Insights into the convergent evolution of fructan biosynthesis in angiosperms from the highly characteristic chicory genome.

Abstract

Fructans in angiosperms play essential roles in physiological functions and environmental adaptations. As a major source of industrial fructans (especially inulin-type), chicory (Cichorium intybus L.) is a model species for studying fructan biosynthesis. However, the genes underlying this process and their evolutionary history in angiosperms remain elusive. We combined multiple sequencing technologies to assemble and annotate the chicory genome and scan its (epi)genomic features, such as genomic components, DNA methylation, and three-dimensional (3D) structure. We also performed a comparative genomics analysis to uncover the associations between key traits and gene families. We achieved a nearly complete chicory genome assembly and found that continuous bursts of a few highly active retrotransposon families largely shaped the (epi)genomic characteristics. The highly methylated genome with its unique 3D structure potentially influences critical biological processes. Our comprehensive comparative genomics analysis deciphered the genetic basis for the rich sesquiterpene content in chicory and indicated that the fructan-accumulating trait resulted from convergent evolution in angiosperms due to shifts in critical sites of fructan-active enzymes. The highly characterized chicory genome provides insight into Asteraceae evolution and fructan biosynthesis in angiosperms.