Skip to main content
Log in

Genotypic characterization of Plasmodiophora brassicae in the paddy-field weed Cardamine occulta and symptomology reveal a distinct pathogen population in Japan

  • Fungal Diseases
  • Published:
Journal of General Plant Pathology Aims and scope Submit manuscript

Abstract

Cruciferous clubroot, caused by the obligate protist Plasmodiophora brassicae, is one of the most destructive diseases of Brassicaceae crops worldwide. Clubroot is also frequently diagnosed in Cardamine occulta, a cruciferous weed in postharvest paddy fields across Japan, but the symptoms differ from those on the crop hosts. Galls were frequently detected in adventitious buds and even aerial parts such as petioles at several growth stages of the weeds. Phylogenetic analysis of concatenated actin gene and internal transcribed spacer 1 (ITS1) and 2 (ITS 2) revealed more variations and mutations (single-nucleotide polymorphisms, oligonucleotide polymorphisms, and insertions/deletions) in this novel population than in any published sequences for cosmopolitan P. brassicae strains from crops including other Japanese field populations (geographic isolates) collected here. Analysis of the ITS2 secondary structure for this newly discovered population provides new insights into diversity and phylogenetic relationships among P. brassicae populations, conclusively confirming its distinctive structure among the universal modeled structure for P. brassicae. Thus, the coevolution of the host weeds with P. brassicae isolates that are highly adapted to rice-paddy environments may significantly contribute to the evolution of P. brassicae on Brassica crops and club root epidemiology and needs further study.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability statement

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Alvarez I, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol 23:417–434

    Article  Google Scholar 

  • Archibald JM, Keeling PJ (2004) Actin and ubiquitin protein sequences support a cercozoan/foraminiferan ancestry for the plasmodiophorid plant pathogens. J Eukaryot Microbiol 51:113–118

    Article  CAS  PubMed  Google Scholar 

  • Bulman S, Richter F, Marschollek S, Benade F, Jülke S, Ludwig-Müller J (2019) Arabidopsis thaliana expressing PbBSMT, a gene encoding a SABATH-type methyltransferase from the plant pathogenic protist Plasmodiophora brassicae, show leaf chlorosis and altered host susceptibility. Plant Biol J 21:120–130

    Article  CAS  Google Scholar 

  • Coleman AW (2003) ITS2 is a double-edged tool for eukaryote evolutionary comparisons. Trends Genet 7:370–375

    Article  Google Scholar 

  • Dixon GR (2009) The occurrence and economic impact of Plasmodiophora brassicae and clubroot disease. J Plant Growth Regul 28:194–202

    Article  CAS  Google Scholar 

  • Gibbs JG (1932) Weed host plants of club-root in New Zealand. NZ J Agric 44:273–276

    Google Scholar 

  • Guillén D, Sánchez S, Rodríguez-Sanoja R (2010) Carbohydrate-binding domains: multiplicity of biological roles. Appl Microbiol Biotechnol 85:1241–1249

    Article  PubMed  Google Scholar 

  • Ito S, Maehara T, Tanaka S, Kameya-Iwaki M, Yano S, Kishi F (1997) Cloning of a single-copy DNA sequence unique to Plasmodiophora brassicae. Physiol Mol Plant Pathol 50:289–300

    Article  CAS  Google Scholar 

  • Jörg S, Tobias M, Marco A, Philipp NS, Thomas D, Matthias W (2006) The internal transcribed spacer 2 database—a web server for (not only) low level phylogenetic analyses. Nucleic Acids Res 34:704–707

    Article  Google Scholar 

  • Kim H, Jo EJ, Yong HC, Jang KS, Choi GJ (2016) Pathotype classification of Plasmodiophora brassicae isolates using clubroot-resistant cultivars of Chinese cabbage. Plant Pathol J 32:423–430

    Article  PubMed  PubMed Central  Google Scholar 

  • Kudoh H (2017) Biology of the weedy species of the genus Cardamine [Brassicaceae] in Japan. J Weed Sci and Tech 62:175–218

