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High throughput transcriptome analysis of coffee reveals prehaustorial resistance in response to Hemileia vastatrix infection

Abstract

Key message

We provide a transcriptional profile of coffee rust interaction and identified putative up regulated resistant genes

Abstract

Coffee rust disease, caused by the fungus Hemileia vastatrix, is one of the major diseases in coffee throughout the world. The use of resistant cultivars is considered to be the most effective control strategy for this disease. To identify candidate genes related to different mechanism defense in coffee, we present a time-course comparative gene expression profile of Caturra (susceptible) and Híbrido de Timor (HdT, resistant) in response to H. vastatrix race XXXIII infection. The main objectives were to obtain a global overview of transcriptome in both interaction, compatible and incompatible, and, specially, analyze up-regulated HdT specific genes with inducible resistant and defense signaling pathways. Using both Coffea canephora as a reference genome and de novo assembly, we obtained 43,159 transcripts. At early infection events (12 and 24 h after infection), HdT responded to the attack of H. vastatrix with a larger number of up-regulated genes than Caturra, which was related to prehaustorial resistance. The genes found in HdT at early hours were involved in receptor-like kinases, response ion fluxes, production of reactive oxygen species, protein phosphorylation, ethylene biosynthesis and callose deposition. We selected 13 up-regulated HdT-exclusive genes to validate by real-time qPCR, which most of them confirmed their higher expression in HdT than in Caturra at early stage of infection. These genes have the potential to assist the development of new coffee rust control strategies. Collectively, our results provide understanding of expression profiles in coffee—H. vastatrix interaction over a time course in susceptible and resistant coffee plants.

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Change history

  • 17 October 2019

    All the transcriptome sequencing data mentioned in the original article is publicly available at the National Center of Biotechnology Information (NCBI).

  • 17 October 2019

    All the transcriptome sequencing data mentioned in the original article is publicly available at the National Center of Biotechnology Information (NCBI).

References

  1. Afzal AJ, Wood AJ, Lightfoot DA (2008) Plant receptor-like serine threonine kinases: roles in signaling and plant defense. Mol Plant Microbe Interact 21:507–517. doi:10.1094/MPMI-21-5-0507

  2. Anders S, Huber W (2012) Differential expression of RNA-Seq data at the gene level—the DESeq package. EMBL 11:R106. doi:10.1186/gb-2010-11-10-r106

  3. Balaji V, Mayrose M, Sherf O, Jacob-Hirsch J, Eichenlaub R, Iraki N, Manulis-Sasson S, Rechavi G, Barash I, Sessa G (2008) Tomato transcriptional changes in response to Clavibacter michiganensis subsp. michiganensis reveal a role for ethylene in disease development. Plant Physiol 146:1797–1809. doi:10.1104/pp.107.115188

  4. Bettencourt AJ (1973) Considerações gerais sobre o “Hibrido de Timor.” Circ. No 23 20

  5. Bettencourt AJ, Rodrigues C (1988) Principles and practice of coffee breeding for resistance to rust and other diseases. Elsevier Appl Sci 3:199–234

  6. Bettgenhaeuser J, Gilbert B, Ayliffe M, Moscou MJ (2014) Nonhost resistance to rust pathogens—a continuation of continua. Front Plant Sci 5:664. doi:10.3389/fpls.2014.00664

  7. Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406. doi:10.1146/annurev.arplant.57.032905.105346

  8. Boyd LA, Ridout C, O’Sullivan DM, Leach JE, Leung H (2013) Plant-pathogen interactions: disease resistance in modern agriculture. Trends Genet 29:233–240. doi:10.1016/j.tig.2012.10.011

  9. Cabral PGC, Zambolim EM, Zambolim L, Lelis TP, Capucho AS, Caixeta ET (2009) Identification of a new race of Hemileia vastatrix in Brazil. Australas Plant Dis Notes 4:129–130

