Conversion between duplicated genes generated by polyploidization contributes to the divergence of poplar and willow.

BACKGROUND: Gene conversion has an important effect on duplicate genes produced by polyploidization. Poplar (Populus trichocarpa) and willow (Salix brachista) are leading models and excellent green plants in the Salicaceae. Although much attention has been paid to the evolution of duplicated genes in poplar and willow, the role of conversion between duplicates generated from polyploidization remains poorly understood. RESULTS: Here, through genomic synteny analyses, we identified duplicate genes generated by the Salicaceae common tetraploidization (SCT) in the poplar and willow genomes. We estimated that at least 0.58% and 0.25% of poplar and willow duplicates were affected by whole-gene conversion after the poplar-willow divergence, with more (5.73% and 2.66%) affected by partial-gene conversion. Moreover, we found that the converted duplicated genes were unevenly distributed on each chromosome in the two genomes, and the well-preserved homoeologous chromosome regions may facilitate the conversion of duplicates. Notably, we found that conversion maintained the similarity of duplicates, likely contributing to the conservation of certain sequences, but is essentially accelerated the rate of evolution and increased species divergence. In addition, we found that converted duplicates tended to have more similar expression patterns than nonconverted duplicates. We found that genes associated with multigene families were preferentially converted. We also found that the genes encoding conserved structural domains associated with specific traits exhibited a high frequency of conversion. CONCLUSIONS: Extensive conversion between duplicate genes generated from the SCT contributes to the diversification of the family Salicaceae and has had long-lasting effects on those genes with important biological functions.

Conversion between 100-million-year-old duplicated genes contributes to rice subspecies divergence.

BACKGROUND: Duplicated gene pairs produced by ancient polyploidy maintain high sequence similarity over a long period of time and may result from illegitimate recombination between homeologous chromosomes. The genomes of Asian cultivated rice Oryza sativa ssp. indica (XI) and Oryza sativa ssp. japonica (GJ) have recently been updated, providing new opportunities for investigating ongoing gene conversion events and their impact on genome evolution. RESULTS: Using comparative genomics and phylogenetic analyses, we evaluated gene conversion rates between duplicated genes produced by polyploidization 100 million years ago (mya) in GJ and XI. At least 5.19-5.77% of genes duplicated across the three rice genomes were affected by whole-gene conversion after the divergence of GJ and XI at ~ 0.4 mya, with more (7.77-9.53%) showing conversion of only portions of genes. Independently converted duplicates surviving in the genomes of different subspecies often use the same donor genes. The ongoing gene conversion frequency was higher near chromosome termini, with a single pair of homoeologous chromosomes, 11 and 12, in each rice genome being most affected. Notably, ongoing gene conversion has maintained similarity between very ancient duplicates, provided opportunities for further gene conversion, and accelerated rice divergence. Chromosome rearrangements after polyploidization are associated with ongoing gene conversion events, and they directly restrict recombination and inhibit duplicated gene conversion between homeologous regions. Furthermore, we found that the converted genes tended to have more similar expression patterns than nonconverted duplicates. Gene conversion affects biological functions associated with multiple genes, such as catalytic activity, implying opportunities for interaction among members of large gene families, such as NBS-LRR disease-resistance genes, contributing to the occurrence of the gene conversion. CONCLUSION: Duplicated genes in rice subspecies generated by grass polyploidization ~ 100 mya remain affected by gene conversion at high frequency, with important implications for the divergence of rice subspecies.

Sequential Paleotetraploidization shaped the carrot genome.

