TY - JOUR
T1 - Clovamide, a Hydroxycinnamic Acid Amide, Is a Resistance Factor Against Phytophthora spp. in Theobroma cacao
AU - Knollenberg, Benjamin J.
AU - Li, Guo Xing
AU - Lambert, Joshua D.
AU - Maximova, Siela N.
AU - Guiltinan, Mark J.
N1 - Funding Information:
We would like to thank Dr. Philip Smith (Metabolomics Facility at the Huck Institutes of the Life Sciences, Pennsylvania State University) for LC-MS/MS operation and guidance in data interpretation. We would also like to thank Allison Brown and Dr. Helene Hopfer (Food Science Department, Pennsylvania State University) for sharing lab space, equipment, and expertise regarding HPLC-DAD method development. Dr. Gong Chen (Chemistry, Pennsylvania State University) generously offered lab space and equipment for the synthesis of clovamide. Funding. This project was supported by The Pennsylvania State University College of Agricultural Sciences, the Huck Institutes of the Life Sciences, the Penn State Endowed Program in the Molecular Biology of Cacao, The J. Franklin Styer Professor of Horticultural Botany Endowment, and the USDA National Institute of Food and Agriculture, Federal Appropriations under Project PEN04569 and Accession Number 1003147.
Publisher Copyright:
© Copyright © 2020 Knollenberg, Li, Lambert, Maximova and Guiltinan.
PY - 2020/12/23
Y1 - 2020/12/23
N2 - 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.
AB - 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.
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U2 - 10.3389/fpls.2020.617520
DO - 10.3389/fpls.2020.617520
M3 - Article
C2 - 33424909
AN - SCOPUS:85099157054
SN - 1664-462X
VL - 11
JO - Frontiers in Plant Science
JF - Frontiers in Plant Science
M1 - 617520
ER -