Phylogenomics of the hyperdiverse daisy tribes: Anthemideae,Astereae, Calenduleae,Gnaphalieae, and Senecioneae

Asteraceae account for 10% of all flowering plant species, and 35%–40% of these are in five closely related tribes that total over 10 000 species. These tribes include Anthemideae, Astereae, Calenduleae, Gnaphalieae, and Senecioneae, which form one of two enormous clades within Subfamily Asteroideae. We took a phylogenomics approach to resolve evolutionary relationships among these five tribes. We sampled the nuclear and plastid genomes via HybSeq target enrichment and genome skimming, and recovered 74 plastid genes and nearly 1000 nuclear loci, known as Conserved Orthologous Sequences. We tested for conflicting support in both data sets and used network analyses to assess patterns of reticulation to explain the early evolutionary history of this lineage, which has experienced whole‐genome duplications and rapid radiations. We found concordance and conflicting support in both data sets and documented four ancient hybridization events. Due to the timing of the early radiation of this five‐tribe lineage, shortly before the Eocene–Oligocene extinction event (34 MYA), early lineages were likely lost, obscuring some details of their early evolutionary history.     

Using phylogenomics to resolve mega-families: An example from Compositae

Next-generation sequencing and phylogenomics hold great promise for elucidating complex relationships among large plant families. Here, we performed targeted capture of low copy sequences followed by next-generation sequencing on the Illumina platform in the large and diverse angiosperm family Compositae (Asteraceae). The family is monophyletic, based on morphology and molecular data, yet many areas of the phylogeny have unresolved polytomies and interpreting phylogenetic patterns has been historically difficult. In order to outline a method and provide a framework and for future phylogenetic studies in the Compositae, we sequenced 23 taxa from across the family in which the relationships were well established as well as a member of the sister family Calyceraceae. We generated nuclear data from 795 loci and assembled chloroplast genomes from off-target capture reads enabling the comparison of nuclear and chloroplast genomes for phylogenetic analyses. We also analyzed multi-copy nuclear genes in our data set using a clustering method during orthology detection, and we applied a network approach to these clusters—analyzing all related locus copies. Using these data, we produced hypotheses of phylogenetic relationships employing both a conservative (restricted to only loci with one copy per targeted locus) and a multigene approach (including all copies per targeted locus). The methods and bioinformatics workflow presented here provide a solid foundation for future work aimed at understanding gene family evolution in the Compositae as well as providing a model for phylogenomic analyses in other plant mega-families.     

Species Richness and Host Specificity among Caterpillar Ensembles on Shrubs in the Andes of Southern Ecuador

Caterpillar ensembles were sampled on 16 species of shrubs from the family Asteraceae and the genus Piper (Piperaceae) in open and forest habitats in the Andean montane forest zone of southern Ecuador between August 2007 and May 2009. Trophic affiliations of caterpillars to the host plants were confirmed in feeding trials. Overall, species richness of herbivorous caterpillars was high (191 species across all plants), but varied strongly between ensembles associated with different plant species (2?C96 lepidopteran species per shrub species). Ensembles on Piper species were characterized by low effective species numbers and high dominance of one or two species of the Geometridae genus Eois Hübner. Low species number and high dominance were also found on latex-bearing Erato polymnioides, whereas ensembles on two other Asteraceae species were far more diverse and less strongly shaped by a few dominant species. The observed diversity patterns fit well to the concept that anti-herbivore defenses of plants are the major factors regulating associated insect ensembles. Local abundance and geographic range of host plants appear to have less influence. Lepidopteran species feeding on Asteraceae were found to be more generalistic than those feeding on Piper species. We conclude that caterpillar ensembles on most, but not all, studied plant species are defined by a small number of dominant species, which usually are narrow host specialists. This pattern was more distinct on Piper shrubs in forest understory, whereas Asteraceae in disturbed habitats had more open caterpillar ensembles.     

Comparative analysis of codon usage patterns in chloroplast genomes of the Asteraceae family

Codon usage bias (CUB) is an important evolutionary feature in a genome and has been widely documented from prokaryotes to eukaryotes. However, the significance of CUB in the Asteraceae family has not been well understood, with no Asteraceae species having been analyzed for this characteristic. Here, we use bioinformatics approaches to comparatively analyze the general patterns and influencing factors of CUB in five Asteraceae chloroplast (cp) genomes. The results indicated that the five genomes had similar codon usage patterns, showing a strong bias towards a high representation of NNA and NNT codons. Neutrality analysis showed that these cp genomes had a narrow GC distribution and no significant correlation was observed between GC₁₂ and GC₃. Parity Rule 2 (PR2) plot analysis revealed that purines were used more frequently than pyrimidines. Effective number of codons (ENc)-plot analysis showed that most genes followed the parabolic line of trajectory, but several genes with low ENc values lying below the expected curve were also observed. Furthermore, correspondence analysis of relative synonymous codon usage (RSCU) yielded a first axis that explained only a partial amount of variation of codon usage. These findings suggested that both natural selection and mutational bias contributed to codon bias, while selection was the major force to shape the codon usage in these Asteraceae cp genomes. Our study, which is the first to investigate codon usage patterns in Asteraceae plastomes, will provide helpful information about codon distribution and variation in these species, and also shed light on the genetic and evolutionary mechanisms of codon biology within this family.     

