Three amphioxus reference genomes reveal gene and chromosome evolution of chordates

The slow-evolving invertebrate amphioxus has an irreplaceable role in advancing our understanding into the vertebrate origin and innovations. Here we resolve the nearly complete chromosomal genomes of three amphioxus species, one of which best recapitulates the 17 chordate ancestor linkage groups. We reconstruct the fusions, retention or rearrangements between descendants of whole genome duplications (WGDs), which gave rise to the extant microchromosomes likely existed in the vertebrate ancestor. Similar to vertebrates, the amphioxus genome gradually establishes its 3D chromatin architecture at the onset of zygotic activation, and forms two topologically associated domains at the Hox gene cluster. We find that all three amphioxus species have ZW sex chromosomes with little sequence differentiation, and their putative sex-determining regions are nonhomologous to each other. Our results illuminate the unappreciated interspecific diversity and developmental dynamics of amphioxus genomes, and provide high-quality references for understanding the mechanisms of chordate functional genome evolution.

The Genome of the “Sea Vomit” Didemnum vexillum

Tunicates are the sister group of vertebrates and thus occupy a key position for investigations into vertebrate innovations as well as into the consequences of the vertebrate-specific genome duplications. Nevertheless, tunicate genomes have not been studied extensively in the past, and comparative studies of tunicate genomes have remained scarce. The carpet sea squirt Didemnum vexillum, commonly known as “sea vomit”, is a colonial tunicate considered an invasive species with substantial ecological and economical risk. We report the assembly of the D. vexillum genome using a hybrid approach that combines 28.5 Gb Illumina and 12.35 Gb of PacBio data. The new hybrid scaffolded assembly has a total size of 517.55 Mb that increases contig length about eightfold compared to previous, Illumina-only assembly. As a consequence of an unusually high genetic diversity of the colonies and the moderate length of the PacBio reads, presumably caused by the unusually acidic milieu of the tunic, the assembly is highly fragmented (L50 = 25,284, N50 = 6539). It is sufficient, however, for comprehensive annotations of both protein-coding genes and non-coding RNAs. Despite its shortcomings, the draft assembly of the “sea vomit” genome provides a valuable resource for comparative tunicate genomics and for the study of the specific properties of colonial ascidians.

Evolution of Lysine-Specific Demethylase 1 and REST Corepressor Gene Families and Their Molecular Interaction

Lysine-specific demethylase 1A (LSD1) binds to RCOR gene family of corepressors to erase transcriptionally active marks on histones. Functional diversity in these complexes depends on the type of RCOR included, which modulates the complex´s catalytic activity. We studied the duplicative history of RCOR and LSD gene families, and analyzed the evolution of their interaction. We found that RCOR genes are the product of the two rounds of whole-genome duplications that occurred early in vertebrate evolution. In contrast, the origin of the LSD genes traces back before to the divergence of animals and plants. Coimmunoprecipitation experiments using resurrected RCOR and LSD1 proteins of the jawed vertebrate ancestor, and the common hop, date the origin of LSD1-RCOR interaction to the ancestor of animals, fungi, and plants. Overall, we trace LSD1-RCOR complex evolution and propose that animal, fungi, and plant non-model species offer advantages in addressing questions about the molecular biology of this epigenetic complex.

Genome-wide identification and expression analysis of the bZIP transcription factors, and functional analysis in response to drought and cold stresses in pear (Pyrus breschneideri)

Background Transcription factors (TFs) are involved in many important biological processes, including cell stretching, histological differentiation, metabolic activity, seed storage, gene regulation, and response to abiotic and biotic stresses. Little is known about the functions, evolutionary history, and expression patterns of basic region-leucine zipper TF family genes in pear, despite the release of the genome of Chinese white pears (“Dangshansuli”). Results Overall, 92 bZIP genes were identified in the pear genome (Pyrus breschneideri). Of these, 83 were randomly distributed on all 17 chromosomes except chromosome 4, and the other 9 genes were located on loose scaffolding. The genes were divided into 14 subgroups. Whole-genome duplications, dispersed duplication, and purifying selection for whole-genome duplications are the main reasons for the expansion of the PbrbZIP gene family. The analysis of functional annotation enrichment indicated that most of the functions of PbrbZIP genes were enriched in Gene Ontology and Kyoto Encyclopedia of Genes and Genomes pathways involved in the abiotic stress response. Next, expression analysis and virus-induced gene silencing results indicated that PbrbZIP genes might play critical roles in response to drought and cold stresses, especially for the genes from subgroups A, C, G, I, and S. Conclusions Ninety-two PbrbZIP genes were identified from the pear genome and classified into 14 subgroups. PbrbZIP genes were mainly expanded from whole-genome duplications and dispersed duplications and retained by purifying selection. PbrbZIP genes were induced by cold and drought stresses and played important roles in drought and cold tolerance. These results provided useful information for further increasing the tolerance of pears to stresses and a foundation to study the cold and drought tolerance mechanism of PbrbZIP genes.

