Symbiotic polydnavirus of a parasite manipulates caterpillar and plant immunity

Ching Wen Tan, Michelle Peiffer, Kelli Hoover, Cristina Rosa, Flor E. Acevedo, Gary Felton

Research output: Contribution to journalArticle

9 Citations (Scopus)

Abstract

Obligate symbioses occur when organisms require symbiotic relationships to survive. Some parasitic wasps of caterpillars possess obligate mutualistic viruses called “polydnaviruses.” Along with eggs, wasps inject polydnavirus inside their caterpillar hosts where the hatching larvae develop inside the caterpillar. Polydnaviruses suppress the immune systems of their caterpillar hosts, which enables egg hatch and wasp larval development. It is unknown whether polydnaviruses also manipulate the salivary proteins of the caterpillar, which may affect the elicitation of plant defenses during feeding by the caterpillar. Here, we show that a polydnavirus of the parasitoid Microplitis croceipes, and not the parasitoid larva itself, drives the regulation of salivary enzymes of the caterpillar Helicoverpa zea that are known to elicit tomato plant-defense responses to herbivores. The polydnavirus suppresses glucose oxidase, which is a primary plant-defense elicitor in the saliva of the H. zea caterpillar. By suppressing plant defenses, the polydnavirus allows the caterpillar to grow at a faster rate, thus improving the host suitability for the parasitoid. Remarkably, polydnaviruses manipulate the phenotypes of the wasp, caterpillar, and host plant, demonstrating that polydnaviruses play far more prominent roles in shaping plant–herbivore interactions than ever considered

Original languageEnglish (US)
Pages (from-to)5199-5204
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number20
DOIs
StatePublished - May 15 2018

Fingerprint

Plant Immunity
Wasps
Parasites
Zea mays
Larva
Salivary Proteins and Peptides
Glucose Oxidase
Herbivory
Symbiosis
Lycopersicon esculentum
Saliva
Eggs
Ovum
Immune System
Viruses
Phenotype
Enzymes

All Science Journal Classification (ASJC) codes

  • General

Cite this

@article{7d3062ae3f874e17adb07072d1151a1b,
title = "Symbiotic polydnavirus of a parasite manipulates caterpillar and plant immunity",
abstract = "Obligate symbioses occur when organisms require symbiotic relationships to survive. Some parasitic wasps of caterpillars possess obligate mutualistic viruses called “polydnaviruses.” Along with eggs, wasps inject polydnavirus inside their caterpillar hosts where the hatching larvae develop inside the caterpillar. Polydnaviruses suppress the immune systems of their caterpillar hosts, which enables egg hatch and wasp larval development. It is unknown whether polydnaviruses also manipulate the salivary proteins of the caterpillar, which may affect the elicitation of plant defenses during feeding by the caterpillar. Here, we show that a polydnavirus of the parasitoid Microplitis croceipes, and not the parasitoid larva itself, drives the regulation of salivary enzymes of the caterpillar Helicoverpa zea that are known to elicit tomato plant-defense responses to herbivores. The polydnavirus suppresses glucose oxidase, which is a primary plant-defense elicitor in the saliva of the H. zea caterpillar. By suppressing plant defenses, the polydnavirus allows the caterpillar to grow at a faster rate, thus improving the host suitability for the parasitoid. Remarkably, polydnaviruses manipulate the phenotypes of the wasp, caterpillar, and host plant, demonstrating that polydnaviruses play far more prominent roles in shaping plant–herbivore interactions than ever considered",
author = "Tan, {Ching Wen} and Michelle Peiffer and Kelli Hoover and Cristina Rosa and Acevedo, {Flor E.} and Gary Felton",
year = "2018",
month = "5",
day = "15",
doi = "10.1073/pnas.1717934115",
language = "English (US)",
volume = "115",
pages = "5199--5204",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "20",

}

Symbiotic polydnavirus of a parasite manipulates caterpillar and plant immunity. / Tan, Ching Wen; Peiffer, Michelle; Hoover, Kelli; Rosa, Cristina; Acevedo, Flor E.; Felton, Gary.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, No. 20, 15.05.2018, p. 5199-5204.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Symbiotic polydnavirus of a parasite manipulates caterpillar and plant immunity

AU - Tan, Ching Wen

AU - Peiffer, Michelle

AU - Hoover, Kelli

AU - Rosa, Cristina

AU - Acevedo, Flor E.

AU - Felton, Gary

PY - 2018/5/15

Y1 - 2018/5/15

N2 - Obligate symbioses occur when organisms require symbiotic relationships to survive. Some parasitic wasps of caterpillars possess obligate mutualistic viruses called “polydnaviruses.” Along with eggs, wasps inject polydnavirus inside their caterpillar hosts where the hatching larvae develop inside the caterpillar. Polydnaviruses suppress the immune systems of their caterpillar hosts, which enables egg hatch and wasp larval development. It is unknown whether polydnaviruses also manipulate the salivary proteins of the caterpillar, which may affect the elicitation of plant defenses during feeding by the caterpillar. Here, we show that a polydnavirus of the parasitoid Microplitis croceipes, and not the parasitoid larva itself, drives the regulation of salivary enzymes of the caterpillar Helicoverpa zea that are known to elicit tomato plant-defense responses to herbivores. The polydnavirus suppresses glucose oxidase, which is a primary plant-defense elicitor in the saliva of the H. zea caterpillar. By suppressing plant defenses, the polydnavirus allows the caterpillar to grow at a faster rate, thus improving the host suitability for the parasitoid. Remarkably, polydnaviruses manipulate the phenotypes of the wasp, caterpillar, and host plant, demonstrating that polydnaviruses play far more prominent roles in shaping plant–herbivore interactions than ever considered

AB - Obligate symbioses occur when organisms require symbiotic relationships to survive. Some parasitic wasps of caterpillars possess obligate mutualistic viruses called “polydnaviruses.” Along with eggs, wasps inject polydnavirus inside their caterpillar hosts where the hatching larvae develop inside the caterpillar. Polydnaviruses suppress the immune systems of their caterpillar hosts, which enables egg hatch and wasp larval development. It is unknown whether polydnaviruses also manipulate the salivary proteins of the caterpillar, which may affect the elicitation of plant defenses during feeding by the caterpillar. Here, we show that a polydnavirus of the parasitoid Microplitis croceipes, and not the parasitoid larva itself, drives the regulation of salivary enzymes of the caterpillar Helicoverpa zea that are known to elicit tomato plant-defense responses to herbivores. The polydnavirus suppresses glucose oxidase, which is a primary plant-defense elicitor in the saliva of the H. zea caterpillar. By suppressing plant defenses, the polydnavirus allows the caterpillar to grow at a faster rate, thus improving the host suitability for the parasitoid. Remarkably, polydnaviruses manipulate the phenotypes of the wasp, caterpillar, and host plant, demonstrating that polydnaviruses play far more prominent roles in shaping plant–herbivore interactions than ever considered

UR - http://www.scopus.com/inward/record.url?scp=85046969129&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85046969129&partnerID=8YFLogxK

U2 - 10.1073/pnas.1717934115

DO - 10.1073/pnas.1717934115

M3 - Article

VL - 115

SP - 5199

EP - 5204

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 20

ER -