Abstract
Emergent diseases are an ever-increasing threat to forests and forest ecosystems and necessitate the development of research tools for species that often may have few pre-existing resources. We sequenced the mRNA expressed by the sudden oak death pathogen Phytophthora ramorum and its most susceptible forest host, tanoak, within the same tissue at two time points after inoculation, and in uninfected tanoak controls. Using the P. ramorum genome to differentiate host and pathogen transcripts, we detected more than 850 P. ramorum transcripts at 5 days post-inoculation and a concurrent upregulation of host genes usually associated with pathogenicity. At 1 day, in contrast, we did not detect pathogen expression or significant enrichment of functional categories of host transcripts relative to controls, highlighting the importance of sequencing depth for in planta studies of host–pathogen interactions. This study highlights processes in molecular host–pathogen interactions in forest trees and provides a first reference transcriptome for tanoak, allowing the preliminary identification of disease-related genes in this study and facilitating future work for this and other members of the family Fagaceae.
Similar content being viewed by others
References
Altschul S (1990) Basic local alignment search tool. J Mol Biol 215:403–410. doi:10.1006/jmbi.1990.9999
Anacker B, Rank N, Hüberli D et al (2008) Susceptibility to Phytophthora ramorum in a key infectious host: landscape variation in host genotype, host phenotype, and environmental factors. New Phytol 177:756–766. doi:10.1111/j.1469-8137.2007.02297.x
Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106. doi:10.1186/gb-2010-11-10-r106
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene Ontology: tool for the unification of biology. Nat Genet 25:25–29. doi:10.1038/75556
Barakat A, DiLoreto D, Zhang Y et al (2009) Comparison of the transcriptomes of American chestnut (Castanea dentata) and Chinese chestnut (Castanea mollissima) in response to the chestnut blight infection. Bmc Plant Biol 9:51. doi:10.1186/1471-2229-9-51
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300
Bergemann SE, Garbelotto M (2006) High diversity of fungi recovered from the roots of mature tanoak (Lithocarpus densiflorus) in northern California. Can J Bot 84:1380–1394. doi:10.1139/b06-097
Bowcutt F (2011) Tanoak target: the rise and fall of herbicide use on a common native tree. Environ Hist 16:197–225. doi:10.1093/envhis/emr032
Brasier C (2008) The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathol 57:792–808. doi:10.1111/j.1365-3059.2008.01886.x
Brasier CM, Cooke DEL, Duncan JM (1999) Origin of a new Phytophthora pathogen through interspecific hybridization. Proc Natl Acad Sci U S A 96:5878–5883. doi:10.1073/pnas.96.10.5878
Brasier C, Beales PA, Kirk SA et al (2005) Phytophthora kernoviae sp. nov., an invasive pathogen causing bleeding stem lesions on forest trees and foliar necrosis of ornamentals in the UK. Mycological Res 109:853–859. doi:10.1017/S0953756205003357
Breshears DD, Allen CD (2002) The importance of rapid, disturbance-induced losses in carbon management and sequestration. Global Ecol Biogeography 11:1–5. doi:10.1046/j.1466-822X.2002.00274.x
Bullard J, Purdom E, Hansen K, Dudoit S (2010) Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. BMC Bioinformatics 11:94. doi:10.1186/1471-2105-11-94
Burdon J, Thrall P, Ericson L (2006) The current and future dynamics of disease in plant communities. Annu Rev Phytopathol 44:19–39. doi:10.1146/annurev.phyto.43.040204.140238
Chang S, Puryear J, Cairney J (2007) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116
