Polyploidy often confers emergent properties, such as the higher fibre productivity and quality of tetraploid cottons than diploid cottons bred for the same environments¹. Here we show that an abrupt five- to sixfold ploidy increase approximately 60 million years (Myr) ago, and allopolyploidy reuniting divergent Gossypium genomes approximately 1–2 Myr ago², conferred about 30–36-fold duplication of ancestral angiosperm (flowering plant) genes in elite cottons (Gossypium hirsutum and Gossypium barbadense), genetic complexity equalled only by Brassica³ among sequenced angiosperms. Nascent fibre evolution, before allopolyploidy, is elucidated by comparison of spinnable-fibred Gossypium herbaceum A and non-spinnable Gossypium longicalyx F genomes to one another and the outgroup D genome of non-spinnable Gossypium raimondii. The sequence of a G. hirsutum A_tD_t (in which ‘t’ indicates tetraploid) cultivar reveals many non-reciprocal DNA exchanges between subgenomes that may have contributed to phenotypic innovation and/or other emergent properties such as ecological adaptation by polyploids. Most DNA-level novelty in G. hirsutum recombines alleles from the D-genome progenitor native to its New World habitat and the Old World A-genome progenitor in which spinnable fibre evolved. Coordinated expression changes in proximal groups of functionally distinct genes, including a nuclear mitochondrial DNA block, may account for clusters of cotton-fibre quantitative trait loci affecting diverse traits. Opportunities abound for dissecting emergent properties of other polyploids, particularly angiosperms, by comparison to diploid progenitors and outgroups.

Polyploidy is an evolutionary innovation for many animals and all flowering plants, but its impact on selection and domestication remains elusive. Here we analyze genome evolution and diversification for all five allopolyploid cotton species, including economically important Upland and Pima cottons. Although these polyploid genomes are conserved in gene content and synteny, they have diversified by subgenomic transposon exchanges that equilibrate genome size, evolutionary rate heterogeneities and positive selection between homoeologs within and among lineages. These differential evolutionary trajectories are accompanied by gene-family diversification and homoeolog expression divergence among polyploid lineages. Selection and domestication drive parallel gene expression similarities in fibers of two cultivated cottons, involving coexpression networks andN⁶-methyladenosine RNA modifications. Furthermore, polyploidy induces recombination suppression, which correlates with altered epigenetic landscapes and can be overcome by wild introgression. These genomic insights will empower efforts to manipulate genetic recombination and modify epigenetic landscapes and target genes for crop improvement.

Cotton fibres are unusually long, single-celled epidermal seed trichomes and a model for plant cell growth, but little is known about the regulation of fibre cell elongation. Here we report that a homeodomain-leucine zipper (HD-ZIP) transcription factor, GhHOX3, controls cotton fibre elongation.GhHOX3genes are localized to the 12th homoeologous chromosome set of allotetraploid cotton cultivars, associated with quantitative trait loci (QTLs) for fibre length. Silencing ofGhHOX3greatly reduces (>80%) fibre length, whereas its overexpression leads to longer fibre. Combined transcriptomic and biochemical analyses identify target genes of GhHOX3 that also contain the L1-boxcis-element, including two cell wall loosening protein genesGhRDL1andGhEXPA1. GhHOX3 interacts with GhHD1, another homeodomain protein, resulting in enhanced transcriptional activity, and with cotton DELLA, GhSLR1, repressor of the growth hormone gibberellin (GA). GhSLR1 interferes with the GhHOX3–GhHD1 interaction and represses target gene transcription. Our results uncover a novel mechanism whereby a homeodomain protein transduces GA signal to promote fibre cell elongation.

Cisandtransregulatory 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 F₁hybrids, revealing genome-wide (~15%) and often compensatorycisandtransregulatory changes under divergence and domestication. The high level oftransevolution (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 central question in evolutionary biology concerns the developmental processes by which new phenotypes arise. An exceptional example of evolutionary innovation is the single-celled seed trichome in Gossypium (“cotton fiber”). We have used fiber development in Gossypium as a system to understand how morphology can rapidly evolve. Fiber has undergone considerable morphological changes between the short, tightly adherent fibers of G. longicalyx and the derived long, spinnable fibers of its closest relative, G. herbaceum, which facilitated cotton domestication. We conducted comparative gene expression profiling across a developmental time-course of fibers from G. longicalyx and G. herbaceum using microarrays with ∼22,000 genes. Expression changes between stages were temporally protracted in G. herbaceum relative to G. longicalyx, reflecting a prolongation of the ancestral developmental program. Gene expression and GO analyses showed that many genes involved with stress responses were upregulated early in G. longicalyx fiber development. Several candidate genes upregulated in G. herbaceum have been implicated in regulating redox levels and cell elongation processes. Three genes previously shown to modulate hydrogen peroxide levels were consistently expressed in domesticated and wild cotton species with long fibers, but expression was not detected by quantitative real time-PCR in wild species with short fibers. Hydrogen peroxide is important for cell elongation, but at high concentrations it becomes toxic, activating stress processes that may lead to early onset of secondary cell wall synthesis and the end of cell elongation. These observations suggest that the evolution of long spinnable fibers in cotton was accompanied by novel expression of genes assisting in the regulation of reactive oxygen species levels. Our data suggest a model for the evolutionary origin of a novel morphology through differential gene regulation causing prolongation of an ancestral developmental program. Human domestication of plants has resulted in dramatic changes in mature structures, often over relatively short time frames. The availability of both wild and domesticated forms of domesticated species provides an opportunity to understand the genetic and developmental steps involved in domestication, thereby providing a model of how the evolutionary process shapes phenotypes. Here we use a comparative approach to explore the evolutionary innovations leading to modern cotton fiber, which represent some of the more remarkable single-celled hairs in the plant kingdom. We used microarrays assaying approximately 22,000 genes to elucidate expression differences across a developmental time-course of fibers from G. longicalyx, representing wild cotton, and G. herbaceum, a cultivated species. Expression changes between stages were temporally elongated in G. herbaceum relative to G. longicalyx, showing that domestication involved a prolongation of an ancestral developmental program. These data and quantitative real time-PCR experiments showed that long, spinnable fiber is associated with a number of genes implicated in regulating redox levels and cell elongation processes, suggesting that the evolution of spinnable cotton fiber entailed a novel metabolic regulatory program

Summary: Allopolyploidy is a prevalent process in plants, having important physiological, ecological and evolutionary consequences. Transcriptomic responses to genomic merger and doubling have been demonstrated in many allopolyploid systems, encompassing a diversity of phenomena including homoeolog expression bias, genome dominance, expression‐level dominance and revamping of co‐expression networks. Notwithstanding the foregoing, there remains a need to develop a conceptual framework that will stimulate a deeper understanding of these diverse phenomena and their mechanistic interrelationships. Here we introduce considerations relevant to this framework with a focus on cis–trans interactions among duplicated genes and alleles in hybrids and allopolyploids. By extending classic allele‐specific expression analysis to the allopolyploid level, we distinguish the distinct effects of progenitor regulatory interactions from the novel intergenomic interactions that arise from genome merger and allopolyploidization. This perspective informs experiments designed to reveal the molecular genetic basis of gene regulatory control, and will facilitate the disentangling of genetic from epigenetic and higher‐order effects that impact gene expression. Finally, we suggest that the extended cis–trans model may help conceptually unify several presently disparate hallmarks of allopolyploid evolution, including genome‐wide expression dominance and biased fractionation, and lead to a new level of understanding of phenotypic novelty accompanying polyploidy.