[en] [en] BACKGROUND AND AIMS: Plant breeders are increasingly turning to crop wild relatives (CWRs) to ensure food security in a rapidly changing environment. However, CWR populations are confronted with various human-induced threats, including hybridisation with their nearby cultivated crops. This might be especially a problem for wild coffee species, which often occur near coffee cultivation areas. Here, we briefly review the evidence for wild Coffea arabica (cultivated as Arabica coffee) and Coffea canephora (cultivated as Robusta coffee) and then focussed on C. canephora in the Yangambi region in the Democratic Republic of the Congo. There, we examined the geographical distribution of cultivated C. canephora and the incidence of hybridisation between cultivated and wild individuals within the rainforest.
METHODS: We collected 71 C. canephora individuals from home gardens and 12 C. canephora individuals from the tropical rainforest in the Yangambi region and genotyped those with Genotyping-by-Sequencing (GBS). We compared those fingerprints with existing GBS data from 388 C. canephora individuals from natural tropical rainforests and the INERA Coffee Collection, a Robusta coffee field gene bank and the most likely source of cultivated genotypes in the area. We then established robust diagnostic fingerprints that genetically differentiate cultivated from wild coffee, identified cultivated-wild hybrids, and mapped their geographical position in the rainforest.
KEY RESULTS: We identified cultivated genotypes and cultivated-wild hybrids in zones with clear anthropogenic activity, and where cultivated C. canephora in the home gardens may serve as a source for crop-to-wild gene flow. We found relatively few hybrids and backcrosses in the rainforests.
CONCLUSIONS: The cultivation of C. canephora in close proximity to its wild gene pool has led to cultivated genotypes and cultivated-wild hybrids appearing within the natural habitats of C. canephora. Yet, given the high genetic similarity between the cultivated and wild gene pool, together with the relatively low incidence of hybridisation, our results indicate that the overall impact in terms of risk of introgression remains limited so far.
Disciplines :
Genetics & genetic processes
Author, co-author :
Verleysen, Lauren ✱; Division of Ecology, Evolution and Biodiversity Conservation, KU Leuven, Leuven, Belgium ; Plant Sciences Unit, Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Melle, Belgium
Depecker, Jonas ✱; Division of Ecology, Evolution and Biodiversity Conservation, KU Leuven, Leuven, Belgium ; Meise Botanic Garden, Meise, Belgium ; KU Leuven Plant Institute, Leuven, Belgium
Bollen, Robrecht; Division of Ecology, Evolution and Biodiversity Conservation, KU Leuven, Leuven, Belgium ; Meise Botanic Garden, Meise, Belgium
Asimonyio, Justin; Centre de Surveillance de la Biodiversité et Université de Kisangani, Kisangani, DR Congo
Tumaini Hatangi, Yves ; Université de Liège - ULiège > TERRA Research Centre ; Meise Botanic Garden ; University of Kisangani
Kambale, Jean-Léon; Centre de Surveillance de la Biodiversité et Université de Kisangani, Kisangani, DR Congo
Mwanga Mwanga, Ithe; Centre de Recherche en Science Naturelles, Lwiro, DR Congo
Ebele, Tshimi; Institut National des Etudes et Recherches Agronomique, Yangambi, DR Congo
Dhed'a, Benoit; Université de Kisangani, Kisangani, DR Congo
Ruttink, Tom ; Plant Sciences Unit, Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Melle, Belgium ; Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium
Vandelook, Filip; Division of Ecology, Evolution and Biodiversity Conservation, KU Leuven, Leuven, Belgium ; Meise Botanic Garden, Meise, Belgium
Honnay, Olivier; Division of Ecology, Evolution and Biodiversity Conservation, KU Leuven, Leuven, Belgium ; KU Leuven Plant Institute, Leuven, Belgium
Aerts R, Berecha G, Gijbels P, et al. 2013. Genetic variation and risks of introgression in the wild Coffea arabica gene pool in south-western Ethiopian montane rainforests. Evolutionary Applications 6: 243–252.
Anderson E, Hubricht L. 1938. Hybridization in Tradescantia. III. The evidence for introgressive hybridization. American Journal of Botany 25: 396–402.
