Barbara Crandall-Stotler

The deepest divergences in land plants inferred from phylogenomic evidence.

Phylogenetic relationships among the four major lineages of land plants (liverworts, mosses, hornworts, and vascular plants) remain vigorously contested; their resolution is essential to our understanding of the origin and early evolution of land plants. We analyzed three different complementary data sets: a multigene supermatrix, a genomic structural character matrix, and a chloroplast genome sequence matrix, using maximum likelihood, maximum parsimony, and compatibility methods. Analyses of all three data sets strongly supported liverworts as the sister to all other land plants, and analyses of the multigene and chloroplast genome matrices provided moderate to strong support for hornworts as the sister to vascular plants. These results highlight the important roles of liverworts and hornworts in two major events of plant evolution: the water-to-land transition and the change from a haploid gametophyte generation-dominant life cycle in bryophytes to a diploid sporophyte generation-dominant life cycle in vascular plants. This study also demonstrates the importance of using a multifaceted approach to resolve difficult nodes in the tree of life. In particular, it is shown here that densely sampled taxon trees built with multiple genes provide an indispensable test of taxon-sparse trees inferred from genome sequences.

PHYLOGENY AND CLASSIFICATION OF THE MARCHANTIOPHYTA

Input from molecular phylogenetics in the past five years has substantially altered concepts of systematic relationships among liverworts. While these studies have confirmed the monophyly of phylum Marchantiophyta, they have demonstrated that many previously recognised ranks within the hierarchy are unnatural and in need of modification. Changes in the ranks of suborder and above have been proposed by various workers, but modifications in the circumscription of genera and families are still required. A comprehensive, phylogenetic classification scheme that integrates morphological data with molecular hypotheses is presented. The scheme includes diagnoses and publication citations for all names above the rank of genus. All currently recognised genera are listed alphabetically in their respective families; subfamilies are not indicated. Major modifications and novel alignments of taxa are thoroughly discussed, with pertinent references provided. Jungermanniaceae is redefined and Solenostomataceae fam. nov. is formally described to accommodate some of the genera excluded from it.

Unraveling the evolutionary history of the liverworts (Marchantiophyta): multiple taxa, genomes and analyses

Abstract Nucleotide sequence data from three chloroplast genes (rbcL, rps4 and psbA), one nuclear gene (the ribosomal LSU) and one mitochondrial gene (nad5) were assembled for 173 species in 117 genera of liverworts, making this the largest molecular phylogeny of the group to date. Analyses of these data provide support for the monophyly of the liverworts, and for previously resolved backbone relationships within the Marchantiophyta. The earliest divergence involves the “simple thalloid” taxa of the Haplomitriaceae and Treubiaceae. A Blasiaceae/complex thalloid clade is resolved as sister to all remaining liverworts. The leafy liverworts do not resolve as monophyletic. The separation of the Aneuraceae/Metzgeriaceae from all other simple thalloids and their placement within the “leafy” clade as sister to the enigmatic leafy genus Pleurozia, as suggested in earlier molecular phylogenies, is also supported by this far larger data set.

World checklist of hornworts and liverworts

Abstract A working checklist of accepted taxa worldwide is vital in achieving the goal of developing an online flora of all known plants by 2020 as part of the Global Strategy for Plant Conservation. We here present the first-ever worldwide checklist for liverworts (Marchantiophyta) and hornworts (Anthocerotophyta) that includes 7486 species in 398 genera representing 92 families from the two phyla. The checklist has far reaching implications and applications, including providing a valuable tool for taxonomists and systematists, analyzing phytogeographic and diversity patterns, aiding in the assessment of floristic and taxonomic knowledge, and identifying geographical gaps in our understanding of the global liverwort and hornwort flora. The checklist is derived from a working data set centralizing nomenclature, taxonomy and geography on a global scale. Prior to this effort a lack of centralization has been a major impediment for the study and analysis of species richness, conservation and systematic research at both regional and global scales. The success of this checklist, initiated in 2008, has been underpinned by its community approach involving taxonomic specialists working towards a consensus on taxonomy, nomenclature and distribution.

