Endosymbionts Differentially Alter Exploratory Probing Behavior of a Nonpersistent Plant Virus Vector

G. Angelella; V. Nalam; P. Nachappa; J. White; I. Kaplan

doi:10.1007/s00248-017-1133-5

Endosymbionts Differentially Alter Exploratory Probing Behavior of a Nonpersistent Plant Virus Vector

G. Angelella, V. Nalam, P. Nachappa, J. White, I. Kaplan

Entomology

Research output: Contribution to journal › Article › peer-review

14 Scopus citations

Abstract

Insect endosymbionts (hereafter, symbionts) can modify plant virus epidemiology by changing the physiology or behavior of vectors, but their role in nonpersistent virus pathosystems remains uninvestigated. Unlike propagative and circulative viruses, nonpersistent plant virus transmission occurs via transient contamination of mouthparts, making direct interaction between symbiont and virus unlikely. Nonpersistent virus transmission occurs during exploratory intracellular punctures with styletiform mouthparts when vectors assess potential host-plant quality prior to phloem feeding. Therefore, we used an electrical penetration graph (EPG) to evaluate plant probing of the cowpea aphid, Aphis craccivora Koch, an important vector of cucurbit viruses, in the presence and absence of two facultative, intracellular symbionts. We tested four isolines of A. craccivora: two isolines were from a clone from black locust (Robinia pseudoacacia L.), one infected with Arsenophonus sp. and one cured, and two derived from a clone from alfalfa (Medicago sativa L.), one infected with Hamiltonella defensa and one cured. We quantified exploratory intracellular punctures, indicated by a waveform potential drop recorded by the EPG, initiation speed and frequency within the initial 15 min on healthy and watermelon mosaic virus-infected pumpkins. Symbiont associations differentially modified exploratory intracellular puncture frequency by aphids, with H. defensa-infected aphids exhibiting depressed probing, and Arsenophonus-infected aphids an increased frequency of probing. Further, there was greater overall aphid probing on virus-infected plants, suggesting that viruses manipulate their vectors to enhance acquisition-transmission rates, independent of symbiont infection. These results suggest facultative symbionts differentially affect plant-host exploration behaviors and potentially nonpersistent virus transmission by vectors.

Original language	English
Pages (from-to)	453-458
Number of pages	6
Journal	Microbial Ecology
Volume	76
Issue number	2
DOIs	https://doi.org/10.1007/s00248-017-1133-5
State	Published - Aug 1 2018

Bibliographical note

Funding Information:
outlier, which is circled. a Locust-origin (Robinia pseudoacia) isolines with and without Arsenophonus infection (BArs,^ BCured,^ respectively). b Alfalfa-origin (Medicago sativa) isolines with and without Hamiltonella defensa infection (BHam,^ BCured,^ respectively). Pds = potential drops, indicating intracellular stylet punctures Acknowledgements We would like to thank Allison Dehnel for shipping Aphis craccivora from J. White’s lab at the University of Kentucky so often to initiate colonies at Purdue for use in this study. We would also like to thank an anonymous reviewer for helpful comments on an earlier version of this article. Funding provided by United States Department of Agriculture-National Institute of Food and Agriculture Predoctoral Fellowship grant 107483. Aphid colonies at the University of Kentucky were maintained on funds from United States Department of Agriculture-National Institute of Food and Agriculture grant 2014-67013-21576.

Funding Information:
We would like to thank Allison Dehnel for shipping Aphis craccivora from J. White’s lab at the University of Kentucky so often to initiate colonies at Purdue for use in this study. We would also like to thank an anonymous reviewer for helpful comments on an earlier version of this article. Funding provided by United States Department of Agriculture-National Institute of Food and Agriculture Predoctoral Fellowship grant 107483. Aphid colonies at the University of Kentucky were maintained on funds from United States Department of Agriculture-National Institute of Food and Agriculture grant 2014-67013-21576. The authors declare that they have no conflict of interest.

Publisher Copyright:
© 2017, Springer Science+Business Media, LLC, part of Springer Nature.