  10. Capucho AS, Zambolim EM, Freitas RL, Haddad F, Caixeta ET, Zambolim L (2012) Identification of race XXXIII of Hemileia vastatrix on Coffea arabica Catimor derivatives in Brazil. Australas Plant Dis Notes 7:189–191. doi:10.1007/s13314-012-0081-7

  11. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676. doi:10.1093/bioinformatics/bti610

  12. Cristancho MA, Botero-Rozo DO, Giraldo W, Tabima J, Riaño-Pachón DM, Escobar C, Rozo Y, Rivera LF, Durán A, Restrepo S, Eilam T, Anikster Y, Gaitán AL (2014) Annotation of a hybrid partial genome of the coffee rust (Hemileia vastatrix) contributes to the gene repertoire catalog of the Pucciniales. Front Plant Sci 5:594. doi:10.3389/fpls.2014.00594

  13. Cruz F, Kalaoun S, Nobile P, Colombo C, Almeida J, Barros LMG, Romano E, Grossi-de-Sá MF, Vaslin M, Alves-Ferreira M (2009) Evaluation of coffee reference genes for relative expression studies by quantitative real-time RT-PCR. Mol Breed 23:607–616. doi:10.1007/s11032-009-9259-x

  14. Davis AP, Tosh J, Ruch N, Fay MF (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. Bot J Linn Soc 167:357–377. doi:10.1111/j.1095-8339.2011.01177.x

  15. De Hoon MJL, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20:1453–1454. doi:10.1093/bioinformatics/bth078

  16. De Wit PJGM, Mehrabi R, Van Den Burg HA, Stergiopoulos I (2009) Fungal effector proteins: past, present and future. Mol Plant Pathol 10:735–747. doi:10.1111/j.1364-3703.2009.00591.x

  17. 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, Daddiego L, De Bellis F, Dussert S, Garsmeur O, Gayraud T, Guignon V, Jahn K, Jamilloux V, Joet T, Labadie K, Lan T, Leclercq J, Lepelley M, Leroy T, Li L-T, Librado P, Lopez L, Munoz A, Noel B, Pallavicini A, Perrotta G, Poncet V, Pot D, Priyono, Rigoreau M, Rouard M, Rozas J, Tranchant-Dubreuil C, VanBuren R, Zhang Q, Andrade AC, Argout X, Bertrand B, de Kochko A, Graziosi G, Henry RJ, Jayarama, Ming R, Nagai C, Rounsley S, Sankoff D, Giuliano G, Albert VA, Wincker P, Lashermes P (2014) The coffee genome provides insight into the convergent evolution of caffeine biosynthesis. Science 345:1181–1184. doi:10.1126/science.1255274

  18. Diniz I, Talhinhas P, Azinheira HG, Várzea V, Medeira C, Maia I, Petitot AS, Nicole M, Fernandez D, do Céu Silva M (2012) Cellular and molecular analyses of coffee resistance to Hemileia vastatrix and nonhost resistance to Uromyces vignae in the resistance-donor genotype HDT832/2. Eur J Plant Pathol 133:141–157. doi:10.1007/s10658-011-9925-9

  19. Duplan V, Rivas S (2014) E3 ubiquitin-ligases and their target proteins during the regulation of plant innate immunity. Front Plant Sci. doi:10.3389/fpls.2014.00042

  20. Ebel J, Scheel D (1997) Signals in host-parasite interactions. In: Carrol GC, Tudzynski P (eds) The Mycota, vol V. Springer, Berlin, pp 85–105

  21. Fernandez D, Santos P, Agostini C, Bon MC, Petitot AS, Silva MC, Guerra-Guimarães L, Ribeiro A, Argout X, Nicole M (2004) Coffee (Coffea arabica L.) genes early expressed during infection by the rust fungus (Hemileia vastatrix). Mol Plant Pathol 5:527–536. doi:10.1111/J.1364-3703.2004.00250.X

