Gossypium Organellar Genome Evolution And Interorganellar Gene Transfer In Land Plants

Cotton is the most important fiber crop plant in the world,including 52 species.Cotton(Gossypium spp.)is commonly grouped into eight diploid genomic groups,designated A-G and K,and one tetraploid genomic group,namely AD.To gain insight into the phylogeny of Gossypium and molecular evolution of the chloroplast or mitochondrial genome in this group,we performed the comparative analyses of 34 Gossypium chloroplast genomes(9 were newly reported here)and 10 Gossypium mitochondrial genomes(8 were newly reported here),respectively.34 Gossypium chloroplast genomes that collectively represent most of the diversity in this genus and 10 Gossypium mitochondrial genomes contain diploid species from A and D as well as allotetraploid species from AD genome groups.The complete nucleotide sequences of cpDNA and mtDNA genomes are provided here,offering a resource for cytonuclear studies in Gossypium.This research also provided new insights into the phylogeny of Gossypium and molecular evolution of the chloroplast and mitochondrial genomes during the diversification of this important genus.In addition,interorganellar gene transfer(IGT)is a ubiquitous,continuing and natural process in land plants that pervades nuclear and organellar DNA dynamics.The main results are as follows:1.Like most higher-plant chloroplast genomes,all cotton species exhibit a conserved quadripartite structure,i.e.,two large inverted repeats(IR)containing most of the ribosomal RNA genes,and two unique regions,LSC(large single sequence)and SSC(small single sequence).Within Gossypium,the IR-single copy region junctions are both variable and homoplasious among species.Two genes,accD and psaJ,exhibited greater rates of synonymous and non-synonymous substitutions than did other genes.Most genes exhibited Ka/Ks ratios suggestive of neutral evolution.2.Gossypium chloroplasts span a small range in size that is mostly attributable to indels that occur in the large single copy(LSC)region of the genome.Phylogenetic analysis of indel distribution demonstrates contrasting evolutionary dynamics in different clades,with a parallel genome downsizing in two genome groups and a biased accumulation of insertions in the clade containing the cultivated cottons leading to large(for Gossypium)chloroplast genomes.Nucleotide distance in non-coding regions was about three times that of coding regions.As expected,distances were smaller within than among genome groups.3.Phylogenetic topologies based on nucleotide and indel data support for the resolution of the 8 genome groups into 6 clades.Using Theobroma cacao as an outgroup,diversification of the genus was dated,yielding results that are in accord with previous estimates of divergence times,but also offering new perspectives on the basal,early radiation of all major clades within the genus as well as gaps in the record indicative of extinctions.Divergence time estimates derived from the cpDNA sequence suggest that the major diploid clades had diverged approximately 10 to 11 million years ago.4.The Gossypium mitogenomes were all assembled as the single circular molecules of lengths about 644kb in diploid D group species,687kb in A group species and 677kb in allotetraploid AD group species,respectively.The genomic structures of mitochondrial in D group species were totally identical but differed to mitogenome of G arboreum(A2),as well as mitogenomes of five species of AD group.There mainly existed six or four large repeats in mitogenome of D group species or A + AD groups species,respectively.These variations in repeat sequences caused the major inversions and translocations within the mitochondrial genome of Gossypium,which mediated frequent multiple intramolecular rearrangement.5.The mitochondrial genome complexity in Gossypium presented eight unique segments in D group species,three specific fragments in A + AD group species and a large segment(more than 11kb)in diploid species.These insertions or deletions were most probably generated from crossovers between repetitive or homologous regions.6.IGT data for Gossypium reveal no sequence-specific preferential DNA transfer for chloroplast-to-nucleus integrants,but apparent preferential transfer of the intergenic atp6-trnW region for mitochondria-to-nucleus transfer events.We confirm a previous unusual report of the integration of 93%of the mitochondrial genome of G.raimondii into chromosome 1.Using RNA-seq data,we show that these integrants with diverged SNP are not expressed in G.hirsutum,while nuclear integrants with 100%identity showing high expressions.7.Here,28 data sets comprising nuclear,mitochondrial and chloroplast genomes from land plants were studied,showing that IGT is common in spermatophytes but less so in bryophytes.Our results provide new perspectives on the occurrence and frequency of IGT events in land plants.