Combined biotic stresses trigger similar transcriptomic responses but contrasting resistance against a chewing herbivore in Brassica nigra

Bonnet, Christelle; Lassueur, Steve; Ponzio, Camille; Gols, Rieta; Dicke, Marcel; Reymond, Philippe

doi:10.1186/s12870-017-1074-7

Cited by 66 publications

(94 citation statements)

References 92 publications

(107 reference statements)

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“…However, while the elm transcriptomic response to elm leaf beetle oviposition treatment was transient and very quickly returned to the control level, other plant species maintain differential expression of a high number of egg‐induced genes for several days (Brassicaceae: Bonnet et al., ; Firtzlaff et al., ; Little et al., ; Solanaceae: Geuss, Stelzer, Lortzing, & Steppuhn, ; Kim et al., ).…”

Section: Discussionmentioning

confidence: 99%

“…However, our study indicates that an oviposition‐mediated early boost in changes of expression levels of a small subset of feeding‐induced genes can contribute to a more effective defence against hatching larvae. Similarly, insect larvae performed worse on previously egg extract‐treated black mustard plants ( B. nigra ), in which <100 feeding‐induced genes were differentially expressed when compared to feeding‐induced plants without prior egg extract treatment (Bonnet et al., ). It is currently an open question whether treatment of B. nigra leaves with insect eggs also mediates an earlier and/or faster regulation of feeding‐responsive genes (as detected in elms).…”

Section: Discussionmentioning

confidence: 99%

“…Plants on which insects deposited their eggs showed numerous transcriptional changes in response to this highly reliable herbivore‐indicating cue (Bonnet et al., ; Bruessow, Gouhier‐Darimont, Buchala, Metraux, & Reymond, ; Firtzlaff, Oberländer, Geiselhardt, Hilker, & Kunze, ; Little, Gouhier‐Darimont, Bruessow, & Reymond, ; Reymond, ). Furthermore, plants on which eggs had previously been deposited—such as Arabidopsis, tomato and tobacco plants—showed a stronger induction of defence‐related genes upon damage by feeding larvae (Bandoly, Grichnik, Hilker, & Steppuhn, ; Bandoly, Hilker, & Steppuhn, ; Kim, Tooker, Luthe, De Moraes, & Felton, ; Lortzing et al., ).…”

Section: Introductionmentioning

confidence: 99%

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Transcriptomic basis for reinforcement of elm antiherbivore defence mediated by insect egg deposition

et al. 2018

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Plant responses to insect egg depositions are known to shape subsequent defensive responses to larvae hatching from the eggs. Elm (Ulmus minor) leaves, on which elm leaf beetles laid their eggs, mount a more efficient defence against larvae hatching from the eggs. However, the molecular mechanisms of this egg‐mediated, improved defence are insufficiently understood and have so far only been studied in annual plants. We analysed the dynamics of transcriptomic changes in larval feeding‐damaged elm leaves with and without prior egg deposition using de novo assembled RNA‐seq data. Compared to egg‐free leaves, egg deposition‐treated leaves showed earlier and/or faster transcriptional regulations, as well as slightly enhanced differential transcriptional regulation after the onset of larval feeding. These early responding transcripts were overrepresented in gene ontology terms associated with post‐translational protein modification, signalling and stress (defence) responses. We found evidence of transcriptional memory in initially egg deposition‐induced transcripts whose differential expression was reset prior to larval hatching, but was more rapidly induced again by subsequent larval feeding. This potential memory effect of prior egg deposition, as well as the earlier/faster and enhanced feeding‐induced differential regulation of transcripts in egg deposition‐treated leaves, may contribute to the egg‐mediated reinforcing effect on the elm's defence against larvae. Hence, our study shows that a plant's experience of a stress‐indicating environmental cue (here: insect eggs) can push the dynamics of the plant's transcriptomic response to subsequent stress (here: larval feeding). Such experience‐mediated acceleration of a stress‐induced plant response may result in improved stress resistance.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Transcriptomic basis for reinforcement of elm antiherbivore defence mediated by insect egg deposition

et al. 2018

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“…Caterpillars of P. brassicae are chewing herbivores, which generally induce the JA/ethylene (ET) pathway as well as ABA (Mewis et al, 2005;Koornneef & Pieterse, 2008;Erb et al, 2012;Vos et al, 2013). Xcr can induce the production of JA and SA (Bonnet et al, 2017), and ET mediates resistance against Xcr (Ton et al, 2002). Both insect herbivores, B. brassicae and P. brassicae, are frequently attacked by parasitic wasps.…”

