[en] High-throughput sequencing (HTS), more specifically RNA sequencing of plant tissues, has become an indispensable tool for plant virologists to detect and identify plant viruses. During the data analysis step, plant virologists typically compare the obtained sequences to reference virus databases. In this way, they are neglecting sequences without homologies to viruses, which usually represent the majority of sequencing reads. We hypothesized that traces of other pathogens might be detected in this unused sequence data. In the present study, our goal was to investigate whether total RNA-seq data, as generated for plant virus detection, is also suitable for the detection of other plant pathogens and pests. As proof of concept, we first analyzed RNA-seq datasets of plant materials with confirmed infections by cellular pathogens in order to check whether these non-viral pathogens could be easily detected in the data. Next, we set up a community effort to re-analyze existing Illumina RNA-seq datasets used for virus detection to check for the potential presence of non-viral pathogens or pests. In total, 101 datasets from 15 participants derived from 51 different plant species were re-analyzed, of which 37 were selected for subsequent in-depth analyses. In 29 of the 37 selected samples (78%), we found convincing traces of non-viral plant pathogens or pests. The organisms most frequently detected in this way were fungi (15/37 datasets), followed by insects (13/37) and mites (9/37). The presence of some of the detected pathogens was confirmed by independent (q)PCRs analyses. After communicating the results, 6 out of the 15 participants indicated that they were unaware of the possible presence of these pathogens in their sample(s). All participants indicated that they would broaden the scope of their bioinformatic analyses in future studies and thus check for the presence of non-viral pathogens. In conclusion, we show that it is possible to detect non-viral pathogens or pests from total RNA-seq datasets, in this case primarily fungi, insects, and mites. With this study, we hope to raise awareness among plant virologists that their data might be useful for fellow plant pathologists in other disciplines (mycology, entomology, bacteriology) as well.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Haegeman, Annelies ; Plant Sciences Unit, Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), 9820 Merelbeke, Belgium
Foucart, Yoika; Plant Sciences Unit, Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), 9820 Merelbeke, Belgium
De Jonghe, Kris ; Plant Sciences Unit, Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), 9820 Merelbeke, Belgium
Goedefroit, Thomas; Plant Sciences Unit, Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), 9820 Merelbeke, Belgium
Al Rwahnih, Maher ; Foundation Plant Services, Department of Plant Pathology, University of California, Davis, CA 95616, USA
Boonham, Neil; School of Natural and Environmental Sciences, Newcastle University, Newcastle Upon Tyne NE1 7RU, UK
Candresse, Thierry ; UMR 1332 Biologie du Fruit et Pathologie, Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (INRAE), Université de Bordeaux, 33882 Villenave-d'Ornon, France
Gaafar, Yahya Z A ; Centre for Plant Health, Canadian Food Inspection Agency, 8801 East Saanich Road, North Saanich, BC V8L 1H3, Canada
Hurtado-Gonzales, Oscar P ; Plant Germplasm Quarantine Program, Animal and Plant Health Inspection Service, United States Department of Agriculture (USDA-APHIS), Beltsville, ML 20705, USA
Kogej Zwitter, Zala ; Department of Biotechnology and Systems Biology, National Institute of Biology (NIB), 1000 Ljubljana, Slovenia ; Jožef Stefan International Postgraduate School, 1000 Ljubljana, Slovenia
Kutnjak, Denis ; Department of Biotechnology and Systems Biology, National Institute of Biology (NIB), 1000 Ljubljana, Slovenia
Lamovšek, Janja; Plant Protection Department, Agricultural Institute of Slovenia (KIS), 1000 Ljubljana, Slovenia