  22. Fernandez D, Tisserant E, Talhinhas P, Azinheira H, Vieira A, Petitot AS, Loureiro A, Poulain J, da Silva C, do Céu Silva M, Duplessis S (2012) 454-pyrosequencing of Coffea arabica leaves infected by the rust fungus Hemileia vastatrix reveals in planta-expressed pathogen-secreted proteins and plant functions in a late compatible plant-rust interaction. Mol Plant Pathol 13:17–37. doi:10.1111/j.1364-3703.2011.00723.x

  23. Flor H (1942) Inheritance of pathogenicity in Melampsora lini. Phytopathology 32:653–669

  24. Freitas RL, Zambolim E, Silva MC, Caixeta ET, Lelis DT, Zambolim L, Sakiyama N (2014) Cytological evaluation of the infection process of Hemileia vastatrix (race XXXIII) in resistant and susceptible coffee. In: Proceedings of the 25th international conference on coffee science (ASIC), pp 42–46. Armenia, Colombia

  25. Ganesh D, Petitot AS, Silva MC, Alary R, Lecouls AC, Fernandez D (2006) Monitoring of the early molecular resistance responses of coffee (Coffea arabica L.) to the rust fungus (Hemileia vastatrix) using real-time quantitative RT-PCR. Plant Sci 170:1045–1051. doi:10.1016/j.plantsci.2005.12.009

  26. Gichuru EK, Ithiru JM, Silva MC, Pereira AP, Varzea VMP (2012) Additional physiological races of coffee leaf rust (Hemileia vastatrix) identified in Kenya. Trop Plant Pathol 37:424–427. doi:10.1590/S1982-56762012000600008

  27. Gill US, Lee S, Mysore KS (2015) Host versus nonhost resistance: distinct wars with similar arsenals. Phytopathology 105:580–587. doi:10.1094/PHYTO-11-14-0298-RVW

  28. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652. doi:10.1038/nbt.1883

  29. Grenville-Briggs LJ, West P van (2005) The biotrophic stages of oomycete–plant interactions. 57:217–243. doi:10.1016/S0065-2164(05)57007-2

  30. Guerra-Guimarães L, Tenente R, Pinheiro C, Chaves I, Silva M, do C, Cardoso FMH, Planchon S, Barros DR, Renaut J, Ricardo CP (2015) Proteomic analysis of apoplastic fluid of Coffea arabica leaves highlights novel biomarkers for resistance against Hemileia vastatrix. Front Plant Sci 6:1–16. doi:10.3389/fpls.2015.00478

  31. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, Macmanes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, Leduc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8:1494–1512. doi:10.1038/nprot.2013.084

  32. Hammond-Kosack KE, Jones JD (1997) Plant disease resistance genes. Annu Rev Plant Physiol Plant Mol Biol 48:575–607

  33. Heath MC (1977) A comparative study of non-host interactions with rust fungi. Physiol Plant Pathol 10:73–88. doi:10.1016/0048-4059(77)90009-1

  34. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19. doi:10.1186/gb-2007-8-2-r19

  35. Ishiga Y, Upplapapti SR, Mysore KS (2013) Expression analysis reveals a role for hydrophobic or epicuticular wax signals in pre-penetration structure formation of Phakopsora pachyrhizi. Plant Signal Behav 8:e26959. doi:10.4161/psb.26959

  36. Jeandet P, Clement C, Courot E, Cordelier S (2013) Modulation of phytoalexin biosynthesis in engineered plants for disease resistance. Int J Mol Sci 14:14136–14170

  37. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329. doi:10.1038/nature05286

  38. Kenn NT (1999) Plant disease resistance: progress in basic understanding and practical application. In: Advances in botanical research. Academic Press, London, pp 291–328

  39. Kumar KRR, Kirti PB (2011) Differential gene expression in Arachis diogoi upon interaction with peanut late leaf spot pathogen, Phaeoisariopsis personata and characterization of a pathogen induced cyclophilin. Plant Mol Biol 75:497–513. doi:10.1007/s11103-011-9747-3

