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 J. Krabbenhoft; Zhen Qin Wang; Steven J. Fleck; Rudy Aussel; Laurence Bellanger; Aline Charpagne; Coralie Fournier; 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; Ching Man Wai; Nicolas Dauchot; Simon Orozco-Arias; Andrea Garavito; Catherine Kiwuka; Pascal Musoli; Anne Nalukenge; Erwan Guichoux; Havinga Reinout; Martin Smit; Lorenzo Carretero-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 Filipe Pereira; Stephane Plaisance; Valerie Poncet; Stephane Rombauts; David Sankoff; Victor A. Albert; Dominique Crouzillat; Alexandre de Kochko; Patrick Descombes

doi:10.1038/s41588-024-01695-w

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 J. Krabbenhoft, Zhen Qin Wang, Steven J. Fleck, Rudy Aussel, Laurence Bellanger, Aline CharpagneCoralie Fournier, 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, Ching Man Wai, Nicolas Dauchot, Simon Orozco-Arias, Andrea Garavito, Catherine Kiwuka, Pascal Musoli, Anne Nalukenge, Erwan Guichoux, Havinga Reinout, Martin Smit, Lorenzo Carretero-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 Filipe Pereira, Stephane Plaisance, Valerie Poncet, Stephane Rombauts, David Sankoff, Victor A. Albert^*, Dominique Crouzillat^*, Alexandre de Kochko^*, Patrick Descombes^*

^*Corresponding author for this work

Biochemistry and Molecular Genetics

Research output: Contribution to journal › Article › peer-review

8 Scopus citations

Abstract

Coffea arabica, an allotetraploid hybrid of Coffea eugenioides and Coffea canephora, is the source of approximately 60% of coffee products worldwide, and its cultivated accessions have undergone several population bottlenecks. We present chromosome-level assemblies of a di-haploid C. arabica accession and modern representatives of its diploid progenitors, C. eugenioides and C. canephora. The three species exhibit largely conserved genome structures between diploid parents and descendant subgenomes, with no obvious global subgenome dominance. We find evidence for a founding polyploidy event 350,000–610,000 years ago, followed by several pre-domestication bottlenecks, resulting in narrow genetic variation. A split between wild accessions and cultivar progenitors occurred ~30.5 thousand years ago, followed by a period of migration between the two populations. Analysis of modern varieties, including lines historically introgressed with C. canephora, highlights their breeding histories and loci that may contribute to pathogen resistance, laying the groundwork for future genomics-based breeding of C. arabica.

Original language	English (US)
Pages (from-to)	721-731
Number of pages	11
Journal	Nature Genetics
Volume	56
Issue number	4
DOIs	https://doi.org/10.1038/s41588-024-01695-w
State	Published - Apr 2024

Funding

We acknowledge the Natural History Museum in London for providing a sample of the C. arabica lectotype. Funding was provided from the Academy of Finland (decisions 318288 and 329441) and a Nanyang Technological University start-up grant (J. Saloj\u00E4rvi); Ecos-Nord grant no. C21MA01 and STIC-AmSud grant no. 21-STIC-13 (R.G. and S.O.-A.); the Academy of Finland, grant no. 343656 (P.R.); NAPI Bioinform\u00E1tica from Funda\u00E7\u00E3o Arauc\u00E1ria and TELearning Project 2021\u201322 (grant no. 21-STIC-13) from STIC-AmSud (A.R.P.); Research Foundation \u2013 Flanders (FWO, grant no. G056517N) (Y.B.); the European Research Council (ERC) under the European Union\u2019s Horizon 2020 research and innovation program (grant no. 833522) and Ghent University (Methusalem funding, grant no. BOF.MET.2021.0005.01) (Y.V.d.P.); the Horizon Europe program, PRO-GRACE project (grant no. 101094738) (G.G.); INCT-Caf\u00E9-CNPq/Fapemig (A.A.); S\u00E3o Paulo State Research Foundation (FAPESP), grant nos. 2016/10896-0 and 2017/01455-2 (D.D. and S.M.C.L.); NSERC and the Canada Research Chairs programs (D.S.); the United States National Science Foundation grant nos. 1442190 and 2030871 (V.A.A.); and Nestl\u00E9 Research (P.D.). J. Saloj\u00E4rvi acknowledges the High Performance Computation Centre at NTU Singapore and University of Helsinki Linux administrators, as well as the CSC \u2013 IT Center for Science, Finland, for computational resources. R.G., P.H., E.C., C.T.D., V.P., A.d.K. and Unit\u00E9 Mixte de Recherche - Diversit\u00E9, adaptation, d\u00E9veloppement des plantes (UMR DIADE) are grateful to The French National Research Institute for Sustainable Development (IRD).

