Section: Microbiology
Topic: Microbiology, Ecology, Population biology

Comparative abundance and diversity of populations of the Pseudomonas syringae and Soft Rot Pectobacteriaceae species complexes throughout the Durance River catchment from its French Alps sources to its delta

Corresponding author(s): Morris, C.E. (cindy.morris@inrae.fr)

10.24072/pcjournal.317 - Peer Community Journal, Volume 3 (2023), article no. e88.

Get full text PDF Peer reviewed and recommended by PCI
article image

Rivers, creeks, streams are integrators of biological, chemical and physical processes occurring in a catchment linking land cover from the headwaters to the outlet.  The dynamics of human and animal pathogens in catchments have been widely studied in a large variety of contexts allowing the optimization of disease risk reduction. In parallel, there is an emerging awareness that crop pathogens might also be disseminated via surface waters especially when they are used for irrigation. However, there are no studies on the extent to which potential plant pathogens are present – nor about their dynamics - along the full course of a catchment. Here we have compared the seasonal dynamics of populations of the Pseudomonas syringae (Psy) and the Soft Rot Pectobacteriaceae (SRP) species complexes along a 270 km stretch of the Durance River from the upstream alpine reaches to the downstream agricultural production areas at the confluence with the Rhone River at Avignon. Among 168 samples collected at 21 sites in fall, winter, spring and summer of 2016 and 2017, Psy strains were detected at all sampling sites and in 156 of the samples at population densities up to 105 bacteria L-1. In contrast, SRP strains were detected in 98 of the samples, mostly from the southern part of the river, at population densities that did not exceed 3 ´ 104 bacteria L-1. Among the biological and chemical parameters that were characterized at each sampling site, temperature was the only factor that explained a significant amount of the variability in population size for both species complexes. Psy densities decreased with increasing temperature whereas SRP densities increased with increasing temperature. River-borne populations of SRP were composed mainly of Pectobacterium versatile and P. aquaticum that have little known epidemiological importance. Only a few strains of Pectobacterium and Dickeya species reputed for their epidemiological impact were observed. In contrast, Psy populations at all sites were dominated by a genetic lineage of phylogroup 2 known from other studies for its broad host range and its geographic and habitat ubiquity. Our observations suggest that surveillance of river water for SRP could be leveraged to signal diagnostic and management reactions to avoid disease outbreaks.  In contrast, the constant presence of Psy throughout the catchment in absence of regular and widespread disease outbreaks due to this group of bacteria suggests that surveillance should focus on future changes in land use, river water conditions and agronomic practices that could destabilize the mechanisms currently holding Psy outbreaks in check.

Published online:
DOI: 10.24072/pcjournal.317
Type: Research article
Mots-clés : plant pathogenic bacteria, microbial ecology, hydrology, surface waters, irrigation

Morris, C.E. 1; Lacroix, C. 1; Chandeysson, C. 1; Guilbaud, C. 1; Monteil, C. 1; Piry, S. 1; Rochelle Newall, E. 2; Fiorini, S. 3; Van Gijsegem, F. 2; Barny, M.A. 2; Berge, O. 1

