Abstract
The hydroxycinnamic acid amides (HCAAs) are a diverse group of plant-specialized phenylpropanoid metabolites distributed widely in the plant kingdom and are known to be involved in tolerance to abiotic and biotic stress. The HCAA clovamide is reported in a small number of distantly related species. To explore the contribution of specialized metabolites to disease resistance in cacao (Theobroma cacao L., chocolate tree), we performed untargeted metabolomics using liquid chromatography – tandem mass spectrometry (LC-MS/MS) and compared the basal metabolite profiles in leaves of two cacao genotypes with contrasting levels of susceptibility to Phytophthora spp. Leaves of the tolerant genotype ‘Scavina 6’ (‘Sca6’) were found to accumulate dramatically higher levels of clovamide and several other HCAAs compared to the susceptible ‘Imperial College Selection 1’ (‘ICS1’). Clovamide was the most abundant metabolite in ‘Sca6’ leaf extracts based on MS signal, and was up to 58-fold higher in ‘Sca6’ than in ‘ICS1’. In vitro assays demonstrated that clovamide inhibits growth of three pathogens of cacao in the genus Phytophthora, is a substrate for cacao polyphenol oxidase, and is a contributor to enzymatic browning. Furthermore, clovamide inhibited proteinase and pectinase in vitro, activities associated with defense in plant-pathogen interactions. Fruit epidermal peels from both genotypes contained substantial amounts of clovamide, but two sulfated HCAAs were present at high abundance exclusively in ‘Sca6’ suggesting a potential functional role of these compounds. The potential to breed cacao with increased HCAAs for improved agricultural performance is discussed.
Highlights
The Food and Agriculture Organization of the United Nations has declared 2020 as the International Year of Plant Health, one of the major goals of which being to “keep plants healthy while protecting the environment” (FAO, 2019)
In this work we describe clovamide, a hydroxycinnamic acid amide (HCAA) metabolite, as an important resistance factor in cacao (Theobroma cacao, chocolate) against pathogens in the genus Phytophthora, an oomycete genus comprised of over 100 species, many of which are globally important plant pathogens with broad host ranges (Thines, 2014)
Clovamide inhibited proteolysis and pectolysis in vitro, was confirmed as a substrate for cacao polyphenol oxidase, and contributed to enzymatic browning in tissue damage assays. Both genotypes tested accumulated clovamide in fruit epidermal peels, but two sulfated HCAAs were accumulated at high levels exclusively in ‘Scavina 6’ (Sca6).’. These results indicate that clovamide accumulation is an important factor in ‘Sca6’ tolerance to Phytophthora spp. in leaves and sulfated HCAAs may play a similar role in fruit peels
Summary
The Food and Agriculture Organization of the United Nations has declared 2020 as the International Year of Plant Health, one of the major goals of which being to “keep plants healthy while protecting the environment” (FAO, 2019). Increasing host plant resistance to pathogens by traditional breeding or genetic engineering is one important strategy to reduce crop losses and the use of pesticides This approach necessitates a more complete understanding of plant resistance, which utilizes an astonishing array of interconnected mechanisms (Wang et al, 2019), including production of defense-related small molecules, or metabolites, with a wide range of structures and activities. HCAAs typically form via the amide condensation of hydroxycinnamoyl-CoA thioesters and amines (Bontpart et al, 2015; Petersen, 2016) They contribute to stress tolerance in numerous plant species due to their high antioxidant activity (Zacares et al, 2007), cell wall reinforcing properties (Gunnaiah et al, 2012), or direct antimicrobial activity (Newman et al, 2001; Kyselka et al, 2018). The role of HCAAs in cacao resistance to Phytophthora spp. has not been described to date
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