  40. Kundu A, Patel A, Paul S, Pal A (2015) Transcript Dynamics at Early Stages of Molecular Interactions of MYMIV with Resistant and Susceptible Genotypes of the Leguminous Host, Vigna mungo. PLoS ONE 10:e0124687. doi:10.1371/journal.pone.0124687

  41. Kushalappa AC, Yogendra KN, Karre S (2016) Plant innate immune response: qualitative and quantitative resistance. CRC Crit Rev Plant Sci 35:38–55. doi:10.1080/07352689.2016.1148980

  42. Labaj PP, Leparc GG, Linggi BE, Markillie LM, Wiley HS, Kreil DP (2011) Characterization and improvement of RNA-Seq precision in quantitative transcript expression profiling. Bioinformatics 27:i383–i391. doi:10.1093/bioinformatics/btr247

  43. Lara-Ávila JP, Isordia-Jasso MI, Castillo-Collazo R, Simpson J, Alpuche-Solís ÁG (2012) Gene expression analysis during interaction of tomato and related wild species with Clavibacter michiganensis subsp. michiganensis. Plant Mol Biol Report 30:498–511. doi:10.1007/s11105-011-0348-8

  44. Lashermes P, Combes M-C, Robert J, Trouslot P, D’Hont A, Anthony F, Charrier A (1999) Molecular characterisation and origin of the Coffea arabica L. genome. Mol Gen Genet MGG 261:259–266. doi:10.1007/s004380050965

  45. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323. doi:10.1186/1471-2105-12-323

  46. Licausi F, Ohme-Takagi M, Perata P (2013) APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol 199:639–649

  47. Loman NJ, Misra RV, Dallman TJ, Constantinidou C, Gharbia SE, Wain J, Pallen MJ (2012) Performance comparison of benchtop high-throughput sequencing platforms. Nat Biotechnol 30:434–439. doi:10.1038/nbt.2198

  48. Lu H (2003) ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response. Plant Cell Online 15:2408–2420. doi:10.1105/tpc.015412

  49. Mellersh DG, Heath MC (2003) An investigation into the involvement of defense signaling pathways in components of the nonhost resistance of Arabidopsis thaliana to rust fungi also reveals a model system for studying rust fungal compatibility. Mol Plant-Microbe Interact 16:398–404. doi:10.1094/MPMI.2003.16.5.398

  50. Mofatto LS, Carneiro F, de A, Vieira, Duarte NG, Vidal KE, Alekcevetch RO, Cotta JC, Verdeil MG, Lapeyre-Montes J-L, Lartaud F, Leroy M, De Bellis T, Pot F, Rodrigues D, Carazzolle GC, Pereira MF, Andrade GAG, Marraccini AC 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 Biol 16:94. doi:10.1186/s12870-016-0777-5

  51. Narusaka M, Kubo Y, Hatakeyama K, Imamura J, Ezura H, Nanasato Y, Tabei Y, Takano Y, Shirasu K NY (2013) Interfamily transfer of dual NB-LRR genes confers resistance to multiple pathogens. PLoS ONE 8:e55954. doi:10.1371/journal.pone.0055954

  52. Niks RE, Rubiales D (2002) Potentially durable resistance mechanisms in plants to specialised fungal pathogens. Euphytica 124:201–216. doi:10.1023/A:1015634617334

  53. Niks RE, Qi X, Marcel TC (2015) quantitative resistance to biotrophic filamentous plant pathogens: concepts, misconceptions, and mechanisms. Annu Rev Phytopathol 53:445–470. doi:10.1146/annurev-phyto-080614-115928

  54. Nirmala J, Drader T, Chen X, Steffenson B, Kleinhofs A (2010) Stem rust spores elicit rapid RPG1 phosphorylation. Mol Plant-Microbe Interact 23:1635–1642. doi:10.1094/MPMI-06-10-0136

  55. Oliveira MDM, Varanda CMR, Félix MRF (2016) Induced resistance during the interaction pathogen x plant and the use of resistance inducers. Phytochem Lett 15:152–158. doi:10.1016/j.phytol.2015.12.011

