Specialist Aphid Feeding Causes Local Activation of Salicylic and Jasmonic Acid Signaling in <i>Arabidopsis</i> Veins

Rubil, Nikoleta; Kalachova, Tetiana; Hauser, Thure P.; Burketová, Lenka

doi:10.1094/mpmi-08-21-0203-sc

Cited by 10 publications

(10 citation statements)

References 18 publications

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“…Phytohormones play an important role in regulating plant-potyvirus and plant-insect interactions. For example, jasmonic acid (JA), salicylic acid (SA), and ethylene (ET) mediate plant defense responses to many phloem feeding insects such as aphids, the primary insect vector for potyviruses [15][16][17]. The JA signaling pathway is required for the induction of protease inhibitors, a protein that has been shown to reduce aphid performance on host plants [18,19].…”

Section: Introductionmentioning

confidence: 99%

“…Moreover, inhibiting the production of the phytohormones abscisic acid and ET was found to be a boon for potyvirus infection [20,21]. The potyviral protein NIaPro was found to alter ET levels and ET-related responses, and the potyviral protein HC-Pro was shown to alter SA levels [4,17,18]. The role of other potyviral proteins in regulating phytohormones and related defenses is not well understood.…”

Section: Introductionmentioning

confidence: 99%

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The Potyviral Protein 6K1 Reduces Plant Proteases Activity during Turnip mosaic virus Infection

Bera

Arena

Ray

et al. 2022

Viruses

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Potyviral genomes encode just 11 major proteins and multifunctionality is associated with most of these proteins at different stages of the virus infection cycle. Some potyviral proteins modulate phytohormones and protein degradation pathways and have either pro- or anti-viral/insect vector functions. Our previous work demonstrated that the potyviral protein 6K1 has an antagonistic effect on vectors when expressed transiently in host plants, suggesting plant defenses are regulated. However, to our knowledge the mechanisms of how 6K1 alters plant defenses and how 6K1 functions are regulated are still limited. Here we show that the 6K1 from Turnip mosaic virus (TuMV) reduces the abundance of transcripts related to jasmonic acid biosynthesis and cysteine protease inhibitors when expressed in Nicotiana benthamiana relative to controls. 6K1 stability increased when cysteine protease activity was inhibited chemically, showing a mechanism to the rapid turnover of 6K1 when expressed in trans. Using RNAseq, qRT-PCR, and enzymatic assays, we demonstrate TuMV reprograms plant protein degradation pathways on the transcriptional level and increases 6K1 stability at later stages in the infection process. Moreover, we show 6K1 decreases plant protease activity in infected plants and increases TuMV accumulation in systemic leaves compared to controls. These results suggest 6K1 has a pro-viral function in addition to the anti-insect vector function we observed previously. Although the host targets of 6K1 and the impacts of 6K1-induced changes in protease activity on insect vectors are still unknown, this study enhances our understanding of the complex interactions occurring between plants, potyviruses, and vectors.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The Potyviral Protein 6K1 Reduces Plant Proteases Activity during Turnip mosaic virus Infection

Bera

Arena

Ray

et al. 2022

Viruses

View full text Add to dashboard Cite

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“…In Arabidopsis , co‐application of SA and JA at low concentrations resulted in transient synergism (Mur et al ., 2006). Aphid feeding on Arabidopsis also resulted in the concomitant induction of SA and JA biosynthetic genes and the upregulation of defence‐related marker genes around feeding sites (Rubil et al ., 2022). Also, in Arabidopsis , SA was shown to activate the JA signalling pathway through the NPR3 and NPR4 receptors as a component of effector‐triggered immunity (Liu et al ., 2016).…”

Section: Discussionmentioning

confidence: 99%

Lack of antagonism between salicylic acid and jasmonate signalling pathways in poplar