Lefebvre, Marie; UMR 1332 Biologie du Fruit et Pathologie, Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (INRAE), Université de Bordeaux, 33882 Villenave-d'Ornon, France
Malapi, Martha; Biotechnology Risk Analysis Program, Animal and Plant Health Inspection Service, United States Department of Agriculture (USDA-APHIS), Riverdale, ML 20737, USA
Mavrič Pleško, Irena; Plant Protection Department, Agricultural Institute of Slovenia (KIS), 1000 Ljubljana, Slovenia
Önder, Serkan ; Department of Plant Protection, Faculty of Agriculture, Eskişehir Osmangazi University, Odunpazarı, Eskişehir 26160, Turkey
Reynard, Jean-Sébastien ; Department of Plant Protection, Agroscope, 1260 Nyon, Switzerland
Salavert Pamblanco, Ferran; School of Natural and Environmental Sciences, Newcastle University, Newcastle Upon Tyne NE1 7RU, UK
Schumpp, Olivier ; Department of Plant Protection, Agroscope, 1260 Nyon, Switzerland
Stevens, Kristian; Foundation Plant Services, Department of Plant Pathology, University of California, Davis, CA 95616, USA
Pal, Chandan; Zespri International Limited, 400 Maunganui Road, Mount Maunganui 3116, New Zealand
Tamisier, Lucie ; Unités GAFL et Pathologie Végétale, Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (INRAE), 84143 Montfavet, France
Ulubaş Serçe, Çiğdem ; Department of Plant Production and Technologies, Faculty of Agricultural Sciences and Technologies, Niğde Ömer Halisdemir University, 51240 Niğde, Turkey
van Duivenbode, Inge; Dutch General Inspection Service for Agricultural Seed and Seed Potatoes (NAK), Randweg 14, 8304 AS Emmeloord, The Netherlands
Waite, David W ; Plant Health and Environment Laboratory, Ministry for Primary Industries, Auckland 1140, New Zealand
Hu, Xiaojun; Plant Germplasm Quarantine Program, Animal and Plant Health Inspection Service, United States Department of Agriculture (USDA-APHIS), Beltsville, ML 20705, USA
Ziebell, Heiko ; Institute for Epidemiology and Pathogen Diagnostics, Federal Research Centre for Cultivated Plants, Julius Kühn Institute (JKI), Messeweg 11-12, 38104 Braunschweig, Germany
Massart, Sébastien ; Université de Liège - ULiège > TERRA Research Centre > Gestion durable des bio-agresseurs
FPS Health Federal Public Service Health, Food Chain Safety and Environment Slovenian Research Agency
Funding text :
This research was partially funded by the Belgian Federal Public Service of Health, Food Chain Safety and Environment (FPS Health) through the contract “RI 18_A-289” and by the Euphresco project “Plant Health Bioinformatics Network” (PHBN) (2018-A-289). This research benefited from COST (European Cooperation in Science and Technology) Action FA1407 (DIVAS). This research was partially financed by Slovenian Research Agency (project and core financing grants No. P4-0072, L7-2632 and P4-0165).
Handelsman J. Rondon M.R. Brady S.F. Clardy J. Goodman R.M. Molecular biological access to the chemistry of unknown soil microbes: A new frontier for natural products Chem. Biol. 1998 5 R245 R249 10.1016/S1074-5521(98)90108-9 9818143
Goldberg B. Sichtig H. Geyer C. Ledeboer N. Weinstock G.M. Making the leap from research laboratory to clinic: Challenges and opportunities for next-generation sequencing in infectious disease diagnostics MBio 2015 6 e01888-15 10.1128/mBio.01888-15 26646014
Forbes J.D. Knox N.C. Ronholm J. Pagotto F. Reimer A. Metagenomics: The next culture-independent game changer Front. Microbiol. 2017 8 1069 10.3389/fmicb.2017.01069 28725217
Lebas B. Adams I. Al Rwahnih M. Baeyen S. Bilodeau G.J. Blouin A.G. Boonham N. Candresse T. Chandelier A. De Jonghe K. et al. Facilitating the adoption of high-throughput sequencing technologies as a plant pest diagnostic test in laboratories: A step-by-step description EPPO Bull. 2022 52 394 418 10.1111/epp.12863
Hardwick S. Deveson I.W. Mercer T.R. Reference standards for next-generation sequencing Nat. Rev. Genet. 2017 18 473 484 10.1038/nrg.2017.44 28626224
Kreuze J.F. Perez A. Untiveros M. Quispe D. Fuentes S. Barker I. Simon R. Complete viral genome sequence and discovery of novel viruses by deep sequencing of small RNAs: A generic method for diagnosis, discovery and sequencing of viruses Virology 2009 388 1 7 10.1016/j.virol.2009.03.024
