Priming by Timing: Arabidopsis thaliana Adjusts Its Priming Response to Lepidoptera Eggs to the Time of Larval Hatching

Valsamakis, Georgios; Bittner, Norbert; Fatouros, Nina E.; Kunze, Reinhard; Hilker, Monika; Lortzing, Tobias

doi:10.3389/fpls.2020.619589

Cited by 27 publications

(48 citation statements)

References 105 publications

(117 reference statements)

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“…In this study, ROS accumulation and cell death were induced in all plant species tested, whereas the strong HR-like necrosis and high PR1 expression was specific to B. nigra and to Pierinae insect species. It is possible that also in other species and accessions in the Brassicaceae that we have not investigated closely, a general immune response lacking a strong cell death is activated by Pieris eggs, as was shown for A. thaliana (Col-0) (Gouhier-Darimont et al, 2013, 2019Stahl et al, 2020;Valsamakis et al 2020). Our data suggest that the strong HR-like necrosis is always accompanied by ROS and high PR1 expression.…”

Section: Molecular and Cellular Responses To Insect Eggsmentioning

confidence: 50%

Insect egg‐killing: a new front on the evolutionary arms‐race between brassicaceous plants and pierid butterflies

et al. 2021

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Summary Evolutionary arms‐races between plants and insect herbivores have long been proposed to generate key innovations such as plant toxins and detoxification mechanisms that can drive diversification of the interacting species. A novel front‐line of plant defence is the killing of herbivorous insect eggs. We test whether an egg‐killing plant trait has an evolutionary basis in such a plant–insect arms‐race. Within the crucifer family (Brassicaceae), some species express a hypersensitive response (HR)‐like necrosis underneath butterfly eggs (Pieridae) that leads to eggs desiccating or falling off the plant. We studied the phylogenetic distribution of this trait, its egg‐killing effect on and elicitation by butterflies, by screening 31 Brassicales species, and nine Pieridae species. We show a clade‐specific induction of strong, egg‐killing HR‐like necrosis mainly in species of the Brassiceae tribe including Brassica crops and close relatives. The necrosis is strongly elicited by pierid butterflies that are specialists of crucifers. Furthermore, HR‐like necrosis is linked to PR1 defence gene expression, accumulation of reactive oxygen species and cell death, eventually leading to egg‐killing. Our findings suggest that the plants’ egg‐killing trait is a new front on the evolutionary arms‐race between Brassicaceae and pierid butterflies beyond the well‐studied plant toxins that have evolved against their caterpillars.

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Section: Molecular and Cellular Responses To Insect Eggsmentioning

confidence: 50%

Insect egg‐killing: a new front on the evolutionary arms‐race between brassicaceous plants and pierid butterflies

et al. 2021

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“…Levels of SA were significantly enhanced in previously egg-treated elm leaves after a larval feeding period of 24 h. Similarly, significantly enhanced SA levels were detected in A. thaliana when laden with eggs by the butterfly Pieris brassicae and subsequently damaged by its hatching larvae for 24 h (Lortzing et al 2019 ; Valsamakis et al 2020 ). In contrast, moth egg depositions upon the annual species Nicotiana attenuata and the perennial S. dulcamara did not affect SA levels in subsequently larval feeding-damaged leaves (Drok et al 2018 ).…”

Section: Discussionmentioning

confidence: 94%

“…For instance, higher JA levels were detected in egg-treated tomato plants 30 min and 60 min after wounding (Kim et al 2012 ). In Arabodpsis thaliana , Valsamakis et al ( 2020 ) found enhanced JA-Ile levels in egg-treated leaves after a 3 h larval feeding period when compared to egg-free, feeding-damaged leaves, but not after a 12 h feeding period. Future studies will need to investigate whether previously egg-laden elm leaves show enhanced JA levels very early on after the onset of larval feeding.…”

Section: Discussionmentioning

confidence: 99%

Responses to larval herbivory in the phenylpropanoid pathway of Ulmus minor are boosted by prior insect egg deposition

