Plastid phylogenomics and green plant phylogeny: almost full circle but not quite there

A study in BMC Evolutionary Biology represents the most comprehensive effort to clarify the phylogeny of green plants using sequences from the plastid genome. This study highlights the strengths and limitations of plastome data for resolving the green plant phylogeny, and points toward an exciting future for plant phylogenetics, during which the vast and largely untapped territory of nuclear genomes will be explored

Phylogenomics and Coalescent Analyses Resolve Extant Seed Plant Relationships

The extant seed plants include more than 260,000 species that belong to five main lineages: angiosperms, conifers, cycads, Ginkgo, and gnetophytes. Despite tremendous effort using molecular data, phylogenetic relationships among these five lineages remain uncertain. Here, we provide the first broad coalescent-based species tree estimation of seed plants using genome-scale nuclear and plastid data By incorporating 305 nuclear genes and 47 plastid genes from 14 species, we identify that i) extant gymnosperms (i.e., conifers, cycads, Ginkgo, and gnetophytes) are monophyletic, ii) gnetophytes exhibit discordant placements within conifers between their nuclear and plastid genomes, and iii) cycads plus Ginkgo form a clade that is sister to all remaining extant gymnosperms. We additionally observe that the placement of Ginkgo inferred from coalescent analyses is congruent across different nucleotide rate partitions. In contrast, the standard concatenation method produces strongly supported, but incongruent placements of Ginkgo between slow- and fast-evolving sites. Specifically, fast-evolving sites yield relationships in conflict with coalescent analyses. We hypothesize that this incongruence may be related to the way in which concatenation methods treat sites with elevated nucleotide substitution rates. More empirical and simulation investigations are needed to understand this potential weakness of concatenation methods

The establishment of Central American migratory corridors and the biogeographic origins of seasonally dry tropical forests in Mexico

Biogeography and community ecology can mutually illuminate the formation of a regional species pool or biome. Here, we apply phylogenetic methods to a large and diverse plant clade, Malpighiaceae, to characterize the formation of its species pool in Mexico, and its occupancy of the seasonally dry tropical forest (SDTF) biome that occurs there. We find that the ~162 species of Mexican Malpighiaceae represent ~33 dispersals from South America beginning in the Eocene and continuing until the Pliocene (~46.4–3.8 Myr). Furthermore, dispersal rates between South America and Mexico show a significant six-fold increase during the mid-Miocene (~23.9 Myr). We hypothesize that this increase marked the availability of Central America as an important corridor for Neotropical plant migration. We additionally demonstrate that this high rate of dispersal contributed substantially more to the phylogenetic diversity of Malpighiaceae in Mexico than in situ diversification. Finally, we show that most lineages arrived in Mexico pre-adapted with regard to one key SDTF trait, total annual precipitation. In contrast, these lineages adapted to a second key trait, precipitation seasonality, in situ as mountain building in the region gave rise to the abiotic parameters of extant SDTF. The timing of this in situ adaptation to seasonal precipitation suggests that SDTF likely originated its modern characteristics by the late Oligocene, but was geographically more restricted until its expansion in the mid-Miocene. These results highlight the complex interplay of dispersal, adaptation, and in situ diversification in the formation of tropical biomes. Our results additionally demonstrate that these processes are not static, and their relevance can change markedly over evolutionary time. This has important implications for understanding the origin of SDTF in Mexico, but also for understanding the temporal and spatial origin of biomes and regional species pools more broadly

Estimating phylogenetic trees from genome-scale data

As researchers collect increasingly large molecular data sets to reconstruct the Tree of Life, the heterogeneity of signals in the genomes of diverse organisms poses challenges for traditional phylogenetic analysis. A class of phylogenetic methods known as "species tree methods" have been proposed to directly address one important source of gene tree heterogeneity, namely the incomplete lineage sorting or deep coalescence that occurs when evolving lineages radiate rapidly, resulting in a diversity of gene trees from a single underlying species tree. Although such methods are gaining in popularity, they are being adopted with caution in some quarters, in part because of an increasing number of examples of strong phylogenetic conflict between concatenation or supermatrix methods and species tree methods. Here we review theory and empirical examples that help clarify these conflicts. Thinking of concatenation as a special case of the more general model provided by the multispecies coalescent can help explain a number of differences in the behavior of the two methods on phylogenomic data sets. Recent work suggests that species tree methods are more robust than concatenation approaches to some of the classic challenges of phylogenetic analysis, including rapidly evolving sites in DNA sequences, base compositional heterogeneity and long branch attraction. We show that approaches such as binning, designed to augment the signal in species tree analyses, can distort the distribution of gene trees and are inconsistent. Computationally efficient species tree methods that incorporate biological realism are a key to phylogenetic analysis of whole genome data.Comment: 39 pages, 3 figure