1 INRAE, Pathologie Végétale, F-84140, Montfavet, France
2 Sorbonne Université, INRAE, IRD, CNRS, UPEC, Institute of Ecology and Environmental Sciences-Paris (iEES-Paris), 4 place Jussieu, F-75252 Paris, France
3 Ecole Normale Supérieure, PSL Research University, CNRS, Centre de recherche en écologie expérimentale et prédictive (CEREEP-Ecotron Ile De France), UAR 3194, 11 chemin de Busseau, F-77140 Saint-Pierre-lès-Nemours, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
@article{10_24072_pcjournal_317,
     author = {Morris, C.E. and Lacroix, C. and Chandeysson, C. and Guilbaud, C. and Monteil, C. and Piry, S. and Rochelle Newall, E. and Fiorini, S. and Van Gijsegem, F. and Barny, M.A. and Berge, O.},
     title = {Comparative abundance and diversity of populations of the {\protect\emph{Pseudomonas} syringae} and {Soft} {Rot} {\protect\emph{Pectobacteriaceae}} species complexes throughout the {Durance} {River} catchment from its {French} {Alps} sources to its delta},
     journal = {Peer Community Journal},
     eid = {e88},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.317},
     language = {en},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.317/}
}
TY  - JOUR
AU  - Morris, C.E.
AU  - Lacroix, C.
AU  - Chandeysson, C.
AU  - Guilbaud, C.
AU  - Monteil, C.
AU  - Piry, S.
AU  - Rochelle Newall, E.
AU  - Fiorini, S.
AU  - Van Gijsegem, F.
AU  - Barny, M.A.
AU  - Berge, O.
TI  - Comparative abundance and diversity of populations of the Pseudomonas syringae and Soft Rot Pectobacteriaceae species complexes throughout the Durance River catchment from its French Alps sources to its delta
JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.317/
DO  - 10.24072/pcjournal.317
LA  - en
ID  - 10_24072_pcjournal_317
ER  - 
%0 Journal Article
%A Morris, C.E.
%A Lacroix, C.
%A Chandeysson, C.
%A Guilbaud, C.
%A Monteil, C.
%A Piry, S.
%A Rochelle Newall, E.
%A Fiorini, S.
%A Van Gijsegem, F.
%A Barny, M.A.
%A Berge, O.
%T Comparative abundance and diversity of populations of the Pseudomonas syringae and Soft Rot Pectobacteriaceae species complexes throughout the Durance River catchment from its French Alps sources to its delta
%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.317/
%R 10.24072/pcjournal.317
%G en
%F 10_24072_pcjournal_317
Morris, C.E.; Lacroix, C.; Chandeysson, C.; Guilbaud, C.; Monteil, C.; Piry, S.; Rochelle Newall, E.; Fiorini, S.; Van Gijsegem, F.; Barny, M.A.; Berge, O. Comparative abundance and diversity of populations of the Pseudomonas syringae and Soft Rot Pectobacteriaceae species complexes throughout the Durance River catchment from its French Alps sources to its delta. Peer Community Journal, Volume 3 (2023), article  no. e88. doi : 10.24072/pcjournal.317. https://peercommunityjournal.org/articles/10.24072/pcjournal.317/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.microbiol.100006

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Allex D, R. B. Les bactérioses des salades : un problème omniprésent, PHM-Rev. Hort., Volume 310 (1990), pp. 45-50

[2] Andrew, J.; Sauquet, E. Climate Change Impacts and Water Management Adaptation in Two Mediterranean-Climate Watersheds: Learning from the Durance and Sacramento Rivers, Water, Volume 9 (2017) no. 2 | DOI

[3] Ben Moussa, H.; Bertrand, C.; Rochelle-Newall, E.; Fiorini, S.; Pédron, J.; Barny, M.-A. The Diversity and Abundance of Soft Rot Pectobacteriaceae Along the Durance River Stream in the Southeast of France Revealed by Multiple Seasonal Surveys, Phytopathology, Volume 112 (2022) no. 8, pp. 1676-1685 | DOI

[4] Ben Moussa, H.; Pédron, J.; Bertrand, C.; Hecquet, A.; Barny, M.-A. Pectobacterium quasiaquaticum sp. nov., isolated from waterways, International Journal of Systematic and Evolutionary Microbiology, Volume 71 (2021) no. 10 | DOI

[5] Berge, O.; Monteil, C. L.; Bartoli, C.; Chandeysson, C.; Guilbaud, C.; Sands, D. C.; Morris, C. E. A User's Guide to a Data Base of the Diversity of Pseudomonas syringae and Its Application to Classifying Strains in This Phylogenetic Complex, PLoS ONE, Volume 9 (2014) no. 9 | DOI

[6] Bizic, M. Treating all pathogens alike: a call for whole-catchment monitoring of plant-pathogens, Peer Community in Microbiology (2023) | DOI

[7] Borschinger, B.; Bartoli, C.; Chandeysson, C.; Guilbaud, C.; Parisi, L.; Bourgeay, J.; Buisson, E.; Morris, C. A set of PCRs for rapid identification and characterization of Pseudomonas syringae phylogroups, Journal of Applied Microbiology, Volume 120 (2016) no. 3, pp. 714-723 | DOI

[8] Callahan, B. J.; McMurdie, P. J.; Rosen, M. J.; Han, A. W.; Johnson, A. J. A.; Holmes, S. P. DADA2: High-resolution sample inference from Illumina amplicon data, Nature Methods, Volume 13 (2016) no. 7, pp. 581-583 | DOI