Fan-shaped Spectrums of Species and Paleopolyploidy for Foundation of Crossbreeding Evolution

Although Darwin‘s evolutionary mutation theory has been widely accepted, many endeavors tried to challenge it. With more and more observation of successful hybridization and hybrids, the sexual isolation between species has become vague. The mechanism of evolution has been expanded from the classical model of evolution to multiple routes of speciation. Furthermore, a fundamental crossbreeding theory has been raised and proved by two lines of evidences: paleopolyploidy and fan-shaped spectrum of species. Ancient genome duplications are widespread throughout eukaryotic lineages, particularly in plants. The genome polyploidization can break through the sexual incompatibility between diploid counterparts to hybridize and produce new species. By comparing characteristics, all species in every taxon, both in the extinct fossil and extant organisms, can be arranged into fan-shaped spectrum according to their similarity: left primitive type-middle advanced type-right primitive type. The species are primitive at the two ends and advanced at the middle. The primitive two species always resemble two types of more primitive species that can be confirmed as their ancestors respectively, and the middle species is half similar to the two ancestors respectively. These suggest that the species in the spectrum come from two different ancestors by crossbreeding and gene combination. As a sum, advanced species originated from crossbreeding of two primitive ancestors, by major method of polyploidization, and proved by results of fan-shaped spectrum of species. Then, sex is the cause, force and opportunity for evolution.

Origin and evolutionary landscape of Nr2f transcription factors across Metazoa

Background Nuclear Receptor Subfamily 2 Group F (Nr2f) orphan nuclear hormone transcription factors (TFs) are fundamental regulators of many developmental processes in invertebrates and vertebrates. Despite the importance of these TFs throughout metazoan development, previous work has not clearly outlined their evolutionary history. Results We integrated molecular phylogeny with comparisons of intron/exon structure, domain architecture, and syntenic conservation to define critical evolutionary events that distinguish the Nr2f gene family in Metazoa. Our data indicate that a single ancestral eumetazoan Nr2f gene predated six main Bilateria subfamilies, which include single Nr2f homologs, here referred to as Nr2f1/2/5/6, that are present in invertebrate protostomes and deuterostomes, Nr2f1/2 homologs in agnathans, and Nr2f1, Nr2f2, Nr2f5, and Nr2f6 orthologs that are found in gnathostomes. Four cnidarian Nr2f1/2/5/6 and three agnathan Nr2f1/2 members are each due to independent expansions, while the vertebrate Nr2f1/Nr2f2 and Nr2f5/Nr2f6 members each form paralogous groups that arose from the established series of whole-genome duplications (WGDs). Nr2f6 members are the most divergent Nr2f subfamily in gnathostomes. Interestingly, in contrast to the other gnathostome Nr2f subfamilies, Nr2f5 has been independently lost in numerous vertebrate lineages. Furthermore, our analysis shows there are differential expansions and losses of Nr2f genes in teleosts following their additional rounds of WGDs. Conclusion Overall, our analysis of Nr2f gene evolution helps to reveal the origins and previously unrecognized relationships of this ancient TF family, which may allow for greater insights into the conservation of Nr2f functions that shape Metazoan body plans.

Evolutionary history of the vertebrate Piwi gene family

PIWIs are regulatory proteins that belong to the Argonaute family. Piwis are primarily expressed in gonads and protect the germline against the mobilization and propagation of transposable elements (TEs) through transcriptional gene silencing. Vertebrate genomes encode up to four Piwi genes: Piwil1, Piwil2, Piwil3 and Piwil4, but their duplication history is unresolved. We leveraged phylogenetics, synteny and expression analyses to address this void. Our phylogenetic analysis suggests Piwil1 and Piwil2 were retained in all vertebrate members. Piwil4 was the result of Piwil1 duplication in the ancestor of gnathostomes, but was independently lost in ray-finned fishes and birds. Further, Piwil3 was derived from a tandem Piwil1 duplication in the common ancestor of marsupial and placental mammals, but was secondarily lost in Atlantogenata (Xenarthra and Afrotheria) and some rodents. The evolutionary rate of Piwil3 is considerably faster than any Piwi among all lineages, but an explanation is lacking. Our expression analyses suggest Piwi expression has mostly been constrained to gonads throughout vertebrate evolution. Vertebrate evolution is marked by two early rounds of whole genome duplication and many multigene families are linked to these events. However, our analyses suggest Piwi expansion was independent of whole genome duplications.

The Overlooked Hybrid: Geographic Distribution and Niche Differentiation Between Spartina Cytotypes (Poaceae) in Wadden Sea Salt Marshes

Whole genome duplications (WGDs) lead to polyploid specimens and are regarded as major drivers for speciation and diversification in plants. One prevalent problem when studying WGDs is that effects of polyploidization in ancient polyploids cannot be disentangled from the consequences of selective evolutionary forces. Cytotypic differences in distribution, phenotypic appearance and in response to surface elevation (determined by HOF-modeling) were identified in a relatively young taxa-group of a hexaploid F1-hybrid (Spartina× townsendii H. Groves & J. Groves, Poaceae) and its dodecaploid descendent (Spartina anglica C.E. Hubbard, Poaceae) using vegetation assessments (1029 plots; 1 × 1 m2) from the European Wadden Sea mainland salt marshes, including elevational and mean high tidal (MHT) data. While the F1-hybrid was mainly present in the eastern part of the Wadden Sea, its dodecaploid descendent occurred in the entire Wadden Sea area. The Spartina cytotypes differed in phenotypes (median of Spartina cover: hexaploid = 25% vs. dodecaploid = 12%) and in elevational niche-optimum (hexaploid = − 49.5 cm MHT vs. dodecaploid = 8.0 cm MHT). High ploidy levels correlated with establishment success in Spartina along geographic gradients but did not seem to increase the capacity to cope with abiotic severity downwards the elevational gradient in salt marshes.