Jinpeng Wang

The oyster genome reveals stress adaptation and complexity of shell formation

The Pacific oyster Crassostrea gigas belongs to one of the most species-rich but genomically poorly explored phyla, the Mollusca. Here we report the sequencing and assembly of the oyster genome using short reads and a fosmid-pooling strategy, along with transcriptomes of development and stress response and the proteome of the shell. The oyster genome is highly polymorphic and rich in repetitive sequences, with some transposable elements still actively shaping variation. Transcriptome studies reveal an extensive set of genes responding to environmental stress. The expansion of genes coding for heat shock protein 70 and inhibitors of apoptosis is probably central to the oyster’s adaptation to sessile life in the highly stressful intertidal zone. Our analyses also show that shell formation in molluscs is more complex than currently understood and involves extensive participation of cells and their exosomes. The oyster genome sequence fills a void in our understanding of the Lophotrochozoa.

Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres

Polyploidy often confers emergent properties, such as the higher fibre productivity and quality of tetraploid cottons than diploid cottons bred for the same environments. Here we show that an abrupt five- to sixfold ploidy increase approximately 60 million years (Myr) ago, and allopolyploidy reuniting divergent Gossypium genomes approximately 1–2 Myr ago, conferred about 30–36-fold duplication of ancestral angiosperm (flowering plant) genes in elite cottons (Gossypium hirsutum and Gossypium barbadense), genetic complexity equalled only by Brassica among sequenced angiosperms. Nascent fibre evolution, before allopolyploidy, is elucidated by comparison of spinnable-fibred Gossypium herbaceum A and non-spinnable Gossypium longicalyx F genomes to one another and the outgroup D genome of non-spinnable Gossypium raimondii. The sequence of a G. hirsutum AtDt (in which ‘t’ indicates tetraploid) cultivar reveals many non-reciprocal DNA exchanges between subgenomes that may have contributed to phenotypic innovation and/or other emergent properties such as ecological adaptation by polyploids. Most DNA-level novelty in G. hirsutum recombines alleles from the D-genome progenitor native to its New World habitat and the Old World A-genome progenitor in which spinnable fibre evolved. Coordinated expression changes in proximal groups of functionally distinct genes, including a nuclear mitochondrial DNA block, may account for clusters of cotton-fibre quantitative trait loci affecting diverse traits. Opportunities abound for dissecting emergent properties of other polyploids, particularly angiosperms, by comparison to diploid progenitors and outgroups.

The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes

Polyploidization has provided much genetic variation for plant adaptive evolution, but the mechanisms by which the molecular evolution of polyploid genomes establishes genetic architecture underlying species differentiation are unclear. Brassica is an ideal model to increase knowledge of polyploid evolution. Here we describe a draft genome sequence of Brassica oleracea, comparing it with that of its sister species B. rapa to reveal numerous chromosome rearrangements and asymmetrical gene loss in duplicated genomic blocks, asymmetrical amplification of transposable elements, differential gene co-retention for specific pathways and variation in gene expression, including alternative splicing, among a large number of paralogous and orthologous genes. Genes related to the production of anticancer phytochemicals and morphological variations illustrate consequences of genome duplication and gene divergence, imparting biochemical and morphological variation to B. oleracea. This study provides insights into Brassica genome evolution and will underpin research into the many important crops in this genus.

Genome Alignment Spanning Major Poaceae Lineages Reveals Heterogeneous Evolutionary Rates and Alters Inferred Dates for Key Evolutionary Events

Multiple comparisons among genomes can clarify their evolution, speciation, and functional innovations. To date, the genome sequences of eight grasses representing the most economically important Poaceae (grass) clades have been published, and their genomic-level comparison is an essential foundation for evolutionary, functional, and translational research. Using a formal and conservative approach, we aligned these genomes. Direct comparison of paralogous gene pairs all duplicated simultaneously reveal striking variation in evolutionary rates among whole genomes, with nucleotide substitution slowest in rice and up to 48% faster in other grasses, adding a new dimension to the value of rice as a grass model. We reconstructed ancestral genome contents for major evolutionary nodes, potentially contributing to understanding the divergence and speciation of grasses. Recent fossil evidence suggests revisions of the estimated dates of key evolutionary events, implying that the pan-grass polyploidization occurred ∼96 million years ago and could not be related to the Cretaceous-Tertiary mass extinction as previously inferred. Adjusted dating to reflect both updated fossil evidence and lineage-specific evolutionary rates suggested that maize subgenome divergence and maize-sorghum divergence were virtually simultaneous, a coincidence that would be explained if polyploidization directly contributed to speciation. This work lays a solid foundation for Poaceae translational genomics.

Hierarchically Aligning 10 Legume Genomes Establishes a Family-Level Genomics Platform

A hierarchical and event-related alignment laid a solid foundation for further genomics exploration in the legume research community and beyond. Mainly due to their economic importance, genomes of 10 legumes, including soybean (Glycine max), wild peanut (Arachis duranensis and Arachis ipaensis), and barrel medic (Medicago truncatula), have been sequenced. However, a family-level comparative genomics analysis has been unavailable. With grape (Vitis vinifera) and selected legume genomes as outgroups, we managed to perform a hierarchical and event-related alignment of these genomes and deconvoluted layers of homologous regions produced by ancestral polyploidizations or speciations. Consequently, we illustrated genomic fractionation characterized by widespread gene losses after the polyploidizations. Notably, high similarity in gene retention between recently duplicated chromosomes in soybean supported the likely autopolyploidy nature of its tetraploid ancestor. Moreover, although most gene losses were nearly random, largely but not fully described by geometric distribution, we showed that polyploidization contributed divergently to the copy number variation of important gene families. Besides, we showed significantly divergent evolutionary levels among legumes and, by performing synonymous nucleotide substitutions at synonymous sites correction, redated major evolutionary events during their expansion. This effort laid a solid foundation for further genomics exploration in the legume research community and beyond. We describe only a tiny fraction of legume comparative genomics analysis that we performed; more information was stored in the newly constructed Legume Comparative Genomics Research Platform (www.legumegrp.org).

