Summary: Interspecific genomic variation can provide a genetic basis for local adaptation and domestication. A series of studies have presented its role of interspecific haplotypes and introgressions in adaptive traits, but few studies have addressed their role in improving agronomic character. Two allotetraploid Gossypium species, Gossypium barbadense (Gb) and G. hirsutum (Gh) originating from the Americas, are cultivated independently. Here, through sequencing and the comparison of one GWAS panel in 229 Gb accessions and two GWAS panels in 491 Gh accessions, we found that most associated loci or functional haplotypes for agronomic traits were highly divergent, representing the strong divergent improvement between Gb and Gh. Using a comprehensive interspecific haplotype map, we revealed that six interspecific introgressions from Gh to Gb were significantly associated with the phenotypic performance of Gb, which could explain 5%–40% of phenotypic variation in yield and fibre qualities. In addition, three introgressions overlapped with six associated loci in Gb, indicating that these introgression regions were under further selection and stabilized during improvement. A single interspecific introgression often possessed yield‐increasing potential but decreased fibre qualities, or the opposite, making it difficult to simultaneously improve yield and fibre qualities. Our study not only has proved the importance of interspecific functional haplotypes or introgressions in the divergent improvement of Gb and Gh, but also supports their potential value in further human‐mediated hybridization or precision breeding.

DNA methylation plays multiple regulatory roles in crop development. However, the relationships of methylation polymorphisms with genetic polymorphisms, gene expression, and phenotypic variation in natural crop populations remain largely unknown. Here, we surveyed high-quality methylomes, transcriptomes, and genomes obtained from the 20-days-post-anthesis (DPA) cotton fibers of 207 accessions and extended the classical framework of population genetics to epigenetics. Over 287 million single methylation polymorphisms (SMPs) were identified, 100 times more than the number of single nucleotide polymorphisms (SNPs). These SMPs were significantly enriched in intragenic regions while depleted in transposable elements. Association analysis further identified a total of 5,426,782 cis-methylation quantitative trait loci (cis-meQTLs), 5078 cis-expression quantitative trait methylation (cis-eQTMs), and 9157 expression quantitative trait loci (eQTLs). Notably, 36.39% of cis-eQTM genes were not associated with genetic variation, indicating that a large number of SMPs associated with gene expression variation are independent of SNPs. In addition, out of the 1715 epigenetic loci associated with yield and fiber quality traits, only 36 (2.10%) were shared with genome-wide association study (GWAS) loci. The construction of multi-omics regulatory networks revealed 43 cis-eQTM genes potentially involved in fiber development, which cannot be identified by GWAS alone. Among these genes, the role of one encoding CBL-interacting protein kinase 10 in fiber length regulation was successfully validated through gene editing. Taken together, our findings prove that DNA methylation data can serve as an additional resource for breeding purposes and can offer opportunities to enhance and expedite the crop improvement process.

Members of the Malvaceae family, including Corchorus spp., Gossypium spp., Bombax spp., and Ceiba spp., are important sources of natural fibers. In the past decade, the genomes of several Malvaceae species have been assembled; however, the evolutionary history of Malvaceae species and the differences in their fiber development remain to be clarified. Here, we report the genome assembly and annotation of two natural fiber plants from the Malvaceae, Bombax ceiba and Ceiba pentandra, whose assembled genome sizes are 783.56 Mb and 1575.47 Mb, respectively. Comparative analysis revealed that whole-genome duplication and Gypsy long terminal repeat retroelements have been the major causes of differences in chromosome number (2n = 14 to 2n = 96) and genome size (234 Mb to 2676 Mb) among Malvaceae species. We also used comparative genomic analyses to reconstruct the ancestral Malvaceae karyotype with 11 proto-chromosomes, providing new insights into the evolutionary trajectories of Malvaceae species. MYB-MIXTA-like 3 is relatively conserved among the Malvaceae and functions in fiber cell-fate determination in the epidermis. It appears to perform this function in any tissue where it is expressed, i.e. in fibers on the endocarp of B. ceiba and in ovule fibers of cotton. We identified a structural variation in a cellulose synthase gene and a higher copy number of cellulose synthase-like genes as possible causes of the finer, less spinnable, weaker fibers of B. ceiba. Our study provides two high-quality genomes of natural fiber plants and offers insights into the evolution of Malvaceae species and differences in their natural fiber formation and development through multi-omics analysis.

The rapid advancement of sequencing technology, including next-generation sequencing (NGS), has greatly improved sequencing efficiency and decreased cost. Consequently, huge amounts of genomic, transcriptomic and epigenetic data concerning cotton species have been generated and released. These large-scale data provide immense opportunities for the study of cotton genomic structure and evolution, population genetic diversity and genome-wide mining of excellent genes for important traits. However, the complexity of NGS data also causes distress, as it cannot be utilized easily. Here, we presented the cotton omics data platform COTTONOMICS (http://cotton.zju.edu.cn/), an easily accessible web database that integrates 32.5 TB of omics data including seven assembled genomes, resequencing data from 1180 allotetraploid cotton accessions and RNA-sequencing (RNA-seq), small RNA-sequencing (smRNA-seq), Chromatin Immunoprecipitation sequencing (ChIP-seq), DNase hypersensitive sites sequencing (DNase-seq) and Bisulfite sequencing (BS-seq). COTTONOMICS allows users to employ various search scenarios and retrieve information concerning the cotton genomes, genomic variation (Single nucleotide polymorphisms (SNPs) and Insertion and Deletion (InDels)), gene expression, smRNA expression, epigenetic regulation and quantitative trait locus (QTLs). The user-friendly web interface offers a variety of modules for storing, retrieving, analyzing and visualizing cotton multi-omics data to diverse ends, thereby enabling users to decipher cotton population genetics and identify potential novel genes that influence agronomically beneficial traits. Database URL: http://cotton.zju.edu.cn

Genome-wide association studies (GWAS) are widely used to detect associations between genetic variants and phenotypes. However, few studies have thoroughly analyzed genes, the fundamental and most crucial functional units. Here, we develop an innovative strategy to translate genomic variants into gene-level functional haplotypes (FHs), effectively reducing the interference from complex genome structure and linkage disequilibrium (LD) present in the conventional genetic mapping framework. Using refined mixed linear models, gene-level FH is regressed with 20 cotton agronomic traits across 245 sets of phenotypic values in 3,724 accessions, directly identifying 532 quantitative trait genes (QTGs) with significant breeding potential. The biological function of a superior fiber quality QTG encoding ferulic acid 5-hydroxylase 1 is experimentally validated. Thereafter, we systematically analyze the genetic basis of cotton domestication and improvement at the gene level. This report provides genomic insight into the genetic dissection and efficient mapping of functional genes in plants.