Transcriptome Arofile of Brassica rapa L. Reveals the Involvement of Jasmonic Acid, Ethylene, and Brassinosteroid Signaling Pathways in Clubroot Resistance

Abstract

Plasmodiophora brassicae is a protozoan pathogen that causes clubroot disease in cruciferous plants, particularly Chinese cabbage (Brassica rapa). A previous study identified a clubroot resistance gene (CRd) conferring race-specific resistance to P. brassicae. However, the defense mechanisms of B. rapa against virulent vs. avirulent P. brassicae are poorly understood. In this study, we carried out a global transcriptional analysis in the clubroot-resistant Chinese cabbage inbred line “85–74” carrying the CRd gene and inoculated with avirulent (LAB-4) or virulent (SCCD-52) P. brassicae. RNA sequencing showed that “85–74” responded most rapidly to SCCD-52 infection, and the number of differentially expressed genes was much higher in SCCD-52-treated as compared to LAB-4-treated plants (5552 vs. 304). Transcriptome profiling revealed that plant hormone signal transduction and plant–pathogen interaction pathways played key roles in the late stages of P. brassicae infection. Genes relating to the salicyclic acid (SA), jasmonic acid (JA)/ethylene (ET), and brassinosteroid (BR) signaling pathways were up-regulated relative to untreated plants in response to LAB-4 infection at 8, 16, and 32 days post-inoculation (dpi) whereas JA, ET, and BR signaling-related genes were not activated in response to SCCD-52, and SA signaling-related genes were up-regulated in both LAB-4 and SCCD-52, suggesting that SA signaling is not the key factor in host resistance to avirulent P. brassicae. In addition, genes associated with phosphorylation and Ca2+ signaling pathways were down-regulated to a greater degree following LAB-4 as compared to SCCD-52 infection at 8 dpi. These results indicate that effector-triggered immunity in “85–74” is more potently activated in response to infection with avirulent P. brassicae and that JA, ET, and BR signaling are important for the host response at the late stage of infection. These findings provide insight into P. brassicae pathotype-specific defense mechanisms in cruciferous crops.

Root Transcriptome and Metabolome Profiling Reveal Key Phytohormone-Related Genes and Pathways Involved Clubroot Resistance in Brassica rapa L.

“…In recent years, several “-omics” studies have focused on understanding the molecular mechanisms of clubroot resistance (CR) ( Jia et al, 2017 ; Fu et al, 2019 ; Ning et al, 2019 ; Summanwar et al, 2021 ; Yuan et al, 2021 ). In Brassica , several studies indicated that the genes involved in cell-wall modification, SA signal transduction, phytoalexin synthesis, chitinase synthesis, Ca 2+ signaling, reactive oxygen gene activation, the signaling metabolism of jasmonate and ethylene (ET), defensive deposition of callose, and the biosynthesis of indole-containing compounds were all significantly upregulated in clubroot-resistant plants ( Devos et al, 2006 ; Chu et al, 2014 ; Zhang et al, 2016 ; Li et al, 2019 ; Zhou et al, 2020 ).…”

Identification of Arabidopsis Phospholipase A Mutants With Increased Susceptibility to Plasmodiophora brassicae

“…Since infection by P. brassicae interferes with root water uptake and leads to drought stress symptoms in the aboveground canopy (Ludwig-Müller, 2009), PLAs might be involved in a clubroot-related drought response in plants. While little is known regarding the role of PLAs in the host response to clubroot, recently published transcriptomic profiles from P. brassicaeinfected B. napus allowed us to identify PLAs showing differential expression following inoculation (Fu et al, 2019;Galindo-González et al, 2020;Zhou et al, 2020b). Therefore, study of the role(s) of PLAs in the host response to clubroot could provide insights into the utility of PLAs in clubroot resistance breeding.…”

“…The expression of PLA 1 -III was modulated in Arabidopsis upon B. cinerea (Grienenberger et al, 2010) challenge, respectively. Expression of an AtPLA 1 -III homolog in CR Chinese cabbage (B. rapa) was induced (BraA07g010560.3C) during the early infection stage (4 dai) following inoculation with a virulent pathotype of P. brassicae (Fu et al, 2019). A homolog of AtPLA 1 -III was downregulated in B. napus (BnaC05g23260D) during the late stage of the clubroot-susceptible response (Galindo-González et al, 2020;Zhou et al, 2020b; Supplementary Figure 2), while two other BnPLA 1 -III homologs (BnaA07g07350D and BnaA09g26150D) were downregulated in both resistant and susceptible reactions, with greater downregulation in the latter (Galindo-González et al, 2020).…”

Endomembrane-Targeting Plasmodiophora brassicae Effectors Modulate PAMP Triggered Immune Responses in Plants

“…A similar pattern of fluorescence distribution, due to membrane raft reorganization, has been observed for GFP- Nb REM4 and FLS2, after flg22 treatment ( Keinath et al, 2010 ; Albers et al, 2019 ). An increase in B. rapa FLS2 (BraA09g021780.3C) transcript levels has been observed after infection with a virulent strain (SCCD-52) of P. brassicae ( Fu et al, 2019 ). The association of Δ sp Pb PE13GFP with this complex suggests that it may have a role in hijacking the endocytosis response and redirecting the process toward a root-wide distribution of the pathogen.…”