Andrews S. 2010. FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc
Arriola PE, Ellstrand NC. 1996. Crop-to-weed gene flow in the genus Sorghum (Poaceae): spontaneous interspecific hybridization between johnsongrass, Sorghum halepense, and crop Sorghum, S. bicolor. American Journal of Botany 83: 1153–1159.
Balvanera P, Pfaff A, Viña A, et al. 2019. Global Assessment Report on Biodiversity and Ecosystem Services of the Intergovernmental Science-policy Platform on Biodiversity and Ecosystem Services, In: Brondizio ES, Settele J, Nho HT, Díaz eds, Secretariat of the Intergovernmental Science-Policy Platform for Biodiversity And Ecosystem Services, Bonn, Germany. 54–200.
Bawin Y, Ruttink T, Staelens A, et al. 2021. Phylogenomic analysis clarifies the evolutionary origin of Coffea arabica. Journal of Systematics and Evolution 59: 953–963.
Bohra A, Kilian B, Sivasankar S, et al. 2022. Reap the crop wild relatives for breeding future crops. Trends in Biotechnology 40: 412–431.
Boot W. 2013. Exploring the holy grail: Geisha Coffee, 10 years on. Roast Magazine May/June 2013: 39–49.
Brozynska M, Furtado A, Henry RJ. 2016. Genomics of crop wild relatives: expanding the gene pool for crop improvement. Plant Biotechnology Journal 14: 1070–1085.
Castañeda-Álvarez NP, Khoury CK, Achicanoy HA, et al. 2016. Global conservation priorities for crop wild relatives. Nature Plants 2: 16022.
Castro Caicedo BL, Cortina Guerrero HA, Roux J, Wingfield MJ. 2013. New coffee (Coffea arabica) genotypes derived from Coffea canephora exhibiting high levels of resistance to leaf rust and Ceratocystis canker. Tropical Plant Pathology 38: 485–494.
Charr J-C, Garavito A, Guyeux C, et al. 2020. Complex evolutionary history of coffees revealed by full plastid genomes and 28,800 nuclear SNP analyses, with particular emphasis on Coffea canephora (Robusta coffee). Molecular Phylogenetics and Evolution 151: 106906.
Coste R. 1955. Les caféiers et les cafés dans le monde. Paris: Editions Larose.
Cramer PJS. 1957. A review of literature of coffee research in Indonesia. SIC Editorial. Inter Turrialba: American Institute of Agricultural Sciences.
Craparo ACW, Van Asten PJA, Läderach P, Jassogne LTP, Grab SW. 2015. Coffea arabica yields in decline in Tanzania due to climate change: global implications. Agricultural and Forest Meteorology 207: 1–10.
Cubry P, De Bellis F, Pot D, Musoli P, Leroy T. 2013. Global analysis of Coffea canephora Pierre ex Froehner (Rubiaceae) from the Guino-Congolese region reveals impacts from climatic refuges and migration effects. Genetic Resources and Crop Evolution 60: 483–501.
Danecek P, Auton A, Abecasis G, et al; 1000 Genomes Project Analysis Group. 2011. The variant call format and VCFtools. Bioinformatics 27: 2156–2158.
Davis AP, Rakotonasolo F. 2021. Six new species of coffee (Coffea) from northern Madagascar. Kew Bulletin 76: 497–511.
Davis AP, Chadburn H, Moat J, O’Sullivan R, Hargreaves S, Lughadha EN. 2019. High extinction risk for wild coffee species and implications for coffee sector sustainability. Science Advances 5: 3473–3489.
Denoeud F, Carretero-Paulet L, Dereeper A, et al. 2014. The coffee genome provides insight into the convergent evolution of caffeine biosynthesis. Science 345: 1181–1184.
Depecker J, Asimonyio JA, Miteho R, et al. 2022. The association between rainforest disturbance and recovery, tree community composition, and community traits in the Yangambi area in the Democratic Republic of the Congo. Journal of Tropical Ecology 38: 426–436.
Depecker J, Verleysen L, Asimonyio JA, et al. 2023. Genetic diversity and structure in wild Robusta coffee (Coffea canephora A. Froehner) populations in Yangambi (DR Congo) and their relation to forest disturbance. Heredity 130: 145–153.