Keywords

Aphis craccivora
Arsenophonus
Endosymbionts
Hamiltonella defensa
Nonpersistent virus transmission
Watermelon mosaic virus

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Ecology
Soil Science

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10.1007/s00248-017-1133-5

Cite this

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title = "Endosymbionts Differentially Alter Exploratory Probing Behavior of a Nonpersistent Plant Virus Vector",

abstract = "Insect endosymbionts (hereafter, symbionts) can modify plant virus epidemiology by changing the physiology or behavior of vectors, but their role in nonpersistent virus pathosystems remains uninvestigated. Unlike propagative and circulative viruses, nonpersistent plant virus transmission occurs via transient contamination of mouthparts, making direct interaction between symbiont and virus unlikely. Nonpersistent virus transmission occurs during exploratory intracellular punctures with styletiform mouthparts when vectors assess potential host-plant quality prior to phloem feeding. Therefore, we used an electrical penetration graph (EPG) to evaluate plant probing of the cowpea aphid, Aphis craccivora Koch, an important vector of cucurbit viruses, in the presence and absence of two facultative, intracellular symbionts. We tested four isolines of A. craccivora: two isolines were from a clone from black locust (Robinia pseudoacacia L.), one infected with Arsenophonus sp. and one cured, and two derived from a clone from alfalfa (Medicago sativa L.), one infected with Hamiltonella defensa and one cured. We quantified exploratory intracellular punctures, indicated by a waveform potential drop recorded by the EPG, initiation speed and frequency within the initial 15 min on healthy and watermelon mosaic virus-infected pumpkins. Symbiont associations differentially modified exploratory intracellular puncture frequency by aphids, with H. defensa-infected aphids exhibiting depressed probing, and Arsenophonus-infected aphids an increased frequency of probing. Further, there was greater overall aphid probing on virus-infected plants, suggesting that viruses manipulate their vectors to enhance acquisition-transmission rates, independent of symbiont infection. These results suggest facultative symbionts differentially affect plant-host exploration behaviors and potentially nonpersistent virus transmission by vectors.",

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author = "G. Angelella and V. Nalam and P. Nachappa and J. White and I. Kaplan",

note = "Funding Information: outlier, which is circled. a Locust-origin (Robinia pseudoacia) isolines with and without Arsenophonus infection (BArs,^ BCured,^ respectively). b Alfalfa-origin (Medicago sativa) isolines with and without Hamiltonella defensa infection (BHam,^ BCured,^ respectively). Pds = potential drops, indicating intracellular stylet punctures Acknowledgements We would like to thank Allison Dehnel for shipping Aphis craccivora from J. White{\textquoteright}s lab at the University of Kentucky so often to initiate colonies at Purdue for use in this study. We would also like to thank an anonymous reviewer for helpful comments on an earlier version of this article. Funding provided by United States Department of Agriculture-National Institute of Food and Agriculture Predoctoral Fellowship grant 107483. Aphid colonies at the University of Kentucky were maintained on funds from United States Department of Agriculture-National Institute of Food and Agriculture grant 2014-67013-21576. Funding Information: We would like to thank Allison Dehnel for shipping Aphis craccivora from J. White{\textquoteright}s lab at the University of Kentucky so often to initiate colonies at Purdue for use in this study. We would also like to thank an anonymous reviewer for helpful comments on an earlier version of this article. Funding provided by United States Department of Agriculture-National Institute of Food and Agriculture Predoctoral Fellowship grant 107483. Aphid colonies at the University of Kentucky were maintained on funds from United States Department of Agriculture-National Institute of Food and Agriculture grant 2014-67013-21576. The authors declare that they have no conflict of interest. Publisher Copyright: {\textcopyright} 2017, Springer Science+Business Media, LLC, part of Springer Nature.",

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doi = "10.1007/s00248-017-1133-5",

language = "English",

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AU - Angelella, G.

AU - Nalam, V.

AU - Nachappa, P.

AU - White, J.

AU - Kaplan, I.

