The Role of Lineage-Specific Gene Family Expansions in Coffee Adaptation: The Case of N-Methyltransferases Involved in Caffeine Biosynthesis

Date: Sunday, January 12, 2014
Time: 5:40 PM
Room: Pacific Salon 4-5 (2nd Floor)
Victor A. Albert , University at Buffalo, Buffalo, NY
Pablo Librado , Universitat de Barcelona, Barcelona, Spain
Christine Tranchant-Dubreuil , IRD UMR DIADE, Montpellier, France
Valerie Poncet , IRD UMR DIADE, Montpellier cedex 5, France
Alexandre de Kochko , IRD UMR DIADE, Montpellier, France
Julio Rozas , Universitat de Barcelona, Barcelona, Spain
Lorenzo Carretero-Paulet , University of Buffalo, Buffalo, NY
Using the new Coffea canephora genome sequence, we examined lineage-specific gene family expansions with potential adaptive value for coffee. We fit two different branch models implemented in the likelihood program BadiRate to 16,917 orthogroups identified in genome-wide comparisons with Arabidopsis, grape and tomato: i) a branch model accounting for coffee-specific expansions in size, and ii) a global ratio model, indicating stable sizes among species. To identify gene functions that may have played special roles during coffee evolution, we statistically examined differential representations of GO terms among expanded orthogroups. 98 out of 4,269 generic GO terms were differentially distributed, mostly corresponding to two main functional categories: defense response (including NBS and R genes) and metabolic process, the latter including different catalytic activities involved in secondary compound synthesis, e.g. flavonoids, terpenoids, phenylpropanoids or alkaloids. Particularly noteworthy was the enrichment in N-methyltransferases (NMTs), the main enzymes involved in the biosynthesis of caffeine, a purine alkaloid accumulated in coffee beans and the most characteristic secondary metabolite of the coffee plant. Phylogenetic analysis of 23 coffee NMTs together with NMTs from cacao and different tea species, including those known to be involved in caffeine biosynthesis, revealed the occurrence of four clades: caffeine biosynthetic NMTs are nested within three species-specific clades, while a fourth clade in coffee includes previously unreported NMTs. Selection analyses in these different NMT clades discounts the possibility of parallel molecular adaptations. Microsynteny analyses permitted unraveling the role of tandem duplications in the expansion of the coffee NMT gene family. Taken as a whole, these results indicate the independent acquisition of caffeine biosynthesis in all three caffeine producing plant species examined, providing an outstanding example of convergent evolution of secondary metabolic pathways followed by coffee-specific gene family expansions through tandem duplication.