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Edwards, E. J.

Publications and source records attributed to Edwards, E. J..

11 recordsLinked to original sources

Phylogenomic analyses of the diverse desert-alpine plant lineage Cistantheae

Deserts and alpine habitats, though ecologically distinct, share similar environmental stressors such as drought and high radiation. Various plant lineages traverse both biomes, which is often associated with transitions in life history strategy, where annuality is more often associated with drier desert habitats and perenniality more common in higher elevations. One such lineage is Cistantheae (Montiaceae), a morphologically diverse herbaceous clade in western North and South America. We aimed to infer a robust phylogeny of the clade as a foundation for taxonomic and comparative work. We used double-digest RADSeq to generate reduced-representation genomic data from over 160 samples representing 48 putative species in Cistantheae. Maximum likelihood and coalescent-based phylogenetic methods were utilized to infer evolutionary relationships across the full clade and within major subclades. We tested for signatures of admixture and introgressive gene flow, and reconstructed ancestral life history and climate niche to identify patterns of correlated evolution. We inferred a well-resolved phylogeny of Cistantheae, providing strong support for relationships among subclades within Cistantheae. While many species relationships were clarified, we also found evidence of rampant gene flow and incomplete lineage sorting, particularly within the annual Cistanthe clade from the Atacama Desert. Life history is evolutionarily labile across the clade, and was strongly correlated with temperature/ precipitation-related bioclimatic variables: annuals tend to occur in hotter, drier environments, while perennials in cooler, wetter. Elevational range was also evolutionarily labile, with several species occupying broad elevational gradients. We present the first densely-sampled, phylogenomic analysis of Cistantheae, providing key insights into species relationships in the clade. Repeated transitions in life history and climate niche, alongside wide elevational ranges, suggest that many Cistantheae species may be preadapted to both arid and montane habitats. This phylogeny will underpin further comparative, taxonomic, and phylogenomic studies in this ecologically important lineage.

evolutionary biology↗

A high-quality genome of the mass-blooming desert plant Cistanthe longiscapa and its photosynthetic behavior related to drought and life history

O_LICrassulacean acid metabolism (CAM) photosynthesis has independently evolved many times in arid-adapted plant lineages. Cistanthe longiscapa (Montiaceae), a desert mass-blooming annual, can upregulate CAM facultatively upon stress such as drought. Few studies, however, consider life history stages when measuring CAM activity or its facultative onset. C_LIO_LITo test the effect of drought and flowering on photosynthetic activity, we assayed Cistanthe individuals in fully-watered and drought conditions, as well as fully-watered individuals at pre-flowering and flowering life stages. We assembled and annotated a chromosome-scale genome of C. longiscapa and compared it with the genome of Portulaca amilis and analyzed differential gene expression. C_LIO_LIResults show significantly upregulated CAM in drought conditions as compared to fully-watered conditions; furthermore, flowering individuals showed slightly higher CAM activity as compared to pre-flowering plants, even when fully-watered. Differential gene expression analyses provide preliminary support for the possible co-regulation of CAM expression and reproduction. C_LIO_LIWe emphasize the potentially missed significance of life history in the CAM literature, and consider how the CAM biochemical module could become co-opted into other plant behaviors and responses, such as the shift to reproduction or flowering in annuals. C_LI

plant biology↗

Transcriptome Analysis Reveals Long-Term Somatic Memory of Stress in The Woody Perennial Crop, Grapevine Vitis Vinifera cv. Cabernet Sauvignon

Plants can generate a molecular memory of stress resulting in primed plants that are more resilient to subsequent stresses occurring days to weeks after the priming event. Whether such a priming effect is maintained over longer periods, and after winter dormancy in perennial plants, is less studied. Here, we used whole transcriptome and methylome sequencing of grapevine plants over two growing seasons to characterize grapevines response to combined drought and heat stress in naive and primed plants. Our results showed changes in expression of genes associated with epigenetic modifications during stress and after stress removal, suggesting the establishment of epigenetic memory of stress. Primed plants had a small number of differentially expressed genes associated with stress response one year after the priming event even in the absence of second stress and presented a stronger transcriptional response than naive plants when re-exposed to stress. Methylome analysis revealed an increase in DNA methylation in primed vines under combined stress, and that methylation patterns were less variable among plants under stress than control plants. We did not observe any correlation between DNA methylation and gene transcription, suggesting that stress-induced expression changes were, at least partially, independent of DNA methylation, with posttranscriptional regulation and histone modifications more likely candidates in the establishment of epigenetic memory. Additionally, we characterized stress responsive genes based on their transcriptional profile and function and propose a new comprehensive and intuitive classification model for stress memory genes in perennials.