[9] Chambre d’Agriculture PACA SRHA Provence Alpes Côte d’Azur: Stratégie Régionale Hydraulique Agricole, 2014 https://paca.chambres-agriculture.fr/fileadmin/user_upload/National/FAL_commun/publications/Provence-Alpes-Cote_d_Azur/rdiagnostic-agriculture_irriguee_paca_2014.pdf(accessed 1 April 2022)

[10] Cigna, J.; Dewaegeneire, P.; Beury, A.; Gobert, V.; Faure, D. A gapA PCR-sequencing Assay for Identifying the Dickeya and Pectobacterium Potato Pathogens, Plant Disease, Volume 101 (2017) no. 7, pp. 1278-1282 | DOI

[11] Duprey, A.; Taib, N.; Leonard, S.; Garin, T.; Flandrois, J.; Nasser, W.; Brochier‐Armanet, C.; Reverchon, S. The phytopathogenic nature of Dickeya aquatica 174/2 and the dynamic early evolution of Dickeya pathogenicity, Environmental Microbiology, Volume 21 (2019) no. 8, pp. 2809-2835 | DOI

[12] Eayre, C. G. Bacteriophages of Erwinia carotovora and Erwinia ananas Isolated from Freshwater Lakes., Plant Disease, Volume 79 (1995) no. 8 | DOI

[13] Escudié, F.; Auer, L.; Bernard, M.; Mariadassou, M.; Cauquil, L.; Vidal, K.; Maman, S.; Hernandez-Raquet, G.; Combes, S.; Pascal, G. FROGS: Find, Rapidly, OTUs with Galaxy Solution, Bioinformatics, Volume 34 (2017) no. 8, pp. 1287-1294 | DOI

[14] Faye, P.; Bertrand, C.; Pédron, J.; Barny, M.-A. Draft genomes of “Pectobacterium peruviense” strains isolated from fresh water in France, Standards in Genomic Sciences, Volume 13 (2018) no. 1 | DOI

[15] Gardan, L.; Cottin, S.; Bollet, C.; Hunault, G. Phenotypic heterogeneity of Pseudomonas syringae van Hall, Research in Microbiology, Volume 142 (1991) no. 9, pp. 995-1003 | DOI

[16] Gorski, L.; Cooley, M. B.; Oryang, D.; Carychao, D.; Nguyen, K.; Luo, Y.; Weinstein, L.; Brown, E.; Allard, M.; Mandrell, R. E.; Chen, Y. Prevalence and Clonal Diversity of over 1,200 Listeria monocytogenes Isolates Collected from Public Access Waters near Produce Production Areas on the Central California Coast during 2011 to 2016, Applied and Environmental Microbiology, Volume 88 (2022) no. 8 | DOI

[17] Guillorit-Rondeau, C.; Malandrin, L.; Samson, R. Identification of two serological flagellar types (H1 and H2) in Pseudomonas syringae pathovars, European Journal of Plant Pathology, Volume 102 (1996) no. 1, pp. 99-104 | DOI

[18] Harrison, M. D.; Franc, G. D.; Maddox, D. A.; Michaud, J. E.; McCarter-Zorner, N. J. Presence of Erwinia carotovora in surface water in North America, Journal of Applied Bacteriology, Volume 62 (1987) no. 6, pp. 565-570 | DOI

[19] Hélias, V.; Hamon, P.; Huchet, E.; Wolf, J. V. D.; Andrivon, D. Two new effective semiselective crystal violet pectate media for isolation of Pectobacterium and Dickeya, Plant Pathology, Volume 61 (2011) no. 2, pp. 339-345 | DOI

[20] Hong, J. C.; Momol, M. T.; Jones, J. B.; Ji, P.; Olson, S. M.; Allen, C.; Perez, A.; Pradhanang, P.; Guven, K. Detection of Ralstonia solanacearum in Irrigation Ponds and Aquatic Weeds Associated with the Ponds in North Florida, Plant Disease, Volume 92 (2008) no. 12, pp. 1674-1682 | DOI

[21] Hugouvieux-Cotte-Pattat, N.; Van Gijsegem, F. Diversity within the Dickeya zeae complex, identification of Dickeya zeae and Dickeya oryzae members, proposal of the novel species Dickeya parazeae sp. nov., International Journal of Systematic and Evolutionary Microbiology, Volume 71 (2021) no. 11 | DOI

