Tracing the Evolutionary Dynamics and the Transcriptional Partitioning of Terpene Synthase Gene Family in Coffea arabica and Its Diploid Progenitors.

Abstract

Terpenes represent a diverse class of plant secondary metabolites that play important roles in development, ecological interactions, and aroma, and are synthesized by the terpene synthase (TPS) gene family. To investigate the evolutionary history and regulatory diversification of this family in coffee, we performed a genome-wide analysis of TPS genes in Coffea arabica and its diploid progenitors, C. canephora and C. eugenioides. Using domain-based searches targeting the PF01397 module, we identified 69 TPS genes in C. arabica, 40 in C. canephora, and 55 in C. eugenioides. Phylogenetic classification, duplication analysis, and synteny mapping revealed that the tandem duplication is the major driver of TPS expansion, with C. arabica retaining progenitor-derived copies alongside limited lineage-specific duplications. Selection analyses indicated that most TPS duplicates from C. arabica are under strong purifying constraint, while only a single orthogroup (OG0000013) showed limited evidence of episodic positive selection with a minor fraction of inferred sites and a lack of strong BEB support. Indicating that adaptive divergence was highly localized against a predominantly conserved evolutionary background. To link evolutionary divergence with transcriptional regulation, RNA-seq data from multiple tissues and developmental stages were analyzed. A substantial proportion of TPS genes were transcriptionally active and exhibited tissue- and stage-specific regulation. While many duplicates showed conserved or asymmetric expression, the OG0000013 duplicates combined localized adaptive sequence divergence with significant upregulation during late seed development. In conclusion, the retention and asymmetric transcription of progenitor-derived homeologs indicate that regulatory partitioning, rather than extensive gene-family innovation, has the dominant evolutionary outcome following allopolyploidization in C. arabica.