Fungi, nematodes and oomycetes belong to the most prominent eukaryotic plant pathogenic organisms. Unicellular organisms from other eukaryotic lineages, commonly addressed as protists, also infect plants. This review provides an introduction to plant pathogenic protists, including algae infecting oomycetes, and their current state of research.

Applied Plant Ecophysiology Haute Ecole Provinciale de Hainaut Condorcet Ath 7800 Belgium

Department of Plant Biology Uppsala BioCentre Linnean Centre for Plant Biology Swedish University of Agricultural Sciences Uppsala SE 75007 Sweden

Faculty of Sciences University of South Bohemia 37005 České Budějovice Czech Republic

Institute of Microbiology University of Innsbruck Innsbruck 6020 Austria

Institute of Parasitology Biology Centre 37005 České Budějovice Czech Republic

Integrated Microbial Biodiversity Canadian Institute for Advanced Research Toronto Ontario M5G 1Z8 Canada

New Zealand Institute for Plant and Food Research Ltd Lincoln 7608 New Zealand

Plant Pathology Institute of Integrative Biology ETH Zurich Zurich 8092 Switzerland

School of Biosciences University of Melbourne Parkville Vic 3010 Australia

School of Biosciences Victorian Marine Science Consortium Queenscliff Vic 3225 Australia

The Scottish Association for Marine Science Scottish Marine Institute Oban PA37 1QA UK

Université catholique de Louvain Earth and Life Institute Louvain la Neuve 1348 Belgium

Zobrazit více v PubMed

Adl, S.M. , Simpson, A.G.B. , Lane, C.E. , Lukes, J. , Bass, D. , Bowser, S.S. , Brown, M.W. , Burki, F. , Dunthorn, M. , Hampl, V. , Heiss, A. , Hoppenrath, M. , Lara, E. , Le Gall, L. , Lynn, D.H. , McManus, H. , Mitchell, E.A. , Mozley‐Stanridge, S.E. , Parfrey, L.W. , Pawlowski, J. , Rueckert, S. , Shadwick, L. , Schoch, C.L. , Smirnov, A. and Spiegel, F.W. (2012) The revised classification of eukaryotes. J. Eukaryot. Microbiol. 59, 429–493. PubMed PMC

Agarwal, A. , Kaul, V. , Faggian, R. , Rookes, J.E. , Ludwig‐Muller, J. and Cahill, D.M. (2011) Analysis of global host gene expression during the primary phase of the Arabidopsis thaliana–Plasmodiophora brassicae interaction. Funct. Plant Biol. 38, 462–478. PubMed

Aist, J.R. and Williams, P.H. (1971) The cytology and kinetics of cabbage root hair penetration by Plasmodiophora brassicae . Can. J. Bot. 49, 2023–2034.

Amano, H. , Suginaga, R. , Arashima, K. and Noda, H. (1995) Immunological detection of the fungal parasite, Pythium sp. – the causative organism of red rot disease in Porphyra‐yezoensis . J. Appl. Phycol. 7, 53–58.

Amon, J.P. (1978) Thraustochytrids and labyrinthulids of terrestrial, aquatic and hypersaline environments of the Great Salt Lake, USA. Mycologia, 70, 1299–1301.

Arasaki, S. (1947) Studies on the rot of Porphyra tenera by Pythium . Nippon Suisan Gakkaishi, 13, 74–90.

Balendres, M.A. , Nichols, D.S. , Tegg, R.S. and Wilson, C.R. (2016) Metabolomes of potato root exudates: compounds that stimulate resting spore germination of the soil‐borne pathogen Spongospora subterranea . J. Agric. Food Chem. 64, 7466–7474. PubMed

Beakes, G.W. , Glockling, S.L. and Sekimoto, S. (2012) The evolutionary phylogeny of the oomycete “fungi”. Protoplasma, 249, 3–19. PubMed

Bi, K. , He, Z. , Gao, Z. , Zhao, Y. , Fu, Y. , Cheng, J. , Xie, J. , Jiang, D. and Chen, T. (2016) Integrated omics study of lipid droplets from Plasmodiophora brassicae . Sci. Rep. 6, 36 965. PubMed PMC

Bigelow, D. , Olsen, M. and Gilbertson, R. (2005) Labyrinthula terrestris sp. nov., a new pathogen of turf grass. Mycologia, 97, 185–190. PubMed

Bittara, F.G. , Thompson, A.L. , Gudmestad, N.C. and Secor, G.A. (2016) Field evaluation of potato genotypes for resistance to powdery scab on tubers and root gall formation caused by Spongospora subterranea . Am. J. Potato Res. 93, 497–508.

Bockelmann, A.‐C. , Tams, V. , Ploog, J. , Schubert, P.R. and Reusch, T.B. (2013) Quantitative PCR reveals strong spatial and temporal variation of the wasting disease pathogen, Labyrinthula zosterae in northern European eelgrass (Zostera marina) beds. PLoS One, 8, e62169. PubMed PMC

Brakel, J. , Werner, F.J. , Tams, V. , Reusch, T.B.H. and Bockelmann, A.C. (2014) Current European Labyrinthula zosterae are not virulent and modulate seagrass (Zostera marina) defense gene expression. PLoS One, 9, e92448. PubMed PMC

Bulman, S. and Braselton, J.P. (2014) Rhizaria: Phytomyxea In: The Mycota VII, Part A, Systematics and Evolution (McLaughlin D. J. and Spatafora J. W., eds.), pp. 99–112. Springer Berlin Heidelberg.

Bulman, S. , Candy, J.M. , Fiers, M. , Lister, R. , Conner, A.J. and Eady, C.C. (2011) Genomics of biotrophic, plant‐infecting plasmodiophorids using in vitro dual cultures. Protist, 162, 449–461. PubMed

Bulman, S.R. and Marshall, J.W. (1998) Detection of Spongospora subterranea in potato tuber lesions using the polymerase chain reaction (PCR). Plant Pathol. 47, 759–766.