plant biology↗

Predicting photosynthetic pathway from anatomy using machine learning

- Plants with Crassulacean acid metabolism (CAM) have long been associated with a specialized anatomy, including succulence and thick photosynthetic tissues. Firm, quantitative boundaries between non-CAM and CAM plants have yet to be established - if they indeed exist. - Using novel computer vision software to measure anatomy, we combined new measurements with published data across flowering plants. We then used machine learning and phylogenetic comparative methods to investigate relationships between CAM and anatomy. - We found significant differences in photosynthetic tissue anatomy between plants with differing CAM phenotypes. Machine learning based classification was over 95% accurate in differentiating CAM from non-CAM anatomy, and had over 70% recall of distinct CAM phenotypes. Phylogenetic least squares regression and threshold analyses revealed that CAM evolution was significantly correlated with increased mesophyll cell size, thicker leaves, and decreased intercellular airspace. - Our findings suggest that machine learning may be used to aid the discovery of new CAM species and that the evolutionary trajectory from non-CAM to strong, obligate CAM requires continual anatomical specialization.

evolutionary biology↗

Insights into Long-term Acclimation Strategies of Grapevines in Response to Multi-decadal Cyclical Drought

The Australian wine industry is currently under pressure to sustain its profitability due to climate change. Therefore, there is a pressing need to explore grapevine genetic diversity and identify superior clones with improved drought resistance. We previously characterised more than 15,000 dry-farmed (for over 65 years) Cabernet Sauvignon clones in a vineyard and identified three drought-tolerant (DT) clones, which can maintain significantly higher intrinsic water use efficiency (WUEi) under limited soil moisture than drought-sensitive (DS) clones. To understand whether DT clones grown under multi-decadal cyclical drought can prime their vegetatively-propagated clonal progenies for future drought events, in this study, all DT and DS vegetative progenies were propagated with commercial clones in the glasshouse. Their physiological and molecular responses were investigated under well-watered and two recurrent drought (D1 and D2) conditions. We observed that concentration of a natural priming agent, {gamma}-amino butyric acid (GABA), were significantly higher in all DT progenies relative to other progenies under drought. Both commercial and DT progenies exhibited improved gas exchange, photosynthetic performance and WUEi under recurrent drought events relative to DS progenies. Our results suggest that DT progenies have adapted to be in a "primed state" to withstand future drought events.

physiology↗

Gene co-expression reveals the modularity and integration of C4 and CAM in Portulaca

C4 photosynthesis and Crassulacean acid metabolism (CAM) have been considered as largely independent adaptations in spite of sharing key biochemical modules. Portulaca is a geographically widespread clade of over 100 annual and perennial angiosperm species that primarily use C4, but facultatively exhibit CAM when drought stressed, a photosynthetic system known as C4+CAM. It has been hypothesized that C4+CAM is rare because of pleiotropic constraints, but these have not been deeply explored. We generated a chromosome-level genome assembly of P. amilis and sampled mRNA from P. amilis and P. oleracea during CAM induction. Gene co-expression network analyses identified C4 and CAM gene modules shared and unique to both Portulaca species. A conserved CAM module linked phosphoenolpyruvate carboxylase (PEPC) to starch turnover during the day-night transition and was enriched in circadian clock regulatory motifs in the P. amilis genome. Preservation of this co-expression module regardless of water status suggests that Portulaca constitutively operate a weak CAM cycle that is transcriptionally and post-transcriptionally upregulated during drought. C4 and CAM mostly used mutually exclusive genes for primary carbon fixation and it is likely that nocturnal CAM malate stores are shuttled into diurnal C4 decarboxylation pathways, but we find evidence that metabolite cycling may occur at low levels. C4 likely evolved in Portulaca through co-option of redundant genes and integration of the diurnal portion of CAM. Thus, the ancestral CAM system did not strongly constrain C4 evolution because photosynthetic gene networks are not co-regulated for both daytime and nighttime functions.