BACKGROUND: Carrot (Daucus carota subsp. carota L.) is an important root crop with an available high-quality genome. The carrot genome is thought to have undergone recursive paleo-polyploidization, but the extent, occurrences, and nature of these events are not clearly defined. RESULTS: Using a previously published comparative genomics pipeline, we reanalysed the carrot genome and characterized genomic fractionation, as well as gene loss and retention, after each of the two tetraploidization events and inferred a dominant and sensitive subgenome for each event. In particular, we found strong evidence of two sequential tetraploidization events, with one (Dc-α) approximately 46-52 million years ago (Mya) and the other (Dc-ß) approximately 77-87 Mya, both likely allotetraploidization in nature. The Dc-ß event was likely common to all Apiales plants, occurring around the divergence of Apiales-Bruniales and after the divergence of Apiales-Asterales, likely playing an important role in the derivation and divergence of Apiales species. Furthermore, we found that rounds of polyploidy events contributed to the expansion of gene families responsible for plastidial methylerythritol phosphate (MEP), the precursor of carotenoid accumulation, and shaped underlying regulatory pathways. The alignment of orthologous and paralogous genes related to different events of polyploidization and speciation constitutes a comparative genomics platform for studying Apiales, Asterales, and many other related species. CONCLUSIONS: Hierarchical inference of homology revealed two tetraploidization events that shaped the carrot genome, which likely contributed to the successful establishment of Apiales plants and the expansion of MEP, upstream of the carotenoid accumulation pathway.

Deciphering the high-quality genome sequence of coriander that causes controversial feelings.

Coriander (Coriandrum sativum L. 2n = 2x = 22), a plant from the Apiaceae family, also called cilantro or Chinese parsley, is a globally important crop used as vegetable, spice, fragrance and traditional medicine. Here, we report a high-quality assembly and analysis of its genome sequence, anchored to 11 chromosomes, with total length of 2118.68 Mb and N50 scaffold length of 160.99 Mb. We found that two whole-genome duplication events, respectively, dated to ~45-52 and ~54-61 million years ago, were shared by the Apiaceae family after their split from lettuce. Unbalanced gene loss and expression are observed between duplicated copies produced by these two events. Gene retention, expression, metabolomics and comparative genomic analyses of terpene synthase (TPS) gene family, involved in terpenoid biosynthesis pathway contributing to coriander's special flavour, revealed that tandem duplication contributed to coriander TPS gene family expansion, especially compared to their carrot counterparts. Notably, a TPS gene highly expressed in all 4 tissues and 3 development stages studied is likely a major-effect gene encoding linalool synthase and myrcene synthase. The present genome sequencing, transcriptome, metabolome and comparative genomic efforts provide valuable insights into the genome evolution and spice trait biology of Apiaceae and other related plants, and facilitated further research into important gene functions and crop improvement.

Paleopolyploidies and Genomic Fractionation in Major Eudicot Clades.

Eudicots account for ~75% of living angiosperms, containing important food and energy crops. Recently, high-quality genome sequences of several eudicots including Aquilegia coerulea and Nelumbo nucifera have become available, providing an opportunity to investigate the early evolutionary characteristics of eudicots. We performed genomic hierarchical and event-related alignments to infer homology within and between representative species of eudicots. The results provide strong evidence for multiple independent polyploidization events during the early diversification of eudicots, three of which are likely to be allopolyploids: The core eudicot-common hexaploidy (ECH), Nelumbo-specific tetraploidy (NST), and Ranunculales-common tetraploidy (RCT). Using different genomes as references, we constructed genomic alignment to list the orthologous and paralogous genes produced by polyploidization and speciation. This could provide a fundamental framework for studying other eudicot genomes and gene(s) evolution. Further, we revealed significantly divergent evolutionary rates among these species. By performing evolutionary rate correction, we dated RCT to be ~118-134 million years ago (Mya), after Ranunculales diverged with core eudicots at ~123-139 Mya. Moreover, we characterized genomic fractionation resulting from gene loss and retention after polyploidizations. Notably, we revealed a high degree of divergence between subgenomes. In particular, synonymous nucleotide substitutions at synonymous sites (Ks) and phylogenomic analyses implied that A. coerulea might provide the subgenome(s) for the gamma-hexaploid hybridization.

Genome structure and evolutionary history of frankincense producing Boswellia sacra.

