Intergenomic gene transfer in diploid and allopolyploid Gossypium

Background: Intergenomic gene transfer (IGT) between nuclear and organellar genomes is a common phenomenon during plant evolution. Gossypium is a useful model to evaluate the genomic consequences of IGT for both diploid and polyploid species. Here, we explore IGT among nuclear, mitochondrial, and plastid genomes of four cotton species, including two allopolyploids and their model diploid progenitors (genome donors, G. arboreum: A2 and G. raimondii: D5). Results: Extensive IGT events exist for both diploid and allotetraploid cotton (Gossypium) species, with the nuclear genome being the predominant recipient of transferred DNA followed by the mitochondrial genome. The nuclear genome has integrated 100 times more foreign sequences than the mitochondrial genome has in total length. In the nucleus, the integrated length of chloroplast DNA (cpDNA) was between 1.87 times (in diploids) to nearly four times (in allopolyploids) greater than that of mitochondrial DNA (mtDNA). In the mitochondrion, the length of nuclear DNA (nuDNA) was typically three times than that of cpDNA. Gossypium mitochondrial genomes integrated three nuclear retrotransposons and eight chloroplast tRNA genes, and incorporated chloroplast DNA prior to divergence between the diploids and allopolyploid formation. For mitochondrial chloroplast-tRNA genes, there were 2-6 bp conserved microhomologies flanking their insertion sites across distantly related genera, which increased to 10 bp microhomologies for the four cotton species studied. For organellar DNA sequences, there are source hotspots, e.g., the atp6-trnW intergenic region in the mitochondrion and the inverted repeat region in the chloroplast. Organellar DNAs in the nucleus were rarely expressed, and at low levels. Surprisingly, there was asymmetry in the survivorship of ancestral insertions following allopolyploidy, with most numts (nuclear mitochondrial insertions) decaying or being lost whereas most nupts (nuclear plastidial insertions) were retained. Conclusions: This study characterized and compared intracellular transfer among nuclear and organellar genomes within two cultivated allopolyploids and their ancestral diploid cotton species. A striking asymmetry in the fate of IGTs in allopolyploid cotton was discovered, with numts being preferentially lost relative to nupts. Our results connect intergenomic gene transfer with allotetraploidy and provide new insight into intracellular genome evolution

A New Species of Cotton from Wake Atoll,Gossypium stephensii(Malvaceae)

Wake Atoll is an isolated chain of three islets located in the Western Pacific. Included in its endemic flora is a representative of the genus Gossypium colloquially referred to as Wake Island cotton. Stanley G. Stephens pointed out that “Wake Island cotton does not resemble closely either the Caribbean or other Pacific forms.” Taking into consideration morphological distinctions, the geographic isolation of Wake Atoll, and newly generated molecular data presented here, we conclude that the cottons of Wake Atoll do in fact represent a new species of Gossypium, here named Gossypium stephensii. This name is chosen to commemorate the eminent natural historian, evolutionary geneticist, and cotton biologist, S. G. Stephens

Rapid evolutionary divergence of Gossypium barbadense and G. hirsutum mitochondrial genomes

Background The mitochondrial genome from upland cotton, G. hirsutum, was previously sequenced. To elucidate the evolution of mitochondrial genomic diversity within a single genus, we sequenced the mitochondrial genome from Sea Island cotton (Gossypium barbadense L.). Methods Mitochondrial DNA from week-old etiolated seedlings was extracted from isolated organelles using discontinuous sucrose density gradient method. Mitochondrial genome was sequenced with Solexa using paired-end, 90 bp read. The clean reads were assembled into contigs using ABySS and finished via additional fosmid and BAC sequencing. Finally, the genome was annotated and analyzed using different softwares. Results The G. barbadense (Sea Island cotton) mitochondrial genome was fully sequenced (677,434-bp) and compared to the mitogenome of upland cotton. The G. barbadensemitochondrial DNA contains seven more genes than that of upland cotton, with a total of 40 protein coding genes (excluding possible pseudogenes), 6 rRNA genes, and 29 tRNA genes. Of these 75 genes, atp1, mttB, nad4, nad9, rrn5, rrn18, and trnD(GTC)-cp were each represented by two identical copies. A single 64 kb repeat was largely responsible for the 9 % difference in genome size between the two mtDNAs. Comparison of genome structures between the two mitochondrial genomes revealed 8 rearranged syntenic regions and several large repeats. The largest repeat was missing from the master chromosome in G. hirsutum. Both mitochondrial genomes contain a duplicated copy of rps3 (rps3-2) in conjunction with a duplication of repeated sequences. Phylogenetic and divergence considerations suggest that a 544-bp fragment of rps3 was transferred to the nuclear genome shortly after divergence of the A- and D- genome diploid cottons. Conclusion These results highlight the insights to the evolution of structural variation between Sea Island and upland cotton mitochondrial genomes

Conservation and Divergence in Duplicated Fiber Coexpression Networks Accompanying Domestication of the Polyploid Gossypium hirsutum L

Gossypium hirsutum L. (Upland cotton) has an evolutionary history involving inter-genomic hybridization, polyploidization, and subsequent domestication. We analyzed the developmental dynamics of the cotton fiber transcriptome accompanying domestication using gene coexpression networks for both joint and homoeologous networks. Remarkably, most genes exhibited expression for at least one homoeolog, confirming previous reports of widespread gene usage in cotton fibers. Most coexpression modules comprising the joint network are preserved in each subgenomic network and are enriched for similar biological processes, showing a general preservation of network modular structure for the two co-resident genomes in the polyploid. Interestingly, only one fifth of homoeologs co-occur in the same module when separated, despite similar modular structures between the joint and homoeologous networks. These results suggest that the genome-wide divergence between homoeologous genes is sufficient to separate their co-expression profiles at the intermodular level, despite conservation of intramodular relationships within each subgenome. Most modules exhibit D-homoeolog expression bias, although specific modules do exhibit A-homoeolog bias. Comparisons between wild and domesticated coexpression networks revealed a much tighter and denser network structure in domesticated fiber, as evidenced by its fewer modules, 13-fold increase in the number of development-related module member genes, and the poor preservation of the wild network topology. These results demonstrate the amazing complexity that underlies the domestication of cotton fiber

