Adaptive potential of Coffea canephora from Uganda in response to climate change.
candidate genes
climate change
environmental association
landscape genomics
target capture
wild coffee
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
03 2022
03 2022
Historique:
revised:
12
11
2021
received:
26
04
2021
accepted:
06
01
2022
pubmed:
22
1
2022
medline:
22
3
2022
entrez:
21
1
2022
Statut:
ppublish
Résumé
Understanding vulnerabilities of plant populations to climate change could help preserve their biodiversity and reveal new elite parents for future breeding programmes. To this end, landscape genomics is a useful approach for assessing putative adaptations to future climatic conditions, especially in long-lived species such as trees. We conducted a population genomics study of 207 Coffea canephora trees from seven forests along different climate gradients in Uganda. For this, we sequenced 323 candidate genes involved in key metabolic and defence pathways in coffee. Seventy-one single nucleotide polymorphisms (SNPs) were found to be significantly associated with bioclimatic variables, and were thereby considered as putatively adaptive loci. These SNPs were linked to key candidate genes, including transcription factors, like DREB-like and MYB family genes controlling plant responses to abiotic stresses, as well as other genes of organoleptic interest, such as the DXMT gene involved in caffeine biosynthesis and a putative pest repellent. These climate-associated genetic markers were used to compute genetic offsets, predicting population responses to future climatic conditions based on local climate change forecasts. Using these measures of maladaptation to future conditions, substantial levels of genetic differentiation between present and future diversity were estimated for all populations and scenarios considered. The populations from the forests Zoka and Budongo, in the northernmost zone of Uganda, appeared to have the lowest genetic offsets under all predicted climate change patterns, while populations from Kalangala and Mabira, in the Lake Victoria region, exhibited the highest genetic offsets. The potential of these findings in terms of ex situ conservation strategies are discussed.
Substances chimiques
Genetic Markers
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1800-1819Informations de copyright
© 2022 John Wiley & Sons Ltd.
Références
Aitken, S. N., Yeaman, S., Holliday, J. A., Wang, T., & Curtis-McLane, S. (2008). Adaptation, migration or extirpation: Climate change outcomes for tree populations. Evolutionary Applications, 1, 95-111. https://doi.org/10.1111/j.1752-4571.2007.00013.x
Alberto, F. J., Aitken, S. N., Alía, R., González-Martínez, S. C., Hänninen, H., Kremer, A., Lefèvre, F., Lenormand, T., Yeaman, S., Whetten, R., & Savolainen, O. (2013). Potential for evolutionary responses to climate change - evidence from tree populations. Global Change Biology, 19, 1645-1661. https://doi.org/10.1111/gcb.12181
Aluka, P. (2013). Genetic and phenotypic diversity of cultivated Robusta coffee (Coffea canephora Pierre) in Uganda and effect of environmental factors on quality. PhD dissertation. University of Nairobi, Kenya. http://thesisbank.jhia.ac.ke/718/
Alves, G. S. C. (2015). Characterization of a candidate gene for drought tolerance in Coffea: the CcDREB1D gene, in contrasting genotypes of Coffea canephora and related species. PhD dissertation, Montpellier SupAgro, France. https://www.supagro.fr/theses/extranet/15-0002_Costa_Alvez.pdf
Alves, G. S. C., Torres, L. F., de Aquino, S. O., Reichel, T., Freire, L. P., Vieira, N. G., Vinecky, F., This, D., Pot, D., Etienne, H., Paiva, L. V., Marraccini, P., & Andrade, A. C. (2018). Nucleotide diversity of the coding and promoter regions of DREB1D, a candidate gene for drought tolerance in Coffea species. Tropical Plant Biology, 11, 31-48. https://doi.org/10.1007/s12042-018-9199-x
Alves, G. S. C., Torres, L. F., Déchamp, E., Breitler, J.-C., Joët, T., Gatineau, F., Andrade, A. C., Bertrand, B., Marraccini, P., & Etienne, H. (2017). Differential fine-tuning of gene expression regulation in coffee leaves by CcDREB1D promoter haplotypes under water deficit. Journal of Experimental Botany, 68, 3017-3031. https://doi.org/10.1093/jxb/erx166
Ashihara, H., Mizuno, K., Yokota, T., & Crozier, A. (2017). Xanthine alkaloids: Occurrence, biosynthesis, and function in plants. In A. D. Kinghorn, H. Falk, S. Gibbons, & J. Kobayashi (Eds.), Progress in the chemistry of organic natural products 105 (pp. 1-88). Springer International Publishing. https://doi.org/10.1007/978-3-319-49712-9_1
Barbosa, A. M., Brown, J. A., Jimenez-Valverde, A., & Real, R. (2016). modEvA: Model evaluation and analysis. R package version 1.3.2. https://CRAN.R-project.org/package=modEvA
Barrett, R. D. H., & Schluter, D. (2008). Adaptation from standing genetic variation. Trends in Ecology & Evolution, 23, 38-44. https://doi.org/10.1016/j.tree.2007.09.008
Basalirwa, C. P. K. (1995). Delineation of Uganda into climatological rainfall zones using the method of principal component analysis. International Journal of Climatology, 15, 1161-1177. https://doi.org/10.1002/joc.3370151008
Bay, R. A., Harrigan, R. J., Underwood, V. L., Gibbs, H. L., Smith, T. B., & Ruegg, K. (2018). Genomic signals of selection predict climate-driven population declines in a migratory bird. Science, 359, 83-86. https://doi.org/10.1126/science.aan4380
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Methodological), 57(1), 289-300.
Berthaud, J., & Charrier, A. (1988). Genetic resources of Coffea. In R. J. Clarke, & R. Macrae (Eds.), Coffee: Agronomy (Vol. 4, pp. 1-42). Elsevier Applied Science Publishers.
Bongers, F. J., Olmo, M., Lopez-Iglesias, B., Anten, N. P. R., & Villar, R. (2017). Drought responses, phenotypic plasticity and survival of Mediterranean species in two different microclimatic sites. Plant Biology, 19(3), 386-395. https://doi.org/10.1111/plb.12544
Bunn, C., Läderach, P., Ovalle Rivera, O., & Kirschke, D. (2015). A bitter cup: Climate change profile of global production of Arabica and Robusta coffee. Climate Change, 129, 89-101. https://doi.org/10.1007/s10584-014-1306-x
Bunn, C., Läderach, P., Pérez Jimenez, J. G., Montagnon, C., & Schilling, T. (2015). Multiclass classification of agro-ecological zones for Arabica coffee: An improved understanding of the impacts of climate change. PLoS One, 10, e0140490. https://doi.org/10.1371/journal.pone.0140490
Capblancq, T., Fitzpatrick, M., Bay, R., Exposito-Alonso, M., & Keller, S. (2020). Genomic prediction of (mal)adaptation across current and future climatic landscapes. Annual Review of Ecology, Evolution, and Systematics, 51, 245-269. https://doi.org/10.1146/annurev-ecolsys-020720-042553
Caye, K., Jumentier, B., Lepeule, J., & François, O. (2019). LFMM 2: Fast and accurate inference of gene-environment associations in genome-wide studies. Molecular Biology and Evolution, 36, 852-860. https://doi.org/10.1093/molbev/msz008
Christmas, M. J., Biffin, E., Breed, M. F., & Lowe, A. J. (2016). Finding needles in a genomic haystack: Targeted capture identifies clear signatures of selection in a nonmodel plant species. Molecular Ecology, 25, 4216-4233. https://doi.org/10.1111/mec.13750
Christmas, M. J., Breed, M. F., & Lowe, A. J. (2016). Constraints to and conservation implications for climate change adaptation in plants. Conservation Genetics, 17, 305-320. https://doi.org/10.1007/s10592-015-0782-5
Costa, T. S. (2014). Análise do perfil transcriptômico e proteômico de raízes de diferentes clones de Coffea canephora em condições de déficit hídrico. PhD dissertation, Federal University of Lavras, Brazil.https://tel.archives-ouvertes.fr/tel-02008137/document
Cotta, M. G. (2017). Molecular mechanisms in the first step of ABA-mediated response in Coffea ssp. (pp. 176). PhD Thesis, Montpellier SupAgro, France.
Cronn, R., Knaus, B. J., Liston, A., Maughan, P. J., Parks, M., Syring, J. V., & Udall, J. (2012). Targeted enrichment strategies for next-generation plant biology. American Journal of Botany, 99, 291-311. https://doi.org/10.3732/ajb.1100356
Cubry, P., De Bellis, F., Pot, D., Musoli, P., & Leroy, T. (2013). Global analysis of Coffea canephora Pierre ex Froehner (Rubiaceae) from the Guineo-Congolese region reveals impacts from climatic refuges and migration effects. Genetic Resources and Crop Evolution, 60, 483-501. https://doi.org/10.1007/s10722-012-9851-5
DaMatta, F. M., & Ramalho, J. C. (2006). Impact of drought and temperature stress on coffee physiology and production: a review. Brazilian Journal of Plant Physiology, 18, 55-81. https://doi.org/10.1590/S1677-04202006000100006
Danecek, P., Auton, A., Abecasis, G., Albers, C. A., Banks, E., DePristo, M. A., Handsaker, R. E., Lunter, G., Marth, G. T., Sherry, S. T., McVean, G., Durbin, R.; 1000 Genomes Project Analysis Group (2011). The variant call format and VCFtools. Bioinformatics, 27, 2156-2158. https://doi.org/10.1093/bioinformatics/btr330
Dasgupta, M. G., Dharanishanthi, V., Agarwal, I., & Krutovsky, K. V. (2015). Development of genetic markers in eucalyptus species by target enrichment and exome sequencing. PLoS One, 10, e0116528. https://doi.org/10.1371/journal.pone.0116528
Davis, A. P., Chadburn, H., Moat, J., O'Sullivan, R., Hargreaves, S., & Nic Lughadha, E. (2019). High extinction risk for wild coffee species and implications for coffee sector sustainability. Science Advances, 5, eaav3473. https://doi.org/10.1126/sciadv.aav3473
Davis, A. P., Gole, T. W., Baena, S., & Moat, J. (2012). The impact of climate change on indigenous Arabica coffee (Coffea arabica): Predicting future trends and identifying priorities. PLoS One, 7, e47981. https://doi.org/10.1371/journal.pone.0047981
Davis, A. P., Govaerts, R., Bridson, D. M., & Stoffelen, P. (2006). An annotated taxonomic conspectus of the genus Coffea (Rubiaceae). Botanical Journal of the Linnean Society, 152, 465-512. https://doi.org/10.1111/j.1095-8339.2006.00584.x
Davis, A. P., Tosh, J., Ruch, N., & Fay, M. F. (2011). Growing coffee: Psilanthus (Rubiaceae) subsumed on the basis of molecular and morphological data; implications for the size, morphology, distribution and evolutionary history of Coffea. Botanical Journal of the Linnean Society, 167, 357-377. https://doi.org/10.1111/j.1095-8339.2011.01177.x
De Mita, S., Thuillet, A.-C., Gay, L., Ahmadi, N., Manel, S., Ronfort, J., & Vigouroux, Y. (2013). Detecting selection along environmental gradients: analysis of eight methods and their effectiveness for outbreeding and selfing populations. Molecular Ecology, 22, 1383-1399. https://doi.org/10.1111/mec.12182
De Villemereuil, P., Frichot, É., Bazin, É., François, O., & Gaggiotti, O. E. (2014). Genome scan methods against more complex models: When and how much should we trust them? Molecular Ecology, 23, 2006-2019. https://doi.org/10.1111/mec.12705
Denoeud, F., Carretero-Paulet, L., Dereeper, A., Droc, G., Guyot, R., Pietrella, M., Zheng, C., Alberti, A., Anthony, F., Aprea, G., Aury, J.-M., Bento, P., Bernard, M., Bocs, S., Campa, C., Cenci, A., Combes, M.-C., Crouzillat, D., Da Silva, C., … Lashermes, P. (2014). The coffee genome provides insight into the convergent evolution of caffeine biosynthesis. Science, 345, 1181-1184. https://doi.org/10.1126/science.1255274
Dereeper, A., Bocs, S., Rouard, M., Guignon, V., Ravel, S., Tranchant-Dubreuil, C., Poncet, V., Garsmeur, O., Lashermes, P., & Droc, G. (2015). The coffee genome hub: A resource for coffee genomes. Nucleic Acids Research, 43, D1028-D1035. https://doi.org/10.1093/nar/gku1108
Elith, J., Kearney, M., & Phillips, S. (2010). The art of modelling range-shifting species. Methods in Ecology and Evolution, 1, 330-342. https://doi.org/10.1111/j.2041-210X.2010.00036.x
Fick, S. E., & Hijmans, R. J. (2017). WorldClim 2: New 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37, 4302-4315. https://doi.org/10.1002/joc.5086
Fisher, R. A. (1925). Statistical methods for research workers. Oliver and Boyd (Edinburgh).
Fitzpatrick, M. C., & Keller, S. R. (2015). Ecological genomics meets community-level modelling of biodiversity: Mapping the genomic landscape of current and future environmental adaptation. Ecology Letters, 18(1), 1-16. https://doi.org/10.1111/ele.12376
Franks, S. J., & Hoffmann, A. A. (2012). Genetics of climate change adaptation. Annual Review of Genetics, 46, 185-208. https://doi.org/10.1146/annurev-genet-110711-155511
Freire, L. P., Marraccini, P., Rodrigues, G. C., & Andrade, A. C. (2013). Analysis of the mannose 6 phosphate reductase gene expression in coffee trees submitted to water deficit. Coffee Science, 8, 17-23. https://doi.org/10.25186/cs.v8i1.306
Frichot, E., & François, O. (2015). LEA: An R package for landscape and ecological association studies. Methods in Ecology and Evolution, 6, 925-929. https://doi.org/10.1111/2041-210X.12382
Frichot, E., Mathieu, F., Trouillon, T., Bouchard, G., & François, O. (2014). Fast and efficient estimation of individual ancestry coefficients. Genetics, 196, 973-983. https://doi.org/10.1534/genetics.113.160572
Frichot, E., Schoville, S. D., Bouchard, G., & François, O. (2013). Testing for associations between loci and environmental gradients using latent factor mixed models. Molecular Biology and Evolution, 30, 1687-1699. https://doi.org/10.1093/molbev/mst063
Fu, Y., Springer, N. M., Gerhardt, D. J., Ying, K., Yeh, C.-T., Wu, W., Swanson-Wagner, R., D'Ascenzo, M., Millard, T., Freeberg, L., Aoyama, N., Kitzman, J., Burgess, D., Richmond, T., Albert, T. J., Barbazuk, W. B., Jeddeloh, J. A., & Schnable, P. S. (2010). Repeat subtraction-mediated sequence capture from a complex genome. The Plant Journal, 62, 898-909. https://doi.org/10.1111/j.1365-313X.2010.04196.x
Fuentes-Pardo, A. P., & Ruzzante, D. E. (2017). Whole-genome sequencing approaches for conservation biology: Advantages, limitations and practical recommendations. Molecular Ecology, 26, 5369-5406. https://doi.org/10.1111/mec.14264
Gain, C., & François, O. (2021). LEA 3: Factor models in population genetics and ecological genomics with R. Molecular Ecology Resources, 21(8), 2738-2748. https://doi.org/10.1111/1755-0998.13366
Geromel, C., Ferreira, L. P., Guerreiro, S. M. C., Cavalari, A. A., Pot, D., Pereira, L. F. P., & Marraccini, P. (2006). Biochemical and genomic analysis of sucrose metabolism during coffee (Coffea arabica) fruit development. Journal of Experimental Botany, 57, 3243-3258. https://doi.org/10.1093/jxb/erl084
Gomez, C., Despinoy, M., Hamon, S., Hamon, P., Salmon, D., Akaffou, D. S., Legnate, H., de Kochko, A., Mangeas, M., & Poncet, V. (2016). Shift in precipitation regime promotes interspecific hybridization of introduced Coffea species. Ecology and Evolution, 6, 3240-3255. https://doi.org/10.1002/ece3.2055
Gomez, C., Dussert, S., Hamon, P., Hamon, S., De Kochko, A., & Poncet, V. (2009). Current genetic differentiation of Coffea canephora Pierre ex A. Froehn in the Guineo-Congolian African zone: Cumulative impact of ancient climatic changes and recent human activities. BMC Evolutionary Biology, 9, 167. https://doi.org/10.1186/1471-2148-9-167
Hale, H., Gardner, E. M., Viruel, J., Pokorny, L., & Johnson, M. G. (2020). Strategies for reducing per-sample costs in target capture sequencing for phylogenomics and population genomics in plants. Applications in Plant Sciences, 8(4), e11337. https://doi.org/10.1002/aps3.11337
Harrisson, K. A., Pavlova, A., Telonis-Scott, M., & Sunnucks, P. (2014). Using genomics to characterize evolutionary potential for conservation of wild populations. Evolutionary Applications, 7, 1008-1025. https://doi.org/10.1111/eva.12149
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965-1978. https://doi.org/10.1002/joc.1276
Hill, C. B., Angessa, T. T., McFawn, L.-A., Wong, D., Tibbits, J., Zhang, X.-Q., Forrest, K., Moody, D., Telfer, P., Westcott, S., Diepeveen, D., Xu, Y., Tan, C., Hayden, M., & Li, C. (2018). Hybridisation-based target enrichment of phenology genes to dissect the genetic basis of yield and adaptation in barley. Plant Biotechnology Journal, 17, 932-944. https://doi.org/10.1111/pbi.13029
Hinniger, C., Caillet, V., Michoux, F., Ben Amor, M., Tanksley, S., Lin, C., & McCarthy, J. (2006). Isolation and characterization of cDNA encoding three dehydrins expressed during Coffea canephora (Robusta) grain development. Annals of Botany, 97, 755-765. https://doi.org/10.1093/aob/mcl032
Hoffmann, A. A., & Sgrò, C. M. (2011). Climate change and evolutionary adaptation. Nature, 470, 479-485. https://doi.org/10.1038/nature09670
Holderegger, R., Buehler, D., Gugerli, F., & Manel, S. (2010). Landscape genetics of plants. Trends in Plant Science, 15, 675-683. https://doi.org/10.1016/j.tplants.2010.09.002
Huang, W., Carbone, M. A., Magwire, M. M., Peiffer, J. A., Lyman, R. F., Stone, E. A., Anholt, R. R. H., & Mackay, T. F. C. (2015). Genetic basis of transcriptome diversity in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 112, E6010-E6019. https://doi.org/10.1073/pnas.1519159112
IPCC (2013). Climate change 2013. The physical science basis. Cambridge University Press.
IPCC (2014). Proceedings of the 5th assessment report, WGII, climate change 2014: Impacts, adaptation, and vulnerability. Cambridge University Press.
Jones, M. R., & Good, J. M. (2016). Targeted capture in evolutionary and ecological genomics. Molecular Ecology, 25(1), 185-202. https://doi.org/10.1111/mec.13304
Joost, S., Bonin, A., Bruford, M. W., Després, L., Conord, C., Erhardt, G., & Taberlet, P. (2007). A spatial analysis method (SAM) to detect candidate loci for selection: Towards a landscape genomics approach to adaptation. Molecular Ecology, 16, 3955-3969. https://doi.org/10.1111/j.1365-294X.2007.03442.x
Jordan, R., Hoffmann, A. A., Dillon, S. K., & Prober, S. M. (2017). Evidence of genomic adaptation to climate in Eucalyptus microcarpa: Implications for adaptive potential to projected climate change. Molecular Ecology, 26, 6002-6020. https://doi.org/10.1111/mec.14341
Kenkel, C. D., & Matz, M. V. (2016). Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nature Ecology & Evolution, 1, 0014. https://doi.org/10.1038/s41559-016-0014
Khan, M. S. (2011). The role of DREB transcription factors in abiotic stress tolerance of plants. Biotechnology and Biotechnological Equipment, 25, 2433-2442. https://doi.org/10.5504/bbeq.2011.0072
Kiwuka, C. (2020). Genetic diversity and phenotypic variation of wild, feral and cultivated Coffea canephora in relation to drought stress. PhD thesis, Wageningen University, The Netherlands.
Kiwuka, C., Goudsmit, E., Tournebize, R., de Aquino, S. O., Douma, J. C., Bellanger, L., Crouzillat, D., Stoffelen, P., Sumirat, U., Legnaté, H., Marraccini, P., de Kochko, A., Andrade, A. C., Mulumba, J. W., Musoli, P., Anten, N. P. R., & Poncet, V. (2021). Genetic diversity of native and cultivated Uganda’s Coffea canephora Pierre ex A. Froehner: Climate influences, breeding potential and diversity conservation. PLoS One, 16(2), e0245965. https://doi.org/10.1371/journal.pone.0245965
Kremer, A., Ronce, O., Robledo-Arnuncio, J. J., Guillaume, F., Bohrer, G., Nathan, R., Bridle, J. R., Gomulkiewicz, R., Klein, E. K., Ritland, K., Kuparinen, A., Gerber, S., & Schueler, S. (2012). Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecology Letters, 15, 378-392. https://doi.org/10.1111/j.1461-0248.2012.01746.x
Kumar, S., Banks, T. W., & Cloutier, S. (2012). SNP discovery through next-generation sequencing and its applications. International Journal of Plant Genomics, 2012, 1-15. https://doi.org/10.1155/2012/831460
Lashermes, P., Combes, M.-C., Robert, J., Trouslot, P., D’Hont, A., Anthony, F., & Charrier, A. (1999). Molecular characterization and origin of the Coffea arabica L genome. Molecular and General Genetics, 261, 259-266. https://doi.org/10.1007/s004380050965
Leamy, L. J., Lee, C. R., Song, Q. J., Mujacic, I., Luo, Y., Chen, C. Y., Li, C., Kjemtrup, S., & Song, B.-H. (2016). Environmental versus geographical effects on genomic variation in wild soybean (Glycine soja) across its native range in northeast Asia. Ecology and Evolution, 6, 6332-6344. https://doi.org/10.1002/ece3.2351
Lepelley, M., Mahesh, V., McCarthy, J., Rigoreau, M., Crouzillat, D., Chabrillange, N., de Kochko, A., & Campa, C. (2012). Characterization, high-resolution mapping and differential expression of three homologous PAL genes in Coffea canephora Pierre (Rubiaceae). Planta, 236, 313-326. https://doi.org/10.1007/s00425-012-1613-2
Leroy, T., Montagnon, C., Charrier, A., & Eskes, A. B. (1993). Reciprocal recurrent selection applied to Coffea canephora Pierre. 1. Characterization and evaluation of breeding populations and value of intergroup hybrids. Euphytica, 67(1-2), 113-125. https://doi.org/10.1007/BF00033776
Li, H., & Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25(14), 1754-1760. https://doi.org/10.1093/bioinformatics/btp324
Li, Y., Zhang, X.-X., Mao, R.-L., Yang, J., Miao, C.-Y., Li, Z., & Qiu, Y.-X. (2017). Ten years of landscape genomics: challenges and opportunities. Frontiers in Plant Science, 8, 2136. https://doi.org/10.3389/fpls.2017.02136
Lotterhos, K. E., & Whitlock, M. C. (2015). The relative power of genome scans to detect local adaptation depends on sampling design and statistical method. Molecular Ecology, 24, 1031-1046. https://doi.org/10.1111/mec.13100
Luikart, G., England, P. R., Tallmon, D., Jordan, S., & Taberlet, P. (2003). The power and promise of population genomics: from genotyping to genome typing. Nature Reviews Genetics, 4, 981. https://doi.org/10.1038/nrg1226
Manel, S., Andrello, M., Henry, K., Verdelet, D., Darracq, A., Guerin, P.-E., Desprez, B., & Devaux, P. (2018). Predicting genotype environmental range from genome-environment associations. Molecular Ecology, 27, 2823-2833. https://doi.org/10.1111/mec.14723
Manel, S., & Holderegger, R. (2013). Ten years of landscape genetics. Trends in Ecology & Evolution, 28, 614-621. https://doi.org/10.1016/j.tree.2013.05.012
Manel, S., Joost, S., Epperson, B. K., Holderegger, R., Storfer, A., Rosenberg, M. S., Scribner, K. T., Bonin, A., & Fortin, M.-J. (2010). Perspectives on the use of landscape genetics to detect genetic adaptive variation in the field. Molecular Ecology, 19, 3760-3772. https://doi.org/10.1111/j.1365-294X.2010.04717.x
Manel, S., Perrier, C., Pratlong, M., Abi-Rached, L., Paganini, J., Pontarotti, P., & Aurelle, D. (2016). Genomic resources and their influence on the detection of the signal of positive selection in genome scans. Molecular Ecology, 25, 170-184. https://doi.org/10.1111/mec.13468
Mariac, C., Bethune, K., de Aquino, S. O., Abdelrahman, M., Barnaud, A., Billot, C., Zekraoui, L., Couderc, M., Kané, N., Andrade, A. C., Marraccini, P., Kiwuka, C., Albar, L., Sabot, F., Poncet, V., Couvreur, T. L. P., Berthouly-Salazar, C., & Vigouroux, Y. (2022). Optimization of capture protocols across species targeting up to 32000 genes and their extension to pooled DNA. bioRxiv. https://doi.org/10.1101/2022.01.10.474775
Mariac, C., Luong, V., Kapran, I., Mamadou, A., Sagnard, F., Deu, M., Chantereau, J., Gerard, B., Ndjeunga, J., Bezançon, G., Pham, J.-L., & Vigouroux, Y. (2006). Diversity of wild and cultivated pearl millet accessions (Pennisetum glaucum [L.] R. Br.) in Niger assessed by microsatellite markers. Theoretical and Applied Genetics, 114, 49-58. https://doi.org/10.1007/s00122-006-0409-9
Mariac, C., Scarcelli, N., Pouzadou, J., Barnaud, A., Billot, C., Faye, A., Kougbeadjo, A., Maillol, V., Martin, G., Sabot, F., Santoni, S., Vigouroux, Y., & Couvreur, T. L. P. (2014). Cost-effective enrichment hybridization capture of chloroplast genomes at deep multiplexing levels for population genetics and phylogeography studies. Molecular Ecology Resources, 14, 1103-1113. https://doi.org/10.1111/1755-0998.12258
Marraccini, P. (2020). Gene expression in coffee. In F. M. Cánovas, U. Lüttge, M. C. Risueño, & H. Pretzsch (Eds.), Progress in botany (Vol. 42, pp. 43-111). Springer. https://doi.org/10.1007/124_2020_42
Marraccini, P., Freire, L. P., Alves, G. S. C., Vieira, N. G., Vinecky, F., Elbelt, S., Ramos, H. J. O., Montagnon, C., Vieira, L. G. E., Leroy, T., Pot, D., Silva, V. A., Rodrigues, G. C., & Andrade, A. C. (2011). RBCS1 expression in coffee: Coffea orthologs, Coffea arabica homeologs, and expression variability between genotypes and under drought stress. BMC Plant Biology, 11, 85. https://doi.org/10.1186/1471-2229-11-85
Marraccini, P., Vinecky, F., Alves, G. S. C., Ramos, H. J. O., Elbelt, S., Vieira, N. G., Carneiro, F. A., Sujii, P. S., Alekcevetch, J. C., Silva, V. A., DaMatta, F. M., Ferrao, M. A. G., Leroy, T., Pot, D., Vieira, L. G. E., da Silva, F. R., & Andrade, A. C. (2012). Differentially expressed genes and proteins upon drought acclimation in tolerant and sensitive genotypes of Coffea canephora. Journal of Experimental Botany, 63, 4191-4212. https://doi.org/10.1093/jxb/ers103
Meinshausen, M., Smith, S. J., Calvin, K., Daniel, J. S., Kainuma, M. L. T., Lamarque, J.-F., Matsumoto, K., Montzka, S. A., Raper, S. C. B., Riahi, K., Thomson, A., Velders, G. J. M., & van Vuuren, D. P. (2011). The RCP greenhouse gas concentrations and their extensions from 1765 to 2300. Climatic Change, 109, 213. https://doi.org/10.1007/s10584-011-0156-z
Merilä, J., & Hendry, A. P. (2014). Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evolutionary Applications, 7, 1-14. https://doi.org/10.1111/eva.12137
Merot-L'Anthoene, V., Tournebize, R., Darracq, O., Rattina, V., Lepelley, M., Bellanger, L., Tranchant-Dubreuil, C., Coulée, M., Pégard, M., Metairon, S., Fournier, C., Stoffelen, P., Janssens, S. B., Kiwuka, C., Musoli, P., Sumirat, U., Legnaté, H., Kambale, J.-L., da Costa Neto, J. F., … Poncet, V. (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. https://doi.org/10.1111/pbi.13066
Miao, C. Y., Li, Y., Yang, J., & Mao, R. L. (2017). Landscape genomics reveal that ecological character determines adaptation: a case study in smoke tree (Cotinus coggygria Scop.). BMC Evolutionary Biology, 17, 202. https://doi.org/10.1186/s12862-017-1055-3
Miniussi, M., Del Terra, L., Savi, T., Pallavicini, A., & Nardini, A. (2015). Aquaporins in Coffea arabica L.: Identification, expression, and impacts on plant water relations and hydraulics. Plant Physiology and Biochemistry, 95, 92-102. https://doi.org/10.1016/j.plaphy.2015.07.024
Mitchell-Olds, T., Willis, J. H., & Goldstein, D. B. (2007). Which evolutionary processes influence natural genetic variation for phenotypic traits? Nature Reviews Genetics, 8, 845. https://doi.org/10.1038/nrg2207
Moat, J., Gole, T. W., & Davis, A. P. (2019). Least concern to endangered: Applying climate change projections profoundly influences the extinction risk assessment for wild Arabica coffee. Global Change Biology, 25, 390-403. https://doi.org/10.1111/gcb.14341
Moat, J., Williams, J., Baena, S., Wilkinson, T., Gole, T. W., Challa, Z. K., Demissew, S., & Davis, A. P. (2017). Resilience potential of the Ethiopian coffee sector under climate change. Nature Plants, 19, 17081. https://doi.org/10.1038/nplants.2017.81
Mofatto, L. S., Carneiro, F. D. A., Vieira, N. G., Duarte, K. E., Vidal, R. O., Alekcevetch, J. C., Cotta, M. G., Verdeil, J.-L., Lapeyre-Montes, F., Lartaud, M., Leroy, T., De Bellis, F., Pot, D., Rodrigues, G. C., Carazzolle, M. F., Pereira, G. A. G., Andrade, A. C., & Marraccini, P. (2016). Identification of candidate genes for drought tolerance in coffee by high-throughput sequencing in the shoot apex of different Coffea arabica cultivars. BMC Plant Biology, 16, 94. https://doi.org/10.1186/s12870-016-0777-5
Montagnon, C., Leroy, T., & Yapo, A. (1992). Genotypic and phenotypic diversity of some coffee groups (Coffea Canephora Pierre) in the collections-Consequences on their use in breeding. Cafe Cacao The, 36(3), 187-198.
Mora, C., Frazier, A. G., Longman, R. J., Dacks, R. S., Walton, M. M., Tong, E. J., Sanchez, J. J., Kaiser, L. R., Stender, Y. O., Anderson, J. M., Ambrosino, C. M., Fernandez-Silva, I., Giuseffi, L. M., & Giambelluca, T. W. (2013). The projected timing of climate departure from recent variability. Nature, 502, 183. https://doi.org/10.1038/nature12540
Musoli, P., Cubry, P., Aluka, P., Billot, C., Dufour, M., De Bellis, F., Pot, D., Bieysse, D., Charrier, A., & Leroy, T. (2009). Genetic differentiation of wild and cultivated populations: diversity of Coffea canephora Pierre in Uganda. Genome, 52, 634-646. https://doi.org/10.1139/G09-037
Neves, L. G., Davis, J. M., Barbazuk, W. B., & Kirst, M. (2013). Whole-exome targeted sequencing of the uncharacterized pine genome. The Plant Journal, 75, 146-156. https://doi.org/10.1111/tpj.12193
Nicholls, J. A., Pennington, R. T., Koenen, E. J. M., Hughes, C. E., Hearn, J., Bunnefeld, L., Dexter, K. G., Stone, G. N., & Kidner, C. A. (2015). Using targeted enrichment of nuclear genes to increase phylogenetic resolution in the neotropical rain forest genus Inga (Leguminosae: Mimosoideae). Frontiers in Plant Science, 6, 710. https://doi.org/10.3389/fpls.2015.00710
Nicotra, A. B., Atkin, O. K., Bonser, S. P., Davidson, A. M., Finnegan, E. J., Mathesius, U., Poot, P., Purugganan, M. D., Richards, C. L., Valladares, F., & van Kleunen, M. (2010). Plant phenotypic plasticity in a changing climate. Trends in Plant Science, 15, 684-692. https://doi.org/10.1016/j.tplants.2010.09.008
Nicotra, A. B., Segal, D. L., Hoyle, G. L., Schrey, A. W., Verhoeven, K. J. F., & Richards, C. L. (2015). Adaptive plasticity and epigenetic variation in response to warming in an Alpine plant. Ecology and Evolution, 5, 634-647. https://doi.org/10.1002/ece3.1329
Nielsen, R. (2005). Molecular signatures of natural selection. Annual Review of Genetics, 39, 197-218. https://doi.org/10.1146/annurev.genet.39.073003.112420
Ovalle-Rivera, O., Läderach, P., Bunn, C., Obersteiner, M., & Schroth, G. (2015). Projected shifts in Coffea arabica suitability among major global producing regions due to climate change. PLoS One, 10, e0124155. https://doi.org/10.1371/journal.pone.0124155
Patterson, N., Price, A. L., & Reich, D. (2006). Population structure and Eigenanalysis. PLoS Genetics, 2, e190. https://doi.org/10.1371/journal.pgen.0020190
Preston, J., Wheeler, J., Heazlewood, J., Li, S. F., & Parish, R. W. (2004). AtMYB32 is required for normal pollen development in Arabidopsis thaliana. The Plant Journal, 40, 979-995. https://doi.org/10.1111/j.1365-313X.2004.02280.x
Privat, I., Foucrier, S., Prins, A., Epalle, T., Eychenne, M., Kandalaft, L., … McCarthy, J. (2008). Differential regulation of grain sucrose accumulation and metabolism in Coffea arabica (Arabica) and Coffea canephora (Robusta) revealed through gene expression and enzyme activity analysis. New Phytologist, 178, 781-797. https://doi.org/10.1111/j.1469-8137.2008.02425.x
Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M. A. R., Bender, D., Maller, J., Sklar, P., de Bakker, P. I. W., Daly, M. J., & Sham, P. C. (2007). PLINK: A tool set for whole-genome association and population-based linkage analyses. The American Journal of Human Genetics, 81, 559-575. https://doi.org/10.1086/519795
R Development Core Team (2015). R: A language and environment for statistical computing. R Foundation for Statistical Computing. http://www.R-project.org ISBN 3-900051-07-0.
Razgour, O., Forester, B., Taggart, J. B., Bekaert, M., Juste, J., Ibáñez, C., Puechmaille, S. J., Novella-Fernandez, R., Alberdi, A., & Manel, S. (2019). Considering adaptive genetic variation in climate change vulnerability assessment reduces species range loss projections. Proceedings of the National Academy of Sciences of the United States of America, 116, 10418-10423. https://doi.org/10.1073/pnas.1820663116
Rellstab, C., Dauphin, B., & Exposito-Alonso, M. (2021). Prospects and limitations of genomic offset in conservation management. Evolutionary Applications, 14, 1202-1212. https://doi.org/10.1111/eva.13205
Rellstab, C., Zoller, S., Walthert, L., Lesur, I., Pluess, A. R., Graf, R., … Gugerli, F. (2016). Signatures of local adaptation in candidate genes of oaks (Quercus spp.) with respect to present and future climatic conditions. Molecular Ecology, 25, 5907-5924. https://doi.org/10.1111/mec.13889
Rhoné, B., Defrance, D., Berthouly-Salazar, C., Mariac, C., Cubry, P., Couderc, M., Dequincey, A., Assoumanne, A., Kane, N. A., Sultan, B., Barnaud, A., & Vigouroux, Y. (2020). Pearl millet genomic vulnerability to climate change in West Africa highlights the need for regional collaboration. Nature Communications, 11(1), 5274. https://doi.org/10.1038/s41467-020-19066-4
Roffler, G. H., Amish, S. J., Smith, S., Cosart, T., Kardos, M., Schwartz, M. K., & Luikart, G. (2016). SNP discovery in candidate adaptive genes using exon capture in a free-ranging alpine ungulate. Molecular Ecology Resources, 16, 1147-1164. https://doi.org/10.1111/1755-0998.12560
Rohland, N., & Reich, D. (2012). Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture. Genome Research, 22, 939-946. https://doi.org/10.1101/gr.128124.111
Ruegg, K., Bay Rachael, A., Anderson Eric, C., Saracco James, F., Harrigan Ryan, J., Whitfield, M., Paxton Eben, H., & Smith Thomas, B. (2018). Ecological genomics predicts climate vulnerability in an endangered southwestern songbird. Ecology Letters. https://doi.org/10.1111/ele.12977
Santos, A. B., & Mazzafera, P. (2012). Dehydrins are highly expressed in water-stressed plants of two coffee species. Tropical Plant Biology, 5, 218-232. https://doi.org/10.1007/s12042-012-9106-9
Santos, A. B., & Mazzafera, P. (2013). Aquaporins and the control of the water status in coffee plants. Theoretical and Experimental Plant Physiology, 25, 79-93. https://doi.org/10.1590/S2197-00252013000200001
Savolainen, O., Lascoux, M., & Merilä, J. (2013). Ecological genomics of local adaptation. Nature Reviews Genetics, 14(11), 807-820. https://doi.org/10.1038/nrg3522
Scarcelli, N., Mariac, C., Couvreur, T. L. P., Faye, A., Richard, D., Sabot, F., … Vigouroux, Y. (2016). Intra-individual polymorphism in chloroplasts from NGS data: Where does it come from and how to handle it? Molecular Ecology Resources, 16, 434-445. https://doi.org/10.1111/1755-0998.12462
Sgrò, C. M., Lowe, A. J., & Hoffmann, A. A. (2011). Building evolutionary resilience for conserving biodiversity under climate change. Evolutionary Applications, 4, 326-337. https://doi.org/10.1111/j.1752-4571.2010.00157.x
Shinozaki, K., & Yamaguchi-Shinozaki, K. (2007). Gene networks involved in drought stress response and tolerance. Journal of Experimental Botany, 58, 221-227. https://doi.org/10.1093/jxb/erl164
Simkin, A. J., Kuntz, M., Moreau, H., & McCarthy, J. (2010). Carotenoid profiling and the expression of carotenoid biosynthetic genes in developing coffee grain. Plant Physiology and Biochemistry, 48, 434-442. https://doi.org/10.1016/j.plaphy.2010.02.007
Simkin, A. J., Moreau, H., Kuntz, M., Pagny, G., Lin, C., Tanksley, S., & McCarthy, J. (2008). An investigation of carotenoid biosynthesis in Coffea canephora and Coffea arabica. Journal of Plant Physiology, 165, 1087-1106. https://doi.org/10.1016/j.jplph.2007.06.016
Sork, V. L. (2018). Genomic studies of local adaptation in natural plant populations. Journal of Heredity, 109, 3-15. https://doi.org/10.1093/jhered/esx091
Sork, V. L., Aitken, S. N., Dyer, R. J., Eckert, A. J., Legendre, P., & Neale, D. B. (2013). Putting the landscape into the genomics of trees: approaches for understanding local adaptation and population responses to changing climate. Tree Genetics & Genomes, 9, 901-911. https://doi.org/10.1007/s11295-013-0596-x
Stracke, R., Werber, M., & Weisshaar, B. (2001). The R2R3-MYB gene family in Arabidopsis thaliana. Current Opinion in Plant Biology, 4, 447-456. https://doi.org/10.1016/S1369-5266(00)00199-0
Thioune, E.-H., McCarthy, J., Gallagher, T., & Osborne, B. (2017). A humidity shock leads to rapid, temperature dependent changes in coffee leaf physiology and gene expression. Tree Physiology, 37, 367-379. https://doi.org/10.1093/treephys/tpw129
Thioune, E.-H., Strickler, S., Gallagher, T., Charpagne, A., Decombes, P., Osborne, B., & McCarthy, J. (2020). Temperature impacts the response of Coffea canephora to decreasing soil water availability. Tropical Plant Biology, 13, 236-250. https://doi.org/10.1007/s12042-020-09254-3
Torres, L. F., Reichel, T., Déchamp, E., de Aquino, S. O., Duarte, K. E., Alves, G. S. C., Silva, A. T., Cotta, M. G., Costa, T. S., Diniz, L. E. C., Breitler, J.-C., Collin, M., Paiva, L. V., Andrade, A. C., Etienne, H., & Marraccini, P. (2019). Expression of DREB-like genes in Coffea canephora and C. arabica subjected to various types of abiotic stress. Tropical Plant Biology, 12, 98-116. https://doi.org/10.1007/s12042-019-09223-5
Tournebize, R., Manel, S., Borner, L., Meynard, C., Vigouroux, Y., Crouzillat, D., … Poncet, V. (2022). Ecological and genomic vulnerability to climate change across native populations of Robusta coffee (Coffea canephora). Global Change Biology. Under revision.
Uefuji, H., Tatsumi, Y., Morimoto, M., Kaothien-Nakayama, P., Ogita, S., & Sano, H. (2005). Caffeine production in tobacco plants by simultaneous expression of three coffee N-methyltrasferases and its potential as a pest repellant. Plant Molecular Biology, 59, 221-227. https://doi.org/10.1007/s11103-005-8520-x
Vangestel, C., Vázquez-Lobo, A., Martínez-García, P. J., Calic, I., Wegrzyn, J. L., & Neale, D. B. (2016). Patterns of neutral and adaptive genetic diversity across the natural range of sugar pine (Pinus lambertiana Dougl.). Tree Genetics & Genomes, 12, 51. https://doi.org/10.1007/s11295-016-0998-7
Vieira, N. G., Carneiro, F. A., Sujii, P. S., Alekcevetch, J. C., Freire, L. P., Vinecky, F., Elbelt, S., Silva, V. A., DaMatta, F. M., Ferrão, M. A. G., Marraccini, P., & Andrade, A. C. (2013). Different molecular mechanisms account for drought tolerance in Coffea canephora var. Conilon. Tropical Plant Biology, 6, 181-190. https://doi.org/10.1007/s12042-013-9126-0
Vinecky, F., da Silva, F. R., & Andrade, A. C. (2012). Análise in silico das bibliotecas de cDNA SH2 e SH3 para a identificação de genes responsivos à seca em cafeeiro. Coffee Science, 7, 1-19. https://doi.org/10.25186/cs.v7i1.155
Yeaman, S. (2015). Local adaptation by alleles of small effect. The American Naturalist, 186(S1), S74-S89. https://doi.org/10.1086/682405