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Dianthus caryophyllus is an economic species often considered excellent cut flowers and is suitable for bouquets and gardens. Here, we assembled the haplotype-resolved genome of D. caryophyllus ‘Aili’ at the chromosome level for the first time. The total lengths of the two assembled haplotypes of carnation were 584.88 Mb for haplotype genome 1 (hap1) and 578.78 Mb for haplotype genome 2 (hap2), respectively. We predicted a total of 44,098 and 42,425 protein-coding genes, respectively. The remarkable structure variation was identified between two haplotypes. Moreover, we identified 403.80 Mb of transposable elements (TEs) in hap1, which accounted for 69.34% of the genome. In contrast, hap2 had 402.70 Mb of TEs, representing 69.61% of the genome. Long terminal repeats were the predominant transposable elements. Phylogenetic analysis showed that the species differentiation time between carnation and gypsophila was estimated to be ~54.43 MYA. The unique gene families of carnation genomes were identified in ‘Aili’ and previously published ‘Francesco’ and ‘Scarlet Queen’. The assembled and annotated haplotype-resolved D. caryophyllus genome not only promises to facilitate molecular biology studies but also contributes to genome-level evolutionary studies.

Carnations are one of the most popular ornamental flowers in the world with varied flower colors that have long attracted breeders and consumers alike. The differences in carnation flower color are mainly the result of the accumulation of flavonoid compounds in the petals. Anthocyanins are a type of flavonoid compound that produce richer colors. The expression of anthocyanin biosynthetic genes is mainly regulated by MYB and bHLH transcription factors. However, these TFs have not been comprehensively reported in popular carnation cultivars. Herein, 106 MYB and 125 bHLH genes were identified in the carnation genome. Gene structure and protein motif analyses show that members of the same subgroup have similar exon/intron and motif organization. Phylogenetic analysis combining the MYB and bHLH TFs from Arabidopsis thaliana separates the carnation DcaMYBs and DcabHLHs into 20 subgroups each. Gene expression (RNAseq) and phylogenetic analysis shows that DcaMYB13 in subgroup S4 and DcabHLH125 in subgroup IIIf have similar expression patterns to those of DFR, ANS, and GT/AT, which regulate anthocyanin accumulation, in the coloring of carnations, and in red-flowered and white-flowered carnations, DcaMYB13 and DcabHLH125 are likely the key genes responsible for the formation of red petals in carnations. These results lay a foundation for the study of MYB and bHLH TFs in carnations and provide valuable information for the functional verification of these genes in studies of tissue-specific regulation of anthocyanin biosynthesis.