Cobb RC, Filipe JAN, Meentemeyer RK et al (2012) Ecosystem transformation by emerging infectious disease: loss of large tanoak from California forests. J Ecology 100(3):712–722. doi:10.1111/j.1365-2745.2012.01960.x
Collins B, Parke J, Lachenbruch B, Hansen E (2009) The effects of Phytophthora ramorum infection on hydraulic conductivity and tylosis formation in tanoak sapwood. Can J Forest Res 39:1766–1776. doi:10.1139/X09-097
Conesa A, Gotz S, Garcia-Gomez JM et al (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676. doi:10.1093/bioinformatics/bti610
Croucher PJP, Mascheretti S, Garbelotto M (2013) Combining field epidemiological information and genetic data to comprehensively reconstruct the invasion history and the microevolution of the sudden oak death agent Phytophthora ramorum (Stramenopila: Oomycetes) in California. Biol Invasions 15:2281–2297. doi: 10.1007/s10530-013-0453-8
Davidson J, Werres S, Garbelotto M, et al. (2003) Sudden Oak Death and associated diseases caused by Phytophthora ramorum. PHP. doi:10.1094/PHP-2003-0707-01-DG
Davidson J, Patterson H, Rizzo D (2008) Sources of inoculum for Phytophthora ramorum in a redwood forest. Phytopathology 98:860–866. doi:10.1094/PHYTO-98-8-0860
Davin LB, Lewis NG (2000) Dirigent proteins and dirigent sites explain the mystery of specificity of radical precursor coupling in lignan and lignin biosynthesis. Plant Physiol 123:453–462. doi:10.1104/pp. 123.2.453
Donahoo R, Blomquist CL, Thomas SL et al (2006) Phytophthora foliorum sp nov., a new species causing leaf blight of azalea. Mycol Res 110:1309–1322. doi:10.1016/j.mycres.2006.07.017
Duran A, Gryzenhout M, Slippers B et al (2008) Phytophthora pinifolia sp nov associated with a serious needle disease of Pinus radiata in Chile. Plant Pathol 57:715–727. doi:10.1111/j.1365-3059.2008.01893.x
Eckert A, Bower A, Wegrzyn J et al (2009) Asssociation genetics of coastal Douglas-fir (Pseudotsuga menziesu var. menziesii, Pinaceae). I. cold-hardiness related traits. Genetics 182:1289–1302. doi:10.1534/genetics.108.102350
Ekblom R, Galindo J (2011) Applications of next generation sequencing in molecular ecology of non-model organisms. Heredity 107:1–15. doi:10.1038/hdy.2010.152
Ellison A, Bank M, Clinton B et al (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3:479–486
Ersoz ES, Wright MH, González-Martínez SC et al (2010) Evolution of disease response genes in Loblolly Pine: insights from candidate genes. PLoS ONE 5:e14234. doi:10.1371/journal.pone.0014234
Erwin DC, Ribeiro OK (1996) Phytophthora diseases worldwide. APS, St. Paul
Fung RWM, Gonzalo M, Fekete C, Kovacs LG, He Y, Marsh E, McIntyre LM, Schachtman DP, Qiu W (2008) Powdery mildew induces defense-oriented reprogramming of the transcriptome in a susceptible but not in a resistant grapevine. Plant Physiol 146:236–249. doi:10.1104/pp. 107.108712
Garbelotto M, Harnik T, Schmidt D (2009) Efficacy of phosphonic acid, metalaxyl-M and copper hydroxide against Phytophthora ramorum in vitro and in planta. Plant Pathol 58:111–119. doi:10.1111/j.1365-3059.2008.01894.x
Grabherr MG, Haas BJ, Yassour M et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotech 29:644–652. doi:10.1038/nbt.1883
Haas BJ, Kamoun S, Zody MC et al (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393–398. doi:10.1038/nature08358
Hansen E, Reeser P, Davidson J et al (2003) Phytophthora nemorosa, a new species causing cankers and leaf blight of forest trees in California and Oregon, USA. Mycotaxon 88:129–138
Hansen E, Kanaskie A, Prospero S et al (2008) Epidemiology of Phytophthora ramorum in Oregon tanoak forests. Can J Forest Res 38:1133–1143. doi:10.1139/X07-217
