australian genus Plagiocarpus is resolved within a clade comprising all Australian genera. Behaimia has been traditionally classified in tribe Millettieae, but our new molecular data and re-assessment of morphological traits have resolved the genus within the early-branching papilionoid tribe Brongniartieae. Characters including the pinnately multifoliolate (vs. unifoliolate) leaves, a sessile (vs. stipitate) ovary, and an indehiscent or late dehiscent one-seeded pod distinguish Behaimia from its closer relatives, the South American genera Cyclolobium and Limadendron.

Plant diversity patterns in neotropical dry forests and their conservation implications.

Seasonally dry tropical forests are distributed across Latin America and the Caribbean and are highly threatened, with less than 10% of their original extent remaining in many countries. Using 835 inventories covering 4660 species of woody plants, we show marked floristic turnover among inventories and regions, which may be higher than in other neotropical biomes, such as savanna. Such high floristic turnover indicates that numerous conservation areas across many countries will be needed to protect the full diversity of tropical dry forests. Our results provide a scientific framework within which national decision-makers can contextualize the floristic significance of their dry forest at a regional and continental scale.

Symbiont shift towards Rhizobium nodulation in a group of phylogenetically related Phaseolus species.

Bean plants from the Phaseolus genus are widely consumed and represent a nitrogen source for human nutrition. They provide biological fertilization by establishing root nodule symbiosis with nitrogen-fixing bacteria. To establish a successful interaction, bean plants and their symbiotic bacteria need to synchronize a proper molecular crosstalk. Within the Phaseolus genus, P. vulgaris has been the prominent species to study nodulation with Rhizobium symbionts. However the Phaseolus genus comprises diverse species whose symbionts have not been analyzed. Here we identified and studied nodule bacteria from representative Phaseolus species not previously analyzed and from all the described wild species related to P. vulgaris. We found Bradyrhizobium in nodules from most species representing all Phaseolus clades except in five phylogenetically related species from the P. vulgaris clade. Therefore we propose that Bradyrhizobium nodulation is common in Phaseolus and that there was a symbiont preference shift to Rhizobium nodulation in few related species. This work sets the basis to further study the genetic basis of this symbiont substitution.

Vigna (Leguminosae) sensu lato: the names and identities of the American segregate genera.

PREMISE OF STUDY: The legume genus Vigna and close relatives have highly elaborated floral morphologies that involve the coiling, bending, and intricate connection of flower parts. Banners, levers, platforms, and pumps have evolved that attract pollinators and then manipulate their movement. Given this three-dimensional floral complexity, the taxonomy of Vigna and relatives has been confounded by the study of mostly two-dimensional museum specimens. A molecular phylogenetic analysis was undertaken in the effort to resolve long-standing taxonomic questions centered on floral morphology. METHODS: The phylogenetic analysis included cpDNA trnK and nuclear ribosomal ITS/5.8S (ITS) sequence variation. The American species were comprehensively sampled and outgroups included Old World relatives. KEY RESULTS: The trnK and ITS data analyses concurred in resolving six well-supported clades of American Vigna that are most closely related to other American genera: Dolichopsis, Macroptilium, Mysanthus, Oryxis, Oxyrhynchus, Phaseolus, Ramirezella, and Strophostyles. These 14 American clades ranked here as genera are resolved as sister to a clade comprising the mainly Old World species of Vigna. CONCLUSIONS: American Vigna clades were reassigned to the genera Ancistrotropis, Cochliasanthus, Condylostylis, Leptospron, Sigmoidotropis, and the newly described Helicotropis. Vigna sensu stricto in the Americas now includes relatively few and mostly pantropical species. Elaborate floral asymmetries are readily used to apomorphically diagnose nearly all of the American genera. The age estimates of the extant diversification of the American and its Old World sister clade are approximately coeval at ca. 6-7 million yr, which belies much greater floral variation in the Americas.

Neotropical mutualism between Acacia and Pseudomyrmex: phylogeny and divergence times.

The interaction between Acacia and Pseudomyrmex is a textbook example of mutualism between ants and plants, nevertheless aspects of its evolutionary biology have not been formally explored. In this paper we analyze primarily the phylogenies of both New World Acacia and of their associated species of ants, and the geographic origin of this mutualism. Until now, there has been no molecular analysis of this relationship in terms of its origin and age. We analyzed three chloroplast markers (matK, psaB-rps14, and trnL-trnF) on a total of 70 taxa of legumes from the subfamily Mimosoideae, and two nuclear regions (long-wavelength rhodopsine and wingless) on a total of 43 taxa of ants from subfamily Pseudomyrmecinae. The monophyly of subgenus Acacia and within the New World lineages that of the myrmecophilous Acacia group was established. In addition, our results supported the monophyly of the genus Pseudomyrmex and of the associated acacia-ants P. ferrugineus group. Using Bayesian methods and calibration data, the estimated divergence times for the groups involved in the mutualism are: 5.44+/-1.93 My for the myrmecophilous acacias and 4.58+/-0.82 My for their associated ant species, implying that their relationship originated in Mesoamerica between the late Miocene to the middle Pliocene, with eventual diversification of both groups in Mexico.

Cryptic speciation in the Caesalpinia hintonii complex (Leguminosae: Caesalpinioideae) in a seasonally dry Mexican forest.

BACKGROUND AND AIMS: [corrected] The Caesalpinia hintonii group comprises six species of endemic shrubs or trees, C. epifanioi, C. hintonii, C. laxa, C. macvaughii, C. melanadenia and C. oyamae, found in scattered patches of seasonally dry forest in the Río Balsas depression and the neighbouring Tehuacán-Cuicatlán valley, which are part of the Mexican morphotectonic province of Sierra Madre del Sur. An evaluation is made of phylogeographic patterns and genetic diversity with a phylogenetic analysis of the C. hintonii complex in order to study the dynamics of speciation in this endemic group of legumes. METHODS: A phylogeographic study based on four highly variable non-coding plastid regions (trnL intron, trnL-F intergenic spacer, trnH-psbA intergenic spacer, and accD-psaI intergenic spacer) was carried out for the Caesalpinia hintonii complex. Five of the six taxa of the C. hintonii complex were included. KEY RESULTS AND CONCLUSIONS: The plastid analyses involving multiple accessions of each taxon from throughout their ranges resolved C. epifanioi and C. hintonii as well-supported clusters, but C. oyamae has two unexpectedly divergent lineages. Two well-supported geographic clades: eastern (C. epifanioi, C. melanadenia and C. oyamae) and western (C. hintonii and C. macvaughii) were established. The analyses performed provide evidence of recent morphostatic radiation in C. oyamae resulting from isolation and local adaptation. This pattern of genetic differentiation without morphological divergence may be a model that fits many groups of tropical woody taxa inhabiting similarly dry forests subjected to shifting selection.