Doyle JJ, Doyle JL. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 11–15.
Ellstrand NC. 2003. Current knowledge of gene flow in plants: implications for transgene flow. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 358: 1163–1170.
Ellstrand NC, Prentice HC, Hancock JF. 1999. Gene flow and introgression from domesticated plants into their wild relatives. Annual Review of Ecology and Systematics 30: 539–563.
El Mousadik A, Petit RJ. 1996. High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theoretical and Applied Genetics 92: 832–839.
Elshire RJ, Glaubitz JC, Sun Q, et al. 2011. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6: e19379.
Ennslin A, Godefroid S. 2020. Ex situ cultivation impacts on plant traits and drought stress response in a multi-species experiment. Biological Conservation 248: 108630.
Ennslin A, Sandner TM, Godefroid S. 2023. Does the reduction of seed dormancy during ex situ cultivation affect the germination and establishment of plants reintroduced into the wild? Journal of Applied Ecology 60: 685–695.
Evanno G, Regnaut S, Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620.
FAO. 2018. The future of food and agriculture - Alternative pathways to 2050. Rome: FAO.
Ferrão MAG, Ferrão RG, da Fonseca AFA, Filho ACVF, Volpi PS. 2019. Origin, geographical dispersion, taxonomy and genetic diversity of Coffea canephora. In: Ferrão RG, da Fonseca AFA, Ferrão MAG, De Mune LH. eds, Conilon Coffee: the Coffea canephora produced in Brazil. Bento Ferreira: Incaper, 85–109.
Fitzpatrick BM. 2012. Estimating ancestry and heterozygosity of hybrids using molecular markers. BMC Evolutionary Biology 12: 131.
Gomez C, Despinoy M, Hamon S, et al. 2016. Shift in precipitation regime promotes interspecific hybridization of introduced Coffea species. Ecology and Evolution 6: 3240–3255.
Goudet J. 2013. hierfstat: estimation and tests of hierarchical F-statistics. R Package version 0:04–10. http://CRAN.R-project.org/package=hierfstat
Gruber B, Unmack PJ, Berry OF, Georges A. 2018. DARTR: an R package to facilitate analysis of SNP data generated from reduced representation genome sequencing. Molecular Ecology Resources 18: 691–699.
Guido Z, Knudson C, Rhiney K. 2020. Will COVID-19 be one shock too many for smallholder coffee livelihoods? World Development 136: 105172.
Ha Y-H, Oh S-H, Lee S-R. 2021. Genetic admixture in the population of wild apple (Malus sieversii) from the Tien Shan Mountains, Kazakhstan. Genes 12: 104.
Hamon P, Grover CE, Davis AP, et al. 2017. 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. Molecular Phylogenetics and Evolution 109: 351–361.
Heywood V. 2015. In situ conservation of plant species – an unattainable goal? Israel Journal of Plant Sciences 63: 211–231.
Heywood V, Casas A, Ford-Lloyd B, Kell S, Maxted N. 2007. Conservation and sustainable use of crop wild relatives. Agriculture, Ecosystems & Environment 121: 245–255.
Hufford MB, Lubinsky P, Pyhäjärvi T, Devengenzo MT, Ellstrand NC, Ross-Ibarra J. 2013. The genomic signature of crop-wild introgression in maize. PLoS Genetics 9: e1003477.
ICO 2023. Coffee market data per year. London, United Kingdom: Data provided by ICO statistical service.
Jaccard P. 1912. The distribution of the flora in the alpine zone. 1. New Phytologist 11: 37–50.
Jaureguiberry P, Titeux N, Wiemers M, et al. 2022. The direct drivers of recent global anthropogenic biodiversity loss. Science Advances 8: 1–12.
Jombart T. 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403–1405.
Kareiva P, Watts S, McDonald R, Boucher T. 2007. Domesticated nature: shaping landscapes and ecosystems for human welfare. Science 316: 1866–1869.
Kearsley E, Verbeeck H, Hufkens K, et al. 2017. Functional community structure of African monodominant Gilbertiodendron dewevrei forest influenced by local environmental filtering. Ecology and Evolution 7: 295–304.