Hansen K, Brenner S, Dudoit S (2010) Biases in Illumina transcriptome sequencing caused by random hexamer priming. Nucleic Acids Res 38:1–7. doi:10.1093/nar/gkq224
Hardham AR, Cahill DM (2010) The role of oomycete effectors in plant–pathogen interactions. Funct Plant Biol 37:919–925. doi:10.1071/FP10073
Hayden K, Ivors K, Wilkinson C, Garbelotto M (2006) TaqMan chemistry for Phytophthora ramorum detection and quantification, with a comparison of diagnostic methods. Phytopathology 96:846–854. doi:10.1094/PHYTO-96-0846
Hayden KJ, Nettel A, Dodd RS, Garbelotto M (2011) Will all the trees fall? Variable resistance to an introduced forest disease in a highly susceptible host. For Ecol Manage 261:1781–1791. doi:10.1016/j.foreco.2011.01.042
Hayden KJ, Garbelotto M, Dodd R, Wright JW (2013) Scaling up from greenhouse resistance to fitness in the field for a host of an emerging forest disease. Evol App. doi:10.1111/eva.12080
Hein I, Gilroy E, Armstrong M, Birch P (2009) The zig-zag-zig in oomycete-plant interactions. Mol Plant Pathol 10:547–562
Hüberli D, Garbelotto M (2011) Phytophthora ramorum is a generalist plant pathogen with differences in virulence between isolates from infectious and dead‐end hosts. Forest Pathol 42:8–13. doi:10.1111/j.1439-0329.2011.00715.x
Isakov O, Modai S, Shomron N (2011) Pathogen detection using short-RNA deep sequencing subtraction and assembly. Bioinformatics 27:2027–2030. doi:10.1093/bioinformatics/btr349
Ivors K, Garbelotto M, Vries I et al (2006) Microsatellite markers identify three lineages of Phytophthora ramorum in US nurseries, yet single lineages in US forest and European nursery populations. Molecular Ecology 15:1493–1505. doi:10.1111/j.1365-294X.2006.02864.x
Jiang R, Govers F (2006) Nonneutral GC3 and retroelement codon mimicry in Phytophthora. J Mol Evol 63:458–472. doi:10.1007/s00239-005-0211-3
Jiang RHY, Tyler BM, Whisson SC et al (2006) Ancient origin of elicitin gene clusters in Phytophthora genomes. Mol Biol Evol 23:338–351. doi:10.1093/molbev/msj039
Jiang R, Tripathy S, Govers F, Tyler B (2008) RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members. Proc Natl Acad Sci U S A 105:4874–4879. doi:10.1073/pnas.0709303105
Kamoun S (2003) Molecular genetics of pathogenic Oomycetes. Eukaryotic Cell 2:191–199. doi:10.1128/EC.2.2.191-199.2003
Kamoun S (2006) A catalogue of the effector secretome of plant pathogenic Oomycetes. Annu Rev Phytopathol 44:41–60. doi:10.1146/annurev.phyto.44.070505.143436
Kasuga T, Kozanitas M, Bui M et al (2012) Phenotypic diversification is associated with host-induced transposon derepression in the sudden oak death pathogen Phytophthora ramorum. PLoS ONE 7:e34728. doi:10.1371/journal.pone.0034728
Kawahara Y, Oono Y, Kanamori H et al (2012) Simultaneous RNA-seq analysis of a mixed transcriptome of rice and blast fungus interaction. PLoS ONE 7:e49423. doi:10.1371/journal.pone.0049423
Kleemann J, Rincon-Rivera LJ, Takahara H et al (2012) Sequential delivery of host-induced virulence effectors by appressoria and intracellular hyphae of the phytopathogen Collectrotrichum higginsianum. PLoS Pathog 8:e1002643. doi:10.1371/journal.ppat.1002643
Kurz WA, Stinson G, Rampley GJ et al (2008) Risk of natural disturbances makes future contribution of Canada’s forests to the global carbon cycle highly uncertain. Proc Natl Acad Sci U S A 105:1551–1555. doi:10.1073/pnas.0708133105
Lamsal S, Cobb RC, Hall Cushman J et al (2011) Spatial estimation of the density and carbon content of host populations for Phytophthora ramorum in California and Oregon. For Ecol Manage 262:989–998. doi:10.1016/j.foreco.2011.05.033
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25. doi:10.1186/gb-2009-10-3-r25