The divergence and positive selection of the plant‐specific BURP‐containing protein family

BURP domain‐containing proteins belong to a plant‐specific protein family and have diverse roles in plant development and stress responses. However, our understanding about the genetic divergence patterns and evolutionary rates of these proteins remain inadequate. In this study, 15 plant genomes were explored to elucidate the genetic origins, divergence, and functions of these proteins. One hundred and twenty‐five BURP protein‐encoding genes were identified from four main plant lineages, including 13 higher plant species. The absence of BURP family genes in unicellular and multicellular algae suggests that this family (1) appeared when plants shifted from relatively stable aquatic environments to land, where conditions are more variable and stressful, and (2) is critical in the adaptation of plants to adverse environments. Promoter analysis revealed that several responsive elements to plant hormones and external environment stresses are concentrated in the promoter region of BURP protein‐encoding genes. This finding confirms that these genes influence plant stress responses. Several segmentally and tandem‐duplicated gene pairs were identified from eight plant species. Thus, in general, BURP domain‐containing genes have been subject to strong positive selection, even though these genes have conformed to different expansion models in different species. Our study also detected certain critical amino acid sites that may have contributed to functional divergence among groups or subgroups. Unexpectedly, all of the critical amino acid residues of functional divergence and positive selection were exclusively located in the C‐terminal region of the BURP domain. In conclusion, our results contribute novel insights into the genetic divergence patterns and evolutionary rates of BURP proteins.     

Phylogenomic analysis reveals dynamic evolutionary history of the Drosophila heterochromatin protein 1 (HP1) gene family

Heterochromatin is the gene-poor, satellite-rich eukaryotic genome compartment that supports many essential cellular processes. The functional diversity of proteins that bind and often epigenetically define heterochromatic DNA sequence reflects the diverse functions supported by this enigmatic genome compartment. Moreover, heterogeneous signatures of selection at chromosomal proteins often mirror the heterogeneity of evolutionary forces that act on heterochromatic DNA. To identify new such surrogates for dissecting heterochromatin function and evolution, we conducted a comprehensive phylogenomic analysis of the Heterochromatin Protein 1 gene family across 40 million years of Drosophila evolution. Our study expands this gene family from 5 genes to at least 26 genes, including several uncharacterized genes in Drosophila melanogaster. The 21 newly defined HP1s introduce unprecedented structural diversity, lineage-restriction, and germline-biased expression patterns into the HP1 family. We find little evidence of positive selection at these HP1 genes in both population genetic and molecular evolution analyses. Instead, we find that dynamic evolution occurs via prolific gene gains and losses. Despite this dynamic gene turnover, the number of HP1 genes is relatively constant across species. We propose that karyotype evolution drives at least some HP1 gene turnover. For example, the loss of the male germline-restricted HP1E in the obscura group coincides with one episode of dramatic karyotypic evolution, including the gain of a neo-Y in this lineage. This expanded compendium of ovary- and testis-restricted HP1 genes revealed by our study, together with correlated gain/loss dynamics and chromosome fission/fusion events, will guide functional analyses of novel roles supported by germline chromatin.     

利用低拷贝核基因重建菊科紫菀亚科族间系统发育关系

紫菀亚科(Asteroideae)是菊科最大的一个亚科, 包含的种数多于被子植物的绝大多数科。目前, 紫菀亚科族间的系统发育关系主要依赖于叶绿体基因信息, 但是叶绿体基因为单亲遗传, 并不能完整反映进化历史。鉴于杂交现象在菊科普遍存在, 故利用核基因可以反映更完整的紫菀亚科进化历史。该研究首次使用从转录组数据(20个新测+11个从NCBI数据库下载)中筛选出的47个直系同源低拷贝核基因来研究紫菀亚科的系统发育关系, 共选取了29个物种, 代表了紫菀亚科20个族中的13个族。用超矩阵分析方法和溯祖推测分析方法各获得了1个稳定的紫菀亚科系统树, 每个树上绝大多数分支都得到了高度支持, 且2个树之间没有明显的冲突。新的紫菀亚科族间系统发育关系揭示了千里光超族应并入紫菀超族, 春黄菊族可能是千里光族与紫菀族杂交起源的, 金鸡菊族很可能也是杂交起源的。该研究结果显示低拷贝核基因可以更好地解决科以下分类阶元的系统发育关系, 对菊科乃至被子植物其它科的系统发育研究具有重要的借鉴意义。     

