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Kinesin is a kind of motor protein, which interacts with microtubule filaments and regulates cellulose synthesis. Cotton fiber is a natural model for studying the cellular development and cellulose synthesis. Therefore, a systematic research of kinesin gene family in cotton (Gossypium spp.) will be beneficial for both understanding the function of kinesin protein and assisting the fiber improvement. Here, we aimed to identify the key kinesin genes present in cotton by combining genome-wide expression profile data, association mapping, and public quantitative trait loci (QTLs) in upland cotton (G. hirsutum L.). Results showed that 159 kinesin genes, including 15 genes of the kinesin-13 gene subfamily, were identified in upland cotton; of which 157 kinesin genes can be traced back to the diploid ancestors, G. raimondii and G. arboreum. Using a combined analysis of public QTLs and genome-wide expression profile information, there were 29 QTLs co-localized together with 28 kinesin genes in upland cotton, including 10 kinesin-13 subfamily genes. Genome-wide expression profile data indicated that, among the 28 co-localized genes, seven kinesin genes were predominantly expressed in fibers or ovules. By association mapping analysis, 30 kinesin genes were significantly associated with three fiber traits, among which a kinesin-13 gene, Ghir_A11G028430, was found to be associated with both cotton boll length and lint weight, and one kinesin-7 gene, Ghir_D04G017880 (Gh_Kinesin7), was significantly associated with fiber strength. In addition, two missense mutations were identified in the motor domain of the Gh_Kinesin7 protein. Overall, the kinesin gene family seemingly plays an important role in cotton fiber and boll development. The exploited kinesin genes will be beneficial for the genetic improvement of fiber quality and yield.

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Kinesin is a kind of motor protein, which interacts with microtubule filaments and regulates cellulose synthesis. Cotton fiber is a natural model for studying the cellular development and cellulose synthesis. Therefore, a systematic research of Kinesin gene family in cotton (Gossypium spp.) will be beneficial for both understanding the function of Kinesin protein and assisting the fiber improvement. Here, we aimed to identify the key Kinesin genes present in cotton by combining genome-wide expression profile data, association mapping, and public quantitative trait loci (QTLs) in upland cotton (Gossypium hirsutum L.). Results showed that 159 Kinesin genes, including 15 genes of the Kinesin-13 gene subfamily, were identified in upland cotton; of which 157 Kinesin genes can be traced back to the diploid ancestors, G. raimondii and G. arboreum. Using a combined analysis of public QTLs and genome-wide expression profile information, there were 29 QTLs co-localized together with 28 Kinesin genes in upland cotton, including 10 Kinesin-13 subfamily genes. Genome-wide expression profile data indicated that, among the 28 co-localized genes, seven Kinesin genes were predominantly expressed in fibers or ovules. By association mapping analysis, 30 Kinesin genes were significantly associated with three fiber traits, among which a Kinesin-13 gene, Ghir_A11G028430, was found to be associated with both cotton boll length and lint weight, and one Kinesin-7 gene, Ghir_D04G017880 (Gh_Kinesin7), was significantly associated with fiber strength. In addition, two missense mutations were identified in the motor domain of the Gh_Kinesin7 protein. Overall, the Kinesin gene family seemingly plays an important role in cotton fiber and boll development. The exploited Kinesin genes will be beneficial for the genetic improvement of fiber quality and yield.

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Red foliated cotton is a typical dominant mutation trait in upland cotton (Gossypium hirsutum). Although mutants have been described, few responsible genes have been identified and characterized. In this study, we performed map-based cloning of the red foliated mutant gene (Re) derived from the cross between G. hirsutum cv. Emian22 and G. barbadense acc. 3-79. Through expression profiling, metabolic pathway analysis, and sequencing of candidate genes, Re was identified as an MYB113 transcription factor. A repeat sequence variation in the promoter region increased the activity of the promoter, which enhanced the expression of Re. Re expression driven by the 35S promoter produced a red foliated phenotype, as expected. When the gene was driven by a fiber elongation-specific promoter, promoter of α-expansin 2 (PGbEXPA2), Re was specifically expressed in 5- to 10-day post-anthesis fibers rather than in other tissues, resulting in brown mature fibers. Re responded to light through phytochrome-interacting factor 4 and formed a dimer with transparent testa 8, which increased its expression as well as that of anthocyanin synthase and UDP-glucose:flavonoid 3-o-glucosyl transferase, and thus activated the entire anthocyanin metabolism pathway. Our research has identified the red foliated mutant gene in cotton, which paves the way for detailed studies of anthocyanin and proanthocyanidin metabolism and pigment accumulation in cotton and provides an alternative strategy for producing brown fiber.

