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Plant phylogenetics and molecular evolution
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Graduate Student Supervision
Doctoral Student Supervision (Jan 2008 - Nov 2020)
No abstract available.
No abstract available.
No abstract available.
Plastid genomes (plastomes) of fully mycoheterotrophic plants (which obtain nutrition from fungi and have lost photosynthesis) may exhibit accelerated substitution rates, gene losses and structural rearrangements compared to their more stable photosynthetic relatives. Distantly related lineages provide independent data points to study plastome degradation. I used Sanger sequencing to assess the utility of three nonphotosynthetic plastid genes in phylogenetic inference of seven monocot families that include mycoheterotrophic taxa. I also assembled full plastome genomes for multiple mycoheterotrophic monocots, a heterotrophic conifer (Parasitaxus, Podocarpaceae) and autotrophic relatives for comparative analysis. Phylogenomic inferences are robust to different likelihood approaches and often extensive gene loss, are generally congruent with the few-gene analyses, and are insensitive to long branches, in contrast to parsimony. Patterns of gene loss and retention are largely in agreement with hypothesized trajectories, starting with plastid NAD(P)H dehydrogenase, followed by the loss of other photosynthesis-related genes, and ending in gradual loss of transcriptional apparatus and other non-photosynthesis related genes. I observed retention (delayed loss?) of genes encoding subunits of plastid-encoded RNA polymerase (Parasitaxus and some species in Petrosavia, Petrosaviaceae), plastid ATP synthase (Petrosavia, perhaps Parasitaxus in modified form) and Rubisco (Petrosavia), consistent with secondary non-photosynthetic functions of the latter two complexes. Some group IIA introns appear to be retained despite the loss of the plastid intron maturase, matK. Retained open reading frames are generally under strong purifying selection in Sciaphila (Triuridaceae). Genome contraction is the major mode of genome rearrangement, with severe reduction seen in some lineages (e.g., Apteria in Burmanniaceae is reduced to ~16 kb). Some mycoheterotrophs are nearly or completely colinear with autotrophic lineages (Geosiris in Iridaceae, at ~123 kb). Others have multiple minor or major rearrangements, which may be unrelated to the presence or absence of an inverted repeat (IR). Four independent IR losses were observed (in Burmanniaceae, Corsiaceae, Petrosaviaceae and Triuridaceae), an extra IR copy evolved in Campylosiphon (Burmanniaceae), and an entire IR re-evolved in Parasitaxus. Shifts in IR boundaries were also found in all mycoheterotrophs. Within-taxon comparisons (e.g., in Corsiaceae and Petrosavia) also underline that idiosyncratic evolutionary changes may occur following each loss of photosynthesis.
In my thesis I aim to improve our phylogenetic and evolutionary knowledge of two ancient and distantly related groups of aquatic flowering plants, Hydatellaceae and Alismatales. While the phylogeny of monocots has received fairly intense scrutiny for two decades, some parts of its diversification have been less frequently investigated. One such lineage is the order Alismatales, which defines one of the deepest splits in monocot evolution. Many families of Alismatales are aquatic or semi-aquatic, and they have been implicated in historical discussions of monocot origins. I evaluate inter-familial relationships in the order, considering a suite of 17 plastid genes for 31 Alismatales taxa for all 13 recognized families. This study improves on our understanding of, and confidence in, higher-order Alismatales relationships. I also uncovered convergent gene loss of plastid-encoded subunits for the NADH dehydrogenase complex. I then expand monocot coverage outside Alismatales by including unpublished and newly sequenced data for otherorders. This large-scale sample facilitated a re-evaluation of monocot phylogeny and molecular dating, the latter using 25 fossil constraints. Previously included in the monocot order Poales, Hydatellaceae are a small family of ephemeral aquatics relatively recently found to be the sister group of water lilies (Cabombaceae and Nymphaeaceae). I present the first molecularphylogeny of the family and evaluate aspects of the family's morphological evolution. I show how sexual system shifts are associated with shifts in otherreproductive traits. I also infer a temporal scale for Hydatellaceae diversification using a two-step Bayesian approach. I use the resulting dated tree to address biogeographic patterns and aspects of niche evolution. I show that its "Gondwanan" distribution is the result of long-distance dispersal and not continental rifting, and demonstrate strong phylogenetic niche conservatism in the family. These studies expand our understanding of evolution in Hydatellaceae, and provide a substantial update to our understanding of Alismatales (and more generally monocot) phylogeny and divergence times.