[22] Ivanović, Ž.; Blagojević, J.; Nikolić, I. Leaf spot disease on Philodendron scandens, Ficus carica and Actinidia deliciosa caused by Pseudomonas syringae pv. syringae in Serbia, European Journal of Plant Pathology, Volume 151 (2018) no. 4, pp. 1107-1113 | DOI

[23] James, E.; Joyce, M. Assessment and Management of Watershed Microbial Contaminants, Critical Reviews in Environmental Science and Technology, Volume 34 (2004) no. 2, pp. 109-139 | DOI

[24] Jorge, P. E.; Harrison, M. D. The association ofErwinia carotovora with surface water in Northeastern Colorado. I. The presence and population of the bacterium in relation to location, season and water temperature, American Potato Journal, Volume 63 (1986) no. 10, pp. 517-531 | DOI

[25] Kuentz, A. Un siècle de variabilité hydro-climatique sur le bassin de la Durance: Recherches historiques et reconstitutions. AgroParisTech, Paris, 2013 (https://pastel.archives-ouvertes.fr/tel-01171004/document)

[26] Lamichhane, J. R.; Bartoli, C. Plant pathogenic bacteria in open irrigation systems: what risk for crop health?, Plant Pathology, Volume 64 (2015) no. 4, pp. 757-766 | DOI

[27] Laurila, J.; Ahola, V.; Lehtinen, A.; Joutsjoki, T.; Hannukkala, A.; Rahkonen, A.; Pirhonen, M. Characterization of Dickeya strains isolated from potato and river water samples in Finland, European Journal of Plant Pathology, Volume 122 (2008) no. 2, pp. 213-225 | DOI

[28] Lecompte, F. Management of soil nitrate heterogeneity resulting from crop rows in a lettuce–tomato rotation under a greenhouse, Agronomy for Sustainable Development, Volume 32 (2011) no. 3, pp. 811-819 | DOI

[29] Lindeberg, M.; Cunnac, S.; Collmer, A. Pseudomonas syringae type III effector repertoires: last words in endless arguments, Trends in Microbiology, Volume 20 (2012) no. 4, pp. 199-208 | DOI

[30] Ma, B.; Hibbing, M. E.; Kim, H.-S.; Reedy, R. M.; Yedidia, I.; Breuer, J.; Breuer, J.; Glasner, J. D.; Perna, N. T.; Kelman, A.; Charkowski, A. O. Host Range and Molecular Phylogenies of the Soft Rot Enterobacterial Genera Pectobacterium and Dickeya, Phytopathology, Volume 97 (2007) no. 9, pp. 1150-1163 | DOI

[31] McCarter-Zorner, N. J.; Franc, G.; Harrison, M.; Michaud, J. E.; Quinn, C.; Sells, I. A.; Graham, D. Soft rot Erwinia bacteria in surface and underground waters in southern Scotland and in Colorado, United States, Journal of Applied Bacteriology, Volume 57 (1984) no. 1, pp. 95-105 | DOI

[32] Monteil, C. L.; Bardin, M.; Morris, C. E. Features of air masses associated with the deposition of Pseudomonas syringae and Botrytis cinerea by rain and snowfall, The ISME Journal, Volume 8 (2014) no. 11, pp. 2290-2304 | DOI

[33] Monteil, C. L.; Lafolie, F.; Laurent, J.; Clement, J.; Simler, R.; Travi, Y.; Morris, C. E. Soil water flow is a source of the plant pathogen Pseudomonas syringae in subalpine headwaters, Environmental Microbiology, Volume 16 (2013) no. 7, pp. 2038-2052 | DOI

[34] Monteil, C. L.; Yahara, K.; Studholme, D. J.; Mageiros, L.; Méric, G.; Swingle, B.; Morris, C. E.; Vinatzer, B. A.; Sheppard, S. K. Population-genomic insights into emergence, crop adaptation and dissemination of Pseudomonas syringae pathogens, Microbial Genomics, Volume 2 (2016) no. 10 | DOI

[35] Morgan, M.; Anders, S.; Lawrence, M.; Aboyoun, P.; Pagès, H.; Gentleman, R. ShortRead: a bioconductor package for input, quality assessment and exploration of high-throughput sequence data, Bioinformatics, Volume 25 (2009) no. 19, pp. 2607-2608 | DOI