Horizontal transfer of an adaptive chimeric photoreceptor from bryophytes to ferns

Significance Despite being one of the oldest groups of land plants, the majority of living ferns resulted from a relatively recent diversification following the rise of angiosperms. To exploit fully the new habitats created by angiosperm-dominated ecosystems, ferns had to evolve novel adaptive strategies to cope with the low-light conditions exerted by the angiosperm canopy. Neochrome, an unconventional photoreceptor that allows ferns to “see the light” better, was likely part of the solution. Surprisingly, we discovered that fern neochrome was derived from a bryophyte lineage via horizontal gene transfer (HGT). This finding not only provides the first evidence that a plant-to-plant HGT can have a profound evolutionary impact but also has implications for the evolution of photosensory systems in plants. Ferns are well known for their shade-dwelling habits. Their ability to thrive under low-light conditions has been linked to the evolution of a novel chimeric photoreceptor—neochrome—that fuses red-sensing phytochrome and blue-sensing phototropin modules into a single gene, thereby optimizing phototropic responses. Despite being implicated in facilitating the diversification of modern ferns, the origin of neochrome has remained a mystery. We present evidence for neochrome in hornworts (a bryophyte lineage) and demonstrate that ferns acquired neochrome from hornworts via horizontal gene transfer (HGT). Fern neochromes are nested within hornwort neochromes in our large-scale phylogenetic reconstructions of phototropin and phytochrome gene families. Divergence date estimates further support the HGT hypothesis, with fern and hornwort neochromes diverging 179 Mya, long after the split between the two plant lineages (at least 400 Mya). By analyzing the draft genome of the hornwort Anthoceros punctatus, we also discovered a previously unidentified phototropin gene that likely represents the ancestral lineage of the neochrome phototropin module. Thus, a neochrome originating in hornworts was transferred horizontally to ferns, where it may have played a significant role in the diversification of modern ferns.

Extant diversity of bryophytes emerged from successive post-Mesozoic diversification bursts

Unraveling the macroevolutionary history of bryophytes, which arose soon after the origin of land plants but exhibit substantially lower species richness than the more recently derived angiosperms, has been challenged by the scarce fossil record. Here we demonstrate that overall estimates of net species diversification are approximately half those reported in ferns and ∼30% those described for angiosperms. Nevertheless, statistical rate analyses on time-calibrated large-scale phylogenies reveal that mosses and liverworts underwent bursts of diversification since the mid-Mesozoic. The diversification rates further increase in specific lineages towards the Cenozoic to reach, in the most recently derived lineages, values that are comparable to those reported in angiosperms. This suggests that low diversification rates do not fully account for current patterns of bryophyte species richness, and we hypothesize that, as in gymnosperms, the low extant bryophyte species richness also results from massive extinctions.

A Revised Classification of the Anthocerotophyta and a Checklist of the Hornworts of North America, North of Mexico

Abstract A hornwort classification that recognizes 11 genera, comprising a hierarchy of two classes, three orders, and four families is proposed. The updated checklist of these bryophytes for North America has been expanded from 11 species in three genera to 17 species in five genera. Application of the genus name Anthoceros in the traditional sense is clarified.

Taxonomy and Classification

This chapter provides a description of all plant families and genera that include putative fully mycoheterotrophic species, excluding initial and partial mycoheterotrophs. The overview covers a total of 17 families, 101 genera, and ca. 880 species. For each family and genus (except for Orchidaceae) a short morphological description is provided followed by notes on taxonomy, distribution, evolution, and ecology. For most genera a line drawing of a representative species is provided. Included families are: Aneuraceae, Burmanniaceae, Corsiaceae, Ericaceae, Gentianaceae, Gleicheniaceae, Iridaceae, Lycopodiaceae, Ophioglossaceae, Orchidaceae, Petrosaviaceae, Podocarpaceae, Polygalaceae, Psilotaceae, Schizaeaceae, Thismiaceae, and Triuridaceae.