ASJC Scopus subject areas

Genetics

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Salojärvi, J., Rambani, A., Yu, Z., Guyot, R., Strickler, S., Lepelley, M., Wang, C., Rajaraman, S., Rastas, P., Zheng, C., Muñoz, D. S., Meidanis, J., Paschoal, A. R., Bawin, Y., Krabbenhoft, T. J., Wang, Z. Q., Fleck, S. J., Aussel, R., Bellanger, L., ... Descombes, P. (2024). The genome and population genomics of allopolyploid Coffea arabica reveal the diversification history of modern coffee cultivars. Nature Genetics, 56(4), 721-731. https://doi.org/10.1038/s41588-024-01695-w

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abstract = "Coffea arabica, an allotetraploid hybrid of Coffea eugenioides and Coffea canephora, is the source of approximately 60% of coffee products worldwide, and its cultivated accessions have undergone several population bottlenecks. We present chromosome-level assemblies of a di-haploid C. arabica accession and modern representatives of its diploid progenitors, C. eugenioides and C. canephora. The three species exhibit largely conserved genome structures between diploid parents and descendant subgenomes, with no obvious global subgenome dominance. We find evidence for a founding polyploidy event 350,000–610,000 years ago, followed by several pre-domestication bottlenecks, resulting in narrow genetic variation. A split between wild accessions and cultivar progenitors occurred ~30.5 thousand years ago, followed by a period of migration between the two populations. Analysis of modern varieties, including lines historically introgressed with C. canephora, highlights their breeding histories and loci that may contribute to pathogen resistance, laying the groundwork for future genomics-based breeding of C. arabica.",

author = "Jarkko Saloj{\"a}rvi and Aditi Rambani and Zhe Yu and Romain Guyot and Susan Strickler and Maud Lepelley and Cui Wang and Sitaram Rajaraman and Pasi Rastas and Chunfang Zheng and Mu{\~n}oz, {Daniella Santos} and Jo{\~a}o Meidanis and Paschoal, {Alexandre Rossi} and Yves Bawin and Krabbenhoft, {Trevor J.} and Wang, {Zhen Qin} and Fleck, {Steven J.} and Rudy Aussel and Laurence Bellanger and Aline Charpagne and Coralie Fournier and Mohamed Kassam and Gregory Lefebvre and Sylviane M{\'e}tairon and D{\'e}borah Moine and Michel Rigoreau and Jens Stolte and Perla Hamon and Emmanuel Couturon and Christine Tranchant-Dubreuil and Minakshi Mukherjee and Tianying Lan and Jan Engelhardt and Peter Stadler and {Correia De Lemos}, {Samara Mireza} and Suzuki, {Suzana Ivamoto} and Ucu Sumirat and Wai, {Ching Man} and Nicolas Dauchot and Simon Orozco-Arias and Andrea Garavito and Catherine Kiwuka and Pascal Musoli and Anne Nalukenge and Erwan Guichoux and Havinga Reinout and Martin Smit and Lorenzo Carretero-Paulet and Filho, {Oliveiro Guerreiro} and Braghini, {Masako Toma} and Lilian Padilha and Sera, {Gustavo Hiroshi} and Tom Ruttink and Robert Henry and Pierre Marraccini and {Van de Peer}, Yves and Alan Andrade and Douglas Domingues and Giovanni Giuliano and Lukas Mueller and Pereira, {Luiz Filipe} and Stephane Plaisance and Valerie Poncet and Stephane Rombauts and David Sankoff and Albert, {Victor A.} and Dominique Crouzillat and {de Kochko}, Alexandre and Patrick Descombes",

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Salojärvi, J, Rambani, A, Yu, Z, Guyot, R, Strickler, S, Lepelley, M, Wang, C, Rajaraman, S, Rastas, P, Zheng, C, Muñoz, DS, Meidanis, J, Paschoal, AR, Bawin, Y, Krabbenhoft, TJ, Wang, ZQ, Fleck, SJ, Aussel, R, Bellanger, L, Charpagne, A, Fournier, C, Kassam, M, Lefebvre, G, Métairon, S, Moine, D, Rigoreau, M, Stolte, J, Hamon, P, Couturon, E, Tranchant-Dubreuil, C, Mukherjee, M, Lan, T, Engelhardt, J, Stadler, P, Correia De Lemos, SM, Suzuki, SI, Sumirat, U, Wai, CM, Dauchot, N, Orozco-Arias, S, Garavito, A, Kiwuka, C, Musoli, P, Nalukenge, A, Guichoux, E, Reinout, H, Smit, M, Carretero-Paulet, L, Filho, OG, Braghini, MT, Padilha, L, Sera, GH, Ruttink, T, Henry, R, Marraccini, P, Van de Peer, Y, Andrade, A, Domingues, D, Giuliano, G, Mueller, L, Pereira, LF, Plaisance, S, Poncet, V, Rombauts, S, Sankoff, D, Albert, VA, Crouzillat, D, de Kochko, A & Descombes, P 2024, 'The genome and population genomics of allopolyploid Coffea arabica reveal the diversification history of modern coffee cultivars', Nature Genetics, vol. 56, no. 4, pp. 721-731. https://doi.org/10.1038/s41588-024-01695-w

