UDP-glycosyltransferases from the UGT73C subfamily in Barbarea vulgaris catalyse Sapogenin 3-O-glucosylation in Saponin-mediated Insect resistance

Jörg Manfred Augustin; Sylvia Drok; Tetsuro  Shinoda; Kazutsuka  Sanmiya; Jens Kvist Nielsen; Bekzod Khakimov; Carl Erik Olsen; Esben Halkjær Hansen; Vera Kuzina Poulsen; Claus Thorn Ekstrøm; Thure Pavlo Hauser; Søren Bak

doi:10.1104/pp.112.202747

UDP-glycosyltransferases from the UGT₇₃C subfamily in Barbarea vulgaris catalyse Sapogenin ₃-O-glucosylation in Saponin-mediated Insect resistance

Jörg Manfred Augustin, Sylvia Drok, Tetsuro Shinoda, Kazutsuka Sanmiya, Jens Kvist Nielsen, Bekzod Khakimov, Carl Erik Olsen, Esben Halkjær Hansen, Vera Kuzina Poulsen, Claus Thorn Ekstrøm, Thure Pavlo Hauser, Søren Bak

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Abstract

Triterpenoid saponins are bioactive metabolites that have evolved recurrently in plants, presumably for defense. Their biosynthesis is poorly understood, as is the relationship between bioactivity and structure. Barbarea vulgaris is the only crucifer known to produce saponins. Hederagenin and oleanolic acid cellobioside make some B. vulgaris plants resistant to important insect pests, while other, susceptible plants produce different saponins. Resistance could be caused by glucosylation of the sapogenins. We identified four family 1 glycosyltransferases (UGTs) that catalyze 3-O-glucosylation of the sapogenins oleanolic acid and hederagenin. Among these, UGT73C10 and UGT73C11 show highest activity, substrate specificity and regiospecificity, and are under positive selection, while UGT73C12 and UGT73C13 show lower substrate specificity and regiospecificity and are under purifying selection. The expression of UGT73C10 and UGT73C11 in different B. vulgaris organs correlates with saponin abundance. Monoglucosylated hederagenin and oleanolic acid were produced in vitro and tested for effects on P. nemorum. 3-O-β-D-Glc hederagenin strongly deterred feeding, while 3-O-β-D-Glc oleanolic acid only had a minor effect, showing that hydroxylation of C23 is important for resistance to this herbivore. The closest homolog in Arabidopsis thaliana, UGT73C5, only showed weak activity toward sapogenins. This indicates that UGT73C10 and UGT73C11 have neofunctionalized to specifically glucosylate sapogenins at the C3 position and demonstrates that C3 monoglucosylation activates resistance. As the UGTs from both the resistant and susceptible types of B. vulgaris glucosylate sapogenins and are not located in the known quantitative trait loci for resistance, the difference between the susceptible and resistant plant types is determined at an earlier stage in saponin biosynthesis.

Original language	English
Journal	Plant Physiology
Volume	160
Issue number	4
Pages (from-to)	1881-1895
Number of pages	15
ISSN	0032-0889
DOIs	https://doi.org/10.1104/pp.112.202747
Publication status	Published - Dec 2012

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10.1104/pp.112.202747

UDP-Glycosyltransferases from the UGT73C Subfamily in Barbarea vulgaris Catalyze Sapogenin 3- O -Glucosylation in Saponin-Mediated Insect ResistanceFinal published version, 661 KB

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Augustin, J. M., Drok, S., Shinoda, T., Sanmiya, K., Nielsen, J. K., Khakimov, B., Olsen, C. E., Hansen, E. H., Poulsen, V. K., Ekstrøm, C. T., Hauser, T. P., & Bak, S. (2012). UDP-glycosyltransferases from the UGT₇₃C subfamily in Barbarea vulgaris catalyse Sapogenin ₃-O-glucosylation in Saponin-mediated Insect resistance. Plant Physiology, 160(4), 1881-1895. https://doi.org/10.1104/pp.112.202747

