Evolution of Glucosinolate Diversity via Whole-Genome Duplications, Gene Rearrangements, and Substrate Promiscuity

Abstract

Over several decades, glucosinolates have become a model system for the study of specialized metabolic diversity in plants. The near-complete identification of biosynthetic enzymes, regulators, and transporters has provided support for the role of gene duplication and subsequent changes in gene expression, protein function, and substrate specificity as the evolutionary bases of glucosinolate diversity. Here, we provide examples of how whole-genome duplications, gene rearrangements, and substrate promiscuity potentiated the evolution of glucosinolate biosynthetic enzymes, regulators, and transporters by natural selection. This in turn may have led to the repeated evolution of glucosinolate metabolism and diversity in higher plants.

Drivers of metabolic diversification: how dynamic genomic neighbourhoods generate new biosynthetic pathways in the Brassicaceae

“…How individual enzymes have evolved to achieve metabolic diversity is relatively well-understood (Benderoth et al, 2006;Weng et al, 2012a;Hofberger et al, 2013;Hamberger & Bak, 2013;Moghe & Last, 2015;Barco & Clay, 2019), whereas the mechanisms of evolution of multi-step pathways are more elusive. In comparison to nonclustered pathways, biosynthetic gene clusters (BGCs) provide unique material with which to systematically study the evolutionary processes underpinning the birth of plant metabolic pathways.…”

Phylogeny and multiple independent whole‐genome duplication events in the Brassicales

“…The relationships among these lineages and clades are unclear. Besides elucidating the relationships within the Brassicaceae, another major area of research has focused on the considerable glucosinolate diversity within the family (Kliebenstein et al, 2001; Ratzka et al, 2002; Züst et al, 2018; Blažević et al, 2019), including the impact of WGD events on the glucosinolate chemical structures (Edger et al, 2015; Barco and Clay, 2019).…”

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

“…They include the A. thaliana-specific benzoyloxy-GSL pathway by the Brassicaceae-specific SG25-type R2R3-MYBs MYB115 and MYB118 (Zhang et al, 2015;Barco et al, 2019a), the Brassicales-specific core GSL pathway by the plant lineagespecific SG3e-type MYCs MYC2-5 (Schweizer et al, 2013;Frerigmann et al, 2014b;Chezem and Clay, 2016); and the Brassicaceae-specific camalexin and A. thaliana-specific 4OH-ICN pathways by the plant lineage-specific WRKY33 (Bednarek et al, 2011;Rinerson et al, 2015;Schluttenhofer and Yuan, 2015;Barco et al, 2019b). MYB51/MYB122 and CYP79B2/CYP79B3 are unique to the GSL-synthesizing plant order Brassicales (Fahey et al, 2001;Bekaert et al, 2012;Barco et al, 2019a), whereas CYP82C2 is a newly duplicated enzyme gene in the A. thaliana-specific 4OH-ICN biosynthetic pathway (Rajniak et al, 2015;Barco et al, 2019b). Our data show that the indole GSL regulator MYB51 interacts with the CYP82C2 promoter at the M and MW regions (Figures 6B, C; Supplementary Image 8) and negatively regulates its expression ( Figure 6A).…”

“…CYP71A13 and CYP71B15/PAD3 convert ICY to camalexin, while flavin-dependent oxidase FOX1/ AtBBE3 and 4-hydroxylase CYP82C2 convert ICY to 4OH-ICN ( Figure 1) (Nafisi et al, 2007;Böttcher et al, 2009;Rajniak et al, 2015). 4M-I3M is synthesized from ANI via glutathione-S-transferases GSTF9-10, g-glutamyl peptidase GGP1, S-alkyl-thiohydroximaste lyase SUR1, UDPglycosyltransferase UGT74B1, sulfotransferase SOT16, 4-hydroxylases CYP81F1-3, and I3M methyltransferases IGMT1-2 ( Figure 1) (Chezem and Clay, 2016;Barco et al, 2019a).…”