The unifying theme of this thesis is adaxial-abaxial or dorsiventral patterning in leaves. The adaxial-abaxial axis sets the thickness of a leaf and without the appropriate juxtaposition of the adaxial and abaxial domains, radialized leaves develop. The underlying genetic mechanisms of the development of these polarity defects started to be elucidated only over the past 20 years in the model Arabidopsis, in particular. I investigated this patterning in a variety of non-model species. Firstly, I investigated the variability of dorsiventral polarity in plants with naturally occurring radialized leaves including Allium, Nepenthes, Krishna fig, Pelargonium, several Cactaceae species, and popREVOLUTA mutant of a poplar hybrid. Subsequent chapters aimed to incorporate morphology and anatomy with molecular genetics in order to elucidate the underlying basis of the phenotype of interest in species that have not been used as model systems for leaf development, including canola and poplar. A novel mutant (lamina epiphylla, lip) was identified in canola, which has adaxialized leaves and leaf-derived organs. Some of the HD-ZIPIII candidate genes were sequenced in canola, but I was unable to determine the location of the LIP mutation. The rest of this thesis focuses on the abaxial greening and unifacial petiole phenotypes seen in some species of poplar that have isobilateral leaves (others in the genus have bifacial leaves). YABBY, KANADI, and HD-ZIPIII genes are some of the major contributors to setting proper adaxial-abaxial polarity and I investigated the relationships of these genes by identifying the orthologs in Arabidopsis, poplar, and eucalyptus (a genus that shares the abaxial greening phenotype with poplar). Further, I studied the species relationships within the genus Populus in order to establish the ancestral state of leaf type. I determined that bifacial leaves are likely derived within the genus. Finally, two poplar species (black cottonwood with bifacial leaves and hybrid aspen with isobilateral leaves) were compared on the basis of morphology, anatomy, and molecular genetics in order to determine the underlying basis of the abaxial greening and unifacial petiole phenotypes in hybrid aspen. I identified a subset of genes that may be involved in determining these phenotypes, but further investigation is needed.
Substantial ambiguities still remain concerning the broad backbone of moss phylogeny. I surveyed 17 slowly evolving plastid genes from representative taxa to reconstruct phylogenetic relationships among the major lineages of mosses in the overall context of land-plant phylogeny. I first designed 78 bryophyte-specific primers and demonstrated that they permit straightforward amplification and sequencing of 14 core genes across a broad range of bryophytes (three of the 17 genes required more effort). In combination, these genes can generate sturdy and well-resolved phylogenetic inferences of higher-order moss phylogeny, with little evidence of conflict among different data partitions or analyses. Liverworts are strongly supported as the sister group of the remaining land plants, and hornworts as sister to vascular plants. Within mosses, besides confirming some previously published findings based on other markers, my results substantiallyimprove support for major branching patterns that were ambiguous before. The monogeneric classes Takakiopsida and Sphagnopsida likely represent the first and second split within moss phylogeny, respectively. However, this result is shown to be sensitive to the strategy used to estimate DNA substitution model parameter values and to different data partitioning methods. Regarding the placement of remaining nonperistomate lineages, the [[[Andreaeobryopsida, Andreaeopsida], Oedipodiopsida], peristomate mosses] arrangement receives moderate to strong support. Among peristomate mosses, relationships among Polytrichopsida, Tetraphidopsida andBryopsida remain unclear, as do the earliest splits within sublcass Bryidae. A Funariidae, [Timmiidae, [Dicranidae, Bryidae]]] arrangement is strongly supported, as are major relationships within subclasses Funariidae and Dicranidae. I also reconstructed the phylogeny of the nonperistomate moss family Andreaeaceae, with a focus on costate taxa, using two complementary sets of plastid markers and taxa. The major subgenera (Andreaea and Chasmocalyx) and sections of Andreaea (Andreaea and Nerviae) are rejected as monophyletic. Well-supported lineages include clades comprising: (1) Andreaea nivalis and A. rigida (northern hemisphere members of subgenus Chasmocalyx) and A. blyttii (section Nerviae); (2) most of the remainder of Nerviae; (3) a mixture of costate and ecostate species from Chasmocalyx, Nerviae,all sampled members of section Andreaea, and subgenus Acroschisma. Relationships among the major lineages, including the root of the family, are all well supported.
No abstract available.
