Comparative genomics reveals the unique evolutionary status of Plasmodiophora brassicae and the essential role of GPCR signaling pathways

Abstract

Plasmodiophora brassicae is an important biotrophic eukaryotic plant pathogen and a member of the rhizarian protists. This biotrophic pathogen causes clubroot in cruciferous plants via novel intracellular mechanisms that are markedly different from those of other biotrophic organisms. To date, genomes from six single spore isolates of P. brassicae have been sequenced. An accurate description of the evolutionary status of this biotrophic protist, however, remains lacking. Here, we determined the draft genome of the P. brassicae ZJ-1 strain. A total of 10,951 protein-coding genes were identified from a 24.1 Mb genome sequence. We applied a comparative genomics approach to prove the Rhizaria supergroup is an independent branch in the eukaryotic evolutionary tree. We also found that the GPCR signaling pathway, the versatile signal transduction to multiple intracellular signaling cascades in response to extracellular signals in eukaryotes, is significantly enriched in P. brassicae-expanded and P. brassicae-specific gene sets. Additionally, treatment with a GPCR inhibitor relieved the symptoms of clubroot and significantly suppressed the development of plasmodia. Our findings suggest that GPCR signal transduction pathways play important roles in the growth, development, and pathogenicity of P. brassicae.

Fertilization alters protistan consumers and parasites in crop‐associated microbiomes

“…Fine-tuning between plant immune response and microbe genomic traits is known to regulate endophytic colonization (Trivedi et al, 2020). Interestingly, the cell-surface G-protein-coupled receptors (GPCRs) mediated signalling pathway are significantly enriched in the Rhizaria supergroup (Bi et al, 2019). GPCRs sense a diverse array of extracellular signals from plant host and are reported to promote endophytic colonization (Xu et al, 2014).…”

Soil microbiota influences clubroot disease by modulatingPlasmodiophora brassicaeandBrassica napustranscriptomes

“…Bi et al . (2019) showed that P. brassicae is able to have perception of external signals thanks to specific signalling pathway and to adapt to its environment. In our study, the very early step of interaction between P. brassicae spores and soil microbiota was not measured.…”

“…During both the spore germination and the primary zoospore stages, the pathogen showed high active metabolisms of chitinous cell wall digestion, starch, citrate cycle, pentose phosphate pathway, pyruvate, trehalose, carbohydrates and lipids (Schwelm et al ., 2015a; Schwelm et al ., 2015b; Bi et al ., 2016). During the second phase of infection, genes involved in basal and lipid metabolism were highly expressed (Bi et al ., 2016), as well as the G‐protein‐coupled receptors pathway‐related genes (Bi et al ., 2019). These active metabolic pathways allow P. brassicae to take up nutrients from the host cells (Kageyama and Asano, 2009; Perez‐Lopez et al ., 2018).…”

The zoospores of the thraustochytrid Aurantiochytrium limacinum: Transcriptional reprogramming and lipid metabolism associated to their specific functions

“…The signalling pathway of GPCRs is spread through the whole living kingdom (de Mendoza et al ., ), e.g. it has been demonstrated that diatoms sense the presence of predators via the GPCR signal transduction pathway (Amato et al ., ) and that in the rhizarian protist Plasmodiophora brassicae GPCR signal transduction pathways underwent a robust expansion and plays a pivotal role in the germination of resting spores (Bi et al ., ). Furthermore, in oomycetes a very peculiar GPCR system evolved (Meijer and Govers, ).…”