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KEY MESSAGE: Rf candidate genes were related to the super D05_PPR-cluster and verified to be individually nonfunctional. Restorer of fertility (Rf) genes of cytoplasmic male sterility (CMS) is commonly found to be PPR (pentatricopeptide repeat) genes, which are mostly located in a cluster of PPR genes with high similarity. Here, Homocap-seq was applied to analyze PPR clusters in 'three lines,' and we found broad variations within the D05_PPR-cluster in a restorer line and deduced that the D05_PPR-cluster was associated with fertility restoration. Genetic mapping of Rf and Homocap-seq analysis of three genotypes in the F2 population validated that the D05_PPR-cluster was the origin of Rf. Three Rf candidates were cloned that were the most actively expressed genes in the D05_PPR-cluster in the restorer line as revealed by their high-depth amplicons. However, further transgenic experiments showed that none of the candidates could restore fertility of the CMS line independently. Then, the members of the brand-new super D05_PPR-cluster in the restorer line, containing 14 full-length PPRs and at least 13 PPR homologous sequences, were identified by long-read resequencing, which validated the effectiveness of variation and expression prediction of Homocap-seq. Additionally, we found that several PPR duplications, including 2 of the 3 Rf candidates, had undergone site-specific selection as potentially important anther development-associated genes. Finally, we proposed that multiple PPRs were coordinately responsible for the fertility restoration of the CMS line.

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The high-quality reference-grade genome for Gossupium tomentosum can greatly promote the progress in biological research and introgression breeding for the mainly cultivated species, G. hirsutum. Here, we report a high-quality genome assembly for G. tomentosum by integrating PacBio and Hi-C technologies. Comparative genomic analysis revealed a large number of genetic variations. Two re-sequencing-based ultra-dense genetic maps were constructed which comprised 4,047,199 and 6,009,681 SNPs, 4120 and 4599 bins and covering 4126.36 cM and 4966.72 cM in the EMF2 (F2 from G. hirsutum × G. tomentosum) and GHF2 (F2 from G. hirsutum × G. barbadense). The EMF2 exhibited lower recombination rate at the whole-genome level as compared with GHF2. We mapped 22 and 33 QTL associated with crossover frequency and predicted Gh_MRE11 and Gh_FIGL1 as the candidate genes governing crossover in the EMF2 and GHF2, respectively. We identified 13 significant QTL that regulate the floral transition, and revealed that Gh_AGL18 was associated with the floral transition. Therefore, our study provides a valuable genomic resource to support a better understanding of cotton interspecific cross and recombination landscape for genetic improvement and breeding in cotton.