et al. 2022

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Summary Salicylic acid (SA) and jasmonic acid (JA) often play distinct roles in plant defence against pathogens. Research from Arabidopsis thaliana has established that SA‐ and JA‐mediated defences are more effective against biotrophs and necrotrophs, respectively. These two hormones often interact antagonistically in response to particular attackers, with the induction of one leading to suppression of the other. Here, we report a contrasting pattern in the woody perennial Populus: positive SA–JA interplay. Using genetically engineered high SA lines of black poplar and wild‐type lines after exogenous hormone application, we quantified SA and JA metabolites, signalling gene transcripts, antifungal flavonoids and resistance to rust (Melampsora larici‐populina). Salicylic acid and JA metabolites were induced concurrently upon rust infection in poplar genotypes with varying resistance levels. Analysis of SA‐hyperaccumulating transgenic poplar lines showed increased jasmonate levels, elevated flavonoid content and enhanced rust resistance, but no discernible reduction in growth. Exogenous application of either SA or JA triggered the accumulation of the other hormone. Expression of pathogenesis‐related (PR) genes, frequently used as markers for SA signalling, was not correlated with SA content, but rather activated in proportion to pathogen infection. We conclude that SA and JA pathways interact positively in poplar resulting in the accumulation of flavonoid phytoalexins.

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“…A controlled ROS burst has been considered the primary plant defence responses mechanism against herbivores [ 90 ]. A quick activation of plant defence signals in the cells surrounding the stylet wound by an aphid in Arabidopsis thaliana was followed by an induction spread along the veins to the whole leaf [ 91 ]. In the neighbouring area to the feeding zone, 90 min after feeding, the photoprotective mechanism Φ NPQ increased more than in the rest of the leaf area to compensate for the higher decrease of Φ PSII in the same zone.…”

Section: Discussionmentioning

confidence: 99%

“…As it has been previously suggested, it can distinguish leaf photosynthetic spatiotemporal heterogeneity that cannot be identified through conventional chlorophyll fluorescence analysis, and it can be used to explore plant response mechanisms to biotic or abiotic stresses [ 50 , 80 , 99 , 100 , 101 , 102 , 103 ]. Plant-insect interactions are getting more defined and comprehensive with the development of novel visualization methods that permit leaf photosynthetic efficiency evaluation after herbivore attack [ 4 , 91 ].…”

Section: Discussionmentioning

confidence: 99%

Reactive Oxygen Species Initiate Defence Responses of Potato Photosystem II to Sap-Sucking Insect Feeding

Sperdouli

Andreadis

Adamakis

et al. 2022

Insects

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Potato, Solanum tuberosum L., one of the most commonly cultivated horticultural crops throughout the world, is susceptible to a variety of herbivory insects. In the present study, we evaluated the consequence of feeding by the sap-sucking insect Halyomorpha halys on potato leaf photosynthetic efficiency. By using chlorophyll fluorescence imaging methodology, we examined photosystem II (PSII) photochemistry in terms of feeding and at the whole leaf area. The role of reactive oxygen species (ROS) in potato’s defence response mechanism immediately after feeding was also assessed. Even 3 min after feeding, increased ROS generation was observed to diffuse through the leaf central vein, probably to act as a long-distance signalling molecule. The proportion of absorbed energy being used in photochemistry (ΦPSII) at the whole leaf level, after 20 min of feeding, was reduced by 8% compared to before feeding due to the decreased number of open PSII reaction centres (qp). After 90 min of feeding, ΦPSII decreased by 46% at the whole leaf level. Meanwhile, at the feeding zones, which were located mainly in the proximity of the leaf midrib, ΦPSII was lower than 85%, with a concurrent increase in singlet-excited oxygen (1O2) generation, which is considered to be harmful. However, the photoprotective mechanism (ΦNPQ), which was highly induced 90 min after feeding, was efficient to compensate for the decrease in the quantum yield of PSII photochemistry (ΦPSII). Therefore, the quantum yield of non-regulated energy loss in PSII (ΦNO), which represents 1O2 generation, remained unaffected at the whole leaf level. We suggest that the potato PSII response to sap-sucking insect feeding underlies the ROS-dependent signalling that occurs immediately and initiates a photoprotective PSII defence response to reduce herbivory damage. A controlled ROS burst can be considered the primary plant defence response mechanism to herbivores.

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Specialist Aphid Feeding Causes Local Activation of Salicylic and Jasmonic Acid Signaling in Arabidopsis Veins

Cited by 10 publications

References 18 publications

The Potyviral Protein 6K1 Reduces Plant Proteases Activity during Turnip mosaic virus Infection

The Potyviral Protein 6K1 Reduces Plant Proteases Activity during Turnip mosaic virus Infection

Lack of antagonism between salicylic acid and jasmonate signalling pathways in poplar

Reactive Oxygen Species Initiate Defence Responses of Potato Photosystem II to Sap-Sucking Insect Feeding

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