Augustin, JM, Drok, S, Shinoda, T, Sanmiya, K, Nielsen, JK, Khakimov, B, Olsen, CE, Hansen, EH, Poulsen, VK, Ekstrøm, CT, Hauser, TP & Bak, S 2012, 'UDP-glycosyltransferases from the UGT₇₃C subfamily in Barbarea vulgaris catalyse Sapogenin ₃-O-glucosylation in Saponin-mediated Insect resistance', Plant Physiology, vol. 160, no. 4, pp. 1881-1895. https://doi.org/10.1104/pp.112.202747

@article{25de01c5488549ff9df1864fa7a88c2c,

title = "UDP-glycosyltransferases from the UGT73C subfamily in Barbarea vulgaris catalyse Sapogenin 3-O-glucosylation in Saponin-mediated Insect resistance",

abstract = "Triterpenoid saponins are bioactive metabolites that have evolved recurrently in plants, presumably for defense. Their biosynthesis is poorly understood, as is the relationship between bioactivity and structure. Barbarea vulgaris is the only crucifer known to produce saponins. Hederagenin and oleanolic acid cellobioside make some B. vulgaris plants resistant to important insect pests, while other, susceptible plants produce different saponins. Resistance could be caused by glucosylation of the sapogenins. We identified four family 1 glycosyltransferases (UGTs) that catalyze 3-O-glucosylation of the sapogenins oleanolic acid and hederagenin. Among these, UGT73C10 and UGT73C11 show highest activity, substrate specificity and regiospecificity, and are under positive selection, while UGT73C12 and UGT73C13 show lower substrate specificity and regiospecificity and are under purifying selection. The expression of UGT73C10 and UGT73C11 in different B. vulgaris organs correlates with saponin abundance. Monoglucosylated hederagenin and oleanolic acid were produced in vitro and tested for effects on P. nemorum. 3-O-β-D-Glc hederagenin strongly deterred feeding, while 3-O-β-D-Glc oleanolic acid only had a minor effect, showing that hydroxylation of C23 is important for resistance to this herbivore. The closest homolog in Arabidopsis thaliana, UGT73C5, only showed weak activity toward sapogenins. This indicates that UGT73C10 and UGT73C11 have neofunctionalized to specifically glucosylate sapogenins at the C3 position and demonstrates that C3 monoglucosylation activates resistance. As the UGTs from both the resistant and susceptible types of B. vulgaris glucosylate sapogenins and are not located in the known quantitative trait loci for resistance, the difference between the susceptible and resistant plant types is determined at an earlier stage in saponin biosynthesis.",

author = "Augustin, {J{\"o}rg Manfred} and Sylvia Drok and Tetsuro Shinoda and Kazutsuka Sanmiya and Nielsen, {Jens Kvist} and Bekzod Khakimov and Olsen, {Carl Erik} and Hansen, {Esben Halkj{\ae}r} and Poulsen, {Vera Kuzina} and Ekstr{\o}m, {Claus Thorn} and Hauser, {Thure Pavlo} and S{\o}ren Bak",

year = "2012",

month = dec,

doi = "10.1104/pp.112.202747",

language = "English",

volume = "160",

pages = "1881--1895",

journal = "Plant Physiology",

issn = "0032-0889",

publisher = "American Society of Plant Biologists",

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TY - JOUR

T1 - UDP-glycosyltransferases from the UGT73C subfamily in Barbarea vulgaris catalyse Sapogenin 3-O-glucosylation in Saponin-mediated Insect resistance