Burki, F. and Keeling, P.J. (2014) Rhizaria. Curr. Biol. 24, R103–R107. PubMed

Burki, F. , Kudryavtsev, A. , Matz, M.V. , Aglyamova, G.V. , Bulman, S. , Fiers, M. , Keeling, P.J. and Pawlowski, J. (2010) Evolution of Rhizaria: new insights from phylogenomic analysis of uncultivated protists. BMC Evol. Biol. 10, 377. PubMed PMC

Butler, C.E. , Jaskowska, E. and Kelly, S. (2017) Genome sequence of Phytomonas françai, a cassava (Manihot esculenta) latex parasite. Genome Announc. 5, e01266–16. PubMed PMC

Camargo, E.P. (1999) Phytomonas and other trypanosomatid parasites of plants and fruit. Adv. Parasitol. 42, 29–112. PubMed

Carré, P. and Pouzet, A. (2014) Rapeseed market, worldwide and in Europe. OCL, 21, D102.

Chen, J. , Pang, W. , Chen, B. , Zhang, C. and Piao, Z. (2015) Transcriptome analysis of Brassica rapa near‐isogenic lines carrying clubroot‐resistant and ‐susceptible alleles in response to Plasmodiophora brassicae during early infection. Front. Plant Sci. 6, 1183. PubMed PMC

Chitrampalam, P. , Goldberg, N. and Olsen, M.W. (2015) Labyrinthula species associated with turfgrasses in Arizona and New Mexico. Eur. J. Plant Pathol. 143, 485–493.

Christianen, M.J.A. , van Belzen, J. , Herman, P.M.J. , van Katwijk, M.M. , Lamers, L.P.M. , van Leent, P.J.M. and Bouma, TJ. (2013) Low‐canopy seagrass beds still provide important coastal protection services. PLoS One, 8, e62413. PubMed PMC

Cock, J.M. , Sterck, L. , Rouze, P. , Scornet, D. , Allen, A.E. , Amoutzias, G. , Anthouard, V. , Artiguenave, F. , Aury, J.M. , Badger, J.H. , Beszteri, B. , Billiau, K. , Bonnet, E. , Bothwell, J.H. , Bowler, C. , Boyen, C. , Brownlee, C. , Carrano, C.J. , Charrier, B. , Cho, G.Y. , Coelho, S.M. , Collén, J. , Corre, E. , Da Silva, C. , Delage, L. , Delaroque, N. , Dittami, S.M. , Doulbeau, S. , Elias, M. , Farnham, G. , Gachon, C.M. , Gschloessl, B. , Heesch, S. , Jabbari, K. , Jubin, C. , Kawai, H. , Kimura, K. , Kloareg, B. , Küpper, F.C. , Lang, D. , Le Bail, A. , Leblanc, C. , Lerouge, P. , Lohr, M. , Lopez, P.J. , Martens, C. , Maumus, F. , Michel, G. , Miranda‐Saavedra, D. , Morales, J. , Moreau, H. , Motomura, T. , Nagasato, C. , Napoli, C.A. , Nelson, D.R. , Nyvall‐Collén, P. , Peters, A.F. , Pommier, C. , Potin, P. , Poulain, J. , Quesneville, H. , Read, B. , Rensing, S.A. , Ritter, A. , Rousvoal, S. , Samanta, M. , Samson, G. , Schroeder, D.C. , Ségurens, B. , Strittmatter, M. , Tonon, T. , Tregear, J.W. , Valentin, K. , von Dassow, P. , Yamagishi, T. , Van de Peer, Y. and Wincker, P. (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature, 465, 617–621. PubMed

Coelho, S.M. , Godfroy, O. , Arun, A. , Le Corguillé, G. , Peters, A.F. and Cock, J.M. (2011) Genetic regulation of life cycle transitions in the brown alga Ectocarpus . Plant Signal. Behav. 6, 1858–1860. PubMed PMC

Collado‐Mercado, E. , Radway, J.C. and Collier, J.L. (2010) Novel uncultivated labyrinthulomycetes revealed by 18S rDNA sequences from seawater and sediment samples. Aquat. Microb. Ecol. 58, 215–228.

Cox, B.A. , Luo, H. and Jones, R. (2014) Polymyxa graminis isolates from Australia: identification in wheat roots and soil, molecular characterization and wide genetic diversity. Phytopathology, 98, 1567–1575. PubMed

Dean, R. , Van Kan, J.A.L. , Pretorius, Z.A. , Hammond‐Kosack, K.E. , Di Pietro, A. , Spanu, P.D. , Rudd, J.J. , Dickman, M. , Kahmann, R. , Ellis, J. and Foster, G.D. (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 13, 414–430. PubMed PMC

Desoignies, N. (2012) Polymyxa betae ‐ Beta vulgaris: understanding the molecular interactions through transcriptome and plant defense analysis. PhD thesis, Université catholique de Louvain, Belgium.

Desoignies, N. and Legreve, A. (2011) In vitro dual culture of Polymyxa betae in Agrobacterium rhizogenes transformed sugar beet hairy roots in liquid media. J. Eukaryot. Microbiol. 58, 424–425. PubMed

Desoignies, N. , Carbonell, J. , Moreau, J.S. , Conesa, A. , Dopazo, J. and Legreve, A. (2014) Molecular interactions between sugar beet and Polymyxa betae during its life cycle. Ann. Appl. Biol. 164, 244–256.

Devos, S. , Laukens, K. , Deckers, P. , Van der Straeten, D. , Beeckman, T. , Inze, D. , Van Onckelen, H. , Witters, E. and Prinsen, E. (2006) A hormone and proteome approach to picturing the initial metabolic events during Plasmodiophora brassicae infection on Arabidopsis . Mol. Plant–Microbe Interact. 19, 1431–1443. PubMed

Di Lucca, A.G.T. , Chipana, E.F.T. , Albujar, M.J.T. , Peralta, W.D. , Piedra, Y.C.M. and Zelada, J.L.A. (2013) Slow wilt: another form of Marchitez in oil palm associated with trypanosomatids in Peru. Trop. Plant Pathol. 38, 522–533.

Diederichsen, E. , Frauen, M. , Linders, E.G.A. , Hatakeyama, K. and Hirai, M. (2009) Status and perspectives of clubroot resistance breeding in crucifer crops. J. Plant Growth Regul. 28, 265–281.

