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New Insights into the Plutella xylostella Detoxifying Enzymes: Sequence Evolution, Structural Similarity, Functional Diversity, and Application Prospects of Glucosinolate Sulfatases.

ABSTRACT: Brassica plants have glucosinolate (GLs)-myrosinase defense mechanisms to deter herbivores. However, Plutella xylostella specifically feeds on Brassica vegetables. The larvae possess three glucosinolate sulfatases (PxGSS1-3) that compete with plant myrosinase for shared GLs substrates and produce nontoxic desulfo-GLs (deGLs). Although PxGSSs are considered potential targets for pest control, the lack of a comprehensive review has hindered the development of PxGSSs-targeted pest control methods. Recent advances in integrative multi-omics analysis, substrate-enzyme kinetics, and molecular biological techniques have elucidated the evolutionary origin and functional diversity of these three PxGSSs. This review summarizes research progress on PxGSSs over the past 20 years, covering sequence properties, evolution, protein modification, enzyme activity, structural variation, substrate specificity, and interaction scenarios based on functional diversity. Finally, we discussed the potential applications of PxGSSs-targeted pest control technologies driven by artificial intelligence, including CRISPR/Cas9-mediated gene drive, transgenic plant-mediated RNAi, small-molecule inhibitors, and peptide inhibitors. These technologies have the potential to overcome current management challenges and promote the development and field application of PxGSSs-targeted pest control.

SUBMITTER: Chen W

PROVIDER: S-EPMC10375594 | biostudies-literature | 2023 Jul

REPOSITORIES: biostudies-literature

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New Insights into the <i>Plutella xylostella</i> Detoxifying Enzymes: Sequence Evolution, Structural Similarity, Functional Diversity, and Application Prospects of Glucosinolate Sulfatases.

Chen Wei W Amir Muhammad Bilal MB Liao Yuan Y Yu Haizhong H He Weiyi W Lu Zhanjun Z

Journal of agricultural and food chemistry 20230718 29

Brassica plants have glucosinolate (GLs)-myrosinase defense mechanisms to deter herbivores. However, <i>Plutella xylostella</i> specifically feeds on Brassica vegetables. The larvae possess three glucosinolate sulfatases (PxGSS1-3) that compete with plant myrosinase for shared GLs substrates and produce nontoxic desulfo-GLs (deGLs). Although PxGSSs are considered potential targets for pest control, the lack of a comprehensive review has hindered the development of PxGSSs-targeted pest control me ...[more]

PMID: 37462091

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Project description:The inducibility of the glucosinolate resistance mechanism is an energy-saving strategy for plants, but whether induction would still be triggered by glucosinolate-tolerant Plutella xylostella (diamondback moth, DBM) after a plant had evolved a new resistance mechanism (e.g., saponins in Barbara vulgaris) was unknown. In B. vulgaris, aromatic glucosinolates derived from homo-phenylalanine are the dominant glucosinolates, but their biosynthesis pathway was unclear. In this study, we used G-type (pest-resistant) and P-type (pest-susceptible) B. vulgaris to compare glucosinolate levels and the expression profiles of their biosynthesis genes before and after infestation by DBM larvae. Two different stereoisomers of hydroxylated aromatic glucosinolates are dominant in G- and P-type B. vulgaris, respectively, and are induced by DBM. The transcripts of genes in the glucosinolate biosynthesis pathway and their corresponding transcription factors were identified from an Illumina dataset of G- and P-type B. vulgaris. Many genes involved or potentially involved in glucosinolate biosynthesis were induced in both plant types. The expression patterns of six DBM induced genes were validated by quantitative PCR (qPCR), while six long-fragment genes were validated by molecular cloning. The core structure biosynthetic genes showed high sequence similarities between the two genotypes. In contrast, the sequence identity of two apparent side chain modification genes, the SHO gene in the G-type and the RHO in P-type plants, showed only 77.50% identity in coding DNA sequences and 65.48% identity in deduced amino acid sequences. The homology to GS-OH in Arabidopsis, DBM induction of the transcript and a series of qPCR and glucosinolate analyses of G-type, P-type and F1 plants indicated that these genes control the production of S and R isomers of 2-hydroxy-2-phenylethyl glucosinolate. These glucosinolates were significantly induced by P. xylostella larvae in both the susceptiple P-type and the resistant G-type, even though saponins are the main DBM-resistance causing metabolites in G-type plants. Indol-3-ylmethylglucosinolate was induced in the G-type only. These data will aid our understanding of the biosynthesis and induction of aromatic glucosinolates at the molecular level and also increase our knowledge of the complex mechanisms underpinning defense induction in plants.

Project description:Diamondback moth (DBM), Plutella xylostella L., is a devastating pest of cabbage worldwide whose feeding attributes are influenced by glucosinolate profiles of the plant. Identifying the specific glucosinolates associated with plants' resistance mechanism can provide cues to novel points of intervention in developing resistant cultivars. We studied the DBM larval feeding preference and extent of damage on cabbage leaves via controlled glass-house and in vitro multiple- and two-choice feeding tests. These feeding attributes were associated with the individual glucosinolate profiles, analyzed by HPLC, of each of the eight cabbage genotypes using multivariate analytical approach to identify the glucosinolates that may have roles in resistance. Both the glass-house and in vitro multiple-choice feeding tests identified the genotype BN4303, BN4059, and BN4072 as the least preferred (resistant) and Rubra, YR Gold and BN3383 as most preferred (susceptible) genotypes by DBM larvae. The principal component analysis separated the genotypes based on lower feeding scores in association with higher contents of glucobrassicin, glucoiberin, glucoiberverin in one direction and 4-hydroxyglucobrassicin, glucoerucin, glucoraphanin, and progoitrin in opposite direction in a way to explain the major variation in resistant versus susceptible genotypes based on their extent of preference and leaf area damage. The simultaneous presence (or higher contents) of glucobrassicin, glucoiberin, and glucoiberverin and the absence (or lower contents) of 4-hydroxyglucobrassicin, glucoerucin, glucoraphanin, and progoitrin in the least preferred genotypes and vice-versa in most preferred genotypes indicated their apparent role as putative repellents and attractants of DBM larvae in cabbage genotypes, respectively. These novel findings add to the current knowledgebase on the roles of glucosinolates in plant-herbivore interactions and will be helpful in setting breeding priorities for improving the resistance against DBM in cabbage using conventional and biotechnological approaches.

Dataset Information

New Insights into the Plutella xylostella Detoxifying Enzymes: Sequence Evolution, Structural Similarity, Functional Diversity, and Application Prospects of Glucosinolate Sulfatases.

Publications

New Insights into the <i>Plutella xylostella</i> Detoxifying Enzymes: Sequence Evolution, Structural Similarity, Functional Diversity, and Application Prospects of Glucosinolate Sulfatases.

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