Massive Mitochondrial Gene Transfer in a Parasitic Flowering Plant Clade

Recent studies have suggested that plant genomes have undergone potentially rampant horizontal gene transfer (HGT), especially in the mitochondrial genome. Parasitic plants have provided the strongest evidence of HGT, which appears to be facilitated by the intimate physical association between the parasites and their hosts. A recent phylogenomic study demonstrated that in the holoparasite Rafflesia cantleyi (Rafflesiaceae), whose close relatives possess the world's largest flowers, about 2.1% of nuclear gene transcripts were likely acquired from its obligate host. Here, we used next-generation sequencing to obtain the 38 protein-coding and ribosomal RNA genes common to the mitochondrial genomes of angiosperms from R. cantleyi and five additional species, including two of its closest relatives and two host species. Strikingly, our phylogenetic analyses conservatively indicate that 24%–41% of these gene sequences show evidence of HGT in Rafflesiaceae, depending on the species. Most of these transgenic sequences possess intact reading frames and are actively transcribed, indicating that they are potentially functional. Additionally, some of these transgenes maintain synteny with their donor and recipient lineages, suggesting that native genes have likely been displaced via homologous recombination. Our study is the first to comprehensively assess the magnitude of HGT in plants involving a genome (i.e., mitochondria) and a species interaction (i.e., parasitism) where it has been hypothesized to be potentially rampant. Our results establish for the first time that, although the magnitude of HGT involving nuclear genes is appreciable in these parasitic plants, HGT involving mitochondrial genes is substantially higher. This may represent a more general pattern for other parasitic plant clades and perhaps more broadly for angiosperms.Organismic and Evolutionary Biolog

Estimating phylogenetic trees from genome-scale data

The heterogeneity of signals in the genomes of diverse organisms poses challenges for traditional phylogenetic analysis. Phylogenetic methods known as “species tree” methods have been proposed to directly address one important source of gene tree heterogeneity, namely the incomplete lineage sorting that occurs when evolving lineages radiate rapidly, resulting in a diversity of gene trees from a single underlying species tree. Here we review theory and empirical examples that help clarify conflicts between species tree and concatenation methods, and misconceptions in the literature about the performance of species tree methods. Considering concatenation as a special case of the multispecies coalescent model helps explain differences in the behavior of the two methods on phylogenomic data sets. Recent work suggests that species tree methods are more robust than concatenation approaches to some of the classic challenges of phylogenetic analysis, including rapidly evolving sites in DNA sequences and long-branch attraction. We show that approaches, such as binning, designed to augment the signal in species tree analyses can distort the distribution of gene trees and are inconsistent. Computationally efficient species tree methods incorporating biological realism are a key to phylogenetic analysis of whole-genome data.Organismic and Evolutionary Biolog

Horizontal transfer of expressed genes in a parasitic flowering plant

Background: Recent studies have shown that plant genomes have potentially undergone rampant horizontal gene transfer (HGT). In plant parasitic systems HGT appears to be facilitated by the intimate physical association between the parasite and its host. HGT in these systems has been invoked when a DNA sequence obtained from a parasite is placed phylogenetically very near to its host rather than with its closest relatives. Studies of HGT in parasitic plants have relied largely on the fortuitous discovery of gene phylogenies that indicate HGT, and no broad systematic search for HGT has been undertaken in parasitic systems where it is most expected to occur. Results: We analyzed the transcriptomes of the holoparasite Rafflesia cantleyi Solms-Laubach and its obligate host Tetrastigma rafflesiae Miq. using phylogenomic approaches. Our analyses show that several dozen actively transcribed genes, most of which appear to be encoded in the nuclear genome, are likely of host origin. We also find that hundreds of vertically inherited genes (VGT) in this parasitic plant exhibit codon usage properties that are more similar to its host than to its closest relatives. Conclusions: Our results establish for the first time a substantive number of HGTs in a plant host-parasite system. The elevated rate of unidirectional host-to- parasite gene transfer raises the possibility that HGTs may provide a fitness benefit to Rafflesia for maintaining these genes. Finally, a similar convergence in codon usage of VGTs has been shown in microbes with high HGT rates, which may help to explain the increase of HGTs in these parasitic plants.Organismic and Evolutionary Biolog