Dieryck, B. , Weyns, J. , Doucet, D. , Bragard, C. and Legreve, A. (2011) Acquisition and transmission of peanut clump virus by Polymyxa graminis on cereal species. Phytopathology, 101, 1149–1158. PubMed

Dixon, G.R. (2009) The occurrence and economic impact of Plasmodiophora brassicae and clubroot disease. J. Plant Growth Regul. 28, 194–202.

Douhan, G.W. , Olsen, M.W. , Herrell, A. , Winder, C. , Wong, F. and Entwistle, K. (2009) Genetic diversity of Labyrinthula terrestris, a newly emergent plant pathogen, and the discovery of new Labyrinthulid organisms. Mycol. Res. 113, 1192–1199. PubMed

Faggian, R. and Strelkov, S.E. (2009) Detection and measurement of Plasmodiophora brassicae . J. Plant Growth Regul. 28, 282–288.

Fähling, M. , Graf, H. and Siemens, J. (2003) Pathotype separation of Plasmodiophora brassicae by the host plant. J. Phytopathol. 151, 425–430.

Falloon, R.E. , Genet, R.A. , Wallace, A.R. and Butler, R.C. (2003) Susceptibility of potato (Solanum tuberosum) cultivars to powdery scab (caused by Spongospora subterranea f. sp subterranea), and relationships between tuber and root infection. Australas. Plant Pathol. 32, 377–385.

Falloon, R.E. , Merz, U. , Butler, R.C. , Curtin, D. , Lister, R.A. and Thomas, S.M. (2016) Root infection of potato by Spongospora subterranea: knowledge review and evidence for decreased plant productivity. Plant Pathol. 65, 422–434.

FAO (2014) Food and Agriculture Organization of the United Nations. Fisheries and Aquaculture Information and Statistics Services. URL http://www.fao.org/figis/ [accessed on Jul 26, 2014].

Fourqurean, J.W. , Duarte, C.M. , Kennedy, H. , Marba, N. , Holmer, M. , Mateo, M.A , Apostolaki, E.T. , Kendrick, G.A. , Krause‐Jensen, D. , McGlathery, K.J. and Serrano, O. (2012) Seagrass ecosystems as a globally significant carbon stock. Nat. Geosci. 5, 505–509.

Gachon, C.M. , Strittmatter, M. , Muller, D.G. , Kleinteich, J. and Kupper, F.C. (2009) Detection of differential host susceptibility to the marine oomycete pathogen Eurychasma dicksonii by real‐time PCR: not all algae are equal. Appl. Environ. Microbiol. 75, 322–328. PubMed PMC

Gachon, C.M. , Sime‐Ngando, T. , Strittmatter, M. , Chambouvet, A. and Kim, G.H. (2010) Algal diseases: spotlight on a black box. Trends Plant Sci. 15, 633–640. PubMed

Gau, R.D. , Merz, U. , Falloon, R.E. and Brunner, P.C. (2013) Global genetics and invasion history of the potato powdery scab pathogen, Spongospora subterranea f.sp subterranea . PLoS One, 8, e67944. PubMed PMC

van de Graaf, P. , Wale, S.J. and Lees, A.K. (2007) Factors affecting the incidence and severity of Spongospora subterranea infection and galling in potato roots. Plant Pathol. 56, 1005–1013.

Graf, H. , Fähling, M. and Siemens, J. (2004) Chromosome polymorphism of the obligate biotrophic parasite Plasmodiophora brassicae . J. Phytopathol. 152, 86–91.

Gravot, A. , Richard, G. , Lime, T. , Lemarié, S. , Jubault, M. , Lariagon, C. , Lemoine, J. , Vicente, J. , Robert‐Seilaniantz, A. , Holdsworth, M.J. and Manzanares‐Dauleux, M.J. (2016) Hypoxia response in Arabidopsis roots infected by Plasmodiophora brassicae supports the development of clubroot. BMC Plant Biol. 16, 251. PubMed PMC

Grenville‐Briggs, L. , Gachon, C.M.M. , Strittmatter, M. , Sterck, L. , Kupper, F.C. and van West, P. (2011) A molecular insight into algal–oomycete warfare: cDNA analysis of Ectocarpus siliculosus infected with the basal oomycete Eurychasma dicksonii . PLoS One, 6, e24500. PubMed PMC

Groner, M.L. , Burge, C.A. , Kim, C.J.S. , Rees, E. , Van Alstyne, K.L. , Yang, S. , Wyllie‐Echeverria, S. and Harvell, C.D. (2016) Plant characteristics associated with widespread variation in eelgrass wasting disease. Dis. Aquat. Organ. 118, 159–168. PubMed

Grsic‐Rausch, S. , Kobelt, P. , Siemens, J.M. , Bischoff, M. and Ludwig‐Müller, J. (2000) Expression and localization of nitrilase during symptom development of the clubroot disease in Arabidopsis . Plant Physiol. 122, 369–378. PubMed PMC

Gutiérrez, P. , Bulman, S. , Alzate, J.F. , Ortíz, M.C. and Marín, M. (2016) Mitochondrial genome sequence of the potato powdery scab pathogen Spongospora subterranea . Mitochondrial DNA A DNA Mapp. Seq. Anal. 27, 58–59. PubMed

Gutiérrez, P.A. , Alzate, J.F. and Montoya, M.M. (2014) Analysis of carbohydrate metabolism genes of Spongospora subterranea using 454 pyrosequencing. Rev. Fac. Nal. Agr. Medellin. 67, 7247–7260.

Hannaert, V. , Saavedra, E. , Duffieux, F. , Szikora, J.P. , Rigden, D.J. , Michels, P.A.M. and Opperdoes, F.R. (2003) Plant‐like traits associated with metabolism of Trypanosoma parasites. Proc. Natl. Acad. Sci. USA, 100, 1067–1071. PubMed PMC

Hatakeyama, K. , Suwabe, K. , Tomita, R.N. , Kato, T. , Nunome, T. , Fukuoka, H. and Matsumoto, S. (2013) Identification and characterization of Crr1a, a gene for resistance to clubroot disease (Plasmodiophora brassicae Woronin) in Brassica rapa L. PLoS One, 8, e54745. PubMed PMC

Hwang, E.K. , Park, C.S. and Kakinuma, M. (2009) Physicochemical responses of Pythium porphyrae (Oomycota), the causative organism of red rot disease in Porphyra to acidification. Aquacult. Res. 40, 1777–1784.

