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

Abstract

Plasmodiophora brassicae, an obligate biotrophic pathogen-causing clubroot disease, can seriously affect Brassica crops worldwide, especially Chinese cabbage. Understanding the transcriptome and metabolome profiling changes during the infection of P. brassicae will provide key insights in understanding the defense mechanism in Brassica crops. In this study, we estimated the phytohormones using targeted metabolome assays and transcriptomic changes using RNA sequencing (RNA-seq) in the roots of resistant (BrT24) and susceptible (Y510-9) plants at 0, 3, 9, and 20 days after inoculation (DAI) with P. brassicae. Differentially expressed genes (DEGs) in resistant vs. susceptible lines across different time points were identified. The weighted gene co-expression network analysis of the DEGs revealed six pathways including “Plant–pathogen interaction” and “Plant hormone signal transduction” and 15 hub genes including pathogenic type III effector avirulence factor gene (RIN4) and auxin-responsive protein (IAA16) to be involved in plants immune response. Inhibition of Indoleacetic acid, cytokinin, jasmonate acid, and salicylic acid contents and changes in related gene expression in R-line may play important roles in regulation of clubroot resistance (CR). Based on the combined metabolome profiling and hormone-related transcriptomic responses, we propose a general model of hormone-mediated defense mechanism. This study definitely enhances our current understanding and paves the way for improving CR in Brassica rapa.

What Can We Learn from -Omics Approaches to Understand Clubroot Disease?

“…The respective defense pathways were supported by the differential regulation of WRKY genes that are known as SA response transcription factors [ 126 ], and SA- as well as ethylene-responsive genes. In another B. rapa comparison of susceptible and resistant cultivars and P. brassicae , the general induction of defense pathways was confirmed but the authors found additional evidence for upregulation of ethylene and brassinosteroids in the resistance response, whereas the SA response was downregulated [ 127 ]. In addition, the role of SA and JA as defense signals was investigated in the comparison of susceptible and resistant B. oleracea var.…”

“…In leaves and roots, but not galls, ABA was induced during the late response [ 39 ] which corresponds to the ABA-related genes that were reported in transcriptomes [ 2 , 120 ]. Furthermore, a comparison of a resistant with a susceptible line and subsequent analysis of their hormonal profiles in addition to the transcriptional response linked ABA to a function in the late susceptible response in roots of B. rapa [ 127 ]. In addition to growth-promoting hormones and abiotic stress signals, the defense compounds JA, SA, and the ethylene precursor ACC were determined.…”

“…In addition to growth-promoting hormones and abiotic stress signals, the defense compounds JA, SA, and the ethylene precursor ACC were determined. A suppression of JA and SA in the resistant line at late stages was found, but their upregulation in the susceptible line [ 127 ]. In another study comparing resistant and susceptible B. rapa ssp.…”

Multi-Omics Approaches to Improve Clubroot Resistance in Brassica with a Special Focus on Brassica oleracea L.

“…pekinensis Isolate Ibaraki-1 Roots 10, 15, 20, 23, 27, 30, 35, 40 and 60 dpi P . Brassicae infection transiently stimulates the transcription of BrIPT1 , 3 , 5 , and 7 (cytokinin synthase genes) before club formation [ 239 ] B. rapa Race 4 Roots 0, 3, 9 and 20 dai Plant hormone signal transduction, plant-pathogen interaction, and fifteen hub genes ( RIN4 and IAA16 ) were involved in immune response [ 240 ] B. napus Pathotype 4 Total root tissue 20 dai The pyramided line (618R) strongly triggers multiple resistance pathways [ 241 ] B . napus subsp.…”

The Upregulated Expression of the Citrus RIN4 Gene in HLB Diseased Citrus Aids Candidatus Liberibacter Asiaticus Infection

“…cubense tropical race 4) infection in both banana-wilt resistant and susceptible banana varieties, suggesting that its down-regulation may be related to the Fusarium wilt disease-resistance of banana [35]. In Brassica rapa, a RIN4 gene was identified as one of the 15 hub genes involving in the plant immune responses to Plasmodiophora brassicae infection [36].…”