Hierarchical and Dynamic Regulation of Defense-Responsive Specialized Metabolism by WRKY and MYB Transcription Factors

Abstract

The plant kingdom produces hundreds of thousands of specialized bioactive metabolites, some with pharmaceutical and biotechnological importance. Their biosynthesis and function have been studied for decades, but comparatively less is known about how transcription factors with overlapping functions and contrasting regulatory activities coordinately control the dynamics and output of plant specialized metabolism. Here, we performed temporal studies on pathogen-infected intact host plants with perturbed transcription factors. We identified WRKY33 as the condition-dependent master regulator and MYB51 as the dual functional regulator in a hierarchical gene network likely responsible for the gene expression dynamics and metabolic fluxes in the camalexin and 4-hydroxy-indole-3-carbonylnitrile (4OH-ICN) pathways. This network may have also facilitated the regulatory capture of the newly evolved 4OH-ICN pathway in Arabidopsis thaliana by the more-conserved transcription factor MYB51. It has long been held that the plasticity of plant specialized metabolism and the canalization of development should be differently regulated; our findings imply a common hierarchical regulatory architecture orchestrated by transcription factors for specialized metabolism and development, making it an attractive target for metabolic engineering.

Trichoderma and the Plant Heritable Priming Responses

“…The R2R3-MYB TFs that only exist in terrestrial plants are capable of binding to the WRKY promoters leading to their expression (e.g., MYB44 directly regulates the expression of WRKY70 ; and MYB51 that of WRKY33 ) [ 89 , 90 ]. MYBs are involved in multiple stress responses, including defence-induced lignification and basal immunity (MYB15), SA-and JA-mediated defence responses and enhancement of ABA signalling (MYB44), indolic glucosinolate biosynthesis upon SA and ET signalling in Arabidopsis and salt/osmotic stress regulation (MYB51), early signalling of rhizosphere-induced systemic defence (MYB72), and auxin modulation and root development through interaction with ARFs (MYB77) [ 89 , 90 , 91 , 92 , 93 ]. The root-specific TF MYB72 is required for JA/ET-dependent systemic resistance and callose accumulation induced by T. asperellum in Arabidopsis plants and also functions as an early node of convergence in the signalling pathways that are induced by different beneficial microorganisms, such as Trichoderma itself and Pseudomonas fluorescens [ 70 ].…”

WRKY33-mediated indole glucosinolate metabolic pathway confers host resistance againstAlternaria brassicicola

“…Trp-derived secondary metabolites (camalexin, 4OH-ICN and IGS) are important components of plant innate immune system, and WRKY33 was reported as an important regulator of camalexin and 4OH-ICN (Mao et al, 2012; Barco et al, 2019; Barco and Clay, 2020) (Figure 3A). To investigate the role of different Trp-derived metabolites in host resistance to A. brassicicola, the temporal expression patterns of Trp-derived secondary metabolic pathway genes were analyzed by qRT-PCR analysis with samples collected at different time points after inoculation with A. brassicicola .…”

“…WRKY TFs specifically bind to motif-containing W-box core sequences, and WRKY33 has been reported to bind to W-box containing the promoter region of MYB51 , CYP79B2 , and CYP79B3 in response to different pathogens (Barco and Clay, 2020). MYB51 is the common TF of Tryptophan-derived secondary metabolites.…”

“…Our RNA-seq data and qRT-PCR analysis indicated that numerous glucosinolates-related genes were induced by A. brassicicola infection (Figure 1D and Figure 3B). Previous researches have shown that CYP79B2 and CYP79B3 were induced intensively upon Botrytis cinerea infection, leading to a significant increase in IAOx, the common precursor of camalexin, 4OH-ICN and IGS (Barco and Clay, 2020). However, CYP79B2 and CYP79B3 were only slightly induced, while CYP83B1, a gene involved in the specific downstream biosynthetic step from IAOx to IGS, was intensively induced upon A. brassicicola infection in the present study (Figure 3B), indicating that IGS pathway might play a more important role in response to host-specific fungi A. brassicicola, rather than to wide-ranging host fungi Botrytis cinerea .…”

Mobility connects: transposable elements wire new transcriptional networks by transferring transcription factor binding motifs

“…After gene duplication, CYPB2C2 in Arabidopsis thaliana acquired WRKY33-related motifs by insertion of a LINE retrotransposon. This generated a new pathogen defense pathway controlled by WRKY33 [64,106].…”