[36] Morris, C. Supplemental Figures & Tables for PCI Journal Microbiology https://doi.org/10.24072/pcjournal.317, Zenodo, 2023 | DOI

[37] Morris, C. E.; Lacroix, C.; Chandeysson, C.; Guilbaud, C.; Monteil, C.; Piry, S.; Rochelle Newall, E.; Fiorini, S.; Van Gijsegem, F.; Barny, M.-A.; Berge, O. Population densities of the Pseudomonas syringae species complex in the Durance river in 2016-2017. Dataset, Recherche Data Gouv, V1, 2023 | DOI

[38] Morris, C. E.; Sands, D. C.; Vanneste, J. L.; Montarry, J.; Oakley, B.; Guilbaud, C.; Glaux, C. Inferring the Evolutionary History of the Plant Pathogen Pseudomonas syringae from Its Biogeography in Headwaters of Rivers in North America, Europe, and New Zealand, mBio, Volume 1 (2010) no. 3 | DOI

[39] Morris, C. E.; Glaux, C.; Latour, X.; Gardan, L.; Samson, R.; Pitrat, M. The Relationship of Host Range, Physiology, and Genotype to Virulence on Cantaloupe in Pseudomonas syringae from Cantaloupe Blight Epidemics in France, Phytopathology, Volume 90 (2000) no. 6, pp. 636-646 | DOI

[40] Morris, C. E.; Kinkel, L. L.; Xiao, K.; Prior, P.; Sands, D. C. Surprising niche for the plant pathogen Pseudomonas syringae, Infection, Genetics and Evolution, Volume 7 (2007) no. 1, pp. 84-92 | DOI

[41] Morris, C. E.; Lamichhane, J. R.; Nikolić, I.; Stanković, S.; Moury, B. The overlapping continuum of host range among strains in the Pseudomonas syringae complex, Phytopathology Research, Volume 1 (2019) no. 1 | DOI

[42] Morris, C. E.; Monteil, C. L.; Berge, O. The Life History of Pseudomonas syringae: Linking Agriculture to Earth System Processes, Annual Review of Phytopathology, Volume 51 (2013) no. 1, pp. 85-104 | DOI

[43] Parisi, L.; Morgaint, B.; Blanco‐Garcia, J.; Guilbaud, C.; Chandeysson, C.; Bourgeay, J. F.; Moronvalle, A.; Brun, L.; Brachet, M. L.; Morris, C. E. Bacteria from four phylogroups of the Pseudomonas syringae complex can cause bacterial canker of apricot, Plant Pathology, Volume 68 (2019) no. 7, pp. 1249-1258 | DOI

[44] Parkinson, N.; Bryant, R.; Bew, J.; Conyers, C.; Stones, R.; Alcock, M.; Elphinstone, J. Application of Variable-Number Tandem-Repeat Typing To Discriminate Ralstonia solanacearum Strains Associated with English Watercourses and Disease Outbreaks, Applied and Environmental Microbiology, Volume 79 (2013) no. 19, pp. 6016-6022 | DOI

[45] Pédron, J.; Bertrand, C.; Taghouti, G.; Portier, P.; Barny, M.-A. Pectobacterium aquaticum sp. nov., isolated from waterways, International Journal of Systematic and Evolutionary Microbiology, Volume 69 (2019) no. 3, pp. 745-751 | DOI

[46] Pédron, J.; Guyon, L.; Lecomte, A.; Blottière, L.; Chandeysson, C.; Rochelle-Newall, E.; Raynaud, X.; Berge, O.; Barny, M.-A. Comparison of Environmental and Culture-Derived Bacterial Communities through 16S Metabarcoding: A Powerful Tool to Assess Media Selectivity and Detect Rare Taxa, Microorganisms, Volume 8 (2020) no. 8 | DOI

[47] Perombelon, M. C. M.; Kelman, A. Ecology of the Soft Rot Erwinias, Annual Review of Phytopathology, Volume 18 (1980) no. 1, pp. 361-387 | DOI

[48] Pietsch, R. B.; Vinatzer, B. A.; Schmale, D. G. Diversity and Abundance of Ice Nucleating Strains of Pseudomonas syringae in a Freshwater Lake in Virginia, USA, Frontiers in Microbiology, Volume 8 (2017) | DOI

