Plant Viruses Induce Plant Volatiles That Are Detected by Aphid Parasitoids

Overview

Journal Sci Rep

Specialty Science

Date 2023 May 30

PMID 37253808

Authors

Panagiotis G Milonas

Eirini Anastasaki

Aikaterini Psoma

Georgios Partsinevelos

Georgios N Fragkopoulos

Oxana Kektsidou

Nikon Vassilakos

Apostolos Kapranas

Affiliations

Soon will be listed here.

Abstract

Aphis gossypii (Sternorrhyncha: Aphididae) aphids are vectors of important plant viruses among which cucumber mosaic virus (CMV) and potato virus Y (PVY). Virus-infected plants attract aphid vectors and affect their behavior and growth performance either positively or negatively depending on mode of transmission. Viruses cause changes in the composition and the amount of volatile organic compounds (VOCs) released by the plant that attract aphids. The aphid parasitoid Aphidius colemani (Hymenoptera: Aphelinidae) has been shown to have higher parasitism and survival rates on aphids fed on virus-infected than aphids fed on non-infected plants. We hypothesized that parasitoids distinguish virus-infected plants and are attracted to them regardless of the presence of their aphid hosts. Herein, we examined the attraction of the A. colemani parasitoid to infected pepper plants with each of CMV or PVY without the presence of aphids. The dynamic headspace technique was used to collect VOCs from non-infected and CMV or PVY-infected pepper plants. Identification was performed with gas chromatography-mass spectrometry (GC-MS). The response of the parasitoids on virus-infected vs non-infected pepper plants was tested by Y-tube olfactometer assays. The results revealed that parasitoids displayed a preference to CMV and PVY infected plants compared to those that were not infected.

Citing Articles

Enhancing aphid resistance in horticultural crops: a breeding prospective.

Zhang L, Chen C, Li Y, Suo C, Zhou W, Liu X Hortic Res. 2024; 11(12):uhae275.

PMID: 39712868 PMC: 11659385. DOI: 10.1093/hr/uhae275.

Multitrophic and Multilevel Interactions Mediated by Volatile Organic Compounds.

Niu D, Xu L, Lin K Insects. 2024; 15(8).

PMID: 39194777 PMC: 11354320. DOI: 10.3390/insects15080572.

Behavior Changes Depending on Volatile Organic Compounds Emitted by Plants Infected with Viruses with Different Modes of Transmission.

Clemente-Orta G, Cabello A, Garzo E, Moreno A, Fereres A Insects. 2024; 15(2).

PMID: 38392512 PMC: 10889700. DOI: 10.3390/insects15020092.

References

Anastasaki E, Drizou F, Milonas P . Electrophysiological and Oviposition Responses of Tuta absoluta Females to Herbivore-Induced Volatiles in Tomato Plants. J Chem Ecol. 2018; 44(3):288-298. DOI: 10.1007/s10886-018-0929-1. View

War A, Sharma H, Paulraj M, War M, Ignacimuthu S . Herbivore induced plant volatiles: their role in plant defense for pest management. Plant Signal Behav. 2011; 6(12):1973-8. PMC: 3337190. DOI: 10.4161/psb.6.12.18053. View

Zhao J, Zhang X, Hong Y, Liu Y . Chloroplast in Plant-Virus Interaction. Front Microbiol. 2016; 7:1565. PMC: 5047884. DOI: 10.3389/fmicb.2016.01565. View

McLeod G, Gries R, Von Reuss S, Rahe J, McIntosh R, Konig W . The pathogen causing Dutch elm disease makes host trees attract insect vectors. Proc Biol Sci. 2005; 272(1580):2499-503. PMC: 1599782. DOI: 10.1098/rspb.2005.3202. View

Ponzio C, Gols R, Weldegergis B, Dicke M . Caterpillar-induced plant volatiles remain a reliable signal for foraging wasps during dual attack with a plant pathogen or non-host insect herbivore. Plant Cell Environ. 2014; 37(8):1924-35. DOI: 10.1111/pce.12301. View

Ojinaga M, Guirao P, Larregla S . A Survey of Main Pepper Crop Viruses in Different Cultivation Systems for the Selection of the Most Appropriate Resistance Genes in Sensitive Local Cultivars in Northern Spain. Plants (Basel). 2022; 11(6). PMC: 8951742. DOI: 10.3390/plants11060719. View

