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Herbivore damage-induced production and specific anti-digestive function of serine and cysteine protease inhibitors in tall goldenrod, Solidago altissima L. (Asteraceae)

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Abstract

Plant protease inhibitors (PIs) are among the most well-studied and widely distributed resistance traits that plants use against their herbivore attackers. There are different types of plant PIs which putatively function against the different types of proteases expressed in insect guts. Serine protease inhibitors (SPIs) and cysteine protease inhibitors (CPIs) are hypothesized to differentially function against the predominant gut proteases in lepidopteran and coleopteran herbivores, respectively. Here, we test the hypothesis that tall goldenrod, Solidago altissima, can specifically respond to damage by different herbivores and differentially induce SPIs and CPIs in response to damage by lepidopteran and coleopteran herbivores. Moreover, we ask if the concerted induction of different types of PIs accounts for variation in induced resistance to herbivory. We altered and optimized a rapid and effective existing methodology to quantitatively analyze both SPI and CPI activity simultaneously from a single tissue sample and to use the same plant extracts directly for characterization of inhibitory effects on insect gut protease activity. We found that both SPIs and CPIs are induced in S. altissima in response to damage, regardless of the damaging herbivore species. However, only SPIs were effective against Spodoptera exigua gut proteases. Our data suggest that plant PI responses are not necessarily specific to the identity of the attacking organism but that different components of generally induced defense traits can specifically affect different herbivore species. While providing an efficient and broadly applicable methodology to analyze multiple PIs extracted from the same tissue, this study furthers our understanding of specificity in induced plant resistance.

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Acknowledgments

We would like to thank Ellen Fagan, Kimberly Morrell, Akane Uesugi, and Justin Porter for assistance with collecting plants and animals. We also thank Robert H. Johnson for introducing us to the intricacies of the Solidago system and advice on how to grow Solidago clones. We thank the editor and three anonymous reviewers for their very constructive comments that significantly improved this paper. We thank the USA National Science Foundation that provided funding for this study through grant awards NSF-IOS 0950225 and NSF-DEB 1010726.

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Correspondence to André Kessler.

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Bode, R.F., Halitschke, R. & Kessler, A. Herbivore damage-induced production and specific anti-digestive function of serine and cysteine protease inhibitors in tall goldenrod, Solidago altissima L. (Asteraceae). Planta 237, 1287–1296 (2013). https://doi.org/10.1007/s00425-013-1845-9

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