    Article  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laila R, Robin AH, Yang K, Choi GJ, Park JI, Nou IS (2017) Detection of ribosomal DNA sequence polymorphisms in the protist Plasmodiophora brassicae for the identification of geographical isolates. Int J Mol Sci 18:84

    Article  PubMed  PubMed Central  Google Scholar 

  • Lihová J, Marhold K, Kudoh H, Koch MA (2006) Worldwide phylogeny and biogeography of Cardamine flexuosa (Brassicaceae) and its relatives. Am J Bot 93:1206–1221

    Article  PubMed  Google Scholar 

  • Mandáková T, Zozomová-Lihová J, Kudoh H, Zhao Y, Lysak MA, Marhold K (2019) The story of promiscuous crucifers: origin and genome evolution of an invasive species, Cardamine occulta (Brassicaceae), and its relatives. Ann Bot 124:209–220

    Article  PubMed  PubMed Central  Google Scholar 

  • Marhold K, Šlenker M, Kudoh H, Zozomová-Lihová J (2016) Cardamine occulta, the correct species name for invasive Asian plants previously classified as C. flexuosa, and its occurrence in Europe. PhytoKeys 5:57–72

    Article  Google Scholar 

  • McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40:349–379

    Article  CAS  PubMed  Google Scholar 

  • Niwa R, Kawahara A, Murakami H, Tanaka S, Ezawa T (2011) Complete structure of nuclear rDNA of the obligate plant parasite Plasmodiophora brassicae: intraspecific polymorphisms in the exon and group I intron of the large subunit rDNA. Protist 162:423–434

    Article  CAS  PubMed  Google Scholar 

  • Nowicki B (1973) Host range of Plasmodiophora brassicae Wor. (in Polish). Acta Agrobot 26:53–61

    Article  Google Scholar 

  • Olszak M, Truman W, Stefanowicz K, Sliwinska E, Ito M, Walerowski P, Rolfe S, Malinowski R (2019) Transcriptional profiling identifies critical steps of cell cycle reprogramming necessary for Plasmodiophora brassicae-driven gall formation in Arabidopsis. Plant J 97:715–729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osaki K, Fujiyama S, Nakayama A (2008) Relation between pathogenicity and genetic variation within Plasmodiophora brassicae. J Gen Plant Pathol 74:281–288

    Article  CAS  Google Scholar 

  • Pang W, Fu P, Li X, Zhan Z, Yu S, Piao Z (2018) Identification and mapping of the clubroot resistance gene CRd in Chinese cabbage (Brassica rapa ssp. pekinensis). Front Plant Sci 9:653

    Article  PubMed  PubMed Central  Google Scholar 

  • Ren L, Xu L, Liu F, Chen K, Sun C, Li J, Fang X (2016) Host range of Plasmodiophora brassicae on cruciferous crops and weeds in China. Plant Dis 100:933–939

    Article  CAS  PubMed  Google Scholar 

  • Riascos D, Ortiz E, Quintero D, Montoya L, Hoyos-Carvajal L (2011) Histopathological and morphological alterations caused by Plasmodiophora brassicae in Brassica oleracea L. Agron Colomb 29:57–61

    Google Scholar 

  • Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins ES, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302

    Article  CAS  PubMed  Google Scholar 

  • Schuller A, Ludwig-Müller J (2016) Histological methods to detect the clubroot pathogen Plasmodiophora brassicae during its complex life cycle. Plant Pathol 65:1223–1237

    Article  CAS  Google Scholar 

  • Schultz J, Maisel S, Gerlach D, Müller T, Wolf M (2005) A common core of secondary structure of the internal transcribed spacer 2 (ITS2) throughout the Eukaryota. RNA 11:361–364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwelm A, Ludwig-Müller J (2021) Molecular pathotyping of Plasmodiophora brassicae-genomes, marker genes, and obstacles. Pathogens 10:259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwelm A, Fogelqvist J, Knaust A, Jülke S, Lilja T, Bonilla-Rosso G, Karlsson M, Shevchenko A, Dhandapani V, Choi SR, Kim HG, Park JY, Lim YP, Ludwig-Müller J, Dixelius C (2015) The Plasmodiophora brassicae genome reveals insights in its life cycle and ancestry of chitin synthases. Sci Rep 5:11153

