A chromosome-scale genome sequence of Aeonium(Aeonium arboreum 'Velour') provides novel insights into the evolution of anthocyanin synthesis

Anthocyanin glycoside is a water-soluble flavonoid compound that colors plants and aids in stress resistance. The mechanism driving the evolution of the anthocyanin synthesis pathway in plants remains unclear. Aeonium plants are highly regarded as model organisms for studying adaptive evolution. These plants can be categorized into various types, each distinguished by the content and distribution of anthocyanins in their leaves. The categories include red leaves, green leaves, black leaves, yellow leaves, and a classification known as the 'spot brocade series. In this study, we successfully assembled and annotated the genome of cultivar 'Aeonium arboreum 'Velour'' at chromosomal level. The genome size is 1,334.85 Mb containing 18 chromosomes in a single set, with a contig N50 of 23.47 Mb and a Scaffold N50 of 25.07 Mb. Through homology prediction, de novo prediction, and transcriptome prediction, we identified 166,228 coding genes, 161,656 of which were successfully annotated in the database. Comparative genomic analysis revealed that Aeonium arboreum 'Velour' underwent an independent genome-wide replication event after differentiating from Sedum album, Kalanchoe laxiflora, and Kalanchoe fedtschenkoi. It also shared a genome-wide replication event with Sedum album and Kalanchoe laxiflora. Aeonium arboreum 'Velour' exhibits a higher number of multi-copy gene families compared to other species. A total of 5,129 gene families unique to Aeonium arboreum 'Velour' were identified, primarily enriched in various metabolic pathways, including monoterpenoid biosynthesis, sesquiterpene and triterpene biosynthesis, cyanamide acid metabolism, flavonoid and flavonol biosynthesis, phosphonate and phosphinate metabolism, fatty acid degradation, biosynthesis of unsaturated fatty acid, ether lipid metabolism, tyrosine metabolism, and isoflavone biosynthesis according to the KEGG pathway analysis. Aeonium arboreum 'Velour' and Sedum album diversion dates back to approximately 43.11 million years ago during the Paleogene period, marked by the expansion of 2,807 gene families. In contrast, the divergence from Kalanchoe laxiflora and Kalanchoe fedtschenkoi began around 57.28 million years ago, with 219 gene families expanding. GO analysis highlighted that most of the expansion or contraction gene families were predominantly enriched in flower organs, leaf organ development, anthocyanin metabolism regulation, and light energy absorption and utilization. Remarkably, anthocyanin metabolism regulation is enriched to 80 expanded genes, including 36 bHLH transcription factors, possibly functioning as photosensitive pigment interaction factors (PIFs). We speculate that flavonoids play a pivotal role in the adaptation of Aeonium arboreum 'Velour' to environmental stress. Moreover, the evolution of the anthocyanin synthesis pathway is potentially driven by the plant's capability to absorb and utilize light energy, especially in high CO2 and high-temperature settings characteristic of the early Paleogene.