Schott

Fuchs

Böttcher

et al. 2021

Planta

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Main conclusion Elms, which have received insect eggs as a ‘warning’ of larval herbivory, enhance their anti-herbivore defences by accumulating salicylic acid and amplifying phenylpropanoid-related transcriptional and metabolic responses to hatching larvae. Abstract Plant responses to insect eggs can result in intensified defences against hatching larvae. In annual plants, this egg-mediated effect is known to be associated with changes in leaf phenylpropanoid levels. However, little is known about how trees—long-living, perennial plants—improve their egg-mediated, anti-herbivore defences. The role of phytohormones and the phenylpropanoid pathway in egg-primed anti-herbivore defences of a tree species has until now been left unexplored. Using targeted and untargeted metabolome analyses we studied how the phenylpropanoid pathway of Ulmus minor responds to egg-laying by the elm leaf beetle and subsequent larval feeding. We found that when compared to untreated leaves, kaempferol and quercetin concentrations increased in feeding-damaged leaves with prior egg deposition, but not in feeding-damaged leaves without eggs. PCR analyses revealed that prior insect egg deposition intensified feeding-induced expression of phenylalanine ammonia lyase (PAL), encoding the gateway enzyme of the phenylpropanoid pathway. Salicylic acid (SA) concentrations were higher in egg-treated, feeding-damaged leaves than in egg-free, feeding-damaged leaves, but SA levels did not increase in response to egg deposition alone—in contrast to observations made of Arabidopsis thaliana. Our results indicate that prior egg deposition induces a SA-mediated response in elms to feeding damage. Furthermore, egg deposition boosts phenylpropanoid biosynthesis in subsequently feeding-damaged leaves by enhanced PAL expression, which results in the accumulation of phenylpropanoid derivatives. As such, the elm tree shows similar, yet distinct, responses to insect eggs and larval feeding as the annual model plant A. thaliana.

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“…These responses were shown to be dependent on EDS1, ISOCHORISMATE SYNTHASE 1/SALICYLIC ACID INDUCTION DEFICIENT 2 (ICS1/SID2) and, partially, (NONEXPRESSER OF PR GENES 1) (NPR1), which are known signaling components of plant defense responses against biotrophic pathogens [26]. Transcriptomics studies in different plants species have con rmed that insect oviposition induces genes associated with SA-and ROS-mediated immune responses and PR1 gene expression [15,24,[27][28][29][30][31][32][33], including in B. nigra and B. rapa [21,34,35]. It is suggested that there is a conserved transcriptional response amongst different plant-insect eggs interactions [36].…”

Section: Introductionmentioning

confidence: 99%

Genetic Analysis Reveals Three Novel QTLs Underpinning a Butterfly Egg-Induced Hypersensitive Response-Like Cell Death in Brassica Rapa

Bassetti

Caarls

Bukovinszkine’Kiss

et al. 2021

Preprint

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Background Cabbage white butterflies (Pieris spp.) can be severe pests of Brassica crops such as Chinese cabbage, Pak choi (Brassica rapa) or cabbages (B. oleracea). Eggs of Pieris spp. can induce a hypersensitive response-like (HR-like) cell death which reduces egg survival in the wild black mustard (B. nigra). Unravelling the genetic basis of this egg-killing trait in Brassica crops could improve crop resistance to herbivory, reducing major crop losses and pesticides use. Here we investigated the genetic architecture of a HR-like cell death induced by P. brassicae eggs in B. rapa. Results A germplasm screening of B. rapa 56 accessions, representing the genetic and geographical diversity of a B. rapa core collection, showed phenotypic variation for cell death. An image-based phenotyping protocol was developed to accurately measure size of HR-like cell death and was then used to identify two accessions that consistently showed weak (R-o-18) or strong cell death response (L58). Screening of 160 RILs derived from these two accessions resulted in three novel QTLs for Pieris brassicae-induced cell death on chromosomes A02 (Pbc1), A03 (Pbc2), and A06 (Pbc3). The three QTLs Pbc1-3 contain cell surface receptors, intracellular receptors and other genes involved in plant immunity processes, such as ROS accumulation and cell death formation. Synteny analysis with A. thaliana suggested that Pbc1 and Pbc2 are novel QTLs associated with this trait, while Pbc3 contains also LecRK-I.1, a gene of A. thaliana previously associated with cell death induced by a P. brassicae egg extract. Conclusions This study provides the first genomic regions associated with the Pieris egg-induced HR-like cell death in a Brassica crop species. It is a step closer towards unravelling the genetic basis of an egg-killing crop resistance trait, paving the way for breeders to further fine-map and validate candidate genes.

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Priming by Timing: Arabidopsis thaliana Adjusts Its Priming Response to Lepidoptera Eggs to the Time of Larval Hatching

Cited by 27 publications

References 105 publications

Insect egg‐killing: a new front on the evolutionary arms‐race between brassicaceous plants and pierid butterflies

Insect egg‐killing: a new front on the evolutionary arms‐race between brassicaceous plants and pierid butterflies

Responses to larval herbivory in the phenylpropanoid pathway of Ulmus minor are boosted by prior insect egg deposition

Genetic Analysis Reveals Three Novel QTLs Underpinning a Butterfly Egg-Induced Hypersensitive Response-Like Cell Death in Brassica Rapa

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