Section: Study Systemmentioning

confidence: 99%

Caterpillars induce jasmonates in flowers and alter plant responses to a second attacker

et al. 2017

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Summary In nature, herbivorous insects and plant pathogens are generally abundant when plants are flowering. Thus, plants face a diversity of attackers during their reproductive phase. Plant responses to one attacker can interfere with responses to a second attacker, and phytohormones that orchestrate plant reproduction are also involved in resistance to insect and pathogen attack. We quantified phytohormonal responses of flowering plants exposed to single or dual attack and studied resistance mechanisms of plants in the flowering stage.Flowering Brassica nigra were exposed to either a chewing caterpillar, a phloem‐feeding aphid or a bacterial pathogen, and plant hormonal responses were compared with dual attack situations. We quantified phytohormones in inflorescences and leaves, and determined the consequences of hormonal changes for components of direct and indirect plant resistance.Caterpillars were the main inducers of jasmonates in inflorescences, and the phytohormonal profile of leaves was not affected by either insect or pathogen attack. Dual attack increased plant resistance to caterpillars, but compromised resistance to aphids. Parasitoid performance was negatively correlated with the performance of their hosts.We conclude that plants prioritize resistance of reproductive tissues over vegetative tissues, and that a chewing herbivore species is the main driver of responses in flowering B. nigra.

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“…Herbivore elicitor regulated 1 is associated with increase of endogenous abscisic acid (ABA) in wild tobacco, Nicotiana attenuata, by impairing catabolism, which suggests that there is crosstalk between the herbivore attack response and the ABA pathway in this plant (Dinh, Baldwin, & Galis, 2013). Although often beneficial, the interactions between multifactor stress responses can be antagonistic and depends on the type of herbivore as well as the plant (Bonnet et al, 2017;Lazebnik, Frago, Dicke, & van Loon, 2014;Suzuki, Rivero, Shulaev, Blumwald, & Mittler, 2014).…”

Section: Introductionmentioning

confidence: 99%

Herbivore exposure alters ion fluxes and improves salt tolerance in a desert shrub

Chen

Cao²,

Guo

et al. 2019

Plant Cell & Environment

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Plants have evolved complex mechanisms that allow them to withstand multiple environmental stresses, including biotic and abiotic stresses. Here, we investigated the interaction between herbivore exposure and salt stress of Ammopiptanthus nanus, a desert shrub. We found that jasmonic acid (JA) was involved in plant responses to both herbivore attack and salt stress, leading to an increased NaCl stress tolerance for herbivore‐pretreated plants and increase in K+/Na+ ratio in roots. Further evidence revealed the mechanism by which herbivore improved plant NaCl tolerance. Herbivore pretreatment reduced K+ efflux and increased Na+ efflux in plants subjected to long‐term, short‐term, or transient NaCl stress. Moreover, herbivore pretreatment promoted H+ efflux by increasing plasma membrane H+‐adenosine triphosphate (ATP)ase activity. This H+ efflux creates a transmembrane proton motive force that drives the Na+/H+ antiporter to expel excess Na+ into the external medium. In addition, high cytosolic Ca2+ was observed in the roots of herbivore‐treated plants exposed to NaCl, and this effect may be regulated by H+‐ATPase. Taken together, herbivore exposure enhances A. nanus tolerance to salt stress by activating the JA‐signalling pathway, increasing plasma membrane H+‐ATPase activity, promoting cytosolic Ca2+ accumulation, and then restricting K+ leakage and reducing Na+ accumulation in the cytosol.

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Combined biotic stresses trigger similar transcriptomic responses but contrasting resistance against a chewing herbivore in Brassica nigra

Cited by 66 publications

References 92 publications

Transcriptomic basis for reinforcement of elm antiherbivore defence mediated by insect egg deposition

Transcriptomic basis for reinforcement of elm antiherbivore defence mediated by insect egg deposition

Caterpillars induce jasmonates in flowers and alter plant responses to a second attacker

Herbivore exposure alters ion fluxes and improves salt tolerance in a desert shrub

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