Kiwuka C, Goudsmit E, Tournebize R, et al. 2021. Genetic diversity of native and cultivated Ugandan Robusta coffee (Coffea canephora Pierre ex A. Froehner): Climate influences, breeding potential and diversity conservation. PLoS One 16: e0245965.
Klein A-M. 2009. Nearby rainforest promotes coffee pollination by increasing spatio-temporal stability in bee species richness. Forest Ecology and Management 258: 1838–1845.
Klein A-M, Cunningham SA, Bos M, Steffan-Dewenter I. 2008. Advances in pollination ecology from tropical plantation crops. Ecology 89: 935–943.
Krishnan S. 2013. Current status of coffee genetic resources and implications for conservation. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 8: 1–9.
Krishnan S. 2014. Genetic Characterization of Geisha Coffee. Final Report. Denver, CO: Denver Botanic Gardens.
Kwit C, Moon HS, Warwick SI, Stewart CN Jr. 2011. Transgene introgression in crop relatives: molecular evidence and mitigation strategies. Trends in Biotechnology 29: 284–293.
Labouisse J-P, Cubry P, Austerlitz F, Rivallan R, Nguyen HA. 2020. New insights on spatial genetic structure and diversity of Coffea canephora (Rubiaceae) in Upper Guinea based on old herbaria. Plant Ecology and Evolution 153: 82–100.
Laikre L, Schwartz MK, Waples RS, Ryman N; GeM Working Group. 2010. Comprising genetic diversity in the wild: unmonitored large-scale release of plants and animals. Trends in Ecology & Evolution 25: 520–529.
Leroy T, De Bellis F, Legnate H, et al. 2014. Developing core collections to optimize the management and the exploitation of diversity of the coffee Coffea canephora. Genetica 142: 185–199.
Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25: 1754–1760.
Li YL, Liu JX. 2018. StructureSelector: a web-based software to select and visualize the optimal number of clusters using multiple methods. Molecular Ecology Resources 18: 176–177.
Li H, Handsaker B, Wysoker A, et al; 1000 Genome Project Data Processing Subgroup. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078–2079.
Macková L, Vít P, Urfus T. 2018. Crop-to-wild hybridization in cherries – Empirical evidence from Prunus fruticose. Evolutionary Applications 11: 1748–1759.
Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMB Net Journal 17: 10–12.
McKenna A, Hanna M, Banks E, et al. 2010. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research 20: 1297–1303.
Meilleur BA, Hodgkin T. 2004. In situ conservation of crop wild relatives: status and trends. Biodiversity and Conservation 13: 663–684.
Merot-L’anthoene V, Tournebize R, Darracq O, et al. 2019. Development and evaluation of a genome-wide Coffee 8.5K SNP array and its application for high-density genetic mapping and for investigating the origin of Coffea arabica L. Plant Biotechnology Journal 17: 1418–1430.
Mertens A, Bawin Y, Vanden Abeele S, et al. 2022. Phylogeography and conservation gaps of Musa balbisiana Colla genetic diversity revealed by microsatellite markers. Genetic Resources and Crop Evolution 69: 2515–2534.
Montagnon C, Leroy T, Eskes AB. 1998a. Amélioration variétale de Coffea canephora. I. Critères et méthodes de selection. Plantations, Recherche, Developpement 5: 18–33.
Montagnon C, Leroy T, Eskes AB. 1998b. Amélioration variétale de Coffea canephora. II. Les programmes de selection et leurs résultats. Plantations, Recherche, Developpement 5: 89–95.
Musoli P, Cubry P, Aluka P, et al. 2009. Genetic differentiation of wild and cultivated populations: diversity of Coffea canephora Pierre in Uganda. Genome 52: 634–646.
Nishio S, Takada N, Terakami S, et al. 2021. Genetic structure analysis of cultivated and wild chestnut populations reveals gene flow from cultivars to natural stands. Scientific Reports 11: 240.
Noirot M, Charrier A, Stoffelen P, Anthony F. 2016. Reproductive isolation, gene flow and speciation in the former Coffea subgenus: a review. Trees 30: 597–608.