Jackson, A.P. (2015) Genome evolution in trypanosomatid parasites. Parasitology, 142, S40–S56. PubMed PMC

Jackson, E.L. , Rowden, A.A. , Attrill, M.J. , Bossey, S.J. and Jones, M.B. (2001) The importance of seagrass beds as a habitat for fishery species. Oceanogr. Mar. Biol. 39, 269–303.

Jahn, L. , Mucha, S. , Bergmann, S. , Horn, C. , Staswick, P. , Steffens, B. , Siemens, J. and Ludwig‐Müller, J. (2013) The clubroot pathogen (Plasmodiophora brassicae) influences auxin signaling to regulate auxin homeostasis in Arabidopsis . Plants, 2, 726–749. PubMed PMC

Jashni, M.K. , Mehrabi, R. , Collemare, J. , Mesarich, C.H. and de Wit, P.J. (2015) The battle in the apoplast: further insights into the roles of proteases and their inhibitors in plant–pathogen interactions. Front. Plant Sci. 6, 584. PubMed PMC

Jaskowska, E. , Butler, C. , Preston, G. and Kelly, S. (2015) Phytomonas: trypanosomatids adapted to plant environments. PLoS Pathog. 11, e1004484. PubMed PMC

Johnson, D.A. and Cummings, T.F. (2015) Effect of powdery scab root galls on yield of potato. Plant Dis. 99, 1396–1403. PubMed

Jones, J.T. , Haegeman, A. , Danchin, E.G.J. , Gaur, H.S. , Helder, J. , Jones, M.G. , Kikuchi, T. , Manzanilla‐López, R. , Palomares‐Rius, J.E. , Wesemael, W.M. and Perry, R.N. (2013) Top 10 plant‐parasitic nematodes in molecular plant pathology. Mol. Plant Pathol. 14, 946–961. PubMed PMC

Jubault, M. , Hamon, C. , Gravot, A. , Lariagon, C. , Delourme, R. , Bouchereau, A. and Manzanares‐Dauleux, M.J. (2008) Differential regulation of root arginine catabolism and polyamine metabolism in clubroot‐susceptible and partially resistant Arabidopsis genotypes. Plant Physiol. 146, 2008–2019. PubMed PMC

Jubault, M. , Lariagon, C. , Taconnat, L. , Renou, J.‐P. , Gravot, A. , Delourme, R. and Manzanares‐Dauleux, M.J. (2013) Partial resistance to clubroot in Arabidopsis is based on changes in the host primary metabolism and targeted cell division and expansion capacity. Funct. Integr. Genomics, 13, 191–205. PubMed PMC

Kamoun, S. , Furzer, O. , Jones, J.D.G. , Judelson, H.S. , Ali, G.S. , Dalio, R.J. , Roy, S.G. , Schena, L. , Zambounis, A. , Panabières, F. and Cahill, D. (2015) The Top 10 oomycete pathogens in molecular plant pathology. Mol. Plant Pathol. 16, 413–434. PubMed PMC

Kanyuka, K. , Ward, E. and Adams, M.J. (2003) Polymyxa graminis and the cereal viruses it transmits: a research challenge. Mol. Plant Pathol. 4, 393–406. PubMed

Kastelein, P. (1987) Investigations on ‘Hartrot’ of coconut and oilpalms in Suriname. PhD dissertation, Rijksuniversiteit te Utrecht, Netherlands.

Kawamura, Y. , Yokoo, K. , Tojo, M. and Hishiike, M. (2005) Distribution of Pythium porphyrae, the causal agent of red rot disease of Porphyrae spp., in the Ariake Sea, Japan. Plant Dis. 89, 1041–1047. PubMed

Kerrigan, J.L. , Olsen, M.W. and Martin, S.B. (2012) Rapid blight of turfgrass. Plant Health Instructor, https://www.apsnet.org/edcenter/intropp/lessons/fungi/other/Pages/RapidBlight.aspx [accessed on Aug 1, 2017].

Kim, G.H. , Moon, K.H. , Kim, J.Y. , Shim, J. and Klochkova, T.A. (2014) A revaluation of algal diseases in Korean Pyropia (Porphyra) sea farms and their economic impact. Algae, 29, 249–265.

Kitajima, E.W. , Vainstein, M.H. and Silveira, J.S.M. (1986) Flagellate protozoan associated with poor development of the root‐system of cassava in the Espirito‐Santo State, Brazil. Phytopathology, 76, 638–642.

Klewer, A. , Luerben, H. , Graf, H. and Siemens, J. (2001) Restriction fragment length polymorphism markers to characterize Plasmodiophora brassicae single‐spore isolates with different virulence patterns. J. Phytopathol. 149, 121–127.

Klochkova, T.A. , Shim, J.B. , Hwang, M.S. and Kim, G.H. (2012) Host–parasite interactions and host species susceptibility of the marine oomycete parasite, Olpidiopsis sp., from Korea that infects red algae. J. Appl. Phycol. 24, 135–144.

Klochkova, T.A. , Shin, Y.J. , Moon, K.H. , Motomura, T. and Kim, G.H. (2016) New species of unicellular obligate parasite, Olpidiopsis pyropiae sp nov., that plagues Pyropia sea farms in Korea. J. Appl. Phycol. 28, 73–83.

Klochkova, T.A. , Jung, S. and Kim, G.H. (2017) Host range and salinity tolerance of Pythium porphyrae may indicate its terrestrial origin. J. Appl. Phycol. 29, 371–379.

Kombrink, A. and Thomma, B.P.H.J. (2013) LysM effectors: secreted proteins supporting fungal life. PLoS Pathog. 9, e1003769. PubMed PMC

Kořený, L. , Sobotka, R.J.K. , Gnipová, A. , Flegontov, P. , Horváth, A. , Oborník, M. , Ayala, F.J. and Lukeš, J. (2012) Aerobic kinetoplastid flagellate Phytomonas does not require heme for viability. Proc. Natl. Acad. Sci. USA, 109, 3808–3813. PubMed PMC

La Barre, S. , Potin, P. , Leblanc, C. and Delage, L. (2010) The halogenated metabolism of brown algae (Phaeophyta), its biological importance and its environmental significance. Mar. Drugs, 8, 988–1010. PubMed PMC

Lafont, A. (1909) Sur la présence d'un Leptomonas, parasite de la classe des Flagelles dans le lates de l'Euphorbia pilulifera. C.r. séances Soc. biol. ses. fil. 66, 1011–1013.