Origination, Expansion, Evolutionary Trajectory, and Expression Bias of AP2/ERF Superfamily in Brassica napus

The AP2/ERF superfamily, one of the most important transcription factor families, plays crucial roles in response to biotic and abiotic stresses. So far, a comprehensive evolutionary inference of its origination and expansion has not been available. Here, we identified 515 AP2/ERF genes in B. napus, a neo-tetraploid forming ~7500 years ago, and found that 82.14% of them were duplicated in the tetraploidization. A prominent subgenome bias was revealed in gene expression, tissue-specific, and gene conversion. Moreover, a large-scale analysis across plants and alga suggested that this superfamily could have been originated from AP2 family, expanding to form other families (ERF, and RAV). This process was accompanied by duplicating and/or alternative deleting AP2 domain, intragenic domain sequence conversion, and/or by acquiring other domains, resulting in copy number variations, alternatively contributing to functional innovation. We found that significant positive selection occurred at certain critical nodes during the evolution of land plants, possibly responding to changing environment. In conclusion, the present research revealed origination, functional innovation, and evolutionary trajectory of the AP2/ERF superfamily, contributing to understanding their roles in plant stress tolerance.

Exon Skipping Event Prediction based on Histone Modifications

Alternative splicing is a tissue and developmental stage specific process and greatly increases the biodiversity of proteins. Besides the trans- and cis-factors on the genome level, the process of RNA splicing is also regulated by epigenetic factors. In the present work, we proposed a new method to predict exon skipping events by using the histone methylation and acetylation information. The maximum relevance minimum redundancy method followed by incremental feature selection was performed to select the optimal feature set. Based on the optimized features, our method obtained an overall accuracy of 68.5% in a 10-fold cross validation test for exon skipping event prediction. It is anticipated that our method may become a useful tool for alternative splicing events prediction and the selected optimal features will provide insights into the regulatory mechanisms of epigenetic factors in alternative splicing.

An Overlooked Paleotetraploidization in Cucurbitaceae

Abstract Cucurbitaceae plants are of considerable biological and economic importance, and genomes of cucumber, watermelon, and melon have been sequenced. However, a comparative genomics exploration of their genome structures and evolution has not been available. Here, we aimed at performing a hierarchical inference of genomic homology resulted from recursive paleopolyploidizations. Unexpectedly, we found that, shortly after a core-eudicot-common hexaploidy, a cucurbit-common tetraploidization (CCT) occurred, overlooked by previous reports. Moreover, we characterized gene loss (and retention) after these respective events, which were significantly unbalanced between inferred subgenomes, and between plants after their split. The inference of a dominant subgenome and a sensitive one suggested an allotetraploid nature of the CCT. Besides, we found divergent evolutionary rates among cucurbits, and after doing rate correction, we dated the CCT to be 90–102 Ma, likely common to all Cucurbitaceae plants, showing its important role in the establishment of the plant family.

Two Highly Similar Poplar Paleo-subgenomes Suggest an Autotetraploid Ancestor of Salicaceae Plants

As a model plant to study perennial trees in the Salicaceae family, the poplar (Populus trichocarpa) genome was sequenced, revealing recurrent paleo-polyploidizations during its evolution. A comparative and hierarchical alignment of its genome to a well-selected reference genome would help us better understand poplar’s genome structure and gene family evolution. Here, by adopting the relatively simpler grape (Vitis vinifera) genome as reference, and by inferring both intra- and inter-genomic gene collinearity, we produced a united alignment of these two genomes and hierarchically distinguished the layers of paralogous and orthologous genes, as related to recursive polyploidizations and speciation. We uncovered homologous blocks in the grape and poplar genomes and also between them. Moreover, we characterized the genes missing and found that poplar had two considerably similar subgenomes (≤0.05 difference in gene deletion) produced by the Salicaceae-common tetraploidization, suggesting its autotetraploid nature. Taken together, this work provides a timely and valuable dataset of orthologous and paralogous genes for further study of the genome structure and functional evolution of poplar and other Salicaceae plants.

Comparative Analysis of Gene Conversion Between Duplicated Regions in Brassica rapa and B. oleracea Genomes

Plant genomes contain many duplicated genes, some of which were produced by recursive polyploidizations. These duplicated genes may evolve interactively and even concertedly through homoeologous recombination. Here, we explored likely gene conversion in Brassica rapa and Brassica oleracea. By checking gene colinearity, we detected 4296 duplicated genes existing in both the species, which were produced by whole-genome triplication from their common ancestor. Incongruities of homologous gene tree topologies indicated that 8 % of these duplicated genes were converted by one another after the divergence of B. rapa and B. oleracea. These converted genes are more often from larger duplicated chromosomal blocks, indicating that illegitimate recombination is more likely to occur between larger homoeologous chromosomal regions. This research contributed to understanding genome stability and gene evolution after polyploidization.