Master's Student Supervision (2010 - 2018)
DNA barcoding is a tool for rapidly identifying species based on short, standardized sequences of DNA, for example in situations where this may be difficult using morphology alone. I assembled a core DNA barcode reference library for southern British Columbia, home to ~54% of the vascular plant species in Canada, using the core plastid barcode loci rbcL and matK, and assessed its utility for identifying species in this region. The library comprises 4,812 sequences obtained from field-collected and herbarium tissue samples, supplemented with sequences downloaded from BOLD and GenBank, with at least one sequence for 75.4% of the vascular plant species occurring below 50°N in British Columbia. Sequence recoverability was significantly higher for rbcL than for matK (93.5% and 80.2%, respectively), and only marginally lower for both markers when using herbarium specimens (90.5% for rbcL and 77.8% for matK), which demonstrates the future feasibility of using museum specimens for completing a southern BC barcode reference library. As a proxy for assessing marker effectiveness, I scored resolution at the level of species and genus using tests of monophyly for Neighbour Joining trees, and performed sequence similarity searches with BLASTn analyses, both for each locus separately and for a dual-locus marker system (rbcL+matK; scored as a cumulative percentage in the BLAST analyses). Ignoring species represented by singleton sequences, the highest overall level of discrimination (66.9% of species and 91.6% of genera) was achieved for BLASTn analysis of rbcL+matK together. This work represents a significant contribution to a nation-wide barcode database, and provides a preliminary platform for ecological and other applications requiring species identification, where traditional methods are not feasible.
Plastid-genome evolution following photosynthesis loss is characterized by substantial change, contrasting with strong conservation in most photosynthetic land plants. Common features of reduced plastid genomes across diverse heterotrophic lineages point to a predictable trajectory of genome degradation, but this has been only partly tested. Here I document the molecular evolution of plastid genomes belonging to several mycoheterotroph lineages in Ericaceae, Gentianaceae and Polygalaceae, which include several independent origins of mycoheterotrophy in eudicot angiosperms that span different time scales since photosynthesis loss. I used next-generation and Sanger sequencing techniques to assemble complete plastomes or gene sets for comparative analyses of gene content and genome structure, and phylogenomic inference. I also sequenced several partially mycoheterotrophic and fully autotrophic relatives. Patterns of gene loss in mycoheterotroph plastomes are generally consistent with a previously hypothesized trajectory of change, starting with the loss of plastid NAD(P)H dehydrogenase before full loss of photosynthesis, and ending (here) with substantial reduction in genes involved in the translation apparatus and other nonphotosynthetic functions. Several retentions (delayed losses) of subunit genes for plastid-encoded polymerase, plastid ATP synthase and Rubisco are also consistent with hypothesized secondary (nonphotosynthetic) functions for these complexes. Two within-genus comparisons (for Epirixanthes in Polygalaceae and Voyria in Gentianaceae) demonstrate substantially different levels of genome degradation, consistent with heterogeneity in rates of genome change after a given origin of full mycoheterotrophy. Mycoheterotrophs in two families (Ericaceae, Polygalaceae) have extensive genome rearrangement compared to most land plants, contrasting with near colinearity in mycoheterotrophic members of Gentianaceae (despite sometimes extensive genome reduction in the latter). However, these contrasting patterns are apparently not associated with transitions to mycoheterotrophy, as photosynthetic relatives in Ericaceae and Polygalaceae are also substantially rearranged—or with inverted repeat loss (evident in Epirixanthes pallida, Polygalaceae), as autotrophic Polygala retains its inverted repeats. Phylogenomic inferences of core eudicot phylogeny made using the retained genes are generally well supported and robust to a variety of phylogenetic approaches, and are also congruent with recent phylogenetic studies in each mycoheterotrophic family.
The order Alismatales is a mostly aquatic group of monocots that displays substantial morphological and life history diversity, including the seagrasses, the only land plants that have re-colonized marine environments. Past phylogenetic studies of the order have either considered a single gene with dense taxonomic sampling, or several genes with thinner sampling. Despite substantial progress based on these studies, multiple phylogenetic uncertainties still remain concerning higher-order phylogenetic relationships. To address these issues, I completed a near-genus level sampling of the core alismatid families and the phylogenetically isolated family Tofieldiaceae, adding these new data to published sequences of Araceae and other monocots, eudicots and ANITA-grade angiosperms. I recovered whole plastid genomes (plastid gene sets representing up to 83 genes per taxa) and analyzed them using maximum likelihood and parsimony approaches. I recovered a well supported phylogenetic backbone for most of the order, with all families supported as monophyletic, and with strong support for most inter- and intrafamilial relationships. A major exception is the relative arrangement of Araceae, core alismatids and Tofieldiaceae; although most analyses recovered Tofieldiaceae as the sister-group of the rest of the order, this result was not well supported. Different partitioning schemes used in the likelihood analyses had little effect on patterns of clade support across the order, and the parsimony and likelihood results were generally highly congruent. I also used the inferred phylogeny of Alismatales to study the loss of the mostly plastid-encoded NADH dehydrogenase enzyme complex in the order. This enzyme is hypothesized to be involved in mitigating photooxidative stress by inducing chlororespiration. The inclusion or exclusion of ndh pseudogenes had little impact on the main phylogenetic results. Previous work hypothesized three independent losses/pseudogenization events within the core alismatids, which I confirmed here. I also inferred an additional loss in Tofieldiaceae, the first example in unsubmerged species of Alismatales. The repeated loss of plastid NADH dehydrogenase may spur future research into the physiological bases of the loss.
- Plastid phylogenomics and molecular evolution of Alismatales (2016)
Cladistics, 32 (2), 160-178
- Transcriptome-derived evidence supports recent polyploidization and a major phylogeographic division in Trithuria submersa (Hydatellaceae, Nymphaeales) (2016)
The New phytologist, 210 (1), 310-23
- Ancient Gondwana break-up explains the distribution of the mycoheterotrophic family Corsiaceae (Liliales) (2015)
Journal of Biogeography, 42 (6), 1123-1136
- Does complete plastid genome sequencing improve species discrimination and phylogenetic resolution in Araucaria? (2015)
Molecular Ecology Resources, 15 (5), 1067-1078
- Monocot fossils suitable for molecular dating analyses (2015)
Botanical Journal of the Linnean Society, 178 (3), 346-374
- Phytochrome diversity in green plants and the origin of canonical plant phytochromes (2015)
Nature Communications, 6
- The evolutionary history of ferns inferred from 25 low-copy nuclear genes (2015)
American Journal of Botany, 102 (7), 1089-1107
- The Highly Reduced Plastome of Mycoheterotrophic Sciaphila (Triuridaceae) Is Colinear with Its Green Relatives and Is under Strong Purifying Selection (2015)
Genome Biology and Evolution, 7 (8), 2220-2236
- The origin and evolution of phototropins (2015)
Frontiers in Plant Science, 6
- Between Two Fern Genomes (2014)
- Data access for the 1,000 Plants (1KP) project (2014)
- Horizontal transfer of an adaptive chimeric photoreceptor from bryophytes to ferns (2014)
Proceedings of the National Academy of Sciences of the United States of America, 111 (18), 6672-6677
- Origin of a novel regulatory module by duplication and degeneration of an ancient plant transcription factor (2014)
Molecular Phylogenetics and Evolution, 81, 159-173
- Paralogous Radiations of PIN Proteins with Multiple Origins of Noncanonical PIN Structure (2014)
Molecular Biology and Evolution, 31 (8), 2042-2060
- Patterns of clade support across the major lineages of moss phylogeny (2014)
Cladistics, 30 (6), 590-606
- Phylotranscriptomic analysis of the origin and early diversification of land plants (2014)
Proceedings of the National Academy of Sciences of the United States of America, 111 (45), E4859-E4868
- Reconstructing the age and historical biogeography of the ancient flowering-plant family Hydatellaceae (Nymphaeales) (2014)
Bmc Evolutionary Biology, 14
- Understanding the spectacular failure of DNA barcoding in willows (Salix): Does this result from a trans-specific selective sweep? (2014)
Molecular Ecology, 23 (19), 4737-4756
- A well-supported phylogenetic framework for the monocot order Alismatales reveals multiple losses of the plastid NADH dehydrogenase complex and a strong long-branch effect (2013)
Early Events in Monocot Evolution, 83, 1-28
- Contrasting patterns of support among plastid genes and genomes for major clades of the monocotyledons (2013)
Early Events in Monocot Evolution, 83, 315-349
- Transcriptome-Mining for Single-Copy Nuclear Markers in Ferns (2013)
Plos One, 8 (10)
- Evaluating Methods for Isolating Total RNA and Predicting the Success of Sequencing Phylogenetically Diverse Plant Transcriptomes (2012)
Plos One, 7 (11)
- MOLECULAR PHYLOGENETICS OF HYDATELLACEAE (NYMPHAEALES): SEXUAL-SYSTEM HOMOPLASY AND A NEW SECTIONAL CLASSIFICATION (2012)
American Journal of Botany, 99 (4), 663-676
- BRYOPHYTE-SPECIFIC PRIMERS FOR RETRIEVING PLASTID GENES SUITABLE FOR PHYLOGENETIC INFERENCE (2011)
American Journal of Botany, 98 (5), E109-E113
- Choosing and Using a Plant DNA Barcode (2011)
Plos One, 6 (5)
- Discriminating plant species in a local temperate flora using the rbcL plus matK DNA barcode (2011)
Methods in Ecology and Evolution, 2 (4), 333-340
- INFERRING THE HIGHER-ORDER PHYLOGENY OF MOSSES (BRYOPHYTA) AND RELATIVES USING A LARGE, MULTIGENE PLASTID DATA SET (2011)
American Journal of Botany, 98 (5), 839-849
- Reconciling Gene and Genome Duplication Events: Using Multiple Nuclear Gene Families to Infer the Phylogeny of the Aquatic Plant Family Pontederiaceae (2011)
Molecular Biology and Evolution, 28 (11), 3009-3018
- Spatial patterns of plant diversity below-ground as revealed by DNA barcoding (2011)
Molecular Ecology, 20 (6), 1289-1302
- ASSEMBLING THE TREE OF THE MONOCOTYLEDONS: PLASTOME SEQUENCE PHYLOGENY AND EVOLUTION OF POALES (2010)
Annals of the Missouri Botanical Garden, 97 (4), 584-616
- Inference of phylogenetic relationships among the subfamilies of grasses (Poaceae: Poales) using meso-scale exemplar-based sampling of the plastid genome (2010)
Botany-Botanique, 88 (1), 65-84
- UTILITY OF A LARGE, MULTIGENE PLASTID DATA SET IN INFERRING HIGHER-ORDER RELATIONSHIPS IN FERNS AND RELATIVES (MONILOPHYTES) (2010)
American Journal of Botany, 97 (9), 1444-1456
- A DNA barcode for land plants (2009)
Proceedings of the National Academy of Sciences of the United States of America, 106 (31), 12794-12797
- Are plant species inherently harder to discriminate than animal species using DNA barcoding markers? (2009)
Molecular Ecology Resources, 9, 130-139
- DIFFERENT GYMNOSPERM OUTGROUPS HAVE (MOSTLY) CONGRUENT SIGNAL REGARDING THE ROOT OF FLOWERING PLANT PHYLOGENY (2009)
American Journal of Botany, 96 (1), 216-227
- INTRODUCTION TO THE DARWIN SPECIAL ISSUE: THE ABOMINABLE MYSTERY (2009)
American Journal of Botany, 96 (1), 3-4
- A phylogenetic study of evolutionary transitions in sexual systems in Australasian wurmbea (Colchicaceae) (2008)
International Journal of Plant Sciences, 169 (1), 141-156
- How well do we understand the overall backbone of cycad phylogeny? New insights from a large, multigene plastid data set (2008)
Molecular Phylogenetics and Evolution, 47 (3), 1232-1237
- Inference of higher-order conifer relationships from a multi-locus plastid data set (2008)
Botany-Botanique, 86 (7), 658-669
- Multiple Multilocus DNA Barcodes from the Plastid Genome Discriminate Plant Species Equally Well (2008)
Plos One, 3 (7)
- Phylogenetic relationships in the monocot order Commelinales, with a focus on Philydraceae (2008)
Botany-Botanique, 86 (7), 719-731
- Plant systematics at the species level - Introduction (2008)
Botany-Botanique, 86 (8), VII-VIII
- The state of plant systematics research - Introduction (2008)
Botany-Botanique, 86 (7), VII
- Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree (2007)
Nature, 446 (7133), 312-315
- Towards a phylogenetic nomenclature of Tracheophyta (2007)
Taxon, 56 (3), 822-846
- Molecular evidence for the systematic positions of two enigmatic mosses: Pterogonidium pulchellum (Sematophyllaceae, Musci) and Piloecium pseudorufescens (Myuriaceae, Musci) (2006)
Canadian Journal of Botany-Revue Canadienne De Botanique, 84 (3), 501-507
- Repeated evolution of net venation and fleshy fruits among monocots in shaded habitats confirms a priori predictions: evidence from an ndhF phylogeny (2005)
Proceedings of the Royal Society B-Biological Sciences, 272 (1571), 1481-1490
- Parallel loss of a slowly evolving intron from two closely related families in asparagales (2004)
Systematic Botany, 29 (2), 296-307
- Patterns of genetic variation in Phialocephala fortinii across a broad latitudinal transect in Canada (2004)
Mycological Research, 108, 955-964
- Phylogenetic reconstruction of the evolution of stylar polymorphisms in Narcissus (Amaryllidaceae) (2004)
American Journal of Botany, 91 (7), 1007-1021