  56. Ozsolak F, Milos P (2010) RNA sequencing: advances, challenges and opportunities. Nat Rev Genet 12:87–98

  57. Peck SC (2003) Early phosphorylation events in biotic stress. Curr Opin Plant Biol 6:334–338. doi:10.1016/S1369-5266(03)00056-6

  58. Pedras MSC, Yaya EE, Glawischnig E (2011) The phytoalexins from cultivated and wild crucifers: chemistry and biology. Nat Prod Rep 28:1381. doi:10.1039/c1np00020a

  59. Pereira AA, Zambolim L, Chaves GM, Sakiyama NS (2000) Cultivar de café resistente à Ferrugem: Oeiras-MG 6851. Rev Ceres 46:121–124

  60. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. doi:10.1093/bioinformatics/btp616

  61. Rodrigues CJ, Bettencourt AJ, Rijo L (1975) Races of the pathogen and resistance to coffee rust. Annu Rev Phytopathol 13:49–70. doi:10.1146/annurev.py.13.090175.000405

  62. Rodrigues Jr CJ, Varzea VMP, Godinho IL, Palma S, Rato RC (1993) New physiologic races of Hemileia vastatrix. In: 15° Colloque Scientifique International sur le café. Montpellier, France, pp 318–321

  63. Rodrigues Jr CJ, Gonçalves MM, Várzea VMP (2004) Importância do Híbrido de Timor para o território e para o melhoramento da cafeicultura mundial. Rev Ciências Agrárias 27:203–213

  64. Rubio M, Rodríguez-Moreno L, Ballester AR, de Moura MC, Bonghi C, Candresse T, Martínez-Gómez P (2015) Analysis of gene expression changes in peach leaves in response to Plum pox virus infection using RNA-SEq. Mol Plant Pathol 16:164–176. doi:10.1111/mpp.12169

  65. Schulze-Lefert P, Panstruga R (2003) Establishment of biotrophy by parasitic fungi and reprogramming of host cells for disease resistance. Annu Rev Phytopathol 41:641–667. doi:10.1146/annurev.phyto.41.061002.083300

  66. Sharma M, Pandey GK (2016) Expansion and function of repeat domain proteins during stress and development in plants. Front Plant Sci 6:1218. doi:10.3389/fpls.2015.01218

  67. Shibuya N, Minami E (2001) Oligosaccharide signalling for defence responses in plant. Physiol Mol Plant Pathol 59:223–233. doi:10.1006/pmpp.2001.0364

  68. Silva MC, Nicole M, Guerra-GuimarÃes L, Rodrigues CJ (2002) Hypersensitive cell death and post-haustorial defence responses arrest the orange rust (Hemileia vastatrix) growth in resistant coffee leaves. Physiol Mol Plant Pathol 60:169–183. doi:10.1006/pmpp.2002.0389

  69. Silva M do, Várzea C, Guerra-Guimarães V, Azinheira L, Fernandez HG, Petitot D, Bertrand A-S, Lashermes B, Nicole P M (2006) Coffee resistance to the main diseases: leaf rust and coffee berry disease. Brazilian J Plant Physiol 18:119–147. doi:10.1590/S1677-04202006000100010

  70. Takahashi S, Yeo Y-S, Zhao Y, O’Maille PE, Greenhagen BT, Noel JP, Coates RM, Chappell J (2007) Functional characterization of premnaspirodiene oxygenase, a cytochrome P450 catalyzing regio- and stereo-specific hydroxylations of diverse sesquiterpene substrates. J Biol Chem 282:31744–31754. doi:10.1074/jbc.M703378200

  71. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-SEq. Bioinformatics 25:1105–1111. doi:10.1093/bioinformatics/btp120

  72. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515. doi:10.1038/nbt.1621

  73. Várzea VMP, Marques DV (2005) Resistance, population variability of Hemileia vastatrix vs. coffee durable. In: Zambolim L, Zambolim E, Várzea VMP (eds) Durable resistance to coffee leaf rust. UFV Press, Viçosa, pp 53–74