Rostas M, Ton J, Mauch-Mani B, Turlings T . Fungal infection reduces herbivore-induced plant volatiles of maize but does not affect naïve parasitoids. J Chem Ecol. 2006; 32(9):1897-909. DOI: 10.1007/s10886-006-9147-3. View

Bruce T, Pickett J . Perception of plant volatile blends by herbivorous insects--finding the right mix. Phytochemistry. 2011; 72(13):1605-11. DOI: 10.1016/j.phytochem.2011.04.011. View

Schettino M, Grasso D, Weldegergis B, Castracani C, Mori A, Dicke M . Response of a Predatory ant to Volatiles Emitted by Aphid- and Caterpillar-Infested Cucumber and Potato Plants. J Chem Ecol. 2017; 43(10):1007-1022. DOI: 10.1007/s10886-017-0887-z. View

10.

Mauck K, De Moraes C, Mescher M . Infection of host plants by Cucumber mosaic virus increases the susceptibility of Myzus persicae aphids to the parasitoid Aphidius colemani. Sci Rep. 2015; 5:10963. PMC: 4455285. DOI: 10.1038/srep10963. View

11.

Kessler A, Baldwin I . Defensive function of herbivore-induced plant volatile emissions in nature. Science. 2001; 291(5511):2141-4. DOI: 10.1126/science.291.5511.2141. View

12.

Menzel T, Weldegergis B, David A, Boland W, Gols R, van Loon J . Synergism in the effect of prior jasmonic acid application on herbivore-induced volatile emission by Lima bean plants: transcription of a monoterpene synthase gene and volatile emission. J Exp Bot. 2014; 65(17):4821-31. PMC: 4144767. DOI: 10.1093/jxb/eru242. View

13.

Ziebell H, Murphy A, Groen S, Tungadi T, Westwood J, Lewsey M . Cucumber mosaic virus and its 2b RNA silencing suppressor modify plant-aphid interactions in tobacco. Sci Rep. 2012; 1:187. PMC: 3240964. DOI: 10.1038/srep00187. View

14.

Danner H, Desurmont G, Cristescu S, van Dam N . Herbivore-induced plant volatiles accurately predict history of coexistence, diet breadth, and feeding mode of herbivores. New Phytol. 2017; 220(3):726-738. DOI: 10.1111/nph.14428. View

15.

Hegde M, Oliveira J, da Costa J, Bleicher E, Santana A, Bruce T . Identification of semiochemicals released by cotton, Gossypium hirsutum, upon infestation by the cotton aphid, Aphis gossypii. J Chem Ecol. 2011; 37(7):741-50. DOI: 10.1007/s10886-011-9980-x. View

16.

Pan L, Miao H, Wang Q, Walling L, Liu S . Virus-induced phytohormone dynamics and their effects on plant-insect interactions. New Phytol. 2021; 230(4):1305-1320. PMC: 8251853. DOI: 10.1111/nph.17261. View

17.

Lewsey M, Murphy A, MacLean D, Dalchau N, Westwood J, Macaulay K . Disruption of two defensive signaling pathways by a viral RNA silencing suppressor. Mol Plant Microbe Interact. 2010; 23(7):835-45. DOI: 10.1094/MPMI-23-7-0835. View

18.

Werner B, Mowry T, Bosque-Perez N, Ding H, Eigenbrode S . Changes in green peach aphid responses to potato leafroll virus-induced volatiles emitted during disease progression. Environ Entomol. 2009; 38(5):1429-38. DOI: 10.1603/022.038.0511. View

19.

Cusumano A, Weldegergis B, Colazza S, Dicke M, Fatouros N . Attraction of egg-killing parasitoids toward induced plant volatiles in a multi-herbivore context. Oecologia. 2015; 179(1):163-74. DOI: 10.1007/s00442-015-3325-3. View

20.

Eigenbrode S, Ding H, Shiel P, Berger P . Volatiles from potato plants infected with potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae). Proc Biol Sci. 2002; 269(1490):455-60. PMC: 1690919. DOI: 10.1098/rspb.2001.1909. View