Lee S-J, Rose JK (2010) Mediation of the transition from biotrophy to necrotrophy in hemibiotrophic plant pathogens by secreted effector proteins. Plant Signal Behav 5:769–772
Le Provost G, Herrera R, Paiva J et al (2007) A micromethod for high throughput RNA extraction in forest trees. Biol Res 40:291–297
Lepoittevin C, Harvengt L, Plomion C, Garnier-Géré P (2011) Association mapping for growth, straightness and wood chemistry traits in the Pinus pinaster Aquitaine breeding population. Tree Genet Genomes 8:113–126. doi:10.1007/s11295-011-0426-y
Li H, Handsaker B, Wysoker A et al (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. doi:10.1093/bioinformatics/btp352
Li R, Gao S, Hernandez AG et al (2012) Deep sequencing of small RNAs in tomato for virus and viroid identification and strain differentiation. PLoS One. doi:10.1371/journal.pone.0037127
Loo J (2009) Ecological impacts of non-indigenous invasive fungi as forest pathogens. Biol Invasions 11:81–96. doi:10.1007/s10530-008-9321-3
Manos P, Cannon C, Oh S (2009) Phylogenetic relationships and taxonomic status of the paleoendemic fagaceae of Western North America: recognition of a new genus, Notholithocarpus. Madrono 55:181–190
Manter DK, Kelsey RG, Karchesy JJ (2007) Photosynthetic declines in Phytophthora ramorum-infected plants develop prior to water stress and in response to exogenous application of elicitins. Phytopathology 97:850–856. doi:10.1094/PHYTO-97-7-0850
Mascheretti S, Croucher P, Vettraino A et al (2008) Reconstruction of the Sudden Oak Death epidemic in California through microsatellite analysis of the pathogen Phytophthora ramorum. Mol Ecol 17:2755–2768. doi:10.1111/j.1365-294X.2008.03773.x
Matsumura H, Reich S, Ito A et al (2003) Gene expression analysis of plant host–pathogen interactions by SuperSAGE. Proc Natl Acad Sci U S A 100:15718–15723. doi:10.1073/pnas.2536670100
McPherson B, Mori S, Wood D et al (2010) Responses of oaks and tanoaks to the sudden oak death pathogen after 8y of monitoring in two coastal California forests. Ecol Manage 259:2248–2255. doi:10.1016/j.foreco.2010.02.020
Meyers KJ, Swiecki TJ, Mitchell AE (2006) Understanding the native Californian diet: identification of condensed and hydrolyzable tannins in tanoak acorns (Lithocarpus densiflorus). J Agric Food Chem 54:7686–7691. doi:10.1021/jf061264t
Moralejo E, Descals E (2011) Diplanetism and microcyclic sporulation in Phytophthora ramorum. Forest Pathol 41:349–354. doi:10.1111/j.1439-0329.2010.00674.x
Mortazavi A, Williams B, McCue K et al (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628. doi:10.1038/nmeth.1226
Neale DB, Kremer A (2011) Forest tree genomics: growing resources and applications. Nat Rev Genet 12:111–122. doi:10.1038/nrg2931
Norelli J, Farrell R, Bassett C et al (2009) Rapid transcriptional response of apple to fire blight disease revealed by cDNA suppression subtractive hybridization analysis. Tree Genet Genomes 5:27–40. doi:10.1007/s11295-008-0164-y
Orłowska E, Fiil A, Kirk H-G et al (2011) Differential gene induction in resistant and susceptible potato cultivars at early stages of infection by Phytophthora infestans. Plant Cell Rep 31:187–203. doi:10.1007/s00299-011-1155-2
Orshinsky AM, Hu J, Opiyo SO et al (2012) RNA-seq analysis of the Sclerotinia homoeocarpa—creeping bentgrass pathosystem. PLoS ONE 7:e41150. doi:10.1371/journal.pone.0041150
Oshlack A, Wakefield MJ (2009) Transcript length bias in RNA-seq data confounds systems biology. Biol Direct 4:14. doi:10.1186/1745-6150-4-14
Pachter L (2011) Models for transcript quantification from RNA-Seq. arXiv.org arXiv:1104.3889v2 [q-bio.GN].