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KEY MESSAGE: One sub-MAGIC population was genotyped using SLAF-seq, and QTLs and candidate genes for agronomic traits were identified in Upland cotton. The agronomic traits of Upland cotton have serious impacts on cotton production, as well as economic benefits. To discover the genetic basis of important agronomic traits in Upland cotton, a subset MAGIC (multi-parent advanced generation inter-cross) population containing 372 lines (SMLs) was selected from an 8-way MAGIC population with 960 lines. The 372 lines and 8 parents were phenotyped in six environments and deeply genotyped by SLAF-seq with 60,495 polymorphic SNPs. The genetic diversity indexes of all SNPs were 0.324 and 0.362 for the parents and MAGIC lines, respectively. The LD decay distance of the SMLs was 600 kb (r2 = 0.1). Genome-wide association mapping was performed using 60,495 SNPs and the phenotypic data of the SMLs, and 177 SNPs were identified to be significantly associated with 9 stable agronomic traits in multiple environments. The identified SNPs were divided into 117 QTLs (quantitative trait loci) by LD decay distance, explaining 5.44% to 31.64% of the phenotypic variation. Among the 117 QTLs, 3 QTLs were stable in multiple environments, and 11 QTL regions were proven to have pleiotropism associated with multiple traits. Within QTL regions, 154 genes were preferentially expressed in correlated tissues, and 8 genes with known functions were identified as priori candidate genes. Two genes, GhACT1 and GhGASL3, reported to have clear functions, were, respectively, located in qFE-A05-4 and qFE-D04-3, two stable QTLs for FE. This study revealed the genetic basis of important agronomic traits of Upland cotton, and the results will facilitate molecular breeding in cotton.

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Nulliplex branch is a key architectural trait in sea-island cotton (Gossypium barbadense L.), but its genetic basis is not well understood. Here we investigated the genetic basis of the nulliplex-branch trait in cotton by combining newly created bulked segregant analysis (BSA)-seq data, published RNA-seq data, and published whole-genome resequencing (WGR) data. We delimited the nulliplex-branch locus (qD07-NB) to D07, region 14.8-17.1 Mb, using various BSA methods and markers. We integrated our BSA data with WGR data of sea-island cotton varieties and detected a missense single-nucleotide polymorphism in the candidate gene (Gbar_D07G011870) of qD07-NB. This gene was under positive selection during sea-island cotton breeding in the Xinjiang Uygur Autonomous Region, China. Notably, the nulliplex-branch varieties possessed a better fiber quality than the long-branch varieties, and a set of high-quality molecular markers was identified for molecular breeding of the nulliplex-branch trait in cotton. We combined BSA-seq and RNA-seq data to compare gene expression profiles between two elite sea-island cotton varieties during three developmental stages. We identified eleven relevant candidate genes, five downregulated and six upregulated, in the qD07-NB locus. This research will expand our understanding of the genetic basis of the nulliplex-branch trait and provide guidance for architecture-focused breeding in cotton. Supplementary Information: The online version contains supplementary material available at 10.1007/s11032-021-01229-w.

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The two new world tetraploid cottons, Gossypium hirsutum and Gossypium barbadense, are cultivated worldwide and are characterised by a high yield and superior fibre quality, respectively. Historical genetic introgression has been reported between them; however, the existence of introgression and its genetic effects on agronomic traits remain unclear with regard to independent breeding of G. hirsutum (Upland cotton) and G. barbadense (Pima cotton) elite cultivars. We collected 159 G. hirsutum and 70 G. barbadense cultivars developed in Xinjiang, China, along with 30 semi-wild accessions of G. hirsutum, to perform interspecific introgression tests, intraspecific selection analyses and genome-wide association studies (GWAS) with fibre quality and yield component traits in multiple environments. In total, we identified seven interspecific introgression events and 52 selective sweep loci in G. hirsutum, as well as 17 interspecific introgression events and 19 selective sweep loci in G. barbadense. Correlation tests between agronomic traits and introgressions showed that introgression loci were mutually beneficial for the improvement of fibre quality and yield traits in both species. In addition, the phenotypic effects of four interspecific introgression events could be detected by intraspecific GWAS, with Gb_INT13 significantly improving fibre yield in G. barbadense. The present study describes the landscape of genetic introgression and selection between the two species, and highlights the genetic effects of introgression among populations, which can be used for future improvement of fibre yield and quality in G. barbadense and G. hirsutum, respectively.