Lamb, J.B. , van de Water, J.A.J.M. , Bourne, D.G. , Altier, C. , Hein, M.Y. , Fiorenza, E.A. , Abu, N. , Jompa, J. and Harvell, C.D. (2017) Seagrass ecosystems reduce exposure to bacterial pathogens of humans, fishes, and invertebrates. Science, 355, 731–733. PubMed

Legreve, A. , Vanpee, B. , Delfosse, P. and Maraite, H. (2000) Host range of tropical and sub‐tropical isolates of Polymyxa graminis . Eur. J. Plant Pathol. 106, 379–389.

Legreve, A. , Delfosse, P. and Maraite, H. (2002) Phylogenetic analysis of Polymyxa species based on nuclear 5.8S and internal transcribed spacers ribosomal DNA sequences. Mycol. Res. 106, 138–147.

Lemarié, S. , Robert‐Seilaniantz, A. , Lariagon, C. , Lemoine, J. , Marnet, N. , Jubault, M. , Manzanares‐Dauleux, M.J. and Gravot, A. (2015) Both the jasmonic acid and the salicylic acid pathways contribute to resistance to the biotrophic clubroot agent Plasmodiophora brassicae in Arabidopsis . Plant Cell Physiol. 56, 2158–2168. PubMed

Lindholm, T. , Lindqvist, C. and Sjöqvist, C. (2016) Occurrence and activity of slime nets, Labyrinthula sp. among aquatic plants in cold and oligohaline Baltic Sea waters. Ann. Bot. Fennici, 53, 139–143.

Lopez, G. , Genty, P. and Ollagnier, M. (1975) Control preventivo de la “Marchitez sorpresiva” del Elaeis guineensis en America Latina. Oleagineux 30, 243–250.

Loureiro, R. , Gachon, C.M. and Rebours, C. (2015) Seaweed cultivation: potential and challenges of crop domestication at an unprecedented pace. New Phytol. 206, 489–492. PubMed

Lovelock, D.A. , Donald, C.E. , Conlan, X.A. and Cahill, D.M. (2013) Salicylic acid suppression of clubroot in broccoli (Brassicae oleracea var. italica) caused by the obligate biotroph Plasmodiophora brassicae . Australas. Plant Pathol. 42, 141–153.

Ludwig‐Müller, J. (2016) Belowground defence strategies against clubroot (Plasmodiophora brassicae) In: Belowground Defence Strategies in Plants (Vos C. M. F. and Kazan K., eds.), pp. 195–219. Cham: Springer International Publishing.

Ludwig‐Müller, J. , Prinsen, E. , Rolfe, S.A. and Scholes, J.D. (2009) Metabolism and plant hormone action during clubroot disease. J. Plant Growth Regul. 28, 229–244.

Ludwig‐Müller, J. , Jülke, S. , Geiß, K. , Richter, F. , Mithöfer, A. , Šola, I. , Rusak, G. , Keenan, S. and Bulman, S. (2015) A novel methyltransferase from the intracellular pathogen Plasmodiophora brassicae methylates salicylic acid. Mol. Plant Pathol. 16, 349–364. PubMed PMC

Ludwig‐Müller, J. , Auer, S. , Jülke, S. and Marschollek, S. (2017) Manipulation of auxin and cytokinin balance during the Plasmodiophora brassicae–Arabidopsis thaliana interaction In: Auxins and Cytokinins in Plant Biology: Methods and Protocols (Dandekar T. and Naseem M., eds.), pp. 41–60. New York, NY: Springer. PubMed

Lukeš, J. , Skalicky, T. , Tyc, J. , Votypka, J. and Yurchenko, V. (2014) Evolution of parasitism in kinetoplastid flagellates. Mol. Biochem. Parasitol. 195, 115–122. PubMed

Malinowski, R. , Smith, J.A. , Fleming, A.J. , Scholes, J.D. and Rolfe, S.A. (2012) Gall formation in clubroot‐infected Arabidopsis results from an increase in existing meristematic activities of the host but is not essential for the completion of the pathogen life cycle. Plant J. 71, 226–238. PubMed

Malinowski, R. , Novák, O. , Borhan, M.H. , Spíchal, L. , Strnad, M. and Rolfe, S.A. (2016) The role of cytokinins in clubroot disease. Eur. J. Plant Pathol. 145, 543–557.

Mansfield, J. , Genin, S. , Magori, S. , Citovsky, V. , Sriariyanum, M. , Ronald, P. , Dow, M.A.X. , Verdier, V. , Beer, S.V. , Machado, M.A. and Toth, I.A.N. (2012) Top 10 plant pathogenic bacteria in molecular plant pathology. Mol. Plant Pathol. 13, 614–629. PubMed PMC

Martin, D.L. , Chiari, Y. , Boone, E. , Sherman, T.D. , Ross, C. , Wyllie‐Echeverria, S. , Gaydos, J.K. and Boettcher, A.A. (2016) Functional, phylogenetic and host‐geographic signatures of Labyrinthula spp. provide for putative species delimitation and a global‐scale view of seagrass wasting disease. Estuar. Coasts, 39, 1–19.

Maslov, D.A. , Votypka, J. , Yurchenko, V. and Lukes, J. (2013) Diversity and phylogeny of insect trypanosomatids: all that is hidden shall be revealed. Trends Parasitol. 29, 43–52. PubMed

McGhee, R.B. and McGhee, A.H. (1979) Biology and structure of Phytomonas staheli sp.n. a trypanosomatid located in sieve tubes of coconut and oil palms. J. Protozool. 26, 348–351.

McGrann, G.R.D. , Grimmer, M.K. , Mutasa‐Goettgens, E.S. and Stevens, M. (2009) Progress towards the understanding and control of sugar beet rhizomania disease. Mol. Plant Pathol. 10, 129–141. PubMed PMC

McKone, K.L. and Tanner, C.E. (2009) Role of salinity in the susceptibility of eelgrass Zostera marina to the wasting disease pathogen Labyrinthula zosterae . Mar. Ecol. Prog. Ser. 377, 123–130.

