Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut.
The plant hormone jasmonic acid (JA) activates host defense responses against a broad spectrum of herbivores. Although it is well established that JA controls the expression of a large set of target genes in response to tissue damage, very few gene products have been shown to play a direct role in reducing herbivore performance. To test the hypothesis that JA-inducible proteins (JIPs) thwart attack by disrupting digestive processes in the insect gut, we used a MS-based approach to identify host proteins that accumulate in the midgut of Manduca sexta larvae reared on tomato (Solanum lycopersicum) plants. We show that two JIPs, arginase and threonine deaminase (TD), act in the M. sexta midgut to catabolize the essential amino acids Arg and Thr, respectively. Transgenic plants that overexpress arginase were more resistant to M. sexta larvae, and this effect was correlated with reduced levels of midgut Arg. We present evidence indicating that the ability of TD to degrade Thr in the midgut is enhanced by herbivore-induced proteolytic removal of the enzyme's C-terminal regulatory domain, which confers negative feedback regulation by isoleucine in planta. Our results demonstrate that the JA signaling pathway strongly influences the midgut protein content of phytophagous insects and support the hypothesis that catabolism of amino acids in the insect digestive tract by host enzymes plays a role in plant protection against herbivores.
Chen
Hui
H
Department of Energy Plant Research Laboratory, Michigan Proteome Consortium, Michigan State University, East Lansing, MI 48824, USA.
Wilkerson
Curtis G
CG
Kuchar
Jason A
JA
Phinney
Brett S
BS
Howe
Gregg A
GA
D000595:Amino Acid Sequence; D000596:Amino Acids / Q000378:metabolism; D000601:Amino Acids, Essential / Q000737:chemistry*; D000641:Ammonia / Q000378:metabolism; D000818:Animals; D002853:Chromatography, Liquid; D003517:Cyclopentanes / Q000494:pharmacology*; D025461:Feedback, Physiological; D005583:Fourier Analysis; D018506:Gene Expression Regulation, Plant; D005838:Genotype; D007113:Immunity, Innate; D007313:Insecta; D007532:Isoleucine / Q000737:chemistry; D018551:Solanum lycopersicum / Q000378:metabolism / Q000469:parasitology; D018402:Manduca; D013058:Mass Spectrometry; D008969:Molecular Sequence Data; D054883:Oxylipins; D010455:Peptides / Q000737:chemistry; D010935:Plant Diseases; D030821:Plants, Genetically Modified; D017434:Protein Structure, Tertiary; D040901:Proteomics / Q000379:methods; D015398:Signal Transduction
D000596:Amino Acids; D000601:Amino Acids, Essential; D003517:Cyclopentanes; D054883:Oxylipins; D010455:Peptides; D007532:Isoleucine; C011006:jasmonic acid; D000641:Ammonia