Transient Expression of Whitefly Effectors in Nicotiana benthamiana Leaves Activates Systemic Immunity Against the Leaf Pathogen Pseudomonas syringae and Soil-Borne Pathogen Ralstonia solanacearum

Infestation of plants with the phloem-feeding whitefly Bemisia tabaci modulates root microbiota and both local and systemic immunity against microbial pathogens. Specifically, aboveground whitefly infestation suppresses pathogen propagation and symptom development caused by the soil-borne pathogens...

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Main Authors: Hae-Ran Lee, Soohyun Lee, Seyeon Park, Paula J. M. van Kleeff, Robert C. Schuurink, Choong-Min Ryu
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-07-01
Series:Frontiers in Ecology and Evolution
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fevo.2018.00090/full
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spelling doaj-2aa85e7f37904902b735c68426715f7f2020-11-24T22:26:41ZengFrontiers Media S.A.Frontiers in Ecology and Evolution2296-701X2018-07-01610.3389/fevo.2018.00090368944Transient Expression of Whitefly Effectors in Nicotiana benthamiana Leaves Activates Systemic Immunity Against the Leaf Pathogen Pseudomonas syringae and Soil-Borne Pathogen Ralstonia solanacearumHae-Ran Lee0Soohyun Lee1Seyeon Park2Paula J. M. van Kleeff3Robert C. Schuurink4Choong-Min Ryu5Choong-Min Ryu6Molecular Phytobacteriology Laboratory, Infectious Disease Research Center, KRIBB, Daejeon, South KoreaMolecular Phytobacteriology Laboratory, Infectious Disease Research Center, KRIBB, Daejeon, South KoreaUniversity of Science and Technology, Daejeon, South KoreaDepartment of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, NetherlandsDepartment of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, NetherlandsMolecular Phytobacteriology Laboratory, Infectious Disease Research Center, KRIBB, Daejeon, South KoreaUniversity of Science and Technology, Daejeon, South KoreaInfestation of plants with the phloem-feeding whitefly Bemisia tabaci modulates root microbiota and both local and systemic immunity against microbial pathogens. Specifically, aboveground whitefly infestation suppresses pathogen propagation and symptom development caused by the soil-borne pathogens Agrobacterium tumefaciens and Ralstonia solanacearum in the root system through systemic signal transduction. Therefore, we hypothesized that secreted protein(s)/non-protein factors from whitefly saliva (referred to as candidate effectors) might function as insect determinants that activate systemic acquired resistance (SAR) in the host plant. Here, we intensively screened a cDNA library constructed from mRNA from whitefly feeding on Nicotiana benthamiana leaves and selected three candidate effectors 2G4, 2G5, and 6A10, that appear to reduce disease development caused by the aboveground pathogen Pseudomonas syringae pv. tabaci and the soil-borne pathogen R. solanacearum. Transient expression of the three candidate effector cDNAs in leaves primed the expression of SAR marker genes NbPR1a and NbPR2 in local and systemic leaves against P. syringae pv. tabaci, while leaf infiