A look back in time: genetic improvement of coffee through the application of biotechnology
DOI:
https://doi.org/10.15517/am.v30i2.34173Keywords:
protoplasts, electroporation, genetic engineering, Agrobacterium tumefaciens, plasmidAbstract
Introduction. Coffee (Coffea spp) is one of the most important crops worldwide, providing economic livelihood to millions of people in developing countries. There are more than 130 species of the Coffea genus, but only three species are commercially cultivated: Coffea arabica L. (2n=4x=44), Coffea canephora P. (2n=2x=22), and Coffea liberica L. (2n=2x=22). Which present limitations for their genetic improvement through conventional programs because of their perennial nature and differences in level of ploidy and incompatibility. Additionally, there are important characteristics such as resistance to pests or pathogens, which are not present in the available germplasm.Genetic engineering techniques have been used to solve this barrier, and significant advances have been generatedduring the last decades. Objective. The objective of this work was to provide an overview of the methodologies and advances in coffee genetic improvement through time, and ends with perspectives about the use of new technologies that have emerged in recent years. Development. The improvement began with the selection by crosses andinterspecific backcrosses, to move to the selection assisted by molecular markers. Subsequently, the culture and fusionof protoplasts was reported, with the disadvantage in the regeneration process. Genetic engineering through physical (electroporation and biolistics), and biological techniques (A. tumefaciens and A. rhizogenes) helped to overcome the limitations of regeneration, although the optimization processes are still laborious, so, new technologies for editing genomes such as CRISPR-Cas9, can solve problems of time and work in the laboratory for the crop. Conclusion.The improvement of coffee began three decades ago and has progressed mainly since the beginning of transgenictechnologies, and with the new techniques of specific modification of genes, the crop will benefit in the coming years.
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References
Acuña, J.R., and M. De-Peña. 1991. Plant regeneration from protoplasts of embryogenic cell suspensions of Coffea arabica L. cv. Caturra. Plant Cell Rep. 10:345-348. doi:10.1007/BF00193156
Agwanda, C.O. 1999. Twenty seven years of coffee breeding in Kenya: prospects for the release of new varieties. 18th International Scientific Colloquium on Coffee. ASIC, FIN. https://www.asic-cafe.org/conference/18th-international-scientific-colloquium-coffee/twenty-seven-years-coffee-breeding-kenya (accessed Mar. 13, 2006).
Agwanda, C., P. Lashermes, P. Trouslot, MC. Combes, and A. Charrier. 1997. Identification of RAPD markers for resistance to coffee berry disease, Colletotrichum kahawae, in arabica coffee. Euphytica 97:241-248. doi:10.1023/A:1003097913349
Albarrán, J.G. 1999. Influencia de los factores químicos y físicos sobre la regeneración de embriones somáticos de Coffea arabica en biorreactor simplificado. Tesis MSc., CATIE, Turrialba, CRI.
Albuquerque, E.V., W. Cunha, A. Barbosa, P. Costa, J. Teixeira, G. Vianna, G. Cabral, D. Fernandez, and M. Grossi. 2009. Transgenic coffee fruits from Coffea arabica genetically modified by bombardment. In Vitro Cell. Dev. Biol. Plant. 45:532-539 doi:10.1007/s11627-009-9254-2
Alemayehu, D. 2017. Review on genetic diversity of coffee (Coffea arabica L) in Ethiopia. Int. J. Forest. Hort. 3(2):18-27. doi:10.20431/2454-9487.0302003
Alpizar, E., E. Dechamp, B. Bertrand, P. Lashermes, and H. Etienne. 2007. Transgenic roots for functional genomics of coffee resistance genes to root-knot nematodes. In: Association for Science and Information on Coffee, editor, Proceedings of the 21st International Conference on Coffee Science. Association for Science and Information on Coffee, Montpellier, FRA. p. 653-659.
Alpizar, E., E. Dechamp, S. Espeout, M. Royer, A. Lecouls, M. Nicole, B. Bertrand, P. Lashermes, and H. Etienne. 2006. Efficient production of Agrobacterium rhizogenes-transformed roots and composite plants for studying gene expression in coffee roots. Plant Cell Rep. 25:959-967 doi:10.1007/s00299-006-0159-9
Alpizar, E., E. Dechamp, F. Lapeyre, C. Guilhaumon, B. Bertrand, C. Jourdan, P. Lashermes, and H. Etienne. 2008. Agrobacterium rhizogenes-transformed roots of coffee (Coffea arabica): Conditions for long-term proliferation, and morphological and molecular characterization. Ann. Bot. 101:929-940 doi:10.1093/aob/mcn027
AMC (Academia Mexicana de Ciencias). 2016. Edición genética con la técnica CRISPR/Cas9.55. AMC, MEX. http://www.coniunctus.amc.edu.mx/boletines/amc_boletin55.pdf (consultado 10 ene. 2018).
Arroyo, A., A. Ku, R. Canche, F. Quiroz, V. Loyola, L. Rodríguez, C. Burgeff, V. Súarez, and E. Castaño. 2008. Expression of WUSCHEL in Coffea canephora causes ectopic morphogenesis and increases somatic embryogenesis. Plant Cell Tiss. Organ Cult. 94:171-180 doi:10.1007/s11240-008-9401-1.
Azofeifa, A. 2006. Uso de marcadores moleculares en plantas; aplicaciones en frutales del trópico. Agron. Mesoam. 17:221-242. doi:10.15517/am.v17i2.5163
Barbón, R., E. Jiménez, A. Capote, V. Gil, y B. Ocaña. 2011. Transformación genética de Coffea arabica cv. Caturra rojo mediante la electroporación de suspensiones celulares embriogénicas. Biotecnol. Veg. 11(1):33-42.
Barbosa, A.E., E. Albuquerque, M. Silva, D. Souza, O. Oliveira, A. Valencia, T. Rocha, and M. Grossi. 2010. α-Amylase inhibitor-1 gene from Phaseolus vulgaris expressed in Coffea arabica plants inhibits α-amylases from the coffee berry borer pest. BMC Biotech. 10:44. doi:10.1186/1472-6750-10-44
Barros, E.V., G.B. Araujo, e A. Brasileiro. 2000. Transformação genética de Coffea arabica através de bombardeamento. SBICafé, BRA. http://www.sbicafe.ufv.br/handle/123456789/652 (acessado 10 Jan. 2018).
Barros, E.V., W.G Cunha, J.B. Teixeira, e A.C.M. Brasileiro. 2001. Expressão do gene Gus em embriões zigóticos e calos embriogênicos de Coffea arabica e C. canephora. Em: F. Mendes, e A. da-Silva, editores, Encontro do talento Estudantil da Embrapa Recursos Genéticos e Biotecnologia. Embrapa, Brasília, BRA. p. 36.
Barton, C., T. Adams, and M. Zarowitz. 1991. Stable transformation of foreign DNA into Coffea arabica plants. In: Association for Science and Information on Coffee, editor, Proceedings of the 14th International Conference on Coffee Science. ASIC, San Francisco, CA, USA. p. 460-464.
Berthouly, M. 1997. Biotecnologías y técnicas de reproducción de materiales promisorios en Coffea arabica. En: E.L. Ibarra, editor, Memorias del XVII Simposio Latinoamericano de Caficultura. IICA-PROMECAFE, San José, CRI. p. 25-49.
Breitler, J.C., E. Dechambreitlerp, C. Campa, L. Zebral, R. Guyot, P. Marraccini, and H. Etienne. 2018. CRISPR/Cas9-mediated efficient targeted mutagenesis has the potential to accelerate the domestication of Coffea canephora. Plant Cell Tiss. Organ Cult. 134:383-394. doi:10.1007/s11240-018-1429-2
Canche, R.L., A. Ku, C. Burgeff, V. Loyola, L. Rodríguez, and E. Castaño. 2006. Genetic transformation of Coffea canephora by vacuum infiltration. Plant Cell Tiss. Organ Cult. 84:373-377. doi:10.1007/s11240-005-9036-4
Carneiro, M.F. 1993. Induction of double haploids on Coffea arabica cultivars via anther or isolated microscopes culture. In: Association for Science and Information on Coffee, editor, 15th International Scientific Colloquium on Coffee. ASIC, Montpellier, France. p. 133.
Cruz, A.R., A. Paixao, F. Machado, M. Barbosa, C. Junqueira, G. Cabral, J. Teixeira, A. Kobayashi, A. Brasileiro, e E. Barros. 2004. Metodologia para obtencao de plantas transformadas de Coffea canephora por co-cultivo de calos embriogenicos com Agrobacterium tumefaciens. Boletim de Pesquisa e Desenvolvimento. Embrapa, BRA.
Cunha, W.G., e E. Barros. 2002. Transformação genética de calos embriogênicos de Coffea arabica via biobalística e seleção em canamicina. Embrapa, BRA. https://ainfo.cnptia.embrapa.br/digital/bitstream/CENARGEN/28564/1/tales2002.pdf (consultado 10 ene. 2018).
Cunha, W.G., F. Machado, G. Vianna, J. Teixeira, e V. Albuquerque. 2004. Obtenção de Coffea arabica geneticamente modificadas por bombardeamento de calos embriogênicos. Boletim de Pesquisa e desenvolvimento. Embrapa, BRA. https://ainfo.cnptia.embrapa.br/digital/bitstream/CENARGEN/28286/1/bp073.pdf (consultado 10 ene. 2018).
Davis, A., R. Govaerts., D. Bridson, and P. Stoffelen. 2006. An annotated taxonomic conspectus of the genus Coffea (Rubiaceae). Bot. J. Linn. Soc. 152:465-512. doi:10.1111/j.1095-8339.2006.00584.x
De-Block, M., LH. Estrella., M. Van-Montagu., J. Schell, and P. Zambryski. 1984. Expression of foreign genes in regenerated plants and in their progeny. EMBO J. 3:1681-1689. doi:10.1002/j.1460-2075.1984.tb02032.x
De-Gluglielmo, Z. 2009. Ingeniería genética aplicada al café. Rev. UDO Agric. 9:475-486.
De-Guglielmo, Z., I. Altosaar, M. Zaidi, and A. Menéndez. 2010a. Transformation of coffee (Coffea arabica L. cv. Catimor) with the cry1ac gene by biolistic, without the use of markers. Braz. J. Biol. 70:387-393.
De-Guglielmo, Z., R. Fernández, L. Hermoso, I. Altosaar, y A. Menéndez. 2010b. Optimización de los parámetros de transformación genética de café mediante biobalística con el gen reportero gus. Acta Biol. Venez. 30(1-2):23-34.
De-Kochko, A., S. Akaffou, A.C. Andrade, C. Campa, D. Crouzillat, R. Guyot, P. Hamon, R. Ming, LA. Mueller, V. Poncet, C. Tranchant, and S. Hamon. 2010. Advances in Coffea genomics. Adv. Bot. Res. 53:23-63. doi:10.1016/s00065-2296(10)53002-7
Denoeud, F., L. Carretero, A. Dereeper, G. Droc, R. Guyot, M. Pietrella, C. Zheng, A. Alberti, F. Anthony, G. Aprea, J. Aury, P. Bento, M. Bernard, S. Bocs, C. Campa, A. Cenci, M. Combes, D. Crouzillat, C. Da-Silva, L. Daddiego, F. De Bellis, S. Dussert, O. Garsmeur, T. Gayraud, V. Guignon, K. Jahn, V. Jamilloux, T. Joet, K. Labadie, T. Lan, J. Leclercq, M. Lepelley, T. Leroy, L. Li, P. Librado, L. Lopez, A. Muñoz, B. Noel, A. Pallavicini, G. Perrotta, V. Poncet, D. Pot, M. Rigoreau, M. Rouard, J. Rozas, C. Tranchant, R. Van-Buren, Q. Zhang, A. Andrade, X. Argout, B. Bertrand, A. De Kochko, G. Graziosi, R. Henry, R. Ming, C. Nagai, S. Rounsley, D. Sankoff, G. Giuliano, V. Albert, P. Wincker, and P. Lashermes. 2014. The coffee genome provides insight into the convergent evolution of caffeine biosynthesis. Science 345:1181-1184. doi:10.1126/science.1255274
Díaz, C., y A. Chaparro. 2012. Métodos de transformación genética de plantas. Rev. U.D.C.A Actual. Divulg. Cient. 15(1):49- 61.
Dufour, M., T. Leroy, C. Carasco, R. Philippe, and C. Fenouillet. 2000. Coffee (Coffea sp.) genetic transformation for insect resistance. In: T. Sera et al., editors, Coffee biotechnology and quality. Springer, Dordrecht, NLD. p. 209-217. doi:10.1007/978-94-017-1068-8_18
Espejo, R., G. Cipriani, G. Rosel, A. Golmirzaie, and W. Roca. 2008. Somatic hybrids obtained by protoplast fusion between Solanum tuberosum L. subsp. tuberosum and the wild species Solanum circaeifolium Bitter. Rev. Peru. Biol. 15:73-78. doi:10.15381/rpb.v15i1.1678
Fernández, R., Z. De-Guglielmo, and A. Menéndez. 2010. Cultivo de tejidos y transformación genética de café. Rev. Invest. 34(71):57-84.
Fernandez, R., and A. Menéndez. 2003. Transient gene expression in secondary somatic embryos from coffee tissues electroporated with the genes gus and bar. Electron. J. Biotechnol. 6:29-35. doi:10.2225/vol6-issue1-fulltext-6
Gatica, A.M., G. Arrieta, and A. Espinoza. 2008. Plant regeneration via indirec somatic embryogenesis and optimisation of genetic transformation in Coffea arabica L. cvs Caturra and Catuaí. Electron. J. Biotechnol. 11:1-11. doi:10.2225/vol11- issue1-fulltext-9
Gatica, A.M., G. Arrieta, and A. Espinoza. 2009. Optimization of coffee (Coffea arabica) transformation parameters using uidA and hpt genes: effect of osmotic pre-treatment, helium pressure and target distance. Rev. Biol. Trop. 57:151-160.
Gichuru, E., C.O. Agwanda, M.C. Combes, E.W. Mutitu, E.C. Ngugi, B. Bertrand, and P. Lashermes. 2008. Identification of molecular markers linked to a gene conferring resistance to coffee berry disease (Colletotrichum kahawae) in Coffea arabica. Plant Pathol. 57:1117-1124. doi:10.1111/j.1365-3059.2008.01846.x
Giménez, C.A., A. Menéndez, y E. De-García. 1996. Efecto del antibiótico kanamicina sobre diferentes explantes del híbrido de café (Coffea sp.) Catimor. Phyton 59:39-46.
Grézes, J., B. Thomasset, and D. Thomas. 1994. Factors influencing protoplasts isolation from Coffea arabica cells. Plant Cell Tiss. Organ Cult. 36:91-97. doi:10.1007/BF00048319
Gutiérrez, A., F. Santacruz, J. Cabrera, y B. Rodríguez. 2003. Mejoramiento genético vegetal in vitro. e-Gnosis 1:4. doi:10.1007/ BF00048319
Hatanaka, T., Y. Choi, T. Kusano, and H. Sano. 1999. Transgenic plants of coffee Coffea canephora from embryogenic callus via Agrobacterium tumefaciens-mediated transformation. Plant Cell Rep. 19:106-110. doi:10.1007/s002990050719
Hendre, P, and R.K. Aggarwal. 2007. DNA markers: Development and application for genetic improvement of coffee. In: R.K. Varshney, and R. Tuberosa, editors, Foreword to the series: Genomics-assisted crop improvement. Genomics Applications in Crops. Springer, Dordrecht, NLD. p. 399-434. doi:10.1007/978-1-4020-6297-1_15
ICAFE (Instituto Del Café de Costa Rica). 2016. Informe sobre la actividad cafetalera de Costa Rica. ICAFE, Heredia, CRI. http://www.icafe.cr/wp-content/uploads/informacion_mercado/informes_actividad/anteriores/2016.pdf (consultado 10 ene. 2018).
Ivamoto, S.T., O. Reis, D. Silva, T. Benedito, F. Freitas, D. Pot, T. Leroy, L. Gonzaga, M. Falsarella, G. Amarante, and L. Protasio. 2017a. Transcriptome analysis of leaves, flowers and fruits perisperm of Coffea arabica L. reveals the differential expression of genes involved in raffinose biosynthesis. PLoS One 12(1):e0169595. doi:10.1371/journal.pone.0169595
Ivamoto, S.T., L. Sakuray, L. Ferreira, C. Kitzberger, M. Scholz, D. Pot, T. Leroy, L. Vieira, D. Domingues, and L. Pereira. 2017b. Diterpenes biochemical profile and transcriptional analysis of cytochrome P450s genes in leaves, roots, flowers, and during Coffea arabica L. fruit development. Plant Physiol. Biochem. 111:340-347. doi:10.1016/j.plaphy.2016.12.004
Kumar, V., K. Satyanarayana, A. Ramakrishna, A. Chandrashekar, and G. Ravishankar. 2007. Evidence for localization of N-methyltransferase (NMT) of caffeine biosynthetic pathway in vacuolar surface of Coffea canephora endosperm elucidated through localization of GUS reporter gene driven by NMT promoter. Curr. Sci. 93:383-386.
Kumar, V., K. Satyanarayana, S. Sarala, E. Indu, P. Giridhar, A. Chandrashekar, and G. Ravishankar. 2006. Stable transformation and direct regeneration in Coffea canephora P ex. Fr. by Agrobacterium rhizogenes mediated transformation without hairy-root phenotype. Plant Cell Rep. 25:214-222 doi:10.1007/s00299-005-0045-x
Kumar, V., V. Sathyanarayana, S. Saarala, P. Giridhar, A. Chandrasekhar, and G. Ravishankar. 2004. Post transcriptional gene silencing for down regulating caffeine biosynthesis in Coffea canephora P. ex Fr. In: Association for Science and Information on Coffee, editor, Proceedings of the 20th International Conference on Coffee Science. ASIC, Bangalore, IND. p. 769-774.
Labouisse, J.P., B. Bellachew, S. Kotecha, and B. Bertrand. 2008. Current status of coffee (Coffea arabica L.) genetic resources in Ethiopia: implications for conservarion. Genet. Resour. Crop Evol. 55:1079-1093. doi:10.1007/s10722-008-9361-7
Lammoglia, M.F., R. Lozano, C. García, C. Avilez, V. Trejo, R. Muñoz, and C. López. 2016. The revolution in genetic engineering: CRISPR/Cas system. Invest. Discap. 5(2):116-128.
Lashermes, P., A. Carvalho, and H. Etienne. 2008. Genomics of coffee, one of the world’s largest traded commodities. In: P.H. Moore, and R. Ming, editors, Genomics of tropical crop plants. Vol. 1. Plants genetics and genomics: Crops and models. Springer, NY, USA. p. 203-226. doi:10.1007/978-0-387-71219-2_9
Lashermes, P., MC. Combes, J. Robert, P. Trouslot, AD. Hont, F. Anthony, and A. Charrier. 1999. Molecular characterization and origin of the Coffea arabica L. genome. Mol. Gen. Genet. 261:259-266. doi:10.1007/s004380050
Lashermes, P., MC. Combes, P. Topart, G. Graziosi, B. Bertrand, and F. Anthony. 2000. Molecular breeding in coffee (Coffea arabica L.). In: T. Sera et al., editors, Coffee biotechnology and quality. Springer, Dondrecht, NLD. p. 101-112. doi:10.1007/978-94-017-1068-8_7
Leroy, T., A. Henry, M. Royer, I. Altosaar, R. Frutos, D. Duris, and R. Philippe. 2000. Genetically modified coffee plants expressing the Bacillus thuringiensis cry1Ac gene for resistance to leaf miner. Plant Cell Rep. 19:382-389. doi:10.1007/ s002990050744
Leroy, T., M. Royer, et M. Paillard. 1997. Introduction de gènes d’intérêt agronomique dans l’espèce Coffea canephora Pierre par transformation avec. Agrobacterium sp. Fr: Association for Science and Information on Coffee, editor, Dix-septième colloque scientifique international sur le café. ASIC, Paris, FRA. p. 439-446.
