Coffea Evolution

picture ©Emmanuel couturon IRD

Wild coffea species db.

Above: Comparison of maternal tree with nuclear tree of Coffea species (Charr et al., 2020). Left: Ancestral state reconstruction for caffeine content showing caffeine-free ancestral coffees (Hamon et. al., 2017).

The popularity of coffee has made it one of the world’s most important commodities ( and the source of livelihood for around 100 million coffee farmers. Despite a huge body of scientific research, much of the fundamental evolutionary data relevant to coffee has been elucidated in the last decade or so. In particular, knowledge of wild coffee species has recently accelerated, including new insights into the two major crop species, Arabica (Coffea arabica) and Robusta coffee (C. canephora), which are largely unchanged from their wild forest relatives. This is still the case for Arabica coffee, despite having been in cultivation for many hundreds, if not thousands, of years. Robusta coffee has had a recent and spectacular ascendancy, having only been in general cultivation for just over 100 years.

Studies with sequence data and large sampling revealed geographic groupings, monophyly for the Mascarene species, and monophyly for a dry-adapted lineage from the western coast of Madagascar. Despite the gradual advances in phylogenetic resolution over time, previous studies failed to provide clear and robust hypotheses of relationships between and among groupings and, more generally, between species. Typically, past studies lacked strong statistical support, especially for early-diverging lineages and for species-level resolution in some geographic areas, most notably Madagascar, which is home to nearly half species of the genus. On the basis of a larger sampling of Psilanthus, and on review of morphological data, Davis et al. (2011) concluded on the systematic placement of the genus Psilanthus into Coffea, although branch support for some relationships was negligible. With the inclusion of Psilanthus, Coffea comprises 124 species (141 with taxa), with a natural distribution covering tropical Africa, Madagascar, Comoros, Mauritius and the Reunion Islands extending to southern and southeast Asia, and Australasia.

Resolving full phylogenetic relationships among recently diverged lineages is one of the greatest challenges in evolutionary biology. Genotyping-by-sequencing (GBS) and restriction site associated DNA sequencing (RADseq) are two technologies that generate sequences for a myriad of orthologous regions scattered throughout entire genomes. They offer a possible solution for phylogenetic studies of recently diverged lineages. Bioinformatic advances have been developed for these technologies, which can be used to resolve phylogenetic relationships at lower taxonomic levels without the requirement of reference genomes.

Here we present our studies on phylogenetic using whole-genome approaches and complete plastid reconstruction.

Discrepancies between maternal and nuclear phylogenies of the two main cultivated coffee species (i.e. Arabica and Robusta) were clearly identified (Guyeux et al., 2019). While Coffea arabica belongs to the Coffea clade, C. canephora, was seemingly more closely related to the Psilanthus clade. In previous works, incongruent plastid and nuclear relationships were also highlighted, but clear conclusions could not be reached mainly due to the low support values obtained for the two molecular trees (nuclear and maternal). All together, these results have an important impact on the current assumption of the evolutionary history of C. canephora as well as between the other wild coffee species.

Using whole plastid genome data for a set of 52 taxa (including Coffea s.s. and Psilanthus) combined with multiple nuclear SNPs we aimed here to address the following research objectives: (1) reconstructing a maternal tree based on complete plastid genomes, (2) characterizing each maternal phylogenetic clade through detection of highly mutated genes and gene mutation rates, (3) independently of the known phylogenetic organization, identifying the internal structure of the studied set of species according to the method of Matar et al. (2019), 4) constructing a nuclear tree based on 28,800 nuclear SNPs. Observation of discrepancies between nuclear and maternal genomes will allow us to gain a better view on the complex evolutionary history of Coffee including Coffea canephora (Robusta coffee).

All together our studies suggest that the evolutionay history is more complex than expected previously. Our current project include now the full spequencing of the genus to understend more precisely the complex relastionships between species and their patterm of genome evolution.

List of publications

Raharimalala, N., Rombauts, S., McCarthy, A. et al. The absence of the caffeine synthase gene is involved in the naturally decaffeinated status of Coffea humblotiana, a wild species from Comoro archipelago. Sci Rep 11, 8119 (2021).

Charr JC, Garavito A, Guyeux C, Crouzillat D, Descombes P, Fournier C, Ly SN, Raharimalala EN, Rakotomalala JJ, Stoffelen P, Janssens S, Hamon P, Guyot R. Complex evolutionary history of coffees revealed by full plastid genomes and 28,800 nuclear SNP analyses, with particular emphasis on Coffea canephora (Robusta coffee). Mol Phylogenet Evol. 2020 Oct;151:106906. doi: 10.1016/j.ympev.2020.106906.

