Cited by 151Insect-Plant Interactions and ControlPlant-Microbe Interactions and ImmunityPlant biochemistry and biosynthesis

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Nicotiana attenuata LECTIN RECEPTOR KINASE1 Suppresses the Insect-Mediated Inhibition of Induced Defense Responses during Manduca sexta Herbivory

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Abstract

Nicotiana attenuata has the capacity to respond specifically to herbivory by its natural herbivore, Manduca sexta, through the perception of elicitors in larval oral secretions. We demonstrate that Lectin receptor kinase 1 (LecRK1) functions during M. sexta herbivory to suppress the insect-mediated inhibition of jasmonic acid (JA)–induced defense responses. Gene function analysis performed by reducing LecRK1 expression in N. attenuata by both virus-induced gene silencing and inverted repeated RNA interference (ir-lecRK1 plants) revealed that LecRK1 was essential to mount a full defense response against M. sexta folivory; larvae growing on ir-lecRK1 plants were 40 to 100% larger than those growing on wild-type plants. The insect-induced accumulation of nicotine, diterpene-glucosides, and trypsin protease inhibitors, as well as the expression of Thr deaminase, was severalfold reduced in ir-lecRK1 plants compared with the wild type. The accumulation of JA and JA-Ile was unaffected during herbivory in ir-lecRK1 plants; however, salicylic acid (SA) accumulation was increased by twofold. The expression of nahG in ir-lecRK1 plants prevented the increased accumulation of SA and restored the defense response against M. sexta herbivory. The results suggest that LecRK1 inhibits the accumulation of SA during herbivory, although other mechanisms may also be affected.

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  • Defense investment is typically titrated through feedback regulation, including positive and negative feedback loops built into early defense signaling and hormonal networks.

    “Defense investment is typically titrated through feedback regulation, including both positive and negative feedback loops that are built into early defense signaling (Hu et al., 2015;Li et al., 2015) and hormonal networks (Gilardoni et al., 2011;Liu et al., 2019).”

    From Plant Secondary Metabolites as Defenses, Regulators, and Primary Metabolites: The Blurred Functional Trichotomy (2020) · cites this paper as Gilardoni et al., 2011

    The Introduction (page unavailable) says JA-induced defenses are modulated positively or negatively by SA and ET. The section ‘The Induction of LecRK1 Expression Is Tightly Regulated by OS/FACs and JAs’ (page unavailable) describes JA checking LecRK1 induction, which in turn tunes SA accumulation. These passages support regulation of defense through hormonal signaling, but do not establish that both positive and negative feedback loops are typically built into hormonal networks. (LLM, conf=0.83)

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Metadata

Authors
Gilardoni, P. A., Hettenhausen, C., Baldwin, I. T., & Bonaventure, G.
Affiliations
  • Max Planck Institute for Chemical Ecology (DE)
  • Max Planck Society (DE)
Venue
The Plant Cell
Published
2011-09-01
Volume
23
Issue
9
Pages
3512-3532
ISSN
  • 1040-4651 (ISSN-L)
  • 1532-298X
OpenAlex
W2103293074
Cited by
151
References
0
Citations by year
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FWCI
12.58
Type
journal article
Language
en
Open access
Locations
  • The Plant Cell (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Max Planck Digital Library (submittedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
Funders
  • Deutsche Forschungsgemeinschaft
  • Max-Planck-Gesellschaft
Topics
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant biochemistry and biosynthesis
Keywords
Nicotiana attenuata, Manduca sexta, lectin receptor kinase, herbivory-induced defense, jasmonic acid, salicylic acid, nicotine accumulation, diterpene glucosides, salicylate hydroxylase, plant-insect interactions, folivory
MeSH terms
Animals, Cloning, Molecular, Cyclopentanes, Molecular Sequence Data, Plant Proteins, Nicotiana, Protein Serine-Threonine Kinases, Sequence Analysis, DNA, Manduca, Gene Expression Regulation, Plant, DNA, Plant, Salicylic Acid, Gene Silencing, Oxylipins, Metabolome, Herbivory

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