A gossypol biosynthetic intermediate disturbs plant defence response

Abstract

Plant secondary metabolites and their biosynthesis have attracted great interest, but investigations of the activities of hidden intermediates remain rare. Gossypol and related sesquiterpenes are the major phytoalexins in cotton. Among the six biosynthetic intermediates recently identified, 8-hydroxy-7-keto-δ-cadinene (C234) crippled the plant disease resistance when accumulated upon gene silencing. C234 harbours an α,β-unsaturated carbonyl thus is a reactive electrophile species. Here, we show that C234 application also dampened the Arabidopsis resistance against the bacterial pathogen Pseudomonas syringae pv. maculicola (Psm). We treated Arabidopsis with C234, Psm and (Psm+C234), and analysed the leaf transcriptomes. While C234 alone exerted a mild effect, it greatly stimulated an over-response to the pathogen. Of the 7335 genes affected in the (Psm+C234)-treated leaves, 3476 were unresponsive without the chemical, in which such functional categories as ‘nucleotides transport’, ‘vesicle transport’, ‘MAP kinases’, ‘G-proteins’, ‘protein assembly and cofactor ligation’ and ‘light reaction’ were enriched, suggesting that C234 disturbed certain physiological processes and the protein complex assembly, leading to distorted defence response and decreased disease resistance. As C234 is efficiently metabolized by CYP71BE79, plants of cotton lineage have evolved a highly active enzyme to prevent the phytotoxic intermediate accumulation during gossypol pathway evolution.This article is part of the theme issue ‘Biotic signalling sheds light on smart pest management’.

Engineering Plant Cytochrome P450s for Enhanced Synthesis of Natural Products: Past Achievements and Future Perspectives

“…For example, gossypol, a sesquiterpene aldehyde that accumulates in cotton seeds, has been demonstrated to exhibit anti-tumor activity against several cancer cells ( Neergheen et al., 2010 ), but there is also evidence pointing to its anti-nutritional properties ( Sunilkumar et al., 2006 ). Fortunately, several related intermediates with potentially similar bioactivities that are less toxic have been identified recently ( Tian et al., 2018 , Tian et al., 2019 ). In these studies, it was shown that cotton uses CYP71BE79, a highly active enzyme, to decorate one of the intermediates (8-hydroxy-7-keto-δ-cadinene) and prevent its phytotoxicity during gossypol synthesis ( Tian et al., 2018 , Tian et al., 2019 ).…”

“…Fortunately, several related intermediates with potentially similar bioactivities that are less toxic have been identified recently ( Tian et al., 2018 , Tian et al., 2019 ). In these studies, it was shown that cotton uses CYP71BE79, a highly active enzyme, to decorate one of the intermediates (8-hydroxy-7-keto-δ-cadinene) and prevent its phytotoxicity during gossypol synthesis ( Tian et al., 2018 , Tian et al., 2019 ). Interestingly, while genes involved in secondary metabolic pathways tend to be clustered in the plant genome ( Field et al., 2011 , Chae et al., 2014 ), the gossypol pathway genes are dispersed, and the three P450s identified belong to different families, suggesting that phylogenetically distant P450s can also act on structurally similar substrates ( Tian et al., 2018 ).…”

Selenium mediated host plant–mite conflict: defense and adaptation

“…Constitutive defenses are the innate physical or chemical factors that exist in plants and can hinder the infection of pathogens and the feeding of herbivores. These include thorns, villi, waxy layers, and chemicals, such as terpenoids and alkaloids 2–4 . Generally, these compounds are distributed in plants and their contents can be changed according to different environmental conditions.…”

“…These include thorns, villi, waxy layers, and chemicals, such as terpenoids and alkaloids. [2][3][4] Generally, these compounds are distributed in plants and their contents can be changed according to different environmental conditions. However, they exist throughout the life of the plant and provide constant protection.…”

Overview: biotic signalling for smart pest management

“…Among the six newly identified intermediates, one (8-hydroxy-7-keto-d-cadinene) has an a, bunsaturated carbonyl group and stimulates the expression of a large number of pathogenesis-related genes, despite the fact that it deteriorates plant resistance to diseases. This paradoxical effect implies that the gossypol pathway may have evolved step by step in the family of Malvaceae [20]. Reactive oxygen species (ROS) also play important roles in the defence response of host plant against various pathogens.…”