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Medicago truncatula Oleanolic-Derived Saponins Are Correlated with Caterpillar Deterrence

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Abstract

Plant resistance mechanisms to insect herbivory can potentially be bred into crops as an important strategy for integrated pest management. Medicago truncatula ecotypes inoculated with the rhizobium Ensifer medicae (Sinorhizobium medica) WSM419 were screened for resistance to herbivory by caterpillars of the beet armyworm, Spodoptera exigua, through leaf and whole plant choice studies; TN1.11 and F83005.5 are identified as the least and most deterrent ecotypes, respectively. In response to caterpillar herbivory, both ecotypes mount a robust burst of plant defensive jasmonate phytohormones. Restriction of caterpillars to either of these ecotypes does not adversely affect pest performance. This argues for an antixenosis (deterrence) resistance mechanism associated with the F83005.5 ecotype. Unbiased metabolomic profiling identified strong ecotype-specific differences in metabolite profile, particularly in the content of oleanolic-derived saponins that may act as antifeedants. Compared to the more susceptible ecotype, F83005.5 has higher levels of oleanolic-type zanhic acid- and medicagenic acid-derived compounds. Together, these data support saponin-mediated deterrence as a resistance mechanism of the F83005.5 ecotype and implicates these compounds as potential antifeedants that could be used in agricultural sustainable pest management strategies.

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Abbreviations

ANOVA:

Analysis of variance

Api:

Apiofuranose

Ara:

Arabinose

Dhex:

Deoxyhexose

Glc:

Glucose

GlcA:

Galacuronic acid

Hex:

Hexose

HexA:

Uronic acid

HPLC-MS/MS:

High performance liquid chromatography-tandem mass spectroscopy

JA:

Jasmonic acid

JA-Ile:

(+)-7-iso-jasmonyl-L-isoleucine

LD:

Least deterrent

MD:

Most deterrent

NMR:

Nuclear magnetic resonance

OPDA:

cis-(+)-12-Oxo-phytodienoic acid

Pen:

Pentose

PCA:

Principal component analysis

Rha:

Rhamnose

UPLC-qTOF-MS:

Ultrahigh performance liquid chromatography-quantitative time-of-flight-mass spectroscopy

Xyl:

Xylose

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Acknowledgements

We thank Drs. J. Howieson and J. Terpolilli (Murdoch University) for the Ensifer medicae WSM419 culture. We thank Jingyuan Ji, Joshua Lee and Yifan Liu for assistance with caterpillar herbivory experiments. We thank the anonymous reviewers of a previous version of this manuscript for their insightful comments. Phytohormone analysis was conducted at the Proteomics & Mass Spectrometry Facility, Danforth Plant Science Center that is supported by a National Science Foundation grant #DBI-1427621 used to purchase a QTRAP LC-MS/MS. This research was funded through a Natural Sciences and Engineering Research Council of Canada grant to JCB.

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  1. Lloyd W. Sumner

    Present address: Department of Biochemistry, University of Missouri, Columbia, MO, 65211, USA

Authors and Affiliations

  1. Department of Plant Science, McGill University, 21,111 Lakeshore, Ste-Anne-de-Bellevue, QC, H9X 3V9, Canada

    Fanping Cai & Jacqueline C. Bede

  2. The Samuel Roberts Noble Foundation, Ardmore, OK, 73401, USA

    Bonnie S. Watson, David V. Huhman & Lloyd W. Sumner

  3. Natural Resource Sciences, McGill University, Ste-Anne-de-Bellevue, QC, H9X 3V9, Canada

    David Meek & Brian T. Driscoll

  4. Department of Chemistry, University of Texas at San Antonio, San Antonio, TX, 78249, USA

    Daniel J. Wherritt

  5. EcoLab, Université de Toulouse, Centre National de Recherche Scientifique, Institute National Polytechnique de Toulouse, Université Paul Sabatier, Toulouse, France

    Cecile Ben & Laurent Gentzbittel

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Cai, F., Watson, B.S., Meek, D. et al. Medicago truncatula Oleanolic-Derived Saponins Are Correlated with Caterpillar Deterrence. J Chem Ecol 43, 712–724 (2017). https://doi.org/10.1007/s10886-017-0863-7

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