Medina, J.M. , Rodrigues, J.C.F. , Moreira, O.C. , Atella, G. , de Souza, W. and Barrabin, H. (2015) Mechanisms of growth inhibition of Phytomonas serpens by the alkaloids tomatine and tomatidine. Mem. Inst. Oswaldo Cruz, 110, 48–55. PubMed PMC

Merz, U. and Falloon, R.E. (2009) Review: powdery scab of potato—increased knowledge of pathogen biology and disease epidemiology for effective disease management. Potato Res. 52, 17–37.

Michel, G. , Tonon, T. , Scornet, D. , Cock, J.M. and Kloareg, B. (2010) The cell wall polysaccharide metabolism of the brown alga Ectocarpus siliculosus. Insights into the evolution of extracellular matrix polysaccharides in Eukaryotes. New Phytol. 188, 82–97. PubMed

Moxham, S.E. and Buczacki, S.T. (1983) Chemical‐composition of the resting spore wall of Plasmodiophora‐brassicae . Trans. Br. Mycol. Soc. 80, 297–304.

Muehlstein, L.K. (1989) Perspectives on the wasting disease of eelgrass Zostera marina . Dis. Aquat. Organ. 7, 211–221.

Muehlstein, L.K. (1992) The host–pathogen interaction in the wasting disease of eelgrass, Zostera marina. Can. J. Bot. 70, 2081–2088.

Muehlstein, L.K. , Porter, D. and Short, F.T. (1988) Labyrinthula sp, a marine slime‐mold producing the symptoms of wasting disease in eelgrass, Zostera‐marina . Mar. Biol. 99, 465–472.

Müller, D.G. , Küpper, F.C. and Küpper, H. (1999) Infection experiments reveal broad host ranges of Eurychasma dicksonii (Oomycota) and Chytridium polysiphoniae (Chytridiomycota), two eukaryotic parasites in marine brown algae (Phaeophyceae). Phycol. Res. 47, 217–223.

Nakamura, Y. , Sasaki, N. , Kobayashi, M. , Ojima, N. , Yasuike, M. , Shigenobu, Y. , Satomi, M. , Fukuma, Y. , Shiwaku, K. , Tsujimoto, A. and Kobayashi, T. (2013) The first symbiont‐free genome sequence of marine red alga, Susabi‐nori (Pyropia yezoensis). PLoS One, 8, e57122. PubMed PMC

Neuhauser, S. , Bulman, S. and Kirchmair, M. (2010) Plasmodiophorids: The Challenge to Understand Soil‐Borne, Obligate Biotrophs with a Multiphasic Life Cycle In: Molecular Identification of Fungi (Gherbawy Y. and Voigt K, eds.), pp. 51–78. Berlin, Heidelberg: Springer Berlin Heidelberg.

Neuhauser, S. , Kirchmair, M. and Gleason, F.H. (2011) The ecological potentials of Phytomyxea (“plasmodiophorids”) in aquatic food webs. Hydrobiologia, 659, 23–35. PubMed PMC

Neuhauser, S. , Kirchmair, M. , Bulman, S. and Bass, D. (2014) Cross‐kingdom host shifts of phytomyxid parasites. BMC Evol. Biol. 14, 33. PubMed PMC

O'Brien, P.A. and Milroy, S.P. (2017) Towards biological control of Spongospora subterranea f. sp subterranea, the causal agent of powdery scab in potato. Australas. Plant Pathol. 46, 1–10.

Olsen, J.L. , Rouze, P. , Verhelst, B. , Lin, Y.C. , Bayer, T. , Collen, J. , Dattolo, E. , De Paoli, E. , Dittami, S. , Maumus, F. and Michel, G. (2016) The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature, 530, 331–335. PubMed

Olsen, M.W. (2007) Labyrinthula terrestris: a new pathogen of cool‐season turfgrasses. Mol. Plant Pathol. 8, 817–820. PubMed

Olsen, Y.S. and Duarte, C.M. (2015) Combined effect of warming and infection by Labyrinthula sp. on the Mediterranean seagrass Cymodocea nodosa . Mar. Ecol. Prog. Ser. 532, 101–109.

Pan, J.W. , del Campo, J. and Keeling, P.J. (2017) Reference tree and environmental sequence diversity of Labyrinthulomycetes. J. Eukaryot. Microbiol. 64, 88–96. PubMed

Park, C.S. and Hwang, E.K. (2015) Biochemical characterization of Pyropia yezoensis‐AP1 strain accompanies the resistance reaction to the red rot disease pathogen, Pythium porphyrae . J. Appl. Phycol. 27, 2149–2156.

Park, C.S. , Kakinuma, M. and Amano, H. (2001) Detection and quantitative analysis of zoospores of Pythium porphyrae, causative organism of red rot disease in Porphyra, by competitive PCR. J. Appl. Phycol. 13, 433–441.

Park, C.S. , Kakinuma, M. and Amano, H. (2006) Forecasting infections of the red rot disease on Porphyra yezoensis Ueda (Rhodophyta) cultivation farms. J. Appl. Phycol. 18, 295–299.

Parthasarathy, M.V. , Van Slobbe, W.G. and Soudant, C. (1976) Trypanosomatid flagellate in the phloem of diseased coconut palms. Science, 192, 1346–1348. PubMed

Päsold, S. , Siegel, I. , Seidel, C. and Ludwig‐Müller, J. (2010) Flavonoid accumulation in Arabidopsis thaliana root galls caused by the obligate biotrophic pathogen Plasmodiophora brassicae . Mol. Plant Pathol. 11, 545–562. PubMed PMC

Petersen, H.E. (1905) Contributions a la connaissance des Phycomycetes marines. Overs. K. Danske Vidensk. Selsk. Forh. 5, 439–488.

