Insect eggs trigger systemic acquired resistance against a fungal and an oomycete pathogen

Alfonso, Esteban; Stahl, Elia; Glauser, Gaëtan; Bellani, Etienne; Raaymakers, Tom M.; Ackerveken, Guido Van den; Zeier, Jürgen; Reymond, Philippe

doi:10.1111/nph.17732

Cited by 11 publications

(12 citation statements)

References 99 publications

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“…Activation of indole metabolism in Arabidopsis is not limited to herbivore-infested plants. For instance, accumulation of IGLs and other indolics was reported in response to various abiotic and biotic stressors such as ROS, PAMPs, microbial pathogens and insect egg recognition ( Sewelam et al, 2014 ; Frerigmann, 2016 ; Frerigmann et al, 2016 ; Stahl et al, 2016 ; Alfonso et al, 2021 ). Genes coding for several PROSCOOPs are induced in response to Botrytis cinerea and Pseudomonas syringae in Arabidopsis and it will be therefore an interesting aspect for further investigations to study if and how SCOOP peptides contribute to the synthesis of IGLs and other indolics in these conditions ( Gully et al, 2019 ).…”

Section: Discussionmentioning

confidence: 99%

The MIK2/SCOOP Signaling System Contributes to Arabidopsis Resistance Against Herbivory by Modulating Jasmonate and Indole Glucosinolate Biosynthesis

Stahl

Martin²,

Glauser³

et al. 2022

Front. Plant Sci.

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Initiation of plant immune signaling requires recognition of conserved molecular patterns from microbes and herbivores by plasma membrane-localized pattern recognition receptors. Additionally, plants produce and secrete numerous small peptide hormones, termed phytocytokines, which act as secondary danger signals to modulate immunity. In Arabidopsis, the Brassicae-specific SERINE RICH ENDOGENOUS PEPTIDE (SCOOP) family consists of 14 members that are perceived by the leucine-rich repeat receptor kinase MALE DISCOVERER 1-INTERACTING RECEPTOR LIKE KINASE 2 (MIK2). Recognition of SCOOP peptides elicits generic early signaling responses but knowledge on how and if SCOOPs modulate specific downstream immune defenses is limited. We report here that depletion of MIK2 or the single PROSCOOP12 precursor results in decreased Arabidopsis resistance against the generalist herbivore Spodoptera littoralis but not the specialist Pieris brassicae. Increased performance of S. littoralis on mik2-1 and proscoop12 is accompanied by a diminished accumulation of jasmonic acid, jasmonate-isoleucine and indolic glucosinolates. Additionally, we show transcriptional activation of the PROSCOOP gene family in response to insect herbivory. Our data therefore indicate that perception of endogenous SCOOP peptides by MIK2 modulates the jasmonate pathway and thereby contributes to enhanced defense against a generalist herbivore.

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Section: Discussionmentioning

confidence: 99%

The MIK2/SCOOP Signaling System Contributes to Arabidopsis Resistance Against Herbivory by Modulating Jasmonate and Indole Glucosinolate Biosynthesis

Stahl

Martin²,

Glauser³

et al. 2022

Front. Plant Sci.

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“…Although HR-like necrosis is a local phenomenon that is limited to the site of egg deposition, the activation of other immune responses is not limited to the perception site. Accumulation of SA, Pip, specific indoles, and PR1 transcript levels were also measured in leaves distal to the site of initial egg recognition [ 12 , 18 ], indicating an activation of systemic immunity upon local egg perception. In addition to direct immune responses, plants also employ indirect defense responses against insect eggs.…”

Section: Perception Of Insect Eggsmentioning

confidence: 99%

Insect egg-induced innate immunity: Who benefits?

2023

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Plants perceive the presence of insect eggs deposited on leaves as a cue of imminent herbivore attack. Consequential plant signaling events include the accumulation of salicylic acid and reactive oxygen species, transcriptional reprogramming, and cell death. Interestingly, egg-induced innate immunity shows similarities with immune responses triggered upon recognition of microbial pathogens, and in recent years, it became apparent that egg perception affects plant–microbe interactions. Here, we highlight recent findings on insect egg-induced innate immunity and how egg-mediated signaling impacts plant–microbe interactions. Ecological considerations beg the question: Who benefits from egg perception in these complex interactions?

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“…Systemic signalling in response to P. brassicae eggs has been reported for Arabidopsis from local to distal leaves ( Hilfiker et al , 2014 ; Alfonso et al , 2021 ), and systemic changes in flowers have been reported in response to leaf herbivory by P. brassicae on flowering B. nigra plants in the form of an emission of floral odour ( Bruinsma et al , 2014 ). However, our results show that Arabidopsis flowers were not primed by egg deposition on the leaves; in fact, the performance of larvae feeding on the flowers of plants that had experienced eggs on their leaves was unaffected ( Fig.…”

Section: Discussionmentioning

confidence: 99%

Priming of Arabidopsis resistance to herbivory by insect egg deposition depends on the plant’s developmental stage

Valsamakis

Bittner

Kunze

et al. 2022

Journal of Experimental Botany

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While traits of plant resistance to herbivory often change during ontogeny, it is unknown whether the primability of this resistance depends on the plant’s developmental stage. Resistance in non-flowering Arabidopsis thaliana against Pieris brassicae larvae is known to be primable by prior egg deposition on leaves. We investigated whether this priming effect is maintained in plants in the flowering stage. Larval performance assays revealed that flowering plants’ resistance to herbivory was not primable by egg deposition. Accordingly, transcriptomes of flowering plants showed almost no response to eggs. In contrast, egg deposition on non-flowering plants enhanced the expression of genes induced by subsequent larval feeding. Strikingly, flowering plants showed constitutively high expression levels of these genes. Larvae performed generally worse on flowering than on non-flowering plants, indicating that flowering plants constitutively resist herbivory. Furthermore, we determined the seed weight in regrown plants that had been exposed to eggs and larvae during the non-flowering or flowering stage. The non-flowering plants benefitted from egg-priming with a smaller loss in seed yield. The seed yield of flowering plants was unaffected by the treatments, indicating tolerance towards the larvae. Our results show that the primability of Arabidopsis’ anti-herbivore defences depends on the plant’s developmental stage.

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Insect eggs trigger systemic acquired resistance against a fungal and an oomycete pathogen

Cited by 11 publications

References 99 publications

The MIK2/SCOOP Signaling System Contributes to Arabidopsis Resistance Against Herbivory by Modulating Jasmonate and Indole Glucosinolate Biosynthesis

The MIK2/SCOOP Signaling System Contributes to Arabidopsis Resistance Against Herbivory by Modulating Jasmonate and Indole Glucosinolate Biosynthesis

Insect egg-induced innate immunity: Who benefits?

Priming of Arabidopsis resistance to herbivory by insect egg deposition depends on the plant’s developmental stage

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