N1 - Funding Information: outlier, which is circled. a Locust-origin (Robinia pseudoacia) isolines with and without Arsenophonus infection (BArs,^ BCured,^ respectively). b Alfalfa-origin (Medicago sativa) isolines with and without Hamiltonella defensa infection (BHam,^ BCured,^ respectively). Pds = potential drops, indicating intracellular stylet punctures Acknowledgements We would like to thank Allison Dehnel for shipping Aphis craccivora from J. White’s lab at the University of Kentucky so often to initiate colonies at Purdue for use in this study. We would also like to thank an anonymous reviewer for helpful comments on an earlier version of this article. Funding provided by United States Department of Agriculture-National Institute of Food and Agriculture Predoctoral Fellowship grant 107483. Aphid colonies at the University of Kentucky were maintained on funds from United States Department of Agriculture-National Institute of Food and Agriculture grant 2014-67013-21576. Funding Information: We would like to thank Allison Dehnel for shipping Aphis craccivora from J. White’s lab at the University of Kentucky so often to initiate colonies at Purdue for use in this study. We would also like to thank an anonymous reviewer for helpful comments on an earlier version of this article. Funding provided by United States Department of Agriculture-National Institute of Food and Agriculture Predoctoral Fellowship grant 107483. Aphid colonies at the University of Kentucky were maintained on funds from United States Department of Agriculture-National Institute of Food and Agriculture grant 2014-67013-21576. The authors declare that they have no conflict of interest. Publisher Copyright: © 2017, Springer Science+Business Media, LLC, part of Springer Nature.

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N2 - Insect endosymbionts (hereafter, symbionts) can modify plant virus epidemiology by changing the physiology or behavior of vectors, but their role in nonpersistent virus pathosystems remains uninvestigated. Unlike propagative and circulative viruses, nonpersistent plant virus transmission occurs via transient contamination of mouthparts, making direct interaction between symbiont and virus unlikely. Nonpersistent virus transmission occurs during exploratory intracellular punctures with styletiform mouthparts when vectors assess potential host-plant quality prior to phloem feeding. Therefore, we used an electrical penetration graph (EPG) to evaluate plant probing of the cowpea aphid, Aphis craccivora Koch, an important vector of cucurbit viruses, in the presence and absence of two facultative, intracellular symbionts. We tested four isolines of A. craccivora: two isolines were from a clone from black locust (Robinia pseudoacacia L.), one infected with Arsenophonus sp. and one cured, and two derived from a clone from alfalfa (Medicago sativa L.), one infected with Hamiltonella defensa and one cured. We quantified exploratory intracellular punctures, indicated by a waveform potential drop recorded by the EPG, initiation speed and frequency within the initial 15 min on healthy and watermelon mosaic virus-infected pumpkins. Symbiont associations differentially modified exploratory intracellular puncture frequency by aphids, with H. defensa-infected aphids exhibiting depressed probing, and Arsenophonus-infected aphids an increased frequency of probing. Further, there was greater overall aphid probing on virus-infected plants, suggesting that viruses manipulate their vectors to enhance acquisition-transmission rates, independent of symbiont infection. These results suggest facultative symbionts differentially affect plant-host exploration behaviors and potentially nonpersistent virus transmission by vectors.

AB - Insect endosymbionts (hereafter, symbionts) can modify plant virus epidemiology by changing the physiology or behavior of vectors, but their role in nonpersistent virus pathosystems remains uninvestigated. Unlike propagative and circulative viruses, nonpersistent plant virus transmission occurs via transient contamination of mouthparts, making direct interaction between symbiont and virus unlikely. Nonpersistent virus transmission occurs during exploratory intracellular punctures with styletiform mouthparts when vectors assess potential host-plant quality prior to phloem feeding. Therefore, we used an electrical penetration graph (EPG) to evaluate plant probing of the cowpea aphid, Aphis craccivora Koch, an important vector of cucurbit viruses, in the presence and absence of two facultative, intracellular symbionts. We tested four isolines of A. craccivora: two isolines were from a clone from black locust (Robinia pseudoacacia L.), one infected with Arsenophonus sp. and one cured, and two derived from a clone from alfalfa (Medicago sativa L.), one infected with Hamiltonella defensa and one cured. We quantified exploratory intracellular punctures, indicated by a waveform potential drop recorded by the EPG, initiation speed and frequency within the initial 15 min on healthy and watermelon mosaic virus-infected pumpkins. Symbiont associations differentially modified exploratory intracellular puncture frequency by aphids, with H. defensa-infected aphids exhibiting depressed probing, and Arsenophonus-infected aphids an increased frequency of probing. Further, there was greater overall aphid probing on virus-infected plants, suggesting that viruses manipulate their vectors to enhance acquisition-transmission rates, independent of symbiont infection. These results suggest facultative symbionts differentially affect plant-host exploration behaviors and potentially nonpersistent virus transmission by vectors.

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Endosymbionts Differentially Alter Exploratory Probing Behavior of a Nonpersistent Plant Virus Vector

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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