Liu, X., S. Wu, J. Xu, C. Sui, and J. Wei. 2017. Application of CRISPR/Cas9 in plant biology. APSB 7:292-302. doi:10.1016/j. apsb.2017.01.002
Llop, P. 2003. Caracterización molecular de la pérdida del poder patógeno en Agrobacterium tumefaciens. Tesis Dr., Universitat De Valencia Servei de Publicacions, Valencia, ESP.
López, K., D. Rodríguez, y J. Vaca. 2013. Optimización de las condiciones de inoculación por biobalística de un Begomovirus en tomate y tabaco. Rev. Colomb. Biotecnol. 15(2):8-17. doi:10.15446/rev.colomb.biote.v15n2.41261
McCown, B.H., and G. Lloyd. 1981. Woody plant medium (WPM)-A mineral nutrient formulation for microculture of woody plant species. HortSci. 16:453-453.
Melese, K. 2016. The role of biotechnology on coffee plant propagation: A current topics paper. J. Biol. Agric. Healthcare 6(5):13-19
Mishra, M.K., S. Devi, A. McCormac, N. Scott, D. Chen, M. Elliott, and A. Slater. 2010. Green fluorescent protein as a visual selection marker for coffee transformation. Biologia 65:639-646 doi:10.2478/s11756-010-0078-7
Mishra, M.K., and A. Slater. 2012. Recent advances in the genetic transformation of coffee. Biotechnol. Res. Int. 2012:580857. doi:10.1155/2012/580857
Mishra, M.K., and H. Sreenath. 2004. High-efficiency Agrobacterium-Mediated transformation of coffee (Coffea canephora Pierre ex. Frohner) using hypocotyl explants. In: Association for Science and Information on Coffee, editor, Proceedings of the 20th International Conference on Coffee Science. ASIC, Bangalore, IND. p. 792-796.
Mishra, M.K., H. Sreenath, A. Jayarama, A. McCormac, S. Devi, M. Elliott, and A. Slater. 2008. Two critical factors: Agrobacterium strain and antibiotics selection regime improve the production of transgenic coffee plants. In: Association for Science and Information on Coffee, editor, Proceedings of the 22th International Association for Coffe Science. ASIC, Campinas, BRA. p. 843-850.
Mishra, M.K., H. Sreenath, and C. Srinivasan. 2002. Agrobacterium-mediated transformation of coffee: an assessment of factors affecting gene transfer efficiency. In: Association for Science and Information on Coffee, editor, Proceedings of the 15th Plantation Crops Symposium Placrosym XV. ASIC, Mysore, IND. p. 251-255.
Montero, W., y V. Jimenéz. 2009. Identificación y selección de híbridos somáticos obtenidos mediante fusión de protoplastos. Biotecnol. Veg. 9(2):67-90.
Morillo, S.X. 2011. Evaluación del control de Agrobacterium tumefaciens mediante la aplicación de agentes antibióticos en rosas. Informe Ing. Agropecu., Universidad de Fuerzas Armadas ESPE, Sangolquí, ECU.