Porcel, B.M. , Denoeud, F. , Opperdoes, F. , Noel, B. , Madoui, M.A. , Hammarton, T.C. , Field, M.C. , Da Silva, C. , Couloux, A. , Poulain, J. and Katinka, M. (2014) The streamlined genome of Phytomonas spp. relative to human pathogenic kinetoplastids reveals a parasite tailored for plants. PLoS Genet. 10, e1004007. PubMed PMC

Preston, T.M. and King, C.A. (2005) Actin‐based motility in the net slime mould Labyrinthula: evidence for the role of myosin in gliding movement. J. Eukaryot. Microbiol. 52, 461–475. PubMed

Qu, X.S. and Christ, B.J. (2004) Genetic variation and phylogeny of Spongospora subterranea f.sp subterranea based on ribosomal DNA sequence analysis. Am. J. Potato Res. 81, 385–394.

Ritter, A. , Goulitquer, S. , Salaun, J.P. , Tonon, T. , Correa, J.A. and Potin, P. (2008) Copper stress induces biosynthesis of octadecanoid and eicosanoid oxygenated derivatives in the brown algal kelp Laminaria digitata . New Phytol. 180, 809–821. PubMed

Rodgers, K.L. and Shears, N.T. (2016) Modelling kelp forest primary production using in situ photosynthesis, biomass and light measurements. Mar. Ecol. Prog. Ser. 553, 67–79.

Rolfe, S.A. , Strelkov, S.E. , Links, M.G. , Clarke, W.E. , Robinson, S.J. , Djavaheri, M. , Malinowski, R. , Haddadi, P. , Kagale, S. , Parkin, I.A. and Taheri, A. (2016) The compact genome of the plant pathogen Plasmodiophora brassicae is adapted to intracellular interactions with host Brassica spp. BMC Genomics, 17, 1–15. PubMed PMC

Scholthof, K.B.G. , Adkins, S. , Czosnek, H. , Palukaitis, P. , Jacquot, E. , Hohn, T. , Hohn, B. , Saunders, K. , Candresse, T. , Ahlquist, P. and Hemenway, C. (2011) Top 10 plant viruses in molecular plant pathology. Mol. Plant Pathol. 12, 938–954. PubMed PMC

Schuller, A. , Kehr, J. and Ludwig‐Müller, J. (2014) Laser microdissection coupled to transcriptional profiling of Arabidopsis roots inoculated by Plasmodiophora brassicae indicates a role for brassinosteroids in clubroot formation. Plant Cell Physiol. 55, 392–411. PubMed

Schwelm, A. , Fogelqvist, J. , Knaust, A. , Jülke, S. , Lilja, T. , Bonilla‐Rosso, G. , Karlsson, M. , Shevchenko, A. , Dhandapani, V. , Choi, S.R. and Kim, H.G. (2015) The Plasmodiophora brassicae genome reveals insights in its life cycle and ancestry of chitin synthases. Sci. Rep. 5, 11 153. PubMed PMC

Schwelm, A. , Berney, C. , Bass, D. , Dixelius, C. and Neuhauser, S. (2016) The large subunit rDNA sequence of Plasmodiophora brassicae does not contain intra‐species polymorphism. Protist, 167, 544–554. PubMed PMC

Sekimoto, S. , Beakes, G.W. , Gachon, C.M.M. , Muller, D.G. , Kupper, F.C. and Honda, D. (2008) The development, ultrastructural cytology, and molecular phylogeny of the basal oomycete Eurychasma dicksonii, infecting the filamentous phaeophyte algae Ectocarpus siliculosus and Pylaiella littoralis . Protist, 159, 299–318. PubMed

Seward, E.A. , Votypka, J. , Kment, P. , Lukeš, J. and Kelly, S. (2016) Description of Phytomonas oxycareni n. sp. from the salivary glands of Oxycarenus lavaterae . Protist, 168, 71–79. PubMed

Shah, F.A. , Falloon, R.E. , Butler, R.C. and Lister, R.A. (2012) Low amounts of Spongospora subterranea sporosorus inoculum cause severe powdery scab, root galling and reduced water use in potato (Solanum tuberosum). Australas. Plant Pathol. 41, 219–228.

Siemens, J. , Keller, I. , Sarx, J. , Kunz, S. , Schuller, A. , Nagel, W. , Schmülling, T. , Parniske, M. and Ludwig‐Müller, J. (2006) Transcriptome analysis of Arabidopsis clubroots indicate a key role for cytokinins in disease development. Mol. Plant–Microbe Interact. 19, 480–494. PubMed

Siemens, J. , Bulman, S. , Rehn, F. and Sundelin, T. (2009) Molecular biology of Plasmodiophora brassicae . J. Plant Growth Regul. 28, 245–251.

Smith, M.J. , Adams, M.J. and Ward, E. (2011) Evidence that Polymyxa species may infect Arabidopsis thaliana . FEMS Microbiol. Lett. 318, 35–40. PubMed

Smith, M.J. , Adams, M.J. and Ward, E. (2013) Ribosomal DNA analyses reveal greater sequence variation in Polymyxa species than previously thought and indicate the possibility of new ribotype‐host–virus associations. Environ. Microbiol. Rep. 5, 143–150. PubMed

Song, T. , Chu, M. , Lahlali, R. , Yu, F. and Peng, G. (2016) Shotgun label‐free proteomic analysis of clubroot (Plasmodiophora brassicae) resistance conferred by the gene Rcr1 in Brassica rapa . Front. Plant Sci. 7, 1013. PubMed PMC

Stahel, G. (1931) Zur Kenntnis der Siebröhrenkrankheit (Phloemnekrose) des Kaffeebaumes in Surinam. II. Phytopathol. Z. 4, 539–548.

Stengel, D.B. and Connan, S. (2015) Marine algae: a source of biomass for biotechnological applications In: Natural Products from Marine Algae: Methods and Protocols (Stengel D. B. and Connan S., eds.), pp. 1–37. New York, NY: Springer. PubMed

Stowell, L.J. , Martin, S.B. , Olsen, M.W. , Bigelow, D. , Kohout, M. , Peterson, P.D. , Camberato, J. and Gelernter, W.D. (2005) Rapid blight: a new plant disease. APSnet Features July 2005. Available at: http://www.apsnet.org/publications/apsnetfeatures/Pages/RapidBlight.aspx. [accessed on Aug 1, 2017].

Strelkov, S.E. , Hwang, S.F. , Manolii, V.P. , Cao, T. and Feindel, D. (2016) Emergence of new virulence phenotypes of Plasmodiophora brassicae on canola (Brassica napus) in Alberta, Canada. Eur. J. Plant. Pathol. 145, 517–529.

