Corrigendum: Plastid Genomes of Five Species of Riverweeds (Podostemaceae): Structural Organization and Comparative Analysis in Malpighiales.

[This corrects the article DOI: 10.3389/fpls.2019.01035.].

Global patterns and determinants of lake macrophyte taxonomic, functional and phylogenetic beta diversity.

Documenting the patterns of biological diversity on Earth has always been a central challenge in macroecology and biogeography. However, for the diverse group of freshwater plants, such research program is still in its infancy. Here, we examined global variation in taxonomic, functional and phylogenetic beta diversity patterns of lake macrophytes using regional data from six continents. A data set of ca. 480 lake macrophyte community observations, together with climatic, geographical and environmental variables, was compiled across 16 regions worldwide. We (a) built the very first phylogeny comprising most freshwater plant lineages; (b) exploited a wide array of functional traits that are important to macrophyte autoecology or that relate to lake ecosystem functioning; (c) assessed if different large-scale beta diversity patterns show a clear latitudinal gradient from the equator to the poles using null models; and (d) employed evolutionary and regression models to first identify the degree to which the studied functional traits show a phylogenetic signal, and then to estimate community-environment relationships at multiple spatial scales. Our results supported the notion that ecological niches evolved independently of phylogeny in macrophyte lineages worldwide. We also showed that taxonomic and phylogenetic beta diversity followed the typical global trend with higher diversity in the tropics. In addition, we were able to confirm that species, multi-trait and lineage compositions were first and foremost structured by climatic conditions at relatively broad spatial scales. Perhaps more importantly, we showed that large-scale processes along latitudinal and elevational gradients have left a strong footprint in the current diversity patterns and community-environment relationships in lake macrophytes. Overall, our results stress the need for an integrative approach to macroecology, biogeography and conservation biology, combining multiple diversity facets at different spatial scales.

Plastid Genomes of Five Species of Riverweeds (Podostemaceae): Structural Organization and Comparative Analysis in Malpighiales.

With the advent of next-generation sequencing technologies, whole-plastome data can be obtained as a byproduct of low-coverage sequencing of the plant genomic DNA. This provides an opportunity to study plastid evolution across groups, as well as testing phylogenetic relationships among taxa. Within the order Malpighiales (∼16,000 spp.), the Podostemaceae (∼300 spp.) stand out for their unique habit, living attached to rocks in fast-flowing aquatic habitats, and displaying highly modified morphologies that confound our understanding of their classification, biology, and evolution. In this study, we used genome skimming data to assemble the full plastid genome of 5 species within Podostemaceae. We analyzed our data in a comparative framework within Malpighiales to determine the structure, gene content, and rearrangements in the plastomes of the family. The Podostemaceae have one of the smallest plastid genomes reported so far for the Malpighiales, possibly due to variation in length of inverted repeat (IR) regions, gene loss, and intergenic region variation. We also detected a major inversion in the large single-copy region unique to the family. The uncommon loss or pseudogenization of ycf1 and ycf2 in angiosperms and in land plants in general is also found to be characteristic of Podostemaceae, but the compensatory mechanisms and implications of this and of the pseudogenization of accD, rpl22, and clpP and loss of rps16 remain to be explained in this group. In addition, we estimated a phylogenetic tree among selected species in Malpighiales. Our findings indicate that the Podostemaceae are a distinct lineage with long branches that suggest faster rates of evolution in the plastome of the group, compared with other taxa in the order. This study lays the foundations for future phylogenomic studies in the family.

Global patterns in the metacommunity structuring of lake macrophytes: regional variations and driving factors.