AU - Augustin, Jörg Manfred

AU - Drok, Sylvia

AU - Shinoda, Tetsuro

AU - Sanmiya, Kazutsuka

AU - Nielsen, Jens Kvist

AU - Khakimov, Bekzod

AU - Olsen, Carl Erik

AU - Hansen, Esben Halkjær

AU - Poulsen, Vera Kuzina

AU - Ekstrøm, Claus Thorn

AU - Hauser, Thure Pavlo

AU - Bak, Søren

PY - 2012/12

Y1 - 2012/12

N2 - Triterpenoid saponins are bioactive metabolites that have evolved recurrently in plants, presumably for defense. Their biosynthesis is poorly understood, as is the relationship between bioactivity and structure. Barbarea vulgaris is the only crucifer known to produce saponins. Hederagenin and oleanolic acid cellobioside make some B. vulgaris plants resistant to important insect pests, while other, susceptible plants produce different saponins. Resistance could be caused by glucosylation of the sapogenins. We identified four family 1 glycosyltransferases (UGTs) that catalyze 3-O-glucosylation of the sapogenins oleanolic acid and hederagenin. Among these, UGT73C10 and UGT73C11 show highest activity, substrate specificity and regiospecificity, and are under positive selection, while UGT73C12 and UGT73C13 show lower substrate specificity and regiospecificity and are under purifying selection. The expression of UGT73C10 and UGT73C11 in different B. vulgaris organs correlates with saponin abundance. Monoglucosylated hederagenin and oleanolic acid were produced in vitro and tested for effects on P. nemorum. 3-O-β-D-Glc hederagenin strongly deterred feeding, while 3-O-β-D-Glc oleanolic acid only had a minor effect, showing that hydroxylation of C23 is important for resistance to this herbivore. The closest homolog in Arabidopsis thaliana, UGT73C5, only showed weak activity toward sapogenins. This indicates that UGT73C10 and UGT73C11 have neofunctionalized to specifically glucosylate sapogenins at the C3 position and demonstrates that C3 monoglucosylation activates resistance. As the UGTs from both the resistant and susceptible types of B. vulgaris glucosylate sapogenins and are not located in the known quantitative trait loci for resistance, the difference between the susceptible and resistant plant types is determined at an earlier stage in saponin biosynthesis.

AB - Triterpenoid saponins are bioactive metabolites that have evolved recurrently in plants, presumably for defense. Their biosynthesis is poorly understood, as is the relationship between bioactivity and structure. Barbarea vulgaris is the only crucifer known to produce saponins. Hederagenin and oleanolic acid cellobioside make some B. vulgaris plants resistant to important insect pests, while other, susceptible plants produce different saponins. Resistance could be caused by glucosylation of the sapogenins. We identified four family 1 glycosyltransferases (UGTs) that catalyze 3-O-glucosylation of the sapogenins oleanolic acid and hederagenin. Among these, UGT73C10 and UGT73C11 show highest activity, substrate specificity and regiospecificity, and are under positive selection, while UGT73C12 and UGT73C13 show lower substrate specificity and regiospecificity and are under purifying selection. The expression of UGT73C10 and UGT73C11 in different B. vulgaris organs correlates with saponin abundance. Monoglucosylated hederagenin and oleanolic acid were produced in vitro and tested for effects on P. nemorum. 3-O-β-D-Glc hederagenin strongly deterred feeding, while 3-O-β-D-Glc oleanolic acid only had a minor effect, showing that hydroxylation of C23 is important for resistance to this herbivore. The closest homolog in Arabidopsis thaliana, UGT73C5, only showed weak activity toward sapogenins. This indicates that UGT73C10 and UGT73C11 have neofunctionalized to specifically glucosylate sapogenins at the C3 position and demonstrates that C3 monoglucosylation activates resistance. As the UGTs from both the resistant and susceptible types of B. vulgaris glucosylate sapogenins and are not located in the known quantitative trait loci for resistance, the difference between the susceptible and resistant plant types is determined at an earlier stage in saponin biosynthesis.

U2 - 10.1104/pp.112.202747

DO - 10.1104/pp.112.202747

M3 - Journal article

C2 - 23027665

SN - 0032-0889

VL - 160

SP - 1881

EP - 1895

JO - Plant Physiology

JF - Plant Physiology

IS - 4

ER -

UDP-glycosyltransferases from the UGT73C subfamily in Barbarea vulgaris catalyse Sapogenin 3-O-glucosylation in Saponin-mediated Insect resistance

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UDP-glycosyltransferases from the UGT₇₃C subfamily in Barbarea vulgaris catalyse Sapogenin ₃-O-glucosylation in Saponin-mediated Insect resistance