O’Connor K, Powell M, Nock C, Shapcott A. 2015. Crop to wild gene flow and genetic diversity in a vulnerable Macademia (Proteaceae) species in New South Wales, Australia. Biological Conservation 191: 504–511.
Poland JA, Rife TW. 2012. Genotyping-by-sequencing for plant breeding and genetics. The Plant Genome 5: 92–102.
Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.
Raj A, Stephens M, Pritschard JK. 2014. fastSTRUCTURE: Variational inference of population structure in large SNP data sets. Genetics 197: 573–589.
Ridley M. 2004. Evolution. Hoboken: Blackwell Publishing.
Rodrigues CJ Jr, Bettencourt AJ, Rijo L. 1975. Races of the pathogen and resistance to coffee rust. Annual Review of Phytopathology 13: 49–70.
R Studio Team 2016. RStudio: Integrated Development for R. Boston, MA: RStudio Inc.
Saeed A, Fatima N. 2021. Wild germplasm: shaping future tomato breeding. In: Azhar, MT., Wani, SH. eds. Wild germplasm for genetic improvement in crop plants. Cambridge: Academic Press, 201–2014.
Scalabrin S, Toniutti L, Di Gaspero G, et al. 2020. A single polyploidization event at the origin of the tetraploid genome of Coffea arabica is responsible for the extremely low genetic variation in wild and cultivated germplasm. Scientific Reports 10: 4642.
Schoen DJ, Brown AHD. 2001. The conservation of wild plant species in seed banks: attention to both taxonomic coverage and population biology will improve the role of seed banks as conservation tools. BioScience 51: 960–966.
Stoffelen P. 1998. Coffea and Psilanthus (Rubiaceae) in tropical Africa: a systematic and palynological study, including a revision of the West and Central African species. PhD Thesis, KU Leuven, Belgium.
Stoffelen P, Anthony F, Janssens S, Noirot M. 2021. A new coffee species from South-West Cameroon, the principal hotspot of diversity for Coffea L. (Coffeeae, Ixoroideae, Rubiaceae) in Africa. Adansonia 43: 277–285.
Todesco M, Pascual MA, Owens GL, et al. 2016. Hybridization and extinction. Evolutionary Applications 9: 892–908.
Tournebize R, Borner L, Manel S, et al. 2022. Ecological and genomic vulnerability to climate change across native populations of Robusta coffee (Coffea canephora). Global Change Biology 28: 4124–4142.
Vanden Abeele S, Janssens SB, Asimonyio JA, et al. 2021. Genetic diversity of wild and cultivated Coffea canephora in northeastern DR Congo and the implications for conservation. American Journal of Botany 108: 2425–2434.
Verleysen L, Bollen R, Kambale J-L, et al. 2023. Characterization of the genetic composition and establishment of a core collection for the INERA Robusta coffee (Coffea canephora) field genebank from the Democratic Republic of Congo. Frontiers in Sustainable Food Systems 7: 1–33.
Verónica EM, Georgina S, Alejandro A, Leonardo G. 2017. Pattern of natural introgression in a Nothofagus hybrid zone from South American temperate forests. Tree Genetics and Genomes 13: 49.
Vi T, Vigouroux Y, Cubry P, et al. 2023. Genome-wide admixture mapping identifies wild ancestry-of-origin segments in cultivated Robusta coffee. Genome Biology and Evolution 15: 1–12.
Wambugu PW, Henry R. 2022. Supporting in situ conservation of the genetic diversity of crop wild relatives using genomics technologies. Molecular Ecology 31: 2207–2222.
Weir BS, Cockerham CC. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.
Zewdie B, Bawin Y, Tack AJM, et al. 2022. Genetic composition and diversity of Arabica coffee in the crop’s centre of origin and its impact on four major fungal diseases. Molecular Ecology 32: 2484–2503.
Zhang J, Kobert K, Flouri T, Stamatakis A. 2014. PEAR: a fast and accurate Illumina Paired-End read mergeR. Bioinformatics 30: 614–620.
Zhang H, Mittal N, Leamy LJ, Barazani O, Song B. 2017. Back into the wild - Apply untapped genetic diversity of wild relatives for crop improvement. Evolutionary Applications 10: 5–24.
