Abstract
Although coffee leaf rust (CLR), caused by Hemileia vastatrix, poses an increasing threat to coffee production in Ethiopia, little is known regarding its genetic diversity and structure and how these are affected by coffee management. Here, we used genetic fingerprinting based on sequence-related amplified polymorphism (SRAP) markers to genotype H. vastatrix samples from different coffee shrubs, across 40 sites, covering four coffee production systems (forest coffee, semi plantation coffee, home garden coffee, and plantation coffee) and different altitudes in Ethiopia. In total, 96 H. vastatrix samples were successfully genotyped with three primer combinations, producing a total of 79 scorable bands. We found 35.44% of amplified bands to be polymorphic, and the polymorphic information content (PIC) was 0.45, suggesting high genetic diversity among our CLR isolates. We also found significant isolation-by-distance across the samples investigated and detected significant differences in fungal genetic composition among plantation coffee and home garden coffee and a marginally significant difference among plantation coffee and forest coffee. Furthermore, we found a significant effect of altitude on CLR genetic composition in the forest coffee and plantation systems. Our results suggest that both spore dispersal and different selection pressures in the different coffee management systems are likely responsible for the observed high genetic diversity and genetic structure of CLR isolates in Ethiopia. When selecting Ethiopian coffee genotypes for crop improvement, it is important that these genotypes carry some resistance against CLR. Because our study shows large variation in genetic composition across relatively short geographical distances, a broad selection of rust isolates must be used for coffee resistance screening.
Similar content being viewed by others
Data availability
Data will be made available on request.
References
Aerts R, Geeraert L, Berecha G, Hundera K, Muys B, De Kort H, Honnay O (2017) Conserving wild Arabica coffee: emerging threats and opportunities. Agr Ecosyst Environ 237:75–79. https://doi.org/10.1016/j.agee.2016.12.023
Arneson PA (2000) Coffee rust. The Plant Health Instr. https://doi.org/10.1094/PHI-I-2000-0718-02
Bebber DP, Holmes T, Gurr SJ (2014) The global spread of crop pests and pathogens. Glob Ecol Biogeogr 23(12):1398–1407. https://doi.org/10.1111/geb.12214
Bekele KB, Senbeta GA, Garedew W, Caixeta ET, Ramírez-Camejo LA, Aime MC (2022) Genetic diversity and population structure of Hemileia vastatrix from Ethiopian Arabica coffee. Arch Phytopathol Plant Protect 55(13):1483–1503. https://doi.org/10.1080/03235408.2021.1983385
Cabral PGC, Maciel Zambolim E, Oliveira SAS, Caixeta ET, Zambolim L (2016) Genetic diversity and structure of Hemileia vastatrix populations on Coffea spp. Plant Pathol 65(2):196–204. https://doi.org/10.1111/ppa.12411
Carvalho CR, Fernandes RC, Carvalho GMA, Barreto RW, Evans HC (2011) Cryptosexuality and the genetic diversity paradox in coffee rust, Hemileia vastatrix. Plos One 6(11):e26387. https://doi.org/10.1371/journal.pone.0026387
Ciola V, Cipollini D (2011) Distribution and host range of a powdery mildew fungus infecting garlic mustard, Alliaria petiolata, in southwestern Ohio. Am Midl Nat 166(1):40–52. https://doi.org/10.1674/0003-0031-166.1.40
Daba G, Helsen K, Berecha G, Lievens B, Debela A, Honnay O (2019) Seasonal and altitudinal differences in coffee leaf rust epidemics on coffee berry disease-resistant varieties in Southwest Ethiopia. Trop Plant Pathol 44(3):244–250. https://doi.org/10.1007/s40858-018-0271-8
Daba G, Berecha G, Lievens B, Hundera K, Helsen K, Honnay O (2022) Contrasting coffee leaf rust epidemics between forest coffee and semi-forest coffee agroforestry systems in SW-Ethiopia. Heliyon 8(12):e11892. https://doi.org/10.1016/j.heliyon.2022.e11892
Davis AP, Wilkinson T, Challa ZK, Williams J, Baena S, Gole TW, Moat J (2018) Coffee atlas of Ethiopia. Royal Botanic Gardens, Kew Publishing (UK)
de Resende ML, Pozza EA, Reichel T, Botelho D (2021) Strategies for coffee leaf rust management in organic crop systems. Agronomy 11(9):1865. https://doi.org/10.3390/agronomy11091865
FAOSTAT (2021) Food and Agriculture Organization of the United Nations. http://www.fao.org/faostat/en/#data/QC. Accessed 12 July 2021
Geeraert L, Aerts R, Jordaens K, Dox I, Wellens S, Couri M, Berecha G, Honnay O (2019) Intensification of Ethiopian coffee agroforestry drives impoverishment of the Arabica coffee flower visiting bee and fly communities. Agrofor Syst 93(5):1729–1739. https://doi.org/10.1007/s10457-018-0280-0
Geleta TD, Dadi DK, Funk C, Garedew W, Eyelade D, Worku A (2022) Downscaled climate change projections in urban centers of Southwest Ethiopia using CORDEX Africa simulations. Climate 10(10):158. https://doi.org/10.3390/cli10100158
Gemeda DO, Korecha D, Garedew W (2022) Monitoring climate extremes using standardized evapotranspiration index and future projection of rainfall and temperature in the wettest parts of southwest Ethiopia. Environ Challenges 7:100517. https://doi.org/10.1016/j.envc.2022.100517
Gichuru E, Alwora G, Gimase J, Kathurima C (2021) Coffee leaf rust (Hemileia vastatrix) in Kenya- a review. Agronomy 11(12):2590. https://doi.org/10.3390/agronomy11122590
Gole TW, Borsch T, Denich M, Teketay D (2008) Floristic composition and environmental factors characterizing coffee forests in southwest Ethiopia. For Ecol Manage 255(7):2138–2150. https://doi.org/10.1016/j.foreco.2007.12.028
Goss EM, Kendig AE, Adhikari A, Lane B, Kortessis N, Holt RD, Clay K, Harmon PF, Flory SL (2020) Disease in invasive plant populations. Annu Rev Phytopathol 58:97–117. https://doi.org/10.1146/annurev-phyto-010820-012757
Gouveia MMC, Ribeiro A, Várzea VM, Rodrigues CJ Jr (2005) Genetic diversity in Hemileia vastatrix based on RAPD markers. Mycologia 97(2):396–404. https://doi.org/10.1080/15572536.2006.11832815
Hiatt D, Flory SL (2020) Populations of a widespread invader and co-occurring native species vary in phenotypic plasticity. New Phytol 225(1):584–594. https://doi.org/10.1111/nph.16225
Hoffmann J (2014) The World Atlas of Coffee: from beans to brewing–coffees explored. Firefly Books, Richmond Hill, ON, Canada, Explained and Enjoyed
Hundera K, Aerts R, Fontaine A, Van Mechelen M, Gijbels P, Honnay O, Muys B (2013) Effects of coffee management intensity on composition, structure, and regeneration status of Ethiopian moist evergreen afromontane forests. Environ Manage 51(3):801–809. https://doi.org/10.1007/s00267-012-9976-5
Jibat M (2020) Review on resistance breeding methods of coffee leaf rust in Ethiopia. Int J Res Agric For 7(6):32–41. https://www.ijraf.org/papers/v7-i6/4.pdf
Kosaraju B, Sannasi S, Mishra MK, Subramani D, Bychappa M (2017) Assessment of genetic diversity of coffee leaf rust pathogen Hemileia vastatrix using SRAP markers. J Phytopathol 165(7–8):486–493. https://doi.org/10.1111/jph.12583
Koutouleas A (2023) Coffee leaf rust: wreaking havoc in coffee production areas across the tropics. Plant Health Cases. Department of Geosciences and Natural Resource Management University of Copenhagen, Copenhagen, Denmark. https://doi.org/10.1079/Planthealthcases.2023.0005
Kushalappa AC, Eskes AB (1989) Advances in coffee rust research. Ann Rev Phytopathol 27(1):503–531
Labouisse JP, Bellachew B, Kotecha S, Bertrand B (2008) Current status of coffee (Coffea arabica L.) genetic resources in Ethiopia: implications for conservation. Genet Resour Crop Evol 55:1079–1093. https://doi.org/10.1007/s10722-008-9361-7
Maia TA, Maciel-Zambolim E, Caixeta ET, Mizubuti ESG, Zambolim L (2013) The population structure of Hemileia vastatrix in Brazil inferred from AFLP. Australas Plant Pathol 42(5):533–542. https://doi.org/10.1007/s13313-013-0213-3
Merle I, Pico J, Granados E, Boudrot A, Tixier P, de Melo Virginio Filho E, Cilas C, Avelino J (2020) Unraveling the complexity of coffee leaf rust behavior and development in different Coffea arabica agro-ecosystems. Phytopathology 110(2):418–427. https://doi.org/10.1094/PHYTO-03-19-0094-R
Mikaberidze A, McDonald BA, Bonhoeffer S (2015) Developing smarter host mixtures to control plant disease. Plant Pathol 64(4):996–1004. https://doi.org/10.1111/ppa.12321
Moat J, Gole TW, Davis AP (2019) Least concern to endangered: applying climate change projections profoundly influences the extinction risk assessment for wild Arabica coffee. Glob Change Biol 25(2):390–403. https://doi.org/10.1111/gcb.14341
Nunes CC, Maffia LA, Mizubuti ESG, Brommonschenkel SH, Silva JC (2009) Genetic diversity of populations of Hemileia vastatrix from organic and conventional coffee plantations in Brazil. Australas Plant Pathol 38(5):445–452. https://doi.org/10.1071/AP09021
Oksanen J, Blanchet FG, Minchin PR, O’Hara RB, Simpson GL, Soly-Mos P, Henry M, Stevens H, Szoecs E, Wagner H (2016) Vegan: community ecology package. https://cran.r-project.org/web/packages/vegan/index.html
Prevost A, Wilkinson MJ (1999) A new system of comparing PCR primers applied to ISSR fingerprinting of potato cultivars. Theor Appl Genet 98(1):107–112. https://doi.org/10.1007/s001220051046
Quispe-Apaza C, Mansilla-Samaniego R, Espejo-Joya R, Bernacchia G, Yabar-Larios M, López-Bonilla C (2021) Spatial and temporal genetic diversity and population structure of hemileia vastatrix from peruvian coffee plantations. Plant Pathol J 37(3):280. https://doi.org/10.5423/PPJ.OA.10.2020.0192
R Core Team (2021) R: a language and environment for statistical computing. https://www.r-project.org/
Ramírez-Camejo LA, Keith LM, Matsumoto T, Sugiyama L, Fukada M, Brann M, Moffitt A, Liu J, Aime MC (2022) Coffee leaf rust (Hemileia vastatrix) from the recent invasion into Hawaii shares a genotypic relationship with Latin American populations. J Fungi 8(2):89. https://doi.org/10.3390/jof8020189
Rhiney K, Guido Z, Knudson C, Avelino J, Bacon CM, Leclerc G, Aime MC, Bebber DP (2021) Epidemics and the future of coffee production. Proc Natl Acad Sci 118(27):281–289. https://doi.org/10.1073/pnas.2023212118
Rieux A, Lapeyre De, de Bellaire L, Zapater MF, Ravigné V, Carlier J (2013) Recent range expansion and agricultural landscape heterogeneity have only minimal effect on the spatial genetic structure of the plant pathogenic fungus Mycosphaerella fijiensis. Heredity 110(1):29–38. https://doi.org/10.1038/hdy.2012.55
Rieux A, Soubeyrand S, Bonnot F, Klein EK, Ngando JE, Mehl A, Ravigne V, Carlier J, Lapeyre De, de Bellaire L (2014) Long-distance wind-dispersal of spores in a fungal plant pathogen: estimation of anisotropic dispersal kernels from an extensive field experiment. Plos One 9(8):e103225. https://doi.org/10.1371/journal.pone.0103225
Ritschel A, Oberwinkler F, Berndt R (2005) Desmosorus, a new rust genus (Uredinales). Mycol Prog 4(4):333–338. https://doi.org/10.1007/s11557-006-0138-0
Rodrigues AS, Silva DN, Várzea V, Paulo OS, Batista D (2022) Worldwide population structure of the coffee rust fungus Hemileia vastatrix is strongly shaped by local adaptation and breeding history. Phytopathology. https://doi.org/10.1094/PHYTO-09-21-0376-R
Rozo Y, Escobar C, Gaitán Á, Cristancho M (2012) Aggressiveness and genetic diversity of Hemileia vastatrix during an epidemic in Colombia. J Phytopathol 160(11–12):732–740. https://doi.org/10.1111/jph.12024
