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 global affection for coffee has elevated it to one of the planet’s key commodities, supporting the livelihood of approximately 100 million coffee farmers. Despite extensive research, significant evolutionary insights into coffee, particularly its wild species, have only been unearthed in recent years. These discoveries shed light on the two primary coffee crops, Arabica (Coffea arabica) and Robusta (C. canephora), which remarkably retain characteristics closely resembling their wild counterparts. Arabica coffee, despite centuries of cultivation, and Robusta coffee, with its relatively brief cultivation history of just over a century, illustrate the dynamic journey from wild forests to global agriculture.

Recent genetic studies have unveiled geographic clusters, confirmed the monophyly of Mascarene species, and identified a monophyly for a lineage adapted to dry conditions along Madagascar's western coast. However, earlier research often lacked the resolution to definitively map relationships within and between these groups, especially for species in biodiversity-rich regions like Madagascar. The integration of Psilanthus into Coffea, following a comprehensive review by Davis et al. (2011), expanded Coffea to include 124 species (141 including taxa), spanning tropical Africa, Madagascar, the Comoros, Mauritius, the Reunion Islands, and extending to parts of Asia and Australasia. This merger, while broadening our understanding, highlighted the complexities of phylogenetic relationships within the genus.

Resolving the phylogeny of closely related lineages remains a formidable challenge in evolutionary biology. Technologies such as genotyping-by-sequencing (GBS) and restriction site associated DNA sequencing (RADseq) generate extensive sequence data across genomes, offering insights into recently diverged lineages. Coupled with bioinformatic advancements, these methods enable the detailed exploration of phylogenetic relationships at finer taxonomic levels, even in the absence of reference genomes.

Our research employs whole-genome and complete plastid genome approaches to delve into the phylogenetic intricacies of coffee. Notably, discrepancies between maternal and nuclear phylogenies of Arabica and Robusta were identified (Guyeux et al., 2019), with Arabica aligning with the Coffea clade and Robusta appearing closer to the Psilanthus clade. This divergence, previously observed but not conclusively resolved due to low support values, significantly impacts our understanding of C. canephora's evolutionary history and its relationship with other wild coffee species.

By analyzing whole plastid genome data from 52 taxa, including Coffea sensu stricto and Psilanthus, alongside multiple nuclear SNPs, we aim to reconstruct a comprehensive maternal tree, identify mutations and mutation rates within maternal phylogenetic clades, and, using the method of Matar et al. (2019), reveal the internal structure of the species set independent of known phylogenies. Constructing a nuclear tree based on 28,800 SNPs will further elucidate the complex evolutionary narrative of coffee, particularly for Coffea canephora.

Our findings suggest a more intricate evolutionary history for coffee than previously thought, prompting ongoing research into the full sequencing of the genus to unravel the detailed relationships between species and their genomic evolution patterns. This ambitious project seeks to deepen our comprehension of coffee's rich biodiversity and evolutionary intricacies, laying the groundwork for future agricultural and conservation strategies.

List of publications

The genome and population genomics of allopolyploid Coffea arabica reveal the diversification history of modern coffee cultivars. Jarkko Salojärvi, Aditi Rambani, Zhe Yu, Romain Guyot, Susan Strickler, Maud Lepelley, Cui Wang, Sitaram Rajaraman, Pasi Rastas, Chunfang Zheng, Daniella Santos Muñoz, João Meidanis, Alexandre Rossi Paschoal, Yves Bawin, Trevor Krabbenhoft, Zhen QinWang, Steven Fleck, Rudy Aussel, Laurence Bellanger, Aline Charpagne, CoralieFournier, Mohamed Kassam, Gregory Lefebvre, Sylviane Métairon, Déborah Moine, Michel Rigoreau, Jens Stolte, Perla Hamon, Emmanuel Couturon, Christine Tranchant-Dubreuil, Minakshi Mukherjee, Tianying Lan, Jan Engelhardt, Peter Stadler, Samara Mireza Correia De Lemos, Suzana Ivamoto Suzuki, Ucu Sumirat, Wai Ching Man, Nicolas Dauchot, Simon Orozco-Arias, Andrea Garavito, Catherine Kiwuka, PascalMusoli, Anne Nalukenge, Erwan Guichoux, Havinga Reinout, Martin Smit, LorenzoCarretero-Paulet, Oliveiro Guerreiro Filho, Masako Toma Braghini, Lilian Padilha, Gustavo Hiroshi Sera, Tom Ruttink, Robert Henry, Pierre Marraccini, Yves Van de Peer, Alan Andrade, Douglas Domingues, Giovanni Giuliano, Lukas Mueller, Luiz FilipePereira, Stephane Plaisance, Valerie Poncet, Stephane Rombauts, David Sankoff, Victor A. Albert, Dominique Crouzillat, Alexandre de Kochko, Patrick Descombes. bioRxiv 2023.09.06.556570; doi: 

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).