Boswellia sacra Flueck (family Burseraceae) tree is wounded to produce frankincense. We report its de novo assembled genome (667.8 Mb) comprising 18,564 high-confidence protein-encoding genes. Comparing conserved single-copy genes across eudicots suggest >97% gene space assembly of B. sacra genome. Evolutionary history shows B. sacra gene-duplications derived from recent paralogous events and retained from ancient hexaploidy shared with other eudicots. The genome indicated a major expansion of Gypsy retroelements in last 2 million years. The B. sacra genetic diversity showed four clades intermixed with a primary genotype-dominating most resin-productive trees. Further, the stem transcriptome revealed that wounding concurrently activates phytohormones signaling, cell wall fortification, and resin terpenoid biosynthesis pathways leading to the synthesis of boswellic acid-a key chemotaxonomic marker of Boswellia. The sequence datasets reported here will serve as a foundation to investigate the genetic determinants of frankincense and other resin-producing species in Burseraceae.

Illegitimate Recombination between Duplicated Genes Generated from Recursive Polyploidizations Accelerated the Divergence of the Genus Arachis.

The peanut (Arachis hypogaea L.) is the leading oil and food crop among the legume family. Extensive duplicate gene pairs generated from recursive polyploidizations with high sequence similarity could result from gene conversion, caused by illegitimate DNA recombination. Here, through synteny-based comparisons of two diploid and three tetraploid peanut genomes, we identified the duplicated genes generated from legume common tetraploidy (LCT) and peanut recent allo-tetraploidy (PRT) within genomes. In each peanut genome (or subgenomes), we inferred that 6.8-13.1% of LCT-related and 11.3-16.5% of PRT-related duplicates were affected by gene conversion, in which the LCT-related duplicates were the most affected by partial gene conversion, whereas the PRT-related duplicates were the most affected by whole gene conversion. Notably, we observed the conversion between duplicates as the long-lasting contribution of polyploidizations accelerated the divergence of different Arachis genomes. Moreover, we found that the converted duplicates are unevenly distributed across the chromosomes and are more often near the ends of the chromosomes in each genome. We also confirmed that well-preserved homoeologous chromosome regions may facilitate duplicates' conversion. In addition, we found that these biological functions contain a higher number of preferentially converted genes, such as catalytic activity-related genes. We identified specific domains that are involved in converted genes, implying that conversions are associated with important traits of peanut growth and development.

Cotton Duplicated Genes Produced by Polyploidy Show Significantly Elevated and Unbalanced Evolutionary Rates, Overwhelmingly Perturbing Gene Tree Topology.

A phylogenetic tree can be used to illustrate the evolutionary relationship between a group of genes, especially duplicated genes, which are sources of genetic innovation and are often a hotspot of research. However, duplicated genes may have complex phylogenetic topologies due to changes in their evolutionary rates. Here, by constructing phylogenetic trees using different methods, we evaluated the phylogenetic relationships of duplicated genes produced by polyploidization in cotton. We found that at least 83.2% of phylogenetic trees did not conform the expected topology. Moreover, cotton homologous gene copy number has little effect on the topology of duplicated genes. Compared with their cacao orthologs, elevated evolutionary rates of cotton genes are responsible for distorted tree topology. Furthermore, as to both branch and site models, we inferred that positive natural selection during the divergence of fiber-development-related MYB genes was likely, and found that the reconstructed tree topology may often overestimate natural selection, as compared to the inference with the expected trees. Therefore, we emphasize the importance of borrowing precious information from gene collinearity in tree construction and evaluation, and have evidence to alert the citation of thousands of previous reports of adaptivity and functional innovation of duplicated genes.

Illegitimate Recombination Between Homeologous Genes in Wheat Genome.