Cabbage family affairs: the evolutionary history of Brassicaceae

Life without the mustard family (Brassicaceae) would be a world without many crop species and the model organism Arabidopsis (Arabidopsis thaliana) that has revolutionized our knowledge in almost every field of modern plant biology. Despite this importance, research breakthroughs in understanding family-wide evolutionary patterns and processes within this flowering plant family were not achieved until the past few years. In this review, we examine recent outcomes from diverse botanical disciplines (taxonomy, systematics, genomics, paleobotany and other fields) to synthesize for the first time a holistic view on the evolutionary history of the mustard family.     

Effects of an adaptive zone shift on morphological and ecological diversification in terapontid fishes

A fundamental goal of evolutionary ecology is understanding the processes responsible for contemporary patterns of morphological diversity and species richness. Transitions across the marine–freshwater interface are regarded as key triggers for adaptive radiation of many clades. Using the Australian terapontid fish family as a model system we employed phylogenetic analyses to compare the rates of ecological (dietary) and morphological evolution between marine and freshwater species of the family. Results suggested significantly higher rates of phenotypic evolution in key dietary and morphological characters in freshwater species compared to marine counterparts. Moreover, there was significant correlation between several of these dietary and morphological characters, suggesting an underlying ecomorphological aspect to these greater rates of phenotypic evolution in freshwater clades. Australia’s biogeographic history, which has precluded colonisation by many of the major ostariophysan fish families that make up much global freshwater fish diversity, appears to have provided the requisite ‘ecological opportunity’ to facilitate the radiation of invading marine-derived fish clades.     

Global pattern of plant utilization across different organisms: Does plant apparency or plant phylogeny matter?

The present study is the first to consider human and nonhuman consumers together to reveal several general patterns of plant utilization. We provide evidence that at a global scale, plant apparency and phylogenetic isolation can be important predictors of plant utilization and consumer diversity. Using the number of species or genera or the distribution area of each plant family as the island “area” and the minimum phylogenetic distance to common plant families as the island “distance”, we fitted presence–area relationships and presence–distance relationships with a binomial GLM (generalized linear model) with a logit link. The presence–absence of consumers among each plant family strongly depended on plant apparency (family size and distribution area); the diversity of consumers increased with plant apparency but decreased with phylogenetic isolation. When consumers extended their host breadth, unapparent plants became more likely to be used. Common uses occurred more often on common plants and their relatives, showing higher host phylogenetic clustering than uncommon uses. On the contrary, highly specialized uses might be related to the rarity of plant chemicals and were therefore very species‐specific. In summary, our results provide a global illustration of plant–consumer combinations and reveal several general patterns of plant utilization across humans, insects and microbes. First, plant apparency and plant phylogenetic isolation generally govern plant utilization value, with uncommon and isolated plants suffering fewer parasites. Second, extension of the breadth of utilized hosts helps explain the presence of consumers on unapparent plants. Finally, the phylogenetic clustering structure of host plants is different between common uses and uncommon uses. The strength of such consistent plant utilization patterns across a diverse set of usage types suggests that the persistence and accumulation of consumer diversity and use value for plant species are determined by similar ecological and evolutionary processes.     

Comparative analysis of NBS domain sequences of NBS-LRR disease resistance genes from sunflower, lettuce, and chicory

Plant resistance to many types of pathogens and pests can be achieved by the presence of disease resistance (R) genes. The nucleotide binding site-leucine rich repeat (NBS-LRR) class of R-genes is the most commonly isolated class of R-genes and makes up a super-family, which is often arranged in the genome as large multi-gene clusters. The NBS domain of these genes can be targeted by polymerase chain reaction (PCR) amplification using degenerate primers. Previous studies have used PCR derived NBS sequences to investigate both ancient R-gene evolution and recent evolution within specific plant families. However, comparative studies with the Asteraceae family have largely been ignored. In this study, we address recent evolution of NBS sequences within the Asteraceae and extend the comparison to the Arabidopsis thaliana genome. Using multiple sets of primers, NBS fragments were amplified from genomic DNA of three species from the family Asteraceae: Helianthus annuus (sunflower), Lactuca sativa (lettuce), and Cichorium intybus (chicory). Analysis suggests that Asteraceae species share distinct families of R-genes, composed of genes related to both coiled-coil (CC) and toll-interleukin-receptor homology (TIR) domain containing NBS-LRR R-genes. Between the most closely related species, (lettuce and chicory) a striking similarity of CC subfamily composition was identified, while sunflower showed less similarity in structure. These sequences were also compared to the A. thaliana genome. Asteraceae NBS gene subfamilies appear to be distinct from Arabidopsis gene clades. These data suggest that NBS families in the Asteraceae family are ancient, but also that gene duplication and gene loss events occur and change the composition of these gene subfamilies over time.     