Insights into the evolution of the New World diploid cottons (Gossypium, subgenus Houzingenia) based on genome sequencing

We employed phylogenomic methods to study molecular evolutionary processes and phylogeny in the geographically widely dispersed New World diploid cottons (Gossypium, subg. Houzingenia). Whole genome resequencing data (average of 33X genomic coverage) were generated to reassess the phylogenetic history of the subgenus and provide a temporal framework for its diversification. Phylogenetic analyses indicate that the subgenus likely originated following trans-oceanic dispersal from Africa about 6.6 mya, but that nearly all of the biodiversity evolved following rapid diversification in the mid-Pleistocene (0.5-2.0 mya), with multiple long-distance dispersals required to account for range expansion to Arizona, the Galapagos Islands, and Peru. Comparative analyses of cpDNA vs. nuclear data indicate that this history was accompanied by several clear cases of interspecific introgression. Repetitive DNAs contribute roughly half of the total 880 Mb genome, but most transposable element families are relatively old and stable among species. In the genic fraction, pairwise synonymous mutation rates average 1% per my, with non-synonymous changes being about seven times less frequent. Over 1.1 million indels were detected and phylogenetically polarized, revealing a two-fold bias toward deletions over small insertions. We suggest that this genome down-sizing bias counteracts genome size growth by TE amplification and insertions, and helps explain the relatively small genomes that are restricted to this subgenus. Compared to the rate of nucleotide substitution, the rate of indel occurrence is much lower averaging about 17 nucleotide substitutions per indel event

Reticulate evolution helps explain apparent homoplasy in floral biology and pollination in baobabs (Adansonia; Bombacoideae; Malvaceae)

Baobabs (Adansonia) are a cohesive group of tropical trees with a disjunct distribution in Australia, Madagascar, and continental Africa, and diverse flowers associated with two pollination modes. We used custom targeted sequence capture in conjunction with new and existing phylogenetic comparative methods to explore the evolution of floral traits and pollination systems while allowing for reticulate evolution. Our analyses suggest that relationships in Adansonia are confounded by reticulation, with network inference methods supporting at least one reticulation event. The best supported hypothesis involves introgression between A. rubrostipa and core Longitubae, both of which are hawkmoth pollinated with yellow/red flowers, but there is also some support for introgression between the African lineage and Malagasy Brevitubae, which are both mammal-pollinated with white flowers. New comparative methods for phylogenetic networks were developed that allow maximum-likelihood inference of ancestral states and were applied to study the apparent homoplasy in floral biology and pollination mode seen in Adansonia. This analysis supports a role for introgressive hybridization in morphological evolution even in a clade with highly divergent and geographically widespread species. Our new comparative methods for discrete traits on species networks are implemented in the software PhyloNetworks

Unraveling cis and trans regulatory evolution during cotton domestication

Cis and trans regulatory divergence underlies phenotypic and evolutionary diversification. Relatively little is understood about the complexity of regulatory evolution accompanying crop domestication, particularly for polyploid plants. Here, we compare the fiber transcriptomes between wild and domesticated cotton (Gossypium hirsutum) and their reciprocal F1 hybrids, revealing genome-wide (~15%) and often compensatory cis and trans regulatory changes under divergence and domestication. The high level of trans evolution (54%–64%) observed is likely enabled by genomic redundancy following polyploidy. Our results reveal that regulatory variation is significantly associated with sequence evolution, inheritance of parental expression patterns, co-expression gene network properties, and genomic loci responsible for domestication traits. With respect to regulatory evolution, the two subgenomes of allotetraploid cotton are often uncoupled. Overall, our work underscores the complexity of regulatory evolution during fiber domestication and may facilitate new approaches for improving cotton and other polyploid plants

A Malvaceae mystery: A mallow maelstrom of genome multiplications and maybe misleading methods?

Previous research suggests that Gossypium has undergone a 5- to 6-fold multiplication following its divergence from Theobroma. However, the number of events, or where they occurred in the Malvaceae phylogeny remains unknown. We analyzed transcriptomic and genomic data from representatives of eight of the nine Malvaceae subfamilies. Phylogenetic analysis of nuclear data placed Dombeya (Dombeyoideae) as sister to the rest of Malvadendrina clade, but the plastid DNA tree strongly supported Durio (Helicteroideae) in this position. Intraspecific Ks plots indicated that all sampled taxa, except Theobroma (Byttnerioideae), Corchorus (Grewioideae), and Dombeya (Dombeyoideae), have experienced whole genome multiplications (WGMs). Quartet analysis suggested WGMs were shared by Malvoideae-Bombacoideae and Sterculioideae-Tilioideae, but did not resolve whether these are shared with each other or Helicteroideae (Durio). Gene tree reconciliation and Bayesian concordance analysis suggested a complex history. Alternative hypotheses are suggested, each involving two independent autotetraploid and one allopolyploid event. They differ in that one entails an allopolyploid origin for the Durio lineage, whereas the other invokes an allopolyploid origin for Malvoideae-Bombacoideae. We highlight the need for more genomic information in the Malvaceae and improved methods to resolve complex evolutionary histories that may include allopolyploidy, incomplete lineage sorting, and variable rates of gene and genome evolution