Parchman TL, Geist KS, Grahnen JA et al (2010) Transcriptome sequencing in an ecologically important tree species: assembly, annotation, and marker discovery. BMC Genomics 11:180. doi:10.1186/1471-2164-11-180
Parke J, Oh E, Voelker S et al (2007) Phytophthora ramorum colonizes tanoak xylem and is associated with reduced stem water transport. Phytopathology 97:1558–1567. doi:10.1094/PHYTO-97-12-1558
Petre B, Morin E, Tisserant E et al (2012) RNA-seq of early-infected poplar leaves by the rust pathogen Melampsora larici-populina uncovers PtSultr3;5, a fungal-induced host sulfate transporter. PLoS ONE 7:e44408. doi:10.1371/journal.pone.0044408
Ramage BS, O’Hara KL, Forrestel AB (2011) Forest transformation resulting from an exotic pathogen: regeneration and tanoak mortality in coast redwood stands affected by sudden oak death. Can J Forest Res 41:763–772. doi:10.1139/x11-020
Rampant PF, Lesur I, Boussardon C et al (2011) Analysis of BAC end sequences in oak, a keystone forest tree species, providing insight into the composition of its genome. BMC Genomics 12:292. doi:10.1186/1471-2164-12-292
Reeser PW, Hansen EM, Sutton W (2007) Phytophthora siskiyouensis, a new species from soil, water, myrtlewood (Umbellularia californica) and tanoak (Lithocarpus densiflorus) in southwestern Oregon. Mycologia 99:639–643. doi:10.3852/mycologia.99.5.639
Risso D, Schwartz K, Sherlock G, Dudoit S (2011) GC-Content normalization for RNA-seq data. BMC Bioinformatics 12:480. doi:10.1186/1471-2105-12-480
Rizzo D, Garbelotto M, Davidson J et al (2002) Phytophthora ramorum as the cause of extensive mortality of Quercus spp. and Lithocarpus densiflorus in California. Plant Dis 86:205–214
Roberts A, Pachter L (2013) Streaming fragment assignment for real-time analysis of sequencing experiments. Nat Meth 10:71–73. doi:10.1038/nmeth.2251
Robertson G, Schein J, Chiu R et al (2010) De novo assembly and analysis of RNA-seq data. Nat Methods 7:909–912. doi:10.1038/nmeth.1517
Sanseverino W, Roma G, De Simone M et al (2010) PRGdb: a bioinformatics platform for plant resistance gene analysis. Nucleic Acids Res 38:D814–D821. doi:10.1093/nar/gkp978
Scott PM, Burgess TI, Barber PA et al (2009) Phytophthora multivora sp nov., a new species recovered from declining Eucalyptus, Banksia, Agonis and other plant species in Western Australia. Persoonia 22:1–13. doi:10.3767/003158509X415450
Seidl MF, Van den Ackerveken G, Govers F, Snel B (2011) A domain-centric analysis of Oomycete plant pathogen genomes reveals unique protein organization. Plant Physiol 155:628–644. doi:10.1104/pp. 110.167841
Shen D, Ye W, Dong S, Wang Y, Dou D (2011) Characterization of intronic structures and alternative splicing in Phytophthora sojae by comparative analysis of expressed sequence tags and genomic sequences. Can J Microbiol 57:84–90. doi:10.1139/W10-103
Sierra R, Rodriguez-R LM, Chaves D et al (2010) Discovery of Phytophthora infestans genes expressed in planta through mining of cDNA libraries. PLOS ONE 5(3):e9847. doi:10.1371/journal.pone.0009847
Stamm E, Parke J (2013) The effect of Phytophthora ramorum on the physiology and xylem function of young tanoak trees. Proceedings of the Fifth Sudden Oak Death Science Symposium, June 19–22, 2012, Petaluma, CA, USA GTR PSWXXX
Tooley P, Kyde K, Englander L (2004) Susceptibility of selected ericaceous ornamental host species to Phytophthora ramorum. Plant Dis 88:993–999