Nester, E.W. 2015. Agrobacterium: nature’s genetic engineer. Front. Plant Sci. 5:730. doi:10.3389/fpls.2014.00730
Ocampo, C.A., and L. Manzanera. 1991. Advances in genetic manipulation of coffee plant. In: Association for Science and Information on Coffee, editor, Proceedings of 14th Colloquium of International Coffee Science Association. ASIC, San Francisco, CA, USA. p. 378-382.
Ogita, S., H. Uefuji, M. Morimoto, and H. Sano. 2004. Application of RNAi to confirm theobromine as the major intermediate for caffeine biosynthesis in coffee plants with potential for construction of decaffeinated varieties. Plant Mol. Biol. 54:931-941. doi:10.1007/s11103-004-0393-x
Orozco, F.J., y D. Schieder. 1982. Aislamiento y cultivo de protoplastos a partir de hojas de café. Cenicafé 33(4):129-136.
Pensabene, G. 2009. Aplicación de la hibridación somática a la mejora de la citrucultura española. Tesis Dr., Universidad Politécnica de Valencia. Valencia, ESP.
Perthuis, B., J. Pradon, C. Montagnon, M. Dufour, and T. Leroy. 2005. Stable resistance against the leaf miner Leucoptera coffeella expressed by genetically transformed Coffea canephora in a pluriannual field experiment in French Guiana. Euphytica 144:321-329. doi:10.1007/s10681-005-8003-9
Ran, F.A., P. Hsu, J. Wright, V. Agarwala, D. Scott, and F. Zhang. 2013. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8:2281-2308. doi:10.1038/nprot.2013.143
Ribas, A.F., E. Dechamp, A. Champion, B. Bertrand, M. Combes, J. Verdeil, F. Lapeyre, P. Lashermes, and H. Etienne. 2011. Agrobacterium-mediated genetic transformation of Coffea arabica (L.) is greatly enhanced by using established embryogenic callus cultures. BMC Plant Biol. 11:92. doi:10.1186/1471-2229-11-92
Ribas, A.F., R.M. Galvão, L.F.P. Pereira, e L.G.E. Vieira. 2006a. Transformação de Coffea arabica com o gene da ACC-oxidase em orientação antisenso. Em: Association for Science and Information on Coffee, editor, Proceedings of the 50th Congreso Brasileiro de Genética. ASIC, São Paulo, BRA. p. 492-493.
Ribas, A.F., A. Kenji, L. Protasio, and L. Esteves. 2006b. Production of herbicide-resistant coffee plants (Coffea canephora P.) via Agrobacterium tumefaciens-mediated transformation. Braz. Arch. Biol. Technol. 49:11-19. doi:10.1590/S1516- 89132006000100002
Ribas, A.F., A. Kobayashi, L. Pereira, and L. Vieira. 2005. Genetic transformation of Coffea canephora by particle bombardment. Biol. Plantarum 49:493-497. doi:10.1007/s10535-005-0038-1
Ribas, A.F., L. Protasio, L. Gonzaga, and E. Vieira. 2006c. Genetic transformation of coffee. Plant Physiol. 18:83-94. doi:10.1590/S1677-04202006000100007
Rosillo, A.G., J. Acuna, A. Gaitan, and M. De-Pena. 2003. Optimised DNA delivery into Coffea arabica suspension culture cells by particle bombardment. Plant Cell Tiss. Organ Cult. 74:45-49. doi:10.1023/A:1023314128543
Sander, J.D., and K. Joung. 2014. CRISPR-CAS systems for editing, regulating and targeting genomes. Nat. Biotechnol. 32:347- 355. doi:10.1038/nbt.2842
Sant’Ana, G.C., L. Pereira, D. Pot, S. Ivamoto, D. Domingues, R. Ferreira, N. Pagiatto, B. Da Silva, L. Nogueira, C. Kitzberger, M. Scholz, F. De-Oliveira, G. Sera, L. Padilha, J. Laboiusse, R. Guyot, P. Charmetant, and T. Leroy. 2018. Genome-wide association study reveals candidate genes influencing lipids and diterpenes contents in Coffea arabica L. Sci. Rep. 8:465. doi:10.1038/s41598-017-18800-1
Schopke, C., L. Muller, and H. Kohlenbach. 1987. Somatic embryogenesis and regeneration of plantlets in protoplast cultures from somatic embryos of coffee (Coffea canephora P. exFr). Plant Cell Tiss. Organ Cult. 8:243-248. doi:10.1007/ BF00040951
Solano, W. 2001. Efecto de las características de cultivo en suspensión celular y en biorreactor con inmersión temporal sobre la propagación masiva de Coffea arabica por embriogénesis somática. Tesis Lic., Universidad de Costa Rica, Turrialba, CRI.