Diversity patterns and conservation gaps of Magnoliaceae species in China

Postponed access: the file will be available after 2023-12-27Magnoliaceae, a primitive group of angiosperms and distinguished ornamental plants with more than 100 species in China, is one of the most threatened plant family in the wild due to logging, habitat loss, over-collection and climate change. To provide a scientific guide of its conservation for policymakers, we explore the diversity patterns of 114 Magnoliaceae species in China using three diversity indices (species richness, weighted endemism, β-diversity) with a spatial resolution of 10 km by 10 km. Two methods, the top 5% richness algorithm and complementary algorithm, are used to identify diversity hotspots. Conservation gaps are recognized by overlapping the diversity hotspots with Chinese nature reserves. Our results indicate that Magnoliaceae species richness and weighted endemism are high in tropical to subtropical low montane forests in southern China, exceptionally high in southernmost Yunnan and boundary of Guizhou, Guangxi and Hunan. The β-diversity are scattered in southern China, suggesting a different species composition among grid cells. We identify 2524 grids as diversity hotspots for Magnoliaceae species in China, with 24 grids covered by three diversity indices (first-level diversity hotspots), 561 grids covered by two indices (second-level diversity hotspots) simultaneously and 1939 grids (76.8%) covered by only one index (third-level diversity hotspots). The first-level diversity hotspots include over 70% of the critically endangered Magnoliaceae species and are the priority areas for Magnoliaceae conservation. However, only 24% of the diversity hotspots fall in nature reserves and only ten grids are from the first-level diversity hotspots. Zhejiang, Guizhou and Fujian have less than 20% of diversity hotspots covered by nature reserves and need attention in future Magnoliaceae conservation. Using multiple diversity indices and algorithms, our study identifies diversity hotspots and conservation gaps and provides scientific basis for Magnoliaceae conservation in future.acceptedVersio

Phylogeny of the Clusioid Clade (Malpighiales): Evidence from the Plastid and Mitochonrial Genomes

• Premise of the study : The clusioid clade includes five families (i.e., Bonnetiaceae, Calophyllaceae, Clusiaceae s.s., Hypericaceae, and Podostemaceae) represented by 94 genera and ~1900 species. Species in this clade form a conspicuous element of tropical forests worldwide and are important in horticulture, timber production, and pharmacology. We conducted a taxon-rich multigene phylogenetic analysis of the clusioids to clarify phylogenetic relationships in this clade. • Methods : We analyzed plastid ( matK , ndhF , and rbcL ) and mitochondrial ( matR ) nucleotide sequence data using parsimony, maximum likelihood, and Bayesian inference. Our combined data set included 194 species representing all major clusioid subclades, plus numerous species spanning the taxonomic, morphological, and biogeographic breadth of the clusioid clade. • Key results : Our results indicate that Tovomita (Clusiaceae s.s.), Harungana and Hypericum (Hypericaceae), and Ledermanniella s.s. and Zeylanidium (Podostemaceae) are not monophyletic. In addition, we place four genera that have not been included in any previous molecular study: Ceratolacis , Diamantina , and Griffi thella (Podostemaceae), and Santomasia (Hypericaceae). Finally, our results indicate that Lianthus , Santomasia , Thornea , and Triadenum can be safely merged into Hypericum (Hypericaceae). • Conclusions : We present the first well-resolved, taxon-rich phylogeny of the clusioid clade. Taxon sampling and resolution within the clade are greatly improved compared to previous studies and provide a strong basis for improving the classification of the group. In addition, our phylogeny will form the foundation for our future work investigating the biogeography of tropical angiosperms that exhibit Gondwanan distributions. DOI:10.3732/ajb.100035