Genome sequence of Gossypium herbaceum and genome updates of Gossypium arboreum and Gossypium hirsutum provide insights into cotton A-genome evolution

Abstract

ultivated cotton is one of the most economically important crop plants in the world. The allotetraploid Upland cotton, G. hirsutum (n = 2x = 26, (AD) 1), currently dominates the world's cotton commerce 1,2. Hybridization between the Old World A-genome progenitor and a New World D-genome ancestor, followed by chromosome doubling, formed the allopolyploid cotton ~1−2 million years ago (Ma) 3,4. Uncertainty regarding the actual A-genome donor of the widely cultivated allotetraploid cotton G. hirsutum has persisted 5-13. A 1 (n = x = 13) and A 2 (n = x = 13), commonly known as African and Asiatic cotton, respectively, are the only two extant diploid A-genome species in the world 14. Stephens first proposed in Nature, using genetic and morphological evidence, that A 2 was the A-genome donor of present-day allopolyploid cottons 6. Gerstel argued via cytogenetic studies that A 1 was more closely related to the A-genome in the allopolyploids than A 2 (ref. 8). Despite recent efforts to sequence the cotton genomes, including Gossypium raimondii (D 5) 15,16 , A 2 (refs. 17,18), (AD) 1 (refs. 10,19-21) and Gossypium barbadense 10,21 ((AD) 2 , a much less cultivated tetraploid cotton), the origin history of the A-genome donor for the tetraploid (AD) 1-genome 5,11,13 and the extent of divergence between the A-genomes remain elusive 22,23. Abundant studies support a Gossypium species resembling D 5 as the D-genome donor 13 , but currently there is no solid evidence to suggest that the actual A-genome donor of tetraploid cottons is either A 2 (refs. 6,7,10,19) or A 1 (refs. 8,9,11-13) as has been suggested. In this study, we assembled A 1 variety africanum for the first time and reassembled high-quality A 2 cultivar Shixiya1 and (AD) 1 genetic standard Texas Marker-1 (TM-1) genomes on the basis of PacBio long reads, paired-end sequencing and high-throughput chromosome conformation capture (Hi-C) technologies. Upon assembling and updating cotton genomes, we revealed the origin of cotton A-genomes, the occurrence of several transposable element (TE) bursts and the genetic divergence of diploid A-genomes worldwide. Also, we identified abundant structural variations (SVs) that have affected the expression of neighboring genes and help explain phenotypic differences among the cotton species. Results Sequencing and assembly of three high-quality cotton genomes. Here we sequenced the A 1-genome var. africanum for the first time by generating ~225-gigabase (Gb) PacBio single-molecule real-time (SMRT) long reads (the N50 (minimum length to cover 50% of the total length) of these reads was 13 kilobases (kb)) with 138-fold genome coverage. We generated an assembly that captured 1,556 megabases (Mb) of genome sequences, consisting of 1,781 contigs with the N50 of these contigs reaching up to 1,915 kb (Table 1). The initial assemblies were then corrected by using highly accurate Illumina paired-end reads (Supplementary Table 1). Finally, 95.69% of total contigs spanning 1,489 Mb were categorized and ordered into 13 chromosome-scale scaffold...

Sequencing Multiple Cotton Genomes Reveals Complex Structures and Lays Foundation for Breeding

“…A more recent estimation of 4.7-5.2 Mya was recently obtained (Chen et al, 2020). The common ancestor of the A 1 and A 2 clade was phylogenetically a sister to the A t -subgenomes of (AD) 1 and of (AD) 2 , and the divergence time for A 1 and A 2 was estimated to be~0.7 Mya, suggesting that allotetraploid formation (~1.0−1.6 Mya) preceded the speciation of A 1 and A 2 (Huang et al, 2020) (Figure 1).…”

“…In view of cotton's importance in human life, intensive efforts have been focused on uncovering the genome mysteries of cotton species. Three diploid cottons and two tetraploid cottons were sequenced, including G. arboreum (Li et al, 2014;Du et al, 2018;Huang et al, 2020), G. herbaceum (Huang et al, 2020), G. raimondii (Wang et al, 2012;Paterson et al, 2012;Udall et al, 2019), G. hirsutum (Li et al, 2015;Zhang et al, 2015;Hu et al, 2019;Wang M. et al, 2019;Chen et al, 2020;Huang et al, 2020) and G. barbadense (Yuan et al, 2015;Liu et al, 2015;Hu et al, 2019;Wang M. et al, 2019;Chen et al, 2020). Detailed genome information is shown in Tables 1 and 2.…”

“…G. arboretum (Li et al, 2014) G. arboretum (Du et al, 2018) G. arboretum (Huang et al, 2020) G. herbaceum (Huang et al, 2020) G. raimondii (Wang et al, 2012) G. raimondii (Paterson et al, 2012) G. raimondii (Udall et al, 2019) Total contigs 40,381 8,223 2,432 1,781 41,307 19,735 187 Contig N50 (kb) 72 1,100 1, G. hirsutum (TM-1,V1.1) (Zhang et al, 2015) G. hirsutum (TM-1) (Wang M. et al, 2019) G. hirsutum (TM-1,V2.1) (Hu et al, 2019) G. hirsutum (TM-1,updated V1) (Huang et al, 2020) G. hirsutum (TM-1) (Chen et al, 2020) G. barbadense (Xinhai21) (Liu et al, 2015) G. barbadense…”

“…africanum, another A-genome diploid cotton, was sequenced using Illumina, PacBio and Hi-C sequence technology. The assembled size was 1,556 Mb with 95.69% (1,489 Mb) of all sequenced oriented and organized into 13 chromosomes (Huang et al, 2020). G. hirsutum, known for its high lint production than any other cultivated cotton species, accounts for more than 90% of commercial cotton production worldwide (Cronn et al, 2003).…”

“…In the assembly V1.1, 218 misassembled scaffolds (442.2 Mb) in the assembly V1.0 was corrected (Zhang et al, 2015). Very recently, by using PacBio, Illumina HiSeq and Hi-C, a much improved G. hirsutum genome sequence was published (Huang et al, 2020).…”