Sondahl, M.R., M. Champman, and N. Sharp. 1980. Protoplast liberation, cell wall construction and callus proliferation in Coffea arabica L. callus tissues. Turrialba 30:161-165.
Souto, L., F. De-Araújo, N. Gomes, K. Duarte, R. Oliveira, J.C. Alekcevetch, M. Guitton, J.L. Verdeil, F. Lapeyre-Montes, M. Lartaud, T. Leroy, F. De-Bellis, D. Pot, G. Costa, M. Falsarella, G. Guimarães, A. Carvalho, and P. Marraccini. 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 Biol. 16:94. doi:10.1186/s12870-016-0777-5
Spiral, J., and V. Petiard. 1991. Protoplast culture and regeneration in coffee species. In: Association for Science and Information on Coffee, editor, Proceedings of the 14th International Conference on Coffee Science. ASIC, San Francisco, CA, USA. p. 383-391.
Spiral, J., C. Thierry, M. Paillard, et V. Petiard. 1993. Obtention de plantules de Coffea canephora Pierre (Robusta) transformées par Agrobacterium rhizogenes. Compt. Rend. l’Academ. Sci. Paris 316(1):1-6.
Sridevi, V., P. Giridhar, P. Simmi, and G. Ravishankar. 2010. Direct shoot organogenesis on hypocotyl explants with collar region from in vitro seedlings of Coffea canephora Pierre ex. Frohner cv. C X R and Agrobacterium tumefaciens-mediated transformation. Plant Cell Tiss. Organ Cult. 101:339-347 doi:10.1007/s11240-010-9694-8
Stein, V.C. 2009. Biotechnological approaches to improve drought tolerance of Coffea arabica. Tesis Dr., Universidade Federal de Lavras, Minas Gerais, BRA.
Sugiyama, M., C. Matsuoka, and T. Takagi. 1995. Transformation of coffea with Agrobacterium rhizogenes. In: Association for Science and Information on Coffee, editor, Proceedings of the 16th International Conference on Coffee Science. ASIC, Kyoto, JPN. p. 853-859.
Tran, H.T., L. Slade, A. Furtado, H. Smyth, and R. Henry. 2016. Advances in genomics for the improvement of quality in coffee. J. Sci. Food Agric. 96:3300-3312. doi:10.1002/jsfa.7692
Valderrama, A.M., R. Arango, y L. Afanador. 2005. Transformación de plantas mediada por Agrobacterium: “Ingeniería Genética Natural Aplicada”. Rev. Fac. Nal. Agr. 58:2569-2585.
Van-Boxtel, J.V. 1994. Studies on genetic transformation of coffee by using electroporation and the biolistic method. PhD. Diss., Univesity of Wageningen, NLD.
Van-Boxtel, J.V., M. Berthouly, C. Carasco, M. Dufour, and A. Eskes. 1995. Transient expression of β-glucuronidase following biolistic delivery of foreign DNA into coffee tissues. Plant Cell Rep. 14:748-752. doi:10.1007/BF00232915
Van-Der-Vossen, H., B. Bertrand, and A. Charrier. 2015. Next generation variety development for sustainable production of arabica coffee (Coffea arabica L.): a review. Euphytica 204:243-256. doi:10.1007/s10681-015-1398-z
Zhong, G.Y. 2001. Genetic issues and pitfalls in transgenic plant breeding. Euphytica 118:137-144. doi:10.1023/A:1004048019670
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