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Summary Replicated trait evolution can provide insights into the mechanisms underlying the evolution of biodiversity. One example of replicated evolution is the awn, an organ elaboration in grass inflorescences.Awns are likely homologous to leaf blades. We hypothesized that awns have evolved repeatedly because a conserved leaf blade developmental program is continuously activated and suppressed over the course of evolution, leading to the repeated emergence and loss of awns. To evaluate predictions arising from our hypothesis, we used ancestral state estimations, comparative genetics, anatomy, and morphology to trace awn evolution.We discovered that awned lemmas that evolved independently share similarities in developmental trajectory. In addition, in two species with independently derived awns and differing awn morphologies (Brachypodium distachyonandAlopecurus myosuroides), we found that orthologs of theYABBYtranscription factor geneDROOPING LEAFare required for awn initiation. Our analyses of awn development inBrachypodium distachyon,Alopecurus myosuroides, andHolcus lanatusalso revealed that differences in the relative expansion of awned lemma compartments can explain diversity in awn morphology at maturity.Our results show that developmental conservation can underlie replicated evolution and can potentiate the evolution of morphological diversity. 

Crop engineering and de novo domestication using gene editing are new frontiers in agriculture. However, outside of well-studied crops and model systems, prioritizing engineering targets remains challenging. Evolution can guide us, revealing genes with deeply conserved roles that have repeatedly been selected in the evolution of plant form. Homologs of the transcription factor genesGRASSY TILLERS1(GT1) andSIX-ROWED SPIKE1(VRS1) have repeatedly been targets of selection in domestication and evolution, where they repress growth in many developmental contexts. This suggests a conserved role for these genes in regulating growth repression. To test this, we determined the roles ofGT1andVRS1homologs in maize (Zea mays) and the distantly related grass brachypodium (Brachypodium distachyon) using gene editing and mutant analysis. In maize,gt1; vrs1-like1(vrl1) mutants have derepressed growth of floral organs. In addition,gt1; vrl1mutants bore more ears and more branches, indicating broad roles in growth repression. In brachypodium,Bdgt1;Bdvrl1mutants have more branches, spikelets, and flowers than wild-type plants, indicating conserved roles forGT1andVRS1homologs in growth suppression overca.59 My of grass evolution. Importantly, many of these traits influence crop productivity. Notably, maizeGT1can suppress growth in arabidopsis (Arabidopsis thaliana) floral organs, despiteca. 160 My of evolution separating the grasses and arabidopsis. Thus,GT1andVRS1maintain their potency as growth regulators across vast timescales and in distinct developmental contexts. This work highlights the power of evolution to inform gene editing in crop improvement. 

Polyploidy is a prominent mechanism of plant speciation and adaptation, yet the mechanistic understandings of duplicated gene regulation remain elusive. Chromatin structure dynamics are suggested to govern gene regulatory control. Here, we characterized genome-wide nucleosome organization and chromatin accessibility in allotetraploid cotton, Gossypium hirsutum (AADD, 2n = 4X = 52), relative to its two diploid parents (AA or DD genome) and their synthetic diploid hybrid (AD), using DNS-seq. The larger A-genome exhibited wider average nucleosome spacing in diploids, and this intergenomic difference diminished in the allopolyploid but not hybrid. Allopolyploidization also exhibited increased accessibility at promoters genome-wide and synchronized cis-regulatory motifs between subgenomes. A prominent cis-acting control was inferred for chromatin dynamics and demonstrated by transposable element removal from promoters. Linking accessibility to gene expression patterns, we found distinct regulatory effects for hybridization and later allopolyploid stages, including nuanced establishment of homoeolog expression bias and expression level dominance. Histone gene expression and nucleosome organization are coordinated through chromatin accessibility. Our study demonstrates the capability to track high-resolution chromatin structure dynamics and reveals their role in the evolution of cis-regulatory landscapes and duplicate gene expression in polyploids, illuminating regulatory ties to subgenomic asymmetry and dominance. 

Significance Floral morphology is immensely diverse. One developmental process acting to shape this diversity is growth suppression. For example, grass flowers exhibit extreme diversity in floral sexuality, arising through differential suppression of stamens or carpels. The genes regulating this growth suppression and how they have evolved remain largely unknown. We discovered that two classic developmental genes with ancient roles in controlling vegetative branching were recruited to suppress carpel development in maize. Our results highlight the power of forward genetics to reveal unpredictable genetic interactions and hidden pleiotropy of developmental genes. More broadly, our findings illustrate how ancient gene functions are recruited to new developmental contexts in the evolution of plant form. 

Abstract Baobabs (Adansonia) are a cohesive group of tropical trees with a disjunct distribution in Australia, Madagascar, and continental Africa, and diverse flowers associated with two pollination modes. We used custom-targeted sequence capture in conjunction with new and existing phylogenetic comparative methods to explore the evolution of floral traits and pollination systems while allowing for reticulate evolution. Our analyses suggest that relationships in Adansonia are confounded by reticulation, with network inference methods supporting at least one reticulation event. The best supported hypothesis involves introgression between Adansonia rubrostipa and core Longitubae, both of which are hawkmoth pollinated with yellow/red flowers, but there is also some support for introgression between the African lineage and Malagasy Brevitubae, which are both mammal-pollinated with white flowers. New comparative methods for phylogenetic networks were developed that allow maximum-likelihood inference of ancestral states and were applied to study the apparent homoplasy in floral biology and pollination mode seen in Adansonia. This analysis supports a role for introgressive hybridization in morphological evolution even in a clade with highly divergent and geographically widespread species. Our new comparative methods for discrete traits on species networks are implemented in the software PhyloNetworks. [Comparative methods; Hyb-Seq; introgression; network inference; population trees; reticulate evolution; species tree inference; targeted sequence capture.]