TY - JOUR

T1 - The genome and population genomics of allopolyploid Coffea arabica reveal the diversification history of modern coffee cultivars

AU - Salojärvi, Jarkko

AU - Rambani, Aditi

AU - Yu, Zhe

AU - Guyot, Romain

AU - Strickler, Susan

AU - Lepelley, Maud

AU - Wang, Cui

AU - Rajaraman, Sitaram

AU - Rastas, Pasi

AU - Zheng, Chunfang

AU - Muñoz, Daniella Santos

AU - Meidanis, João

AU - Paschoal, Alexandre Rossi

AU - Bawin, Yves

AU - Krabbenhoft, Trevor J.

AU - Wang, Zhen Qin

AU - Fleck, Steven J.

AU - Aussel, Rudy

AU - Bellanger, Laurence

AU - Charpagne, Aline

AU - Fournier, Coralie

AU - Kassam, Mohamed

AU - Lefebvre, Gregory

AU - Métairon, Sylviane

AU - Moine, Déborah

AU - Rigoreau, Michel

AU - Stolte, Jens

AU - Hamon, Perla

AU - Couturon, Emmanuel

AU - Tranchant-Dubreuil, Christine

AU - Mukherjee, Minakshi

AU - Lan, Tianying

AU - Engelhardt, Jan

AU - Stadler, Peter

AU - Correia De Lemos, Samara Mireza

AU - Suzuki, Suzana Ivamoto

AU - Sumirat, Ucu

AU - Wai, Ching Man

AU - Dauchot, Nicolas

AU - Orozco-Arias, Simon

AU - Garavito, Andrea

AU - Kiwuka, Catherine

AU - Musoli, Pascal

AU - Nalukenge, Anne

AU - Guichoux, Erwan

AU - Reinout, Havinga

AU - Smit, Martin

AU - Carretero-Paulet, Lorenzo

AU - Filho, Oliveiro Guerreiro

AU - Braghini, Masako Toma

AU - Padilha, Lilian

AU - Sera, Gustavo Hiroshi

AU - Ruttink, Tom

AU - Henry, Robert

AU - Marraccini, Pierre

AU - Van de Peer, Yves

AU - Andrade, Alan

AU - Domingues, Douglas

AU - Giuliano, Giovanni

AU - Mueller, Lukas

AU - Pereira, Luiz Filipe

AU - Plaisance, Stephane

AU - Poncet, Valerie

AU - Rombauts, Stephane

AU - Sankoff, David

AU - Albert, Victor A.

AU - Crouzillat, Dominique

AU - de Kochko, Alexandre

AU - Descombes, Patrick

PY - 2024/4

Y1 - 2024/4

N2 - Coffea arabica, an allotetraploid hybrid of Coffea eugenioides and Coffea canephora, is the source of approximately 60% of coffee products worldwide, and its cultivated accessions have undergone several population bottlenecks. We present chromosome-level assemblies of a di-haploid C. arabica accession and modern representatives of its diploid progenitors, C. eugenioides and C. canephora. The three species exhibit largely conserved genome structures between diploid parents and descendant subgenomes, with no obvious global subgenome dominance. We find evidence for a founding polyploidy event 350,000–610,000 years ago, followed by several pre-domestication bottlenecks, resulting in narrow genetic variation. A split between wild accessions and cultivar progenitors occurred ~30.5 thousand years ago, followed by a period of migration between the two populations. Analysis of modern varieties, including lines historically introgressed with C. canephora, highlights their breeding histories and loci that may contribute to pathogen resistance, laying the groundwork for future genomics-based breeding of C. arabica.

AB - Coffea arabica, an allotetraploid hybrid of Coffea eugenioides and Coffea canephora, is the source of approximately 60% of coffee products worldwide, and its cultivated accessions have undergone several population bottlenecks. We present chromosome-level assemblies of a di-haploid C. arabica accession and modern representatives of its diploid progenitors, C. eugenioides and C. canephora. The three species exhibit largely conserved genome structures between diploid parents and descendant subgenomes, with no obvious global subgenome dominance. We find evidence for a founding polyploidy event 350,000–610,000 years ago, followed by several pre-domestication bottlenecks, resulting in narrow genetic variation. A split between wild accessions and cultivar progenitors occurred ~30.5 thousand years ago, followed by a period of migration between the two populations. Analysis of modern varieties, including lines historically introgressed with C. canephora, highlights their breeding histories and loci that may contribute to pathogen resistance, laying the groundwork for future genomics-based breeding of C. arabica.

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JF - Nature Genetics

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ER -

The genome and population genomics of allopolyploid Coffea arabica reveal the diversification history of modern coffee cultivars

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