Polyploidies produce a large number of duplicated regions and genes in genomes, which have a long-term impact and stimulate genetic innovation. The high similarity between homeologous chromosomes, forming different subgenomes, or homologous regions after genome repatterning, may permit illegitimate DNA recombination. Here, based on gene colinearity, we aligned the (sub)genomes of common wheat (Triticum aestivum, AABBDD genotype) and its relatives, including Triticum urartu (AA), Aegilops tauschii (DD), and T. turgidum ssp. dicoccoides (AABB) to detect the homeologous (paralogous or orthologous) colinear genes within and between (sub)genomes. Besides, we inferred more ancient paralogous regions produced by a much ancient grass-common tetraploidization. By comparing the sequence similarity between paralogous and orthologous genes, we assumed abnormality in the topology of constructed gene trees, which could be explained by gene conversion as a result of illegitimate recombination. We found large numbers of inferred converted genes (>2,000 gene pairs) suggested long-lasting genome instability of the hexaploid plant, and preferential donor roles by DD genes. Though illegitimate recombination was much restricted, duplicated genes produced by an ancient whole-genome duplication, which occurred millions of years ago, also showed evidence of likely gene conversion. As to biological function, we found that ~40% catalytic genes in colinearity, including those involved in starch biosynthesis, were likely affected by gene conversion. The present study will contribute to understanding the functional and structural innovation of the common wheat genome.

Alignment of Rutaceae Genomes Reveals Lower Genome Fractionation Level Than Eudicot Genomes Affected by Extra Polyploidization.

Owing to their nutritional and commercial values, the genomes of several citrus plants have been sequenced, and the genome of one close relative in the Rutaceae family, atalantia (Atalantia buxifolia), has also been sequenced. Here, we show a family-level comparative analysis of Rutaceae genomes. By using grape as the outgroup and checking cross-genome gene collinearity, we systematically performed a hierarchical and event-related alignment of Rutaceae genomes, and produced a gene list defining homologous regions based on ancestral polyploidization or speciation. We characterized genome fractionation resulting from gene loss or relocation, and found that erosion of gene collinearity could largely be described by a geometric distribution. Moreover, we found that well-assembled Rutaceae genomes retained significantly more genes (65-82%) than other eudicots affected by recursive polyploidization. Additionally, we showed divergent evolutionary rates among Rutaceae plants, with sweet orange evolving faster than others, and by performing evolutionary rate correction, re-dated major evolutionary events during their evolution. We deduced that the divergence between the Rutaceae family and grape occurred about 81.15-91.74 million years ago (mya), while the split between citrus and atalantia plants occurred <10 mya. In addition, we showed that polyploidization led to a copy number expansion of key gene families contributing to the biosynthesis of vitamin C. Overall, the present effort provides an important comparative genomics resource and lays a foundation to understand the evolution and functional innovation of Rutaceae genomes.

Polyploidy Index and Its Implications for the Evolution of Polyploids.

Polyploidy has contributed to the divergence and domestication of plants; however, estimation of the relative roles that different types of polyploidy have played during evolution has been difficult. Unbalanced and balanced gene removal was previously related to allopolyploidies and autopolyploidies, respectively. Here, to infer the types of polyploidies and evaluate their evolutionary effects, we devised a statistic, the Polyploidy-index or P-index, to characterize the degree of divergence between subgenomes of a polyploidy, to find whether there has been a balanced or unbalanced gene removal from the homoeologous regions. Based on a P-index threshold of 0.3 that distinguishes between known or previously inferred allo- or autopolyploidies, we found that 87.5% of 24 angiosperm paleo-polyploidies were likely produced by allopolyploidizations, responsible for establishment of major tribes such as Poaceae and Fabaceae, and large groups such as monocots and eudicots. These findings suggest that >99.7% of plant genomes likely derived directly from allopolyploidies, with autopolyploidies responsible for the establishment of only a few small genera, including Glycine, Malus, and Populus, each containing tens of species. Overall, these findings show that polyploids with high divergence between subgenomes (presumably allopolyploids) established the major plant groups, possibly through secondary contact between previously isolated populations and hybrid vigor associated with their re-joining.