PHYLOGENETIC IMPLICATIONS OF CHLOROPLAST DNA RESTRICTION SITE VARIATION IN THE MUTISIEAE (ASTERACEAE)

Phylogenetic relationships among 13 species in the tribe Mutisieae and a single species from each of three other tribes in the Asteraceae were assessed by chloroplast DNA restriction site mapping. Initially, 211 restriction site mutations were detected among 16 species using 10 restriction enzymes. Examination of 12 of these species using nine more enzymes revealed 179 additional restriction site mutations. Phylogenetic analyses of restriction site mutations were performed using both Dolio and Wagner parsimony, and the resulting monophyletic groups were statistically tested by the bootstrap method. The phylogenetic trees confirm an ancient evolutionary split in the Asteraceae that was previously suggested by the distribution of a chloroplast DNA inversion. The subtribe Barnadesiinae of the tribe Mutisieae is shown to be the ancestral group within the Asteraceae. The molecular phylogenies also confirm the paraphyly of the Mutisieae and provide statistical support for the monophyly of three of its four currently recognized subtribes (Barnadesiinae, Mutisiinae, and Nassauviinae). The fourth subtribe, Gochnatiinae, is shown to be paraphyletic. Within the subtribes, several closely related generic pairs are identified. Chloroplast DNA sequence divergence among genera of the Asteraceae ranges between 0.7 and 5.4%, which is relatively low in comparison to other angiosperm groups. This suggests that the Asteraceae is either a relatively young family or that its chloroplast DNA has evolved at a slower rate than in other families.     

Genome‐wide survey of nuclear protein‐coding markers for beetle phylogenetics and their application in resolving both deep and shallow‐level divergences

Beetles (Coleoptera) are the most diverse and species‐rich insect group, representing an impressive explosive radiation in the evolutionary history of insects, and their evolutionary relationships are often difficult to resolve. The amount of ‘traditional markers’ (e.g. mitochondrial genes and nuclear rDNAs) for beetle phylogenetics is small, and these markers often lack sufficient signals in resolving relationships for such a rapidly radiating lineage. Here, based on the available genome data of beetles and other related insect species, we performed a genome‐wide survey to search nuclear protein‐coding (NPC) genes suitable for research on beetle phylogenetics. As a result, we identified 1470 candidate loci, which provided a valuable data resource to the beetle evolutionary research community for NPC marker development. We randomly chose 180 candidate loci from the database to design primers and successfully developed 95 NPC markers which can be PCR amplified from standard genomic DNA extracts. These new nuclear markers are universally applicable across Coleoptera, with an average amplification success rate of 90%. To test the phylogenetic utility, we used them to investigate the backbone phylogeny of Coleoptera (18 families sampled) and the family Coccinellidae (39 species sampled). Both phylogenies are well resolved (average bootstrap support >95%), showing that our markers can be used to address phylogenetic questions of various evolutionary depth (from species level to family level). In general, the newly developed nuclear markers are much easier to use and more phylogenetically informative than the ‘traditional markers’, and show great potential to expedite resolution of many parts in the Beetle Tree of Life.     

Molecular evolution of the phytochrome gene family in sorghum: changing rates of synonymous and replacement evolution

The photoreceptor phytochromes, encoded by a small gene family, are responsible for controlling the expression of a number of light-responsive genes and photomorphogenic events, including agronomically important phenotypes such as flowering time and shade-avoidance behavior. The understanding and control of flowering time are particularly important goals in sorghum cultivar development for diverse environments, and naturally occurring variation in the phytochrome genes might prove useful in breeding programs. Also of interest is whether variation observed at the phytochrome loci in domesticated sorghum, or in particular races, is a result of human selection. Population genetic studies can reveal evidence of such selection in patterns of polymorphism and divergence. In this study we report a population genetic analysis of the PHY gene family in Sorghum bicolor (L.) Moench in a diverse panel including both cultivated and wild accessions. We show that the level of nucleotide variation in all gene family members is about half the average for this species, consistent with purifying selection acting on these loci. However, the rate of amino acid substitution is accelerated at PHYC compared to the other two loci. In comparisons to a closely related sorghum species, PHYC shows a pattern of intermediate frequency amino acid changes that differ from the patterns observed in comparisons across longer evolutionary distances. There is also a departure from expected patterns of polymorphism and divergence at synonymous sites in PHYC, although the data do not fit a simple model of directional or diversifying selection. Cultivated sorghum has a level of variation similar to that of wild relatives (ssp. verticilliflorum), but many polymorphisms are subspecies-specific, including several amino acid variants.