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The quality of fiber is significant in the upland cotton industry. As complex quantitative traits, fiber quality traits are worth studying at a genetic level. To investigate the genetic architecture of fiber quality traits, we conducted an association analysis using a multi-parent advanced generation inter-cross (MAGIC) population developed from eight parents and comprised of 960 lines. The reliable phenotypic data for six major fiber traits of the MAGIC population were collected from five environments in three locations. Phenotypic analysis showed that the MAGIC lines have a wider variation amplitude and coefficient than the founders. A total of 284 polymorphic SSR markers among eight parents screened from a high-density genetic map were used to genotype the MAGIC population. The MAGIC population showed abundant genetic variation and fast linkage disequilibrium (LD) decay (0.76 cM, r2 > 0.1), which revealed the advantages of high efficiency and power in QTL exploration. Association mapping via a mixed linear model identified 52 significant loci associated with six fiber quality traits; 14 of them were mapped in reported QTL regions with fiber-related or other agronomic traits. Nine markers demonstrated the pleiotropism that controls more than two fiber traits. Furthermore, two SSR markers, BNL1231 and BNL3452, were authenticated as hotspots that were mapped with multi-traits. In addition, we provided candidate regions and screened six candidate genes for identified loci according to the LD decay distance. Our results provide valuable QTL for further genetic mapping and will facilitate marker-based breeding for fiber quality in cotton.

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Brown fibre cotton is an environmental-friendly resource that plays a key role in the textile industry. However, the fibre quality and yield of natural brown cotton are poor, and fundamental research on brown cotton is relatively scarce. To understand the genetic basis of brown fibre cotton, we constructed linkage and association populations to systematically examine brown fibre accessions. We fine-mapped the brown fibre region, Lc1 , and dissected it into 2 loci, qBF-A07-1 and qBF-A07-2. The qBF-A07-1 locus mediates the initiation of brown fibre production, whereas the shade of the brown fibre is affected by the interaction between qBF-A07-1 and qBF-A07-2. Gh_A07G2341 and Gh_A07G0100 were identified as candidate genes for qBF-A07-1 and qBF-A07-2, respectively. Haploid analysis of the signals significantly associated with these two loci showed that most tetraploid modern brown cotton accessions exhibit the introgression signature of Gossypium barbadense. We identified 10 quantitative trait loci (QTLs) for fibre yield and 19 QTLs for fibre quality through a genome-wide association study (GWAS) and found that qBF-A07-2 negatively affects fibre yield and quality through an epistatic interaction with qBF-A07-1. This study sheds light on the genetics of fibre colour and lint-related traits in brown fibre cotton, which will guide the elite cultivars breeding of brown fibre cotton.

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MicroRNAs (miRNAs) modulate many biological processes through inactivation of specific mRNA targets such as those encoding transcription factors. A delicate spatial/temporal balance between specific miRNAs and their targets is central to achieving the appropriate biological outcomes. Somatic embryogenesis in cotton (Gossypium hirsutum), which goes through initial cellular dedifferentiation, callus proliferation, and somatic embryo development, is of great importance for both fundamental research and biotechnological applications. In this study, we characterize the function of the GhmiR157a-GhSPL10 miRNA-transcription factor module during somatic embryogenesis in cotton. We show that overexpression of GhSPL10, a target of GhmiR157a, increases free auxin and ethylene content and expression of associated signaling pathways, activates the flavonoid biosynthesis pathway, and promotes initial cellular dedifferentiation and callus proliferation. Inhibition of expression of the flavonoid synthesis gene F3H in GhSPL10 overexpression lines (35S:rSPL10-7) blocked callus initiation, while exogenous application of several types of flavonol promoted callus proliferation, associated with cell cycle-related gene expression. Inhibition of ethylene synthesis by aminoethoxyvinylglycine treatment in the 35S:rSPL10-7 line severely inhibited callus initiation, while activation of ethylene signaling through 1-aminocyclopropane 1-carboxylic acid treatment, EIN2 overexpression, or inhibition of the ethylene negative regulator CTR1 by RNA interference promoted flavonoid-related gene expression and flavonol accumulation. These results show that an up-regulation of ethylene signaling and the activation of flavonoid biosynthesis in GhSPL10 overexpression lines were associated with initial cellular dedifferentiation and callus proliferation. Our results demonstrate the importance of a GhmiR157a-GhSPL10 gene module in regulating somatic embryogenesis via hormonal and flavonoid pathways.

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