Adams I.P. Glover R.H. Monger W.A. Mumford R. Jackeviciene E. Navalinskiene M. Samuitiene M. Boonham N. Next-generation sequencing and metagenomic analysis: A universal diagnostic tool in plant virology Mol. Plant Pathol. 2009 10 537 545 10.1111/j.1364-3703.2009.00545.x
Al Rwahnih M. Daubert S. Golino D. Rowhani A. Deep sequencing analysis of RNAs from a grapevine showing Syrah decline symptoms reveals a multiple virus infection that includes a novel virus Virology 2009 387 395 401 10.1016/j.virol.2009.02.028
Donaire L. Wang Y. Gonzalez-Ibeas D. Mayer K.F. Aranda M.A. Llave C. Deep-sequencing of plant viral small RNAs reveals effective and widespread targeting of viral genomes Virology 2009 392 203 214 10.1016/j.virol.2009.07.005
Massart S. Olmos A. Jijakli H. Candresse T. Current impact and future directions of high throughput sequencing in plant virus diagnostics Virus Res. 2014 188 90 96 10.1016/j.virusres.2014.03.029 24717426
Pecman A. Kutnjak D. Gutiérrez-Aguirre I. Adams I. Fox A. Boonham N. Ravnikar M. Next generation sequencing for detection and discovery of plant viruses and viroids: Comparison of two approaches Front. Microbiol. 2017 8 1998 10.3389/fmicb.2017.01998 29081770
Adams I. Fox A. Diagnosis of plant viruses using next-generation sequencing and metagenomic analysis Current Research Topics in Plant Virology Wang A. Zhou X. Springer International Publishing Cham, Switzerland 2016 323 335
Maree H.J. Fox A. Al Rwahnih M. Boonham N. Application of HTS for routine plant virus diagnostics: State of the art and challenges Front. Plant Sci. 2018 9 1082 10.3389/fpls.2018.01082 30210506
Tedersoo L. Drenkhan R. Anslan S. Morales-Rodriguez C. Cleary M. High-throughput identification and diagnostics of pathogens and pests: Overview and practical recommendations Mol. Ecol. Resour. 2019 19 47 76 10.1111/1755-0998.12959
Badial A.B. Sherman D. Stone A. Gopakumar A. Wilson V. Schneider W. King J. Nanopore sequencing as a surveillance tool for plant pathogens in plant and insect tissues Plant Dis. 2018 102 1648 1652 10.1094/PDIS-04-17-0488-RE
Chalupowicz L. Dombrovsky A. Gaba V. Luria N. Reuven M. Beerman A. Lachman O. Dror O. Nissan G. Manulis-Sasson S. Diagnosis of plant diseases using the Nanopore sequencing platform Plant Pathol. 2019 68 229 238 10.1111/ppa.12957
Espindola A. Schneider W. Hoyt P.R. Marek S.M. Garzon C. A new approach for detecting fungal and oomycete plant pathogens in next generation sequencing metagenome data utilising electronic probes Int. J. Data Min. Bioinform. 2015 12 115 128 10.1504/IJDMB.2015.069422
Stobbe A.H. Daniels J. Espindola A.S. Verma R. Melcher U. Ochoa-Corona F. Garzon C. Fletcher J. Schneider W. E-probe Diagnostic Nucleic acid Analysis (EDNA): A theoretical approach for handling of next generation sequencing data for diagnostics J. Microbiol. Methods 2013 94 356 366 10.1016/j.mimet.2013.07.002
Gómez-Rodríguez C. Timmermans M.J.T.N. Crampton-Platt A. Vogler A.P. Intraspecific genetic variation in complex assemblages from mitochondrial metagenomics: Comparison with DNA barcodes Methods Ecol. Evol. 2017 8 248 256 10.1111/2041-210X.12667
Adams I.P. Fox A. Boonham N. Massart S. De Jonghe K. The impact of high throughput sequencing on plant health diagnostics Eur. J. Plant Pathol. 2018 152 909 919 10.1007/s10658-018-1570-0
Gaafar Y.Z.A. Ziebell H. Comparative study on three viral enrichment approaches based on RNA extraction for plant virus/viroid detection using high-throughput sequencing PLoS ONE 2020 15 e0237951 10.1371/journal.pone.0237951 32841302
Kutnjak D. Tamisier L. Adams I. Boonham N. Candresse T. Chiumenti M. De Jonghe K. Kreuze J.F. Lefebvre M. Silva G. et al. A primer on the analysis of high-throughput sequencing data for detection of plant viruses Microorganisms 2021 9 841 10.3390/microorganisms9040841 33920047