Guyeux C, Charr JC, Tran HTM, Furtado A, Henry RJ, Crouzillat D, Guyot R, Hamon P. Evaluation of chloroplast genome annotation tools and application to analysis of the evolution of coffee species. PLoS One. 2019 Jun 12;14(6):e0216347. doi: 10.1371/journal.pone.0216347.

Sant'Ana GC, Pereira LFP, Pot D, Ivamoto ST, Domingues DS, Ferreira RV, Pagiatto NF, da Silva BSR, Nogueira LM, Kitzberger CSG, Scholz MBS, de Oliveira FF, Sera GH, Padilha L, Labouisse JP, Guyot R, Charmetant P, Leroy T. Genome-wide association study reveals candidate genes influencing lipids and diterpenes contents in Coffea arabica L. Sci Rep. 2018 Jan 11;8(1):465. doi: 10.1038/s41598-017-18800-1.

Hamon P, Grover CE, Davis AP, Rakotomalala JJ, Raharimalala NE, Albert VA, Sreenath HL, Stoffelen P, Mitchell SE, Couturon E, Hamon S, de Kochko A, Crouzillat D, Rigoreau M, Sumirat U, Akaffou S, Guyot R. Genotyping-by-sequencing provides the first well-resolved phylogeny for coffee (Coffea) and insights into the evolution of caffeine content in its species: GBS coffee phylogeny and the evolution of caffeine content. Mol Phylogenet Evol. 2017 Apr;109:351-361. doi: 10.1016/j.ympev.2017.02.009.

Guyot R, Darré T, Dupeyron M, de Kochko A, Hamon S, Couturon E, Crouzillat D, Rigoreau M, Rakotomalala JJ, Raharimalala NE, Akaffou SD, Hamon P. Partial sequencing reveals the transposable element composition of Coffea genomes and provides evidence for distinct evolutionary stories. Mol Genet Genomics. 2016 Oct;291(5):1979-90. doi: 10.1007/s00438-016-1235-7.

Denoeud F, Carretero-Paulet L, Dereeper A, Droc G, Guyot R, Pietrella M, Zheng C, Alberti A, Anthony F, Aprea G, Aury JM, Bento P, Bernard M, Bocs S, Campa C, Cenci A, Combes MC, Crouzillat D, Da Silva C, Daddiego L, De Bellis F, Dussert S, Garsmeur O, Gayraud T, Guignon V, Jahn K, Jamilloux V, Joët T, Labadie K, Lan T, Leclercq J, Lepelley M, Leroy T, Li LT, Librado P, Lopez L, Muñoz A, Noel B, Pallavicini A, Perrotta G, Poncet V, Pot D, Priyono, Rigoreau M, Rouard M, Rozas J, Tranchant-Dubreuil C, VanBuren R, Zhang Q, Andrade AC, Argout X, Bertrand B, de Kochko A, Graziosi G, Henry RJ, Jayarama, Ming R, Nagai C, Rounsley S, Sankoff D, Giuliano G, Albert VA, Wincker P, Lashermes P. The coffee genome provides insight into the convergent evolution of caffeine biosynthesis. Science. 2014 Sep 5;345(6201):1181-4. doi: 10.1126/science.1255274.

Dereeper A, Guyot R, Tranchant-Dubreuil C, Anthony F, Argout X, de Bellis F, Combes MC, Gavory F, de Kochko A, Kudrna D, Leroy T, Poulain J, Rondeau M, Song X, Wing R, Lashermes P. BAC-end sequences analysis provides first insights into coffee (Coffea canephora P.) genome composition and evolution. Plant Mol Biol. 2013 Oct;83(3):177-89. doi: 10.1007/s11103-013-0077-5. Epub 2013 May 25. PMID: 23708951.

Razafinarivo, N.J., Rakotomalala, JJ., Brown, S.C. et al. Geographical gradients in the genome size variation of wild coffee trees (Coffea) native to Africa and Indian Ocean islands. Tree Genetics & Genomes 8, 1345–1358 (2012).

Yu Q, Guyot R, de Kochko A, Byers A, Navajas-Pérez R, Langston BJ, Dubreuil-Tranchant C, Paterson AH, Poncet V, Nagai C, Ming R. Micro-collinearity and genome evolution in the vicinity of an ethylene receptor gene of cultivated diploid and allotetraploid coffee species (Coffea). Plant J. 2011 Jul;67(2):305-17. doi: 10.1111/j.1365-313X.2011.04590.x.

Guyot, R., de la Mare, M., Viader, V. et al. Microcollinearity in an ethylene receptor coding gene region of the Coffea canephora genome is extensively conserved with Vitis vinifera and other distant dicotyledonous sequenced genomes. BMC Plant Biol 9, 22 (2009).