    Article  PubMed  PubMed Central  Google Scholar 

  • Schwelm A, Berney C, Dixelius C, Bass D, Neuhauser S (2016a) The large subunit rDNA sequence of Plasmodiophora brassicae does not contain intra-species polymorphism. Protist 16:544–554

    Article  Google Scholar 

  • Schwelm A, Dixelius C, Ludwig-Müller J (2016b) New kid on the block—the clubroot pathogen genome moves the plasmodiophorids into the genomic era. Eur J Plant Pathol 145:531–542

    Article  Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Article  CAS  PubMed  Google Scholar 

  • Tanaka S, Ito S (2013) Pathogenic and genetic diversity in Plasmodiophora brassicae (clubroot) from Japan. J Gen Plant Pathol 79:297–306

    Article  Google Scholar 

  • Tanaka S, Ito S, Kameya-Iwaki M, Katumoto K, Nishi Y (1993) Occurrence and distribution of clubroot disease on two cruciferous weeds, Cardamine flexuosa and C. scutata, in Japan. Trans Mycol Soc Jpn 34:381–388

    Google Scholar 

  • Tanaka S, Murai K, Ito S, Katsumoto K, Nishi Y (1994) The occurrence of clubroot disease of wasabi (Eutrema wasabi Maxim.) and its possible source of infection (in Japanese). Ann Phytopathol Soc Jpn 60:257–259

    Article  Google Scholar 

  • Tanaka S, Mizui Y, Terasaki H, Ito S (2006) Distribution of clubroot disease of a cruciferous weed, Cardamine flexuosa, in major isolated islands, Hokkaido and Okinawa, in Japan. Mycoscience 47:72–77

    Article  Google Scholar 

  • Tso HH, Galindo-González L, Strelkov SE (2021) Current and future pathotyping platforms for Plasmodiophora brassicae in Canada. Plants 10:1446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yatsu Y, Kachi N, Kudoh H (2003) Ecological distribution and phenology of an invasive species, Cardamine hirsuta L., and its native counterpart, C. flexuosa With., in central Japan. Plant Species Biol 18:35–42

    Article  Google Scholar 

  • Zamani-Noor N, Brand S, Söchting HP (2022) Effect of pathogen virulence on pathogenicity, host range, and reproduction of Plasmodiophora brassicae, the causal agent of clubroot disease. Plant Dis 106:57–64

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Feng J, Manolii VP, Strelkov SE, Hwang SF (2015) Characterization of a gene identified in pathotype 5 of the clubroot pathogen Plasmodiophora brassicae. Phytopathology 105:764–770

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Tian W, Gao Z, Wang G, Zhao H (2020) Phylogenetic utility of rRNA ITS2 sequence-structure under functional constraint. Int J Mol Sci 3:417–434

    Google Scholar 

Download references

Funding

This work was supported by the Japanese Government (Monbukagakusyo) Scholarship (A. T. P. Lam).

Author information

Authors and Affiliations

Authors

Contributions

ATPL: carried out the experiment, writing original draft, visualization. KS: investigation. YY: investigation. ST: methodology. SI: supervision, conceptualization, methodology, manuscript review and editing. All authors contributed to the article and approved the submitted version.

Corresponding author

Correspondence to Shin-ichi Ito.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

This article does not contain any studies on humans or animals.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lam, A.T.P., Sasaki, K., Yanagi, Y. et al. Genotypic characterization of Plasmodiophora brassicae in the paddy-field weed Cardamine occulta and symptomology reveal a distinct pathogen population in Japan. J Gen Plant Pathol 89, 1–11 (2023). https://doi.org/10.1007/s10327-022-01106-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10327-022-01106-0

Keywords

Navigation