Plant genetic relatedness and volatile-mediated signalling between Solanum tuberosum plants in response to herbivory by Spodoptera exigua

Martín-Cacheda, Lucía; Vázquez‐González, Carla; Rasmann, Sergio; Röder, Grégory; Abdala‐Roberts, Luis; Moreira, Xoaquín

doi:10.1016/j.phytochem.2022.113561

Cited by 3 publications

(4 citation statements)

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“…Consistent with emitter VOC results, receiver plants exposed to herbivore-damaged emitters were more resistant to herbivory given by a significantly lower percentage of leaf removed by S. exigua compared to receivers exposed to undamaged emitters. Similar results have been reported for other crop and non-crop species including maize, cabbage, and Scots pine (Ton et al 2007 ; Peng et al 2011 ; Karban et al 2014 ; Ninkovic et al 2021 ; Yu et al 2022 ), as well as our recent work with potato and S. exigua (Vázquez-González et al 2022 ; Martín-Cacheda et al 2023 ). Interestingly, in some of these prior studies we found no evidence of signalling effects between potato plants in response to herbivory by the specialist beetle Leptinotarsa decemlineata (Abdala-Roberts et al 2022 ) or to infection by the generalist pathogenic fungus Sclerotinia sclerotiorum (Moreira et al 2021 ).…”

Section: Discussionsupporting

confidence: 86%

“…Emitter plants subjected to S. exigua leaf damage exhibited a 2.5-fold increase in total VOCs released as well as significant VOC compositional changes relative to undamaged emitters, corroborating recent results from another study also using this insect to induce potato seedlings (Vázquez-González et al 2022 ). Further analyses by individual compounds showed that damaged emitters released higher concentrations of compounds including the homoterpene nonatriene and sesquiterpenes β- elemene, ( E )-β-farnesene, and β-bisabolene, all of which were also significantly induced by S. exigua herbivory in previous studies with potato (Vázquez-González et al 2022 ; Martín-Cacheda et al 2023 ). In particular, β-bisabolene, nonatriene, and ( E )-β-farnesene are known or suspected to be toxic or repellent compounds against phytophagous insects, as well as mediate plant-plant signalling (reviewed by Rosenkranz et al 2021 ).…”

Section: Discussionmentioning

confidence: 70%

“…One of the most economically important pests on this crop is the beet armyworm ( Spodoptera exigua (Hubner), Lepidoptera: Noctuidae), a generalist insect that feeds on leaves and tubers causing significant reductions in plant growth and yield (Brown and Dewhurst 1975 ). Importantly, previous work by our group has shown that leaf damage by S. exigua significantly increases total VOC emission as well as leads to compositional changes in VOC blends in young potato plants (Vázquez-González et al 2022 ; Martín-Cacheda et al 2023 ). In turn, these herbivore-induced changes in VOC emissions trigger plant-plant signalling which results in heightened resistance to herbivory in neighbouring undamaged plants (Vázquez-González et al 2022 ; Martín-Cacheda et al 2023 ).…”

Section: Methodsmentioning

confidence: 85%

“…Importantly, previous work by our group has shown that leaf damage by S. exigua significantly increases total VOC emission as well as leads to compositional changes in VOC blends in young potato plants (Vázquez-González et al 2022 ; Martín-Cacheda et al 2023 ). In turn, these herbivore-induced changes in VOC emissions trigger plant-plant signalling which results in heightened resistance to herbivory in neighbouring undamaged plants (Vázquez-González et al 2022 ; Martín-Cacheda et al 2023 ).…”

Section: Methodsmentioning

confidence: 85%

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Volatile-Mediated Signalling Between Potato Plants in Response to Insect Herbivory is not Contingent on Soil Nutrients

et al. 2023

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Plant-plant signalling via volatile organic compounds (VOCs) has been studied intensively, but its contingency on abiotic conditions (e.g., soil nutrients, drought, warming) is poorly understood. To address this gap, we carried out a greenhouse experiment testing whether soil nutrients influenced signalling between potato (Solanum tuberosum) plants in response to insect leaf herbivory by the generalist caterpillar Spodoptera exigua. We placed pairs of plants in plastic cages, where one plant acted as a VOC emitter and the other as a receiver. We factorially manipulated soil nutrients for both emitter and receiver plants, namely: unfertilized (baseline soil nutrients) vs. fertilized (augmented nutrients). Then, to test for signalling effects, half of the emitters within each fertilization level were damaged by S. exigua larvae and the other half remained undamaged. Three days after placing larvae, we collected VOCs from emitter plants to test for herbivory and fertilization effects on VOC emissions and placed S. exigua larvae on receivers to test for signalling effects on leaf consumption and larval mass gain as proxies of induced resistance. We found that herbivory increased total VOC emissions and altered VOC composition by emitter plants, but these effects were not contingent on fertilization. In addition, bioassay results showed that receivers exposed to VOCs from herbivore-damaged emitters had lower levels of herbivory compared to receivers exposed to undamaged emitters. However, and consistent with VOC results, fertilization did not influence herbivore-induced signalling effects on receiver resistance to herbivory. In sum, we found evidence of S. exigua-induced signalling effects on resistance to herbivory in potato plants but such effects were not affected by increased soil nutrients. These results call for further work testing signalling effects under broader range of nutrient concentration levels (including nutrient limitation), teasing apart the effects of specific nutrients, and incorporating other abiotic factors likely to interact or covary with soil nutrients.

