Sarah Mathews

The Origin and Evolution of Phototropins

Plant phototropism, the ability to bend toward or away from light, is predominantly controlled by blue-light photoreceptors, the phototropins. Although phototropins have been well-characterized in Arabidopsis thaliana, their evolutionary history is largely unknown. In this study, we complete an in-depth survey of phototropin homologs across land plants and algae using newly available transcriptomic and genomic data. We show that phototropins originated in an ancestor of Viridiplantae (land plants + green algae). Phototropins repeatedly underwent independent duplications in most major land-plant lineages (mosses, lycophytes, ferns, and seed plants), but remained single-copy genes in liverworts and hornworts—an evolutionary pattern shared with another family of photoreceptors, the phytochromes. Following each major duplication event, the phototropins differentiated in parallel, resulting in two specialized, yet partially overlapping, functional forms that primarily mediate either low- or high-light responses. Our detailed phylogeny enables us to not only uncover new phototropin lineages, but also link our understanding of phototropin function in Arabidopsis with what is known in Adiantum and Physcomitrella (the major model organisms outside of flowering plants). We propose that the convergent functional divergences of phototropin paralogs likely contributed to the success of plants through time in adapting to habitats with diverse and heterogeneous light conditions.

Optimal data partitioning, multispecies coalescent and Bayesian concordance analyses resolve early divergences of the grape family (Vitaceae)

Evolutionary rate heterogeneity and rapid radiations are common phenomena in organismal evolution and represent major challenges for reconstructing deep‐level phylogenies. Here we detected substantial conflicts in and among data sets as well as uncertainty concerning relationships among lineages of Vitaceae from individual gene trees, supernetworks and tree certainty values. Congruent deep‐level relationships of Vitaceae were retrieved by comprehensive comparisons of results from optimal partitioning analyses, multispecies coalescent approaches and the Bayesian concordance method. We found that partitioning schemes selected by PartitionFinder were preferred over those by gene or by codon position, and the unpartitioned model usually performed the worst. For a data set with conflicting signals, however, the unpartitioned model outperformed models that included more partitions, demonstrating some limitations to the effectiveness of concatenation for these data. For a transcriptome data set, fast coalescent methods (STAR and MP‐EST) and a Bayesian concordance approach yielded congruent topologies with trees from the concatenated analyses and previous studies. Our results highlight that well‐resolved gene trees are critical for the effectiveness of coalescent‐based methods. Future efforts to improve the accuracy of phylogenomic analyses should emphasize the development of new methods that can accommodate multiple biological processes and tolerate missing data while remaining computationally tractable.

Evolutionary history of the angiosperm flora of China

High species diversity may result from recent rapid speciation in a ‘cradle’ and/or the gradual accumulation and preservation of species over time in a ‘museum’. China harbours nearly 10% of angiosperm species worldwide and has long been considered as both a museum, owing to the presence of many species with hypothesized ancient origins, and a cradle, as many lineages have originated as recent topographic changes and climatic shifts—such as the formation of the Qinghai–Tibetan Plateau and the development of the monsoon—provided new habitats that promoted remarkable radiation. However, no detailed phylogenetic study has addressed when and how the major components of the Chinese angiosperm flora assembled to form the present-day vegetation. Here we investigate the spatio-temporal divergence patterns of the Chinese flora using a dated phylogeny of 92% of the angiosperm genera for the region, a nearly complete species-level tree comprising 26,978 species and detailed spatial distribution data. We found that 66% of the angiosperm genera in China did not originate until early in the Miocene epoch (23 million years ago (Mya)). The flora of eastern China bears a signature of older divergence (mean divergence times of 22.04–25.39 Mya), phylogenetic overdispersion (spatial co-occurrence of distant relatives) and higher phylogenetic diversity. In western China, the flora shows more recent divergence (mean divergence times of 15.29–18.86 Mya), pronounced phylogenetic clustering (co-occurrence of close relatives) and lower phylogenetic diversity. Analyses of species-level phylogenetic diversity using simulated branch lengths yielded results similar to genus-level patterns. Our analyses indicate that eastern China represents a floristic museum, and western China an evolutionary cradle, for herbaceous genera; eastern China has served as both a museum and a cradle for woody genera. These results identify areas of high species richness and phylogenetic diversity, and provide a foundation on which to build conservation efforts in China.