We studied community-environment relationships of lake macrophytes at two metacommunity scales using data from 16 regions across the world. More specifically, we examined (a) whether the lake macrophyte communities respond similar to key local environmental factors, major climate variables and lake spatial locations in each of the regions (i.e., within-region approach) and (b) how well can explained variability in the community-environment relationships across multiple lake macrophyte metacommunities be accounted for by elevation range, spatial extent, latitude, longitude, and age of the oldest lake within each metacommunity (i.e., across-region approach). In the within-region approach, we employed partial redundancy analyses together with variation partitioning to investigate the relative importance of local variables, climate variables, and spatial location on lake macrophytes among the study regions. In the across-region approach, we used adjusted R2 values of the variation partitioning to model the community-environment relationships across multiple metacommunities using linear regression and commonality analysis. We found that niche filtering related to local lake-level environmental conditions was the dominant force structuring macrophytes within metacommunities. However, our results also revealed that elevation range associated with climate (increasing temperature amplitude affecting macrophytes) and spatial location (likely due to dispersal limitation) was important for macrophytes based on the findings of the across-metacommunities analysis. These findings suggest that different determinants influence macrophyte metacommunities within different regions, thus showing context dependency. Moreover, our study emphasized that the use of a single metacommunity scale gives incomplete information on the environmental features explaining variation in macrophyte communities.

Silica bodies in leaves of neotropical Podostemaceae: taxonomic and phylogenetic perspectives.

Background and Aims: The presence, location and morphology of silica bodies are informative anatomical characters in angiosperms, mainly in Poales. In Podostemaceae, a strictly aquatic family, these structures are mentioned frequently, but there is limited insight into their location and morphological features. In the present study we focused on describing and analysing the morphological diversity of silica bodies in leaves of neotropical Podostemaceae at the intra- and interspecific levels to determine their taxonomic and phylogenetic relevance. Methods: We studied 103 specimens distributed across 40 species. Silica body morphological traits were analysed under light and scanning electron microscopy. Additionally, data from three species of Hypericaceae (sister group) were retrieved from the literature. A phylogenetic framework based on four molecular markers was built in order to reconstruct ancestral character states related to silica bodies in neotropical Podostemaceae. Key Results: Silica bodies were detected in epidermal, subepidermal and perivascular cells, presenting different shapes and surface morphology. Presence and location were used for primary differentiation while surface morphology and lumen (presence and shape) were used for finer distinctions. Intraspecific comparisons among samples showed that the length and width of these structures were highly variable. Maximum parsimony and maximum likelihood analyses for ancestral character reconstruction were congruent. Three out of five characters showed a statistically strong phylogenetic signal. Conclusions: Silica bodies were reported for the first time for 19 taxa, and their morphological diversity is greater than reported in previous studies. Their presence can be considered an apomorphy in Podostemaceae. Although some significant differences were detected in length and width, qualitative characters are more informative at both specific and generic ranks.

Dispersal largely explains the Gondwanan distribution of the ancient tropical clusioid plant clade.

PREMISE OF THE STUDY: The clusioid clade (Malpighiales) has an ancient fossil record (∼90 Ma) and extant representatives exhibit a pantropical distribution represented on all former Gondwanan landmasses (Africa, Australia, India, Madagascar, and South America) except Antarctica. Several biogeographers have hypothesized that the clusioid distribution is an example of Gondwanan vicariance. Our aim is to test the hypothesis that the modern distribution of the clusioid clade is largely explained by Gondwanan fragmentation. METHODS: Using a four gene, 207-taxon data set we simultaneously estimated the phylogeny and divergence times of the clusioid clade using a Bayesian Markov chain Monte Carlo approach. Ancestral Area Reconstructions (AARs) were then conducted on a distribution of 1000 trees and summarized on a reduced phylogeny. KEY RESULTS: Divergence time estimates and AARs revealed only two or four cladogenic events that are potentially consistent with Gondwanan vicariance, depending on the placement of the ancient fossil Paleoclusia. In contrast, dispersal occurred on > 25% of the branches, indicating the current distribution of the clade likely reflects extensive recent dispersal during the Cenozoic (< 65 Ma), most of which occurred after the beginning of the Eocene (∼56 Ma). CONCLUSIONS: These results support growing evidence that suggests many traditionally recognized angiosperm clades (families and genera) are too young for their distributions to have been influenced strictly by Gondwanan fragmentation. Instead, it appears that corridors of dispersal may be the best explanation for numerous angiosperm clades with Gondwanan distributions.

Phylogeny of the clusioid clade (Malpighiales): evidence from the plastid and mitochondrial 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 Griffithella (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.