Divergence times and the evolution of morphological complexity in an early land plant lineage (Marchantiopsida) with a slow molecular rate

We present a complete generic-level phylogeny of the complex thalloid liverworts, a lineage that includes the model system Marchantia polymorpha. The complex thalloids are remarkable for their slow rate of molecular evolution and for being the only extant plant lineage to differentiate gas exchange tissues in the gametophyte generation. We estimated the divergence times and analyzed the evolutionary trends of morphological traits, including air chambers, rhizoids and specialized reproductive structures. A multilocus dataset was analyzed using maximum likelihood and Bayesian approaches. Relative rates were estimated using local clocks. Our phylogeny cements the early branching in complex thalloids. Marchantia is supported in one of the earliest divergent lineages. The rate of evolution in organellar loci is slower than for other liverwort lineages, except for two annual lineages. Most genera diverged in the Cretaceous. Marchantia polymorpha diversified in the Late Miocene, giving a minimum age estimate for the evolution of its sex chromosomes. The complex thalloid ancestor, excluding Blasiales, is reconstructed as a plant with a carpocephalum, with filament-less air chambers opening via compound pores, and without pegged rhizoids. Our comprehensive study of the group provides a temporal framework for the analysis of the evolution of critical traits essential for plants during land colonization.

Phylogenetic Relationships and Morphological Evolution in a Major Clade of Leafy Liverworts (Phylum Marchantiophyta, Order Jungermanniales): Suborder Jungermanniineae

Abstract— The suborder Jungermanniineae of the Jungermanniales is a major lineage of leafy liverworts, recognized in recent classifications to include 15 families. Gametophytes within the suborder are morphologically diverse, but commonly anisophyllous to distichous, usually with succubous, rarely transverse or incubuous, leaf insertions. Sporophytes are frequently, but not universally, enclosed by stemderived perigynia or coelocaules, often accompanied by perianth reduction or loss and some level of geocauly or marsupial development. We herein provide the first comprehensive molecular phylogeny of this geographically widespread suborder, using sequences generated from one nuclear (rpb2), two mitochondrial (nad1 and rps3), and seven plastid (atpB, psbA, psbT-H, rbcL, rps4, trnG and trnL) loci, sampled from 279 accessions representing 163 species in 57 genera. Ancestral states were reconstructed for 14 morphological characters generally considered taxonomically diagnostic for families in the suborder. Our phylogenetic analyses support the return of Leiomylia (=Mylia anomala) to the Myliaceae, removal of Myliaceae from the Jungermanniineae, and validation of the monogeneric suborder Myliineae subord. nov. to house it. Eighteen families are recognized within the Jungermanniineae, nine of which are monogeneric; namely, Endogemmataceae, Harpanthaceae, Gyrothyraceae, Arnelliaceae, Saccogynaceae, Geocalycaceae, Jackiellaceae, Notoscyphaceae stat. nov., and Trichotemnomaceae. The generic compositions of other families are modified as follows: Saccogynidium is transferred from Geocalycaceae to a newly named subfamily of Acrobolbaceae, Acrobolbaceae subf. Saccogynidioideae, and one other subfamily of the Acrobolbaceae is validated, Acrobolbaceae subf. Austrolophozioideae; Hygrobiella is included in Antheliaceae (previously in Cephaloziaceae or its own family); Jungermanniaceae is broadened to include Mesoptychiaceae and Delavayellaceae; Cryptocoleopsis and Nardia are transferred from Solenostomataceae to Gymnomitriaceae; Gottschelia, Herzogobryum, and Nothogymnomitrion are excluded from the Jungermanniineae; Solenostomataceae is recognized to include Solenostoma, Arctoscyphus, Cryptocolea, and Diplocolea. Additional nomenclatural changes include recognizing Horikawaella as a synonym of Solenostoma and Apomarsupella as a synonym of Gymnomitrion, establishing two new subgenera of Solenostoma, Solenostoma subg. Metasolenostoma and Solenostoma subg. Eucalyx, and transferring Jungermannia conchata to Cephalozia. Morphological character state reconstructions identify dioecious inflorescences, gametangia on leading stems, flagelliform or stoloniferous branches absent, dorsal leaf insertions not overlapping the stem midline, large underleaves, and lack of gemmae as ancestral within the Jungermanniineae. All morphological characters appear to be moderately to highly homoplasious within the suborder.