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Section: Discussionsupporting

confidence: 86%

Section: Discussionmentioning

confidence: 70%

Section: Methodsmentioning

confidence: 85%

Section: Methodsmentioning

confidence: 85%

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Volatile-Mediated Signalling Between Potato Plants in Response to Insect Herbivory is not Contingent on Soil Nutrients

et al. 2023

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Testing the joint effects of arbuscular mycorrhizal fungi and ants on insect herbivory on potato plants

Moreira,

Martín-Cacheda,

Quiroga

et al. 2024

Planta

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Main conclusion Ants, but not mycorrhizae, significantly affected insect leaf-chewing herbivory on potato plants. However, there was no evidence of mutualistic interactive effects on herbivory. Abstract Plants associate with both aboveground and belowground mutualists, two prominent examples being ants and arbuscular mycorrhizal fungi (AMF), respectively. While both of these mutualisms have been extensively studied, joint manipulations testing their independent and interactive (non-additive) effects on plants are rare. To address this gap, we conducted a joint test of ant and AMF effects on herbivory by leaf-chewing insects attacking potato (Solanum tuberosum) plants, and further measured plant traits likely mediating mutualist effects on herbivory. In a field experiment, we factorially manipulated the presence of AMF (two levels: control and mycorrhization) and ants (two levels: exclusion and presence) and quantified the concentration of leaf phenolic compounds acting as direct defenses, as well as plant volatile organic compound (VOC) emissions potentially mediating direct (e.g., herbivore repellents) or indirect (e.g., ant attractants) defense. Moreover, we measured ant abundance and performed a dual-choice greenhouse experiment testing for effects of VOC blends (mimicking those emitted by control vs. AMF-inoculated plants) on ant attraction as a mechanism for indirect defense. Ant presence significantly reduced herbivory whereas mycorrhization had no detectable influence on herbivory and mutualist effects operated independently. Plant trait measurements indicated that mycorrhization had no effect on leaf phenolics but significantly increased VOC emissions. However, mycorrhization did not affect ant abundance and there was no evidence of AMF effects on herbivory operating via ant-mediated defense. Consistently, the dual-choice assay showed no effect of AMF-induced volatile blends on ant attraction. Together, these results suggest that herbivory on potato plants responds mainly to top-down (ant-mediated) rather than bottom-up (AMF-mediated) control, an asymmetry in effects which could have precluded mutualist non-additive effects on herbivory. Further research on this, as well as other plant systems, is needed to examine the ecological contexts under which mutualist interactive effects are more or less likely to emerge and their impacts on plant fitness and associated communities.

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Test of Specificity in Signalling between Potato Plants in Response to Infection by Fusarium Solani and Phytophthora Infestans

Martín-Cacheda,

Röder,

Abdala-Roberts

et al. 2024

J Chem Ecol

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Plant-plant signalling via volatile organic compounds (VOCs) in response to insect herbivory has been widely studied, but its occurrence and specificity in response to pathogen attack has received much less attention. To fill this gap, we carried out a greenhouse experiment using two fungal pathogens (Fusarium solani and Phytophthora infestans) to test for specificity in VOC induction and signalling between potato plants (Solanum tuberosum). We paired potato plants in plastic cages, one acting as VOC emitter and the other as receiver, and subjected emitters to one of the following treatments: no infection (control), infected by F. solani, or infected by P. infestans. We measured total emission and composition of VOCs released by emitter plants to test for pathogen-specificity in VOC induction, and then conducted a pathogen infection bioassay to assess resistance levels on receiver plants by subjecting half of the receivers of each emitter treatment to F. solani infection and the other half to P. infestans infection. This allowed us to test for specificity in plant VOC signalling by comparing its effects on conspecific and heterospecific sequential infections. Results showed that infection by neither F. solani or P. infestans produced quantitative (total emissions) or qualitative (compositional) changes in VOC emissions. Mirroring these patterns, emitter infection treatment (control vs. pathogen infection) did not produce a significant change in pathogen infection levels on receiver plants in any case (i.e., either for conspecific or heterospecific sequential infections), indicating a lack of signalling effects which precluded pathogen-based specificity in signalling. We discuss possible mechanisms for lack of pathogen effects on VOC emissions and call for future work testing for pathogen specificity in plant-plant signalling and its implications for plant-pathogen interactions under ecologically relevant scenarios involving infections by multiple pathogens.

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Plant genetic relatedness and volatile-mediated signalling between Solanum tuberosum plants in response to herbivory by Spodoptera exigua

Cited by 3 publications

References 42 publications

Volatile-Mediated Signalling Between Potato Plants in Response to Insect Herbivory is not Contingent on Soil Nutrients

Volatile-Mediated Signalling Between Potato Plants in Response to Insect Herbivory is not Contingent on Soil Nutrients

Testing the joint effects of arbuscular mycorrhizal fungi and ants on insect herbivory on potato plants

Test of Specificity in Signalling between Potato Plants in Response to Infection by Fusarium Solani and Phytophthora Infestans

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