[49] Portier, P.; Pédron, J.; Taghouti, G.; Dutrieux, C.; Barny, M.-A. Updated Taxonomy of Pectobacterium Genus in the CIRM-CFBP Bacterial Collection: When Newly Described Species Reveal “Old” Endemic Population, Microorganisms, Volume 8 (2020) no. 9 | DOI

[50] Potrykus, M.; Golanowska, M.; Sledz, W.; Zoledowska, S.; Motyka, A.; Kolodziejska, A.; Butrymowicz, J.; Lojkowska, E. Biodiversity of Dickeya spp. Isolated from Potato Plants and Water Sources in Temperate Climate, Plant Disease, Volume 100 (2016) no. 2, pp. 408-417 | DOI

[51] R Core Team R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria , 2020 (https://www.R-project.org/)

[52] Rankinen, K.; Butterfield, D.; Faneca Sànchez, M.; Grizzetti, B.; Whitehead, P.; Pitkänen, T.; Uusi-Kämppä, J.; Leckie, H. The INCA-Pathogens model: An application to the Loimijoki River basin in Finland, Science of The Total Environment, Volume 572 (2016), pp. 1611-1621 | DOI

[53] Sarkar, S. F.; Guttman, D. S. Evolution of the Core Genome of Pseudomonas syringae, a Highly Clonal, Endemic PlantPathogen, Applied and Environmental Microbiology, Volume 70 (2004) no. 4, pp. 1999-2012 | DOI

[54] Stopelli, E.; Conen, F.; Guilbaud, C.; Zopfi, J.; Alewell, C.; Morris, C. E. Ice nucleators, bacterial cells and Pseudomonas syringae in precipitation at Jungfraujoch, Biogeosciences, Volume 14 (2017) no. 5, pp. 1189-1196 | DOI

[55] Tomlinson, D. L.; Elphinstone, J. G.; Soliman, M. Y.; Hanafy, M. S.; Shoala, T. M.; Abd El-Fatah, H.; Agag, S. H.; Kamal, M.; Abd El-Aliem, M. M.; Fawzi, F. G.; Stead, D. E.; Janse, J. D. Recovery of Ralstonia solanacearum from canal water in traditional potato-growing areas of Egypt but not from designated Pest-Free Areas (PFAs), European Journal of Plant Pathology, Volume 125 (2009) no. 4, pp. 589-601 | DOI

[56] Toth, I. K.; Barny, M.-a.; Brurberg, M. B.; Condemine, G.; Czajkowski, R.; Elphinstone, J. G.; Helias, V.; Johnson, S. B.; Moleleki, L. N.; Pirhonen, M.; Rossmann, S.; Tsror, L.; van der Waals, J. E.; van der Wolf, J. M.; Van Gijsegem, F.; Yedidia, I. Pectobacterium and Dickeya: Environment to Disease Development, Plant Diseases Caused by Dickeya and Pectobacterium Species, Springer International Publishing, Cham, 2021, pp. 39-84 | DOI

[57] Waleron, M.; Misztak, A.; Waleron, M.; Franczuk, M.; Wielgomas, B.; Waleron, K. Transfer of Pectobacterium carotovorum subsp. carotovorum strains isolated from potatoes grown at high altitudes to Pectobacterium peruviense sp. nov., Systematic and Applied Microbiology, Volume 41 (2018) no. 2, pp. 85-93 | DOI

[58] Whitehead, P.; Leckie, H.; Rankinen, K.; Butterfield, D.; Futter, M.; Bussi, G. An INCA model for pathogens in rivers and catchments: Model structure, sensitivity analysis and application to the River Thames catchment, UK, Science of The Total Environment, Volume 572 (2016), pp. 1601-1610 | DOI

[59] Wickham, H. ggplot2: Elegant Graphics for Data Analysis, Use R!, Springer International Publishing, Cham, 2016 | DOI

[60] Zappia, R. E.; Hüberli, D.; Hardy, G. E. S. J.; Bayliss, K. L. Fungi and oomycetes in open irrigation systems: knowledge gaps and biosecurity implications, Plant Pathology, Volume 63 (2014) no. 5, pp. 961-972 | DOI

Cited by Sources:

block.super