Strittmatter, M. , Grenville‐Briggs, L.J. , Breithut, L. , van West, P. , Gachon, C.M.M. and Kupper, F.C. (2016) Infection of the brown alga Ectocarpus siliculosus by the oomycete Eurychasma dicksonii induces oxidative stress and halogen metabolism. Plant Cell Environ. 39, 259–271. PubMed PMC

Sullivan, B.K. , Sherman, T.D. , Damare, V.S. , Lilje, O. and Gleason, F.H. (2013) Potential roles of Labyrinthula spp. in global seagrass population declines. Fungal Ecol. 6, 328–338.

Sullivan, B.K. , Robinson, K.L. , Trevathan‐Tackett, S.M. , Lilje, E.S. , Gleason, F.H. and Lilje, O. (2016) The first isolation and characterisation of the protist Labyrinthula sp. in Southeastern Australia. J. Eukaryot. Microbiol. 64, 504–513. PubMed

Tamada, T. and Kondo, H. (2013) Biological and genetic diversity of plasmodiophorid‐transmitted viruses and their vectors. J. Gen. Plant Pathol. 79, 307–320.

Trevathan‐Tackett, S.M. , Lane, A.L. , Bishop, N. and Ross, C. (2015) Metabolites derived from the tropical seagrass Thalassia testudinum are bioactive against pathogenic Labyrinthula sp. Aquat. Bot. 122, 1–8.

Tsirigoti, A. , Beakes, G.W. , Herve, C. , Gachon, C.M. and Katsaros, C. (2015) Attachment, penetration and early host defense mechanisms during the infection of filamentous brown algae by Eurychasma dicksonii . Protoplasma, 252, 845–856. PubMed

Tsui, C.K. , Marshall, W. , Yokoyama, R. , Honda, D. , Lippmeier, J.C. , Craven, K.D. , Peterson, P.D. and Berbee, M.L. (2009) Labyrinthulomycetes phylogeny and its implications for the evolutionary loss of chloroplasts and gain of ectoplasmic gliding. Mol. Phylogenet. Evol. 50, 129–140. PubMed

Uppalapati, S.R. and Fujita, Y. (2000) Carbohydrate regulation of attachment, encystment, and appressorium formation by Pythium porphyrae (Oomycota) zoospores on Porphyra yezoensis (Rhodophyta). J. Phycol. 36, 359–366.

Uppalapati, S.R. and Fujita, Y. (2001) The relative resistances of Porphyra species (Bangiales, Rhodophyta) to infection by Pythium porphyrae (Peronosporales, Oomycota). Bot. Mar. 44, 1–7.

Vaianopoulos, C. , Bragard, C. , Moreau, V. , Maraite, H. and Legreve, A. (2007) Identification and quantification of Polymyxa graminis f. sp temperata and P. graminis f. sp tepida on barley and wheat. Plant Dis. 91, 857–864. PubMed

Vergeer, L.H.T. , Aarts, T.L. and Degroot, J.D. (1995) The wasting disease and the effect of abiotic factors (light‐intensity, temperature, salinity) and infection with Labyrinthula zosterae on the phenolic content of Zostera marina shoots. Aquat. Bot. 52, 35–44.

Vishniac, H.S. (1955) The nutritional requirements of isolates of Labyrinthula spp. J. Gen. Microbiol. 12, 455–463. PubMed

Walsh, J.A. , Clay, C.M. and Miller, A. (1989) A new virus disease of watercress in England. EPPO Bull. 19, 463–470.

Ward, E. , Kanyuka, K. , Motteram, J. , Kornyukhin, D. and Adams, M.J. (2005) The use of conventional and quantitative real‐time PCR assays for Polymyxa graminis to examine host plant resistance, inoculum levels and intraspecific variation. New Phytol. 165, 875–885. PubMed

Ward, L.I. , Fenn, M.G.E. and Henry, C.M. (2004) A rapid method for direct detection of Polymyxa DNA in soil. Plant Pathol. 53, 485–490.

Woronin, M. (1877) Plasmodiophora brassicae, der Organismus, der die unter dem Namen Hernie bekannte Krankheit der Kohlpflanzen verursacht. Arb. St. Petersburger naturf. Ges. 8, 169–201.

Wu, S. , Sun, J. , Chi, S. , Wang, L. , Wang, X. , Liu, C. , Li, X. , Yin, J. , Liu, T. and Yu, J. (2014) Transcriptome sequencing of essential marine brown and red algal species in China and its significance in algal biology and phylogeny. Acta Oceanol. Sin. 33, 1–12.

Young, E.L. (1943) Studies on Labyrinthula. The etiologic agent of the wasting disease of eel‐grass. Am. J. Bot. 30, 586–593.

Zamani‐Noor, N. (2017) Variation in pathotypes and virulence of Plasmodiophora brassicae populations in Germany. Plant Pathol. 66, 316–324.

Zambounis, A. , Elias, M. , Sterck, L. , Maumus, F. , Gachon, C.M. (2012) Highly dynamic exon shuffling in candidate pathogen receptors … what if brown algae were capable of adaptive immunity? Mol. Biol. Evol. 29, 1263–1276. PubMed PMC

Zhang, D.P. , Burroughs, A.M. , Vidal, N.D. , Iyer, L.M. and Aravind, L. (2016a) Transposons to toxins: the provenance, architecture and diversification of a widespread class of eukaryotic effectors. Nucleic Acids Res. 44, 3513–3533. PubMed PMC

Zhang, X. , Liu, Y. , Fang, Z. , Li, Z. , Yang, L. , Zhuang, M. , Zhang, Y. and Lv, H. (2016b) Comparative transcriptome analysis between Broccoli (Brassica oleracea var. italica) and wild cabbage (Brassica macrocarpa Guss.) in response to Plasmodiophora brassicae during different infection stages. Front. Plant Sci. 7, 1929. PubMed PMC

Ziegler, A. , Fomitcheva, V. , Zakri, A.M. and Kastirr, U. (2016) Occurrence of Polymyxa graminis ribotypes in Germany and their association with different host plants and viruses. Cereal Res. Commun. 44, 251–262.

Euglenozoa: taxonomy, diversity and ecology, symbioses and viruses