Variation in seed size is structured by dispersal syndrome and cone morphology in conifers and other nonflowering seed plants

Seed size varies tremendously in plants and its evolution is influenced by multiple ecological and biological factors that are difficult to disentangle. In this study, we focus on understanding the role of seed dispersal by animals in the evolution of seed size in conifers, the most diverse extant nonflowering seed plant group. Relationships among seed size, dispersal syndrome, climate and cone morphology were analyzed across conifers using quantitative models of character evolution and phylogenetic regression techniques. Dispersal syndrome is a more consistent predictor of seed size within major extant conifer clades than climate. Seeds are generally larger in animal-dispersed than wind-dispersed species, and particular cone morphologies are consistently associated with specific ranges in seed size. Seed size and cone morphology evolve in a correlated manner in many animal-dispersed conifers, following a trade-off that minimizes the total size of the dispersal unit. These relationships are also present in other nonflowering seed plant groups, and have been important in the evolution of seeds and cones at least over the Cenozoic and perhaps over much of the later Mesozoic.

The phycocyanobilin chromophore of streptophyte algal phytochromes is synthesized by HY2

Land plant phytochromes perceive red and far-red light to control growth and development, using the linear tetrapyrrole (bilin) chromophore phytochromobilin (PΦB). Phytochromes from streptophyte algae, sister species to land plants, instead use phycocyanobilin (PCB). PCB and PΦB are synthesized by different ferredoxin-dependent bilin reductases (FDBRs): PΦB is synthesized by HY2, whereas PCB is synthesized by PcyA. The pathway for PCB biosynthesis in streptophyte algae is unknown. We used phylogenetic analysis and heterologous reconstitution of bilin biosynthesis to investigate bilin biosynthesis in streptophyte algae. Phylogenetic results suggest that PcyA is present in chlorophytes and prasinophytes but absent in streptophytes. A system reconstituting bilin biosynthesis in Escherichia coli was modified to utilize HY2 from the streptophyte alga Klebsormidium flaccidum (KflaHY2). The resulting bilin was incorporated into model cyanobacterial photoreceptors and into phytochrome from the early-diverging streptophyte alga Mesostigma viride (MvirPHY1). All photoreceptors tested incorporate PCB rather than PΦB, indicating that KflaHY2 is sufficient for PCB synthesis without any other algal protein. MvirPHY1 exhibits a red-far-red photocycle similar to those seen in other streptophyte algal phytochromes. These results demonstrate that streptophyte algae use HY2 to synthesize PCB, consistent with the hypothesis that PΦB synthesis arose late in HY2 evolution.

An overview of extant conifer evolution from the perspective of the fossil record

PREMISE OF THE STUDY Conifers are an important living seed plant lineage with an extensive fossil record spanning more than 300 million years. The group therefore provides an excellent opportunity to explore congruence and conflict between dated molecular phylogenies and the fossil record. METHODS We surveyed the current state of knowledge in conifer phylogenetics to present a new time-calibrated molecular tree that samples ~90% of extant species diversity. We compared phylogenetic relationships and estimated divergence ages in this new phylogeny with the paleobotanical record, focusing on clades that are species-rich and well known from fossils. KEY RESULTS Molecular topologies and estimated divergence ages largely agree with the fossil record in Cupressaceae, conflict with it in Araucariaceae, and are ambiguous in Pinaceae and Podocarpaceae. Molecular phylogenies provide insights into some fundamental questions in conifer evolution, such as the origin of their seed cones, but using them to reconstruct the evolutionary history of specific traits can be challenging. CONCLUSIONS Molecular phylogenies are useful for answering deep questions in conifer evolution if they depend on understanding relationships among extant lineages. Because of extinction, however, molecular datasets poorly sample diversity from periods much earlier than the Late Cretaceous. This fundamentally limits their utility for understanding deep patterns of character evolution and resolving the overall pattern of conifer phylogeny.