Tooley P, Browning M, Kyde K, Berner D (2009) Effect of temperature and moisture period on infection of Rhododendron “Cunningham’s White” by Phytophthora ramorum. Phytopathology 99:1045–1052. doi:10.1094/PHYTO-99-9-1045
Trapnell C, Pachter L, Salzberg S (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105–1111. doi:10.1093/bioinformatics/btp120
Trapnell C, Williams BA, Pertea G et al (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
Trapnell C, Roberts A, Goff L et al (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protocols 7:562–578. doi:10.1038/nprot.2012.016
Tyler B, Tripathy S, Zhang X et al (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313:1261–1266. doi:10.1126/science.1128796
Ueno S, Provost GL, Léger V, et al (2010) Bioinformatic analysis of ESTs collected by Sanger and pyrosequencing methods for a keystone forest tree species: oak. BMC Genomics 11:650. doi:10.1186/1471-2164-11-650
Van Loon LC, Van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55:85–97. doi:10.1006/pmpp.1999.0213
Waring K, O’Hara K (2008) Redwood/tanoak stand development and response to tanoak mortality caused by Phytophthora ramorum. Ecol Manage 255:2650–2658. doi:10.1016/j.foreco.2008.01.025
Weber G, Shendure J, Tanenbaum DM et al (2002) Identification of foreign gene sequences by transcript filtering against the human genome. Nat Genet 30:141–142. doi:10.1038/ng818
Westermann AJ, Gorski SA, Vogel J (2012) Dual RNA-seq of pathogen and host. Nat Rev Micro 10:618–630. doi:10.1038/nrmicro2852
Wheeler N, Sederoff R (2009) Role of genomics in the potential restoration of the American chestnut. Tree Genet Genomes 5:181–187. doi:10.1007/s11295-008-0180-y
Win J, Krasileva KV, Kamoun S et al (2012) Sequence divergent RXLR effectors share a structural fold conserved across plant pathogenic Oomycete species. PLoS Pathog 8:e1002400. doi:10.1371/journal.ppat.1002400
Winnenburg R, Baldwin TK, Urban M et al (2006) PHI-base: a new database for pathogen host interactions. Nucleic Acids Res 34:D459–D464. doi:10.1093/nar/gkj047
Xu Y, Stange-Thomann N, Weber G et al (2003) Pathogen discovery from human tissue by sequence-based computational subtraction. Genomics 81:329–335. doi:10.1016/S0888-7543(02)00043-5
Acknowledgments
We are grateful for funding provided by the Western Forest Transcriptome Survey of the USDA-Forest Service: Pacific Northwest Research Station, Pacific Southwest Research Station, and Rocky Mountain Research Stations; the Gordon and Betty Moore Foundation; and the National Science Foundation Ecology of Infectious Diseases Program. We thank Abdelali Barakat, Kenan Celtik, Tara Jennings, Alex Lundquist, Barb Rotz, and Chris Sullivan for generous assistance.
Data archiving statement
This Transcriptome Shotgun Assembly project has been deposited at DDBJ/EMBL/GenBank under the accession GAOS00000000. The version described in this paper is the first version, GAOS01000000.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J. Wegrzyn
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 1.32 MB)
Rights and permissions
About this article
Cite this article
Hayden, K.J., Garbelotto, M., Knaus, B.J. et al. Dual RNA-seq of the plant pathogen Phytophthora ramorum and its tanoak host. Tree Genetics & Genomes 10, 489–502 (2014). https://doi.org/10.1007/s11295-014-0698-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11295-014-0698-0