Santana MF, Zambolim EM, Caixeta ET, Zambolim L (2018) Population genetic structure of the coffee pathogen Hemileia vastatrix in Minas Gerais. Brazil Trop Plant Pathol 43(5):473–476. https://doi.org/10.1007/s40858-018-0246-9
Serrote CML, Reiniger LRS, Silva KB, dos Santos Rabaiolli SM, Stefanel CM (2020) Determining the polymorphism information content of a molecular marker. Gene 726:144175. https://doi.org/10.1016/j.gene.2019.144175
Silva DN, Várzea V, Paulo OS, Batista D (2018) Population genomic footprints of host adaptation, introgression and recombination in coffee leaf rust. Mol Plant Pathol 19(7):1742–1753. https://doi.org/10.1111/mpp.12657
Silva MDC, Guerra-Guimarães L, Diniz I, Loureiro A, Azinheira H, Pereira AP, Tavares S, Batista D, Várzea V (2022) An overview of the mechanisms involved in coffee-Hemileia vastatrix interactions: plant and pathogen perspectives. Agronomy 12(2):326. https://doi.org/10.3390/agronomy12020326
Singh BK, Delgado-Baquerizo M, Egidi E, Guirado E, Leach JE, Liu H, Trivedi P (2023) Climate change impacts on plant pathogens, food security and paths forward. Nat Rev Microbiol 1–17. https://doi.org/10.1038/s41579-023-00900-7
Stukenbrock EH, McDonald BA (2008) The origins of plant pathogens in agro-ecosystems. Annu Rev Phytopathol 46:75–100. https://doi.org/10.1146/annurev.phyto.010708.154114
Teketay D (1999) History, botany and ecological requirements of coffee. Walia 20:28–50. https://doi.org/10.10520/AJA00837059_213
Waller JM, Bigger M, Hillocks RJ (2007) Coffee pests, diseases and their management. CABI, Wallingford, Oxon, UK
Acknowledgements
We are grateful to all farm owners in the Gera, Goma, and Mana districts to allow us to work in the different coffee production systems studied and to provide us with all the necessary information during the field work. Furthermore, we thankfully acknowledge Wendimu Bekele, Freweyni Michael, Dinkina Mijena, Nezif Yesuf, Miressa Raji, and Nasir Abba Macca for their help during sample collection and artificial fungal inoculation in the greenhouses at Jimma University College of Agriculture and Veterinary Medicine (JUCAVM). We also gratefully acknowledge Ethiopian Biodiversity Institute (EBI) for permitting material transfer of our coffee leaf rust spore samples with (Ref. No. EBI 71/300086/2018) for genetic diversity analysis at KU Leuven, Belgium
Funding
This work was supported by VLIR-UOS, the Institutional University Cooperation program between Katholieke Universiteit Leuven and Jimma University.
Author information
Authors and Affiliations
Contributions
Gerba Daba, Gezahegn Berecha, Bart Lievens, and Olivier Honnay designed the study. Gerba Daba performed the field work. Gerba Daba, Bart Lievens, and Olivier Honnay led the writing of the manuscript. Robin Daelemans and Gerba Daba performed the statistical analyses. Margot W. J. Geerinck, Christel Verreth, and Sam Crauwels performed the molecular analysis, including data analysis. All authors contributed to the data interpretation and to the drafts of this manuscript and approved publication of the final manuscript.
Corresponding author
Ethics declarations
Ethics approval
Our data do not contain any studies involving human participants or animals.
Consent to participate
All authors read and approved the manuscript.
Consent for publication
All authors read and approved the manuscript.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Daba, G., Daelemans, R., Berecha, G. et al. Genetic diversity and structure of the coffee leaf rust fungus Hemileia vastatrix across different coffee management systems in Ethiopia. Int Microbiol 27, 525–534 (2024). https://doi.org/10.1007/s10123-023-00409-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10123-023-00409-2