  74. Voegele RT, Mendgen K (2003) Rust haustoria: nutrient uptake and beyond. New Phytol 159:93–100. doi:10.1046/j.1469-8137.2003.00761.x

  75. Wang Y-S, Pi L-Y, Chen X, Chakrabarty PK, Jiang J, De Leon AL, Liu G-Z, Li L, Benny U, Oard J, Ronald PC, Song W-Y (2006) Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell Online 18:3635–3646. doi:10.1105/tpc.106.046730

  76. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63. doi:10.1038/nrg2484

  77. Wang X, McCallum BD, Fetch T, Bakkeren G, Saville BJ (2015) Sr36- and Sr5-mediated resistance response to Puccinia graminis f. sp. tritici is associated with callose deposition in wheat guard cells. Phytopathology 105:728–737. doi:10.1094/PHYTO-08-14-0213-R

  78. Westermann AJ, Gorski SA, Vogel J (2012) Dual RNA-seq of pathogen and host. Nat Rev Microbiol 10:618–630. doi:10.1038/nrmicro2852

  79. Xin M, Wang X, Peng H, Yao Y, Xie C, Han Y, Ni Z, Sun Q (2012) Transcriptome comparison of susceptible and resistant wheat in response to powdery mildew infection. Genom Proteom Bioinform 10:94–106. doi:10.1016/j.gpb.2012.05.002

  80. Young SA, Guo A, Guikema JA, White FF, Leach JE (1995) Rice cationic peroxidase accumulates in xylem vessels during incompatible interactions with Xanthomonas oryzae pv oryzae. Plant Physiol 107:1333–1341. doi:10.1104/pp.107.4.1333

  81. Yuyama PM, Junior OR, Ivamoto ST, Domingues DS, Carazzolle MF, Pereira GA, Charmetant P, Leroy T, Pereira LP (2016) Transcriptome analysis in Coffea eugenioides, an Arabica coffee ancestor, reveals differentially expressed genes in leaves and fruits. Mol Genet Genom 291:323–336. doi:10.1007/s00438-015-1111-x

  82. Zambolim L (2016) Current status and management of coffee leaf rust in Brazil. Trop Plant Pathol 41:1–8. doi:10.1007/s40858-016-0065-9

  83. Zhang J, Kobert K, Flouri T, Stamatakis A (2014) PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30:614–620. doi:10.1093/bioinformatics/btt593

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Acknowledgements

We thank Jorge Badel for his helpful suggestions during the preparation of the manuscript. We are also grateful to CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for the scholarship and Brazilian Coffee Research and Development Consortium (Consórcio Brasileiro de Pesquisa e Desenvolvimento do Café – CBP&D/Café), the Foundation for Research Support of the state of Minas Gerais (FAPEMIG), National Council of Scientific and Technological Development (CNPq), and National Institutes of Science and Technology of Coffee (INCT/Café) for the financial support, DTI (Diretoria de Tecnologia da Informação) of the Universidade Federal de Viçosa and LGE (Laborátorio de Genômica e Expressão) of the Universidade Estadual de Campinas for providing bioinformatics facilities.

Author information

JCF, LCM and MFC analyzed the sequencing data for transcriptome assembly; RDLFL and EMZ developed the biological experiments for the sequencing; JCF and SSF developed the qPCR experiments; Wrote the manuscript draft: JCF, SSF and ETC edited and revised the manuscript; ETC and LZ formulated the idea.

Correspondence to Eveline Teixeira Caixeta.

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Juan Carlos Florez and Luciana Souto Mofatto have contributed equally to this work.

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Florez, J.C., Mofatto, L.S., do Livramento Freitas-Lopes, R. et al. High throughput transcriptome analysis of coffee reveals prehaustorial resistance in response to Hemileia vastatrix infection. Plant Mol Biol 95, 607–623 (2017) doi:10.1007/s11103-017-0676-7

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Keywords

  • Coffee rust
  • Transcriptome
  • Biotrophic interaction
  • Disease resistance