Chandler J.A. Liu R.M. Bennett S.N. RNA Shotgun metagenomic sequencing of northern California (USA) mosquitoes uncovers viruses, bacteria, and fungi Front. Microbiol. 2015 6 185 10.3389/fmicb.2015.00185
Toffolatti S.L. De Lorenzis G. Brilli M. Moser M. Shariati V. Tavakol E. Maddalena G. Passera A. Casati P. Pindo M. et al. Novel aspects on the interaction between grapevine and Plasmopara viticola: Dual-RNA-seq analysis highlights gene expression dynamics in the pathogen and the plant during the battle for infection Genes 2020 3 261 10.3390/genes11030261
Kawahara Y. Oono Y. Kanamori H. Matsumoto T. Itoh T. Minami E. Simultaneous RNA-seq analysis of a mixed transcriptome of rice and blast fungus interaction PLoS ONE 2012 7 e49423 10.1371/journal.pone.0049423 23139845
Musungu B. Bhatnagar D. Quiniou S. Brown R.L. Payne G.A. O’Brian G. Fakhoury A.M. Geisler M. Use of Dual RNA-seq for systems biology analysis of Zea mays and Aspergillus flavus interaction Front. Microbiol. 2020 11 853 10.3389/fmicb.2020.00853 32582038
Nerva L. Garcia J.F. Favaretto F. Giudice G. Moffa L. Sandrini M. Cantu D. Zanzotto A. Gardiman M. Velasco R. et al. The hidden world within plants: Metatranscriptomics unveils the complexity of wood microbiomes J. Exp. Bot. 2022 73 2682 2697 10.1093/jxb/erac032
Law S.R. Serrano A.R. Daguerre Y. Sundh J. Schneider A.N. Stangl Z.R. Castro D. Grabherr M. Näsholm T. Street N.R. et al. Metatranscriptomics captures dynamic shifts in mycorrhizal coordination in boreal forests Proc. Natl. Acad. Sci. USA 2022 119 e2118852119 10.1073/pnas.2118852119
Llontop M.E.M. Sharma P. Flores M.A. Yang S. Pollok J. Tian L. Huang C. Rideout S. Heath L.S. Li S. et al. Strain-level identification of bacterial tomato pathogens directly from metagenomic sequences Phytopathology 2020 110 768 779 10.1094/PHYTO-09-19-0351-R
Xu R. Adam L. Chapados J. Soliman A. Daayf F. Tambong J.T. MinION Nanopore-based detection of Clavibacter nebraskensis, the corn Goss’s wilt pathogen, and bacteriomic profiling of necrotic lesions of naturally-infected leaf samples PLoS ONE 2021 16 e0245333 10.1371/journal.pone.0245333
Hu Y. Green G.S. Milgate A.W. Stone E.A. Rathjen J.P. Schwessinger B. Pathogen detection and microbiome analysis of infected wheat using a portable DNA sequencer Phytobiomes J. 2019 3 92 101 10.1094/PBIOMES-01-19-0004-R
Loit K. Adamson K. Bahram M. Puusepp R. Anslan S. Kiiker R. Drenkhan R. Tedersood L. Relative performance of MinION (Oxford Nanopore Technologies) versus Sequel (Pacific Biosciences) third-generation sequencing instruments in identification of agricultural and forest fungal pathogens Appl. Environ. Microbiol. 2019 85 e01368-19 10.1128/AEM.01368-19 31444199
Yang S. Johnson M.A. Hansen M.A. Bush E. Li S. Vinatzer B.A. Metagenomic sequencing for detection and identification of the boxwood blight pathogen Calonectria pseudonaviculata Sci. Rep. 2022 12 1399 10.1038/s41598-022-05381-x
Johnson M.A. Liu H. Bush E. Sharma P. Yang S. Mazloom R. Heath L.S. Nita M. Li S. Vinatzer B.A. Investigating plant disease outbreaks with long-read metagenomics: Sensitive detection and highly resolved phylogenetic reconstruction applied to Xylella fastidiosa Microb. Genomics 2022 8 000822 10.1099/mgen.0.000822
Kulik T. Molcan T. Fiedorowicz G. van Diepeningen A. Stakheev A. Treder K. Olszewski J. Bilska K. Beyer M. Pasquali M. et al. Whole-genome single nucleotide polymorphism analysis for typing the pandemic pathogen Fusarium graminearum sensu stricto Front. Microbiol. 2022 13 885978 10.3389/fmicb.2022.885978 35923405
Rong W. Rollin J. Hanafi M. Roux N. Massart S. Validation of high throughput sequencing as virus indexing test for Musa germplasm: Performance criteria evaluation and contamination monitoring using an alien control PhytoFrontiers 2022 1 35 10.1094/PHYTOFR-03-22-0030-FI
Malnoy M. Martens S. Norelli J.L. Barny M.-A. Sundin G.W. Smits T.H.M. Duffy B. Fire blight: Applied genomic insights of the pathogen and host Annu. Rev. Phytopathol. 2012 50 475 494 10.1146/annurev-phyto-081211-172931