Primers for Castilleja and their Utility Across Orobanchaceae: II. Single-Copy Nuclear Loci

Premise of the study: We developed primers targeting nuclear loci in Castilleja with the goal of reconstructing the evolutionary history of this challenging clade. These primers were tested across other major clades in Orobanchaceae to assess their broader utility. Methods and Results: We assembled low-coverage genomes for three taxa in Castilleja and developed primer combinations for the single-copy conserved ortholog set (COSII) and the pentatricopeptide repeat (PPR) gene family. These primer combinations were designed to take advantage of the Fluidigm microfluidic PCR platform and are well suited for high-throughput sequencing applications. Eighty-seven primers were designed for Castilleja, and 27 were found to have broader utility in Orobanchaceae. Conclusions: These results demonstrate the utility of these primers, not only across Castilleja, but for other lineages within Orobanchaceae as well. This expanded molecular toolkit will be an asset to future phylogenetic studies in Castilleja and throughout Orobanchaceae.

Primers for castilleja and their utility across orobanchaceae: I. Chloroplast primers

Premise of the study: Chloroplast primers were developed from genomic data for the taxonomically challenging genus Castilleja. We further tested the broader utility of these primers across Orobanchaceae, identifying a core set of chloroplast primers amplifying across the clade. Methods and Results: Using a combination of three low-coverage Castilleja genomes and sequence data from 12 Castilleja plastomes, 76 primer combinations were specifically designed and tested for Castilleja. The primers targeted the most variable portions of the plastome and were validated for their applicability across the clade. Of these, 38 primer combinations were subsequently evaluated in silico and then validated across other major clades in Orobanchaceae. Conclusions: These results demonstrate the utility of these primers, not only across Castilleja, but for other clades in Orobanchaceae— particularly hemiparasitic lineages—and will contribute to future phylogenetic studies of this important clade of parasitic plants.

Algae hold clues to eukaryotic origins of plant phytochromes

Plants use phytochrome photoreceptors to determine their proximity to other plants, to gauge the intensity of vegetational shade, and to determine whether they are near the surface of bare soil or buried under leaf litter. In each case, phytochromes are measuring the ratio of red (R) to far-red (FR) light in the environment, and plants are using the information to elicit critical developmental responses, such as delaying the germination of seeds under a leaf litter or growing taller and reproducing earlier when neighbors impinge on their access to light (1). In open environments, the R:FR ratio is near 1; under a dense canopy or under leaf litter, it may fall to as low as 0.2, due to absorption of most of the light available for photosynthesis (400–700 nm) by plant pigments. Similarly, in soils, short wavelengths are scattered in the first few millimeters, whereas longer wavelengths penetrate more deeply. The ability of phytochrome to measure the R:FR ratio arises from its photoreversibility. It interconverts between two forms, a red absorbing form (Pr) and a far-red absorbing form (Pfr), which occur in a dynamic equilibrium determined by the R:FR ratio in ambient light. Although phytochromes have diversified independently in mosses, ferns, and seed plants (2), the different members of the phytochrome family in these lineages and across plants have very similar absorption maxima, centered on 660 nm for Pr and 730 nm for Pfr. For plants in terrestrial environments, the importance of the R:FR ratio is universal, and the spectral properties of phytochromes appear to have changed little through the ∼500 million years of land plant evolution. The origins of phytochrome, however, have remained mysterious. In PNAS, Duanmu et al. (3) provide evidence that … [↵][1]1Email: sarah.mathews{at}csiro.au. [1]: #xref-corresp-1-1

Empirical evidence of fixed and homeostatic patterns of polyploid advantage in a keystone grass exposed to drought and heat stress

A long-standing hypothesis in evolutionary biology is that polyploid plants have a fitness advantage over diploids in climatically variable or extreme habitats. Here we provide the first empirical evidence that polyploid advantage in these environments is caused by two distinct processes: homeostatic maintenance of reproductive output under elevated abiotic stress, and fixed differences in seed development. In an outdoor climate manipulation experiment using coastal to inland Australian populations of the perennial grass Themeda triandra Forssk., we found that total output of viable seed in drought- and heat-stressed tetraploid plants was over four times higher than in diploids, despite being equal under more favourable growing conditions. Tetraploids also consistently produced heavier seeds with longer hygroscopic awns, traits which increase propagule fitness in extreme environments. These differences add to fitness benefits associated with broader-scale local adaptation of inland T. triandra populations to drought stress. Our study provides evidence that nucleotypic effects of genome size and increased reproductive flexibility can jointly underlie polyploid advantage in plants in stressful environments, and argue that ploidy can be an important criterion for selecting plant populations for use in genetic rescue, restoration and revegetation projects, including in habitats affected by climate change.