evolutionary biology↗

Modeling phylogenetic biome shifts on a planet with a past

The spatial distribution of biomes has changed considerably over deep time, so the geographical opportunity for an evolutionary lineage to shift into a new biome may depend on how the availability and connectivity of biomes has varied temporally. To better understand how lineages shift between biomes in space and time, we developed a phylogenetic biome shift model in which each lineage shifts between biomes and disperses between regions at rates that depend on the lineages biome affinity and location relative to the spatiotemporal distribution of biomes at any given time. To study the behavior of the biome shift model in an empirical setting, we developed a literature-based representation of paleobiome structure for three mesic forest biomes, six regions, and eight time strata, ranging from the Late Cretaceous (100 Ma) through the present. We then fitted the model to a time-calibrated phylogeny of 119 Viburnum species to compare how the results responded to various realistic or unrealistic assumptions about paleobiome structure. Ancestral biome estimates that account for paleobiome dynamics reconstructed a warm temperate (or tropical) origin of Viburnum, which is consistent with previous fossil-based estimates of ancestral biomes. Imposing unrealistic paleobiome distributions led to ancestral biome estimates that eliminated support for tropical origins, and instead inflated support for cold temperate ancestry throughout the warmer Paleocene and Eocene. The biome shift model we describe is applicable to the study of evolutionary systems beyond Viburnum, and the core mechanisms of our model are extensible to the design of richer phylogenetic models of historical biogeography and/or lineage diversification. We conclude that biome shift models that account for dynamic geographical opportunities are important for inferring ancestral biomes that are compatible with our understanding of Earth history.

evolutionary biology↗

Joint phylogenetic estimation of geographic movements and biome shifts during the global diversification of Viburnum

Phylogeny, fossils, biogeography, and biome occupancy provide evidence that reflects the singular evolutionary history of a clade. Despite the connections that bind them together, these lines of evidence are most often studied separately, by first inferring a fossil-dated molecular phylogeny, then mapping on ancestral ranges and biomes inferred from extant species. Here we jointly model the evolution of biogeographic ranges, biome affinities, and molecular sequences, incorporating fossils to estimate a dated phylogeny for all of the 163 extant species of the woody plant clade Viburnum (Adoxaceae) that we currently recognize. Our analyses indicate that while the major Viburnum lineages evolved in the Eocene, the majority of extant species originated since the Miocene. Viburnum radiated first in Asia, in warm, broad-leaved evergreen (lucidophyllous) forests. Within Asia we infer several early shifts into more tropical forests, and multiple shifts into forests that experience prolonged freezing. From Asia we infer two early movements into the New World. These two lineages probably first occupied warm temperate forests and adapted later to spreading cold climates. One of these lineages (Porphyrotinus) occupied cloud forests and moved south through the mountains of the Neotropics. Several other movements into North America took place more recently, facilitated by prior adaptations to freezing in the Old World. We also infer four disjunctions between Asia and Europe: the Tinus lineage is the oldest and probably occupied warm forests when it spread, while the other three were more recent and in cold-adapted lineages. These results variously contradict published accounts, especially the view that Viburnum radiated initially in cold forests and, accordingly, maintained vessel elements with scalariform perforations. We explored how the location and biome assignments of fossils affected our inference of ancestral areas and biome states. Our results are sensitive to, but not entirely dependent upon, the inclusion of fossil biome data. We argue that it will be critical to take advantage of all available lines of evidence to decipher events in the distant past, and the joint estimation approach developed here provides cautious hope even when fossil evidence is limited.

evolutionary biology↗

Diversification in evolutionary arenas -- assessment and synthesis

Understanding how and why rates of evolutionary diversification vary is a key issue in evolutionary biology, ecology, and biogeography, and the metaphorical concepts of adaptive radiation and evolutionary stasis describe two opposing aspects causing variation in diversification rates. Here we review the central concepts in the evolutionary diversification literature and synthesize these into a simple, general framework for studying rates of diversification and quantifying their underlying dynamics, which can be applied across clades and regions and across spatial and temporal scales. Our framework describes the diversification rate (d) as a function of the abiotic environment (a), the biotic environment (b) and clade-specific phenotypes or traits (c); thus d[~]a,b,c. We refer to the four components (a-d) and their interactions collectively as the Evolutionary Arena. We outline analytical approaches to this framework and present a case study on conifers, for which we parameterise the general model. We also discuss three conceptual examples: the Lupinus radiation in the Andes in the context of emerging ecological opportunity and fluctuating connectivity due to climatic oscillations; oceanic island radiations in the context of island formation and erosion; and biotically driven radiations of the Mediterranean orchid genus Ophrys. The results of the conifer case study are consistent with the long-standing scenario that low competition and high rates of niche evolution promote diversification. The conceptual examples illustrate how using the synthetic Evolutionary Arena framework helps to identify and structure future directions for research on evolutionary radiations. In this way, the Evolutionary Arena framework promotes a more general understanding of variation in evolutionary rates by making quantitative results comparable between case studies, thereby allowing new syntheses of evolutionary and ecological processes to emerge.

evolutionary biology↗

Targeted Enrichment of Large Gene Families for Phylogenetic Inference: Phylogeny and Molecular Evolution of Photosynthesis Genes in the Portullugo (Caryophyllales)

Hybrid enrichment is an increasingly popular approach for obtaining hundreds of loci for phylogenetic analysis across many taxa quickly and cheaply. The genes targeted for sequencing are typically single-copy loci, which facilitate a more straightforward sequence assembly and homology assignment process. However, single copy loci are relatively uncommon elements of most genomes, and as such may provide a biased evolutionary history. Furthermore, this approach limits the inclusion of most genes of functional interest, which often belong to multi-gene families. Here we demonstrate the feasibility of including large gene families in hybrid enrichment protocols for phylogeny reconstruction and subsequent analyses of molecular evolution, using a new set of bait sequences designed for the \"portullugo\" (Caryophyllales), a moderately sized lineage of flowering plants (~2200 species) that includes the cacti and harbors many evolutionary transitions to C4 and CAM photosynthesis. Including multi-gene families allowed us to simultaneously infer a robust phylogeny and construct a dense sampling of sequences for a major enzyme of C4 and CAM photosynthesis, which revealed the accumulation of adaptive amino acid substitutions associated with C4 and CAM origins in particular paralogs. Our final set of matrices for phylogenetic analyses included 75-218 loci across 74 taxa, with ~50% matrix completeness across datasets. Phylogenetic resolution was greatly improved across the tree, at both shallow and deep levels. Concatenation and coalescent-based approaches both resolve with strong support the sister lineage of the cacti: Anacampserotaceae + Portulacaceae, two lineages of mostly diminutive succulent herbs of warm, arid regions. In spite of this congruence, BUCKy concordance analyses demonstrated strong and conflicting signals across gene trees for the resolution of the sister group of the cacti. Our results add to the growing number of examples illustrating the complexity of phylogenetic signals in genomic-scale data.

evolutionary biology↗

Anchored Phylogenomics of Angiosperms I: Assessing the Robustness of Phylogenetic Estimates

An important goal of the angiosperm systematics community has been to develop a shared approach to molecular data collection, such that phylogenomic data sets from different focal clades can be combined for meta-studies across the entire group. Although significant progress has been made through efforts such as DNA barcoding, transcriptome sequencing, and whole-plastid sequencing, the community current lacks a cost efficient methodology for collecting nuclear phylogenomic data across all angiosperms. Here, we leverage genomic resources from 43 angiosperm species to develop enrichment probes useful for collecting ~500 loci from non-model taxa across the diversity of angiosperms. By taking an anchored phylogenomics approach, in which probes are designed to represent sequence diversity across the group, we are able to efficiently target loci with sufficient phylogenetic signal to resolve deep, intermediate, and shallow angiosperm relationships. After demonstrating the utility of this resource, we present a method that generates a heat map for each node on a phylogeny that reveals the sensitivity of support for the node across analysis conditions, as well as different locus, site, and taxon schemes. Focusing on the effect of locus and site sampling, we use this approach to statistically evaluate relative support for the alternative relationships among eudicots, monocots, and magnoliids. Although the results from supermatrix and coalescent analyses are largely consistent across the tree, we find support for this deep relationship to be more sensitive to the particular choice of sites and loci when a supermatrix approach as employed. Averaged across analysis approaches and data subsampling schemes, our data support a eudicot-monocot sister relationship, which is supported by a number of recent angiosperm studies.

evolutionary biology↗