Jacques M.A. Arlat M. Boulanger A. Boureau T. Carrère S. Cesbron S. Chen N.W.G. Cociancich S. Darrasse A. Denancé N. et al. Using ecology, physiology, and genomics to understand host specificity in Xanthomonas Annu. Rev. Phytopathol. 2016 54 163 187 10.1146/annurev-phyto-080615-100147
Hu J. Wei Z. Kowalchuk G.A. Xu Y. Shen Q. Jousset A. Rhizosphere microbiome functional diversity and pathogen invasion resistance build up during plant development Environ. Microbiol. 2020 22 5005 5018 10.1111/1462-2920.15097
Lazcano C. Boyd E. Holmes G. Hewavitharana S. Pasulka A. Ivors K. The rhizosphere microbiome plays a role in the resistance to soil-borne pathogens and nutrient uptake of strawberry cultivars under field conditions Sci. Rep. 2021 11 3188 10.1038/s41598-021-82768-2
Ye S.H. Siddle K.J. Park D.J. Sabeti P.C. Benchmarking metagenomics tools for taxonomic classification Cell 2019 178 779 794 10.1016/j.cell.2019.07.010 31398336
Kalantar K.L. Carvalho T. De Bourcy C.F.A. Dimitrov B. Dingle G. Egger R. Han J. Holmes O.B. Juan Y.F. King R. et al. IDseq—An open source cloud-based pipeline and analysis service for metagenomic pathogen detection and monitoring Gigascience 2021 9 giaa111 10.1093/gigascience/giaa111 33057676
Menzel P. Ng K.L. Krogh A. Fast and sensitive taxonomic classification for metagenomics with Kaiju Nat. Commun. 2016 7 11257 10.1038/ncomms11257 27071849
Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads EMBnet. J. 2011 17 10 12 10.14806/ej.17.1.200
Wood D.E. Lu J. Langmead B. Improved metagenomic analysis with Kraken 2 Genome Biol. 2019 20 257 10.1186/s13059-019-1891-0 31779668
Sayers E.W. Beck J. Brister J.R. Bolton E.E. Canese K. Comeau D.C. Funk K. Ketter A. Kim S. Kimchi A. et al. Database resources of the National Center for Biotechnology Information Nucleic Acids Res. 2020 48 D9 D16 10.1093/nar/gkz899
Ondov B.D. Bergman N.H. Phillippy A.M. Interactive metagenomic visualization in a web browser BMC Bioinform. 2011 12 385 10.1186/1471-2105-12-385
Yilmaz P. Parfrey L.W. Yarza P. Gerken J. Pruesse E. Quast C. Schweer T. Peplies J. Ludwig W. Glöckner F.O. The SILVA and “all-species Living Tree Project (LTP)” taxonomic frameworks Nucleic Acids Res. 2014 42 643 648 10.1093/nar/gkt1209
Li H. Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform Bioinformatics 2009 25 1754 1760 10.1093/bioinformatics/btp324
Li H. Handsaker B. Wysoker A. Fennell T. Ruan J. Homer N. Marth G. Abecasis G. Durbin R. The Sequence Alignment/Map format and SAMtools Bioinformatics 2009 25 2078 2079
Wickham H. ggplot2 Elegant Graphics for Data Analysis Springer New York, NY, USA 2016
R Core Team R Core Team R: A Language and Environment for Statistical Computing R Foundation for Statistical Computing Vienna, Austria 2020 Available online: http//www.R-project.org/ (accessed on 1 March 2023)
RStudio Team RStudio: Integrated Development for R RStudio, Inc. Boston, MA, USA 2020 Available online: http://www.rstudio.com (accessed on 1 March 2023)
Muzhinji N. Dube J. de Haan E. Woodhall J. van der Waals J. Development of a TaqMan PCR assay for specific detection and quantification of Pectobacterium brasiliense in potato tubers and soil Eur. J. Plant Pathol. 2020 158 521 532 10.1007/s10658-020-02097-4
Hodgetts J. Boonham N. Mumford R. Dickinson M. Panel of 23S rRNA gene-based real-time PCR assays for improved universal and group-specific detection of phytoplasmas Appl. Environ. Microbiol. 2009 75 2945 2950 10.1128/AEM.02610-08 19270148
Fan X. Zhang J. Yang L. Wu M. Chen W. Li G. Development of PCR-based assays for detecting and differentiating three species of Botrytis infecting broad bean Plant Dis. 2015 99 691 698 10.1094/PDIS-07-14-0701-RE 30699675
Chakdar H. Goswami S.K. Singh E. Choudhary P. Yadav J. Kashyap P.L. Srivastava A.K. Saxena A.K. noxB-based marker for Alternaria spp.: A new diagnostic marker for specific and early detection in crop plants 3 Biotech 2019 9 249 10.1007/s13205-019-1779-4 31218173
Wickham H. Francois R. Henry L. Müller K. dplyr: A Grammar of Data Manipulation. R Packag. Version 1.0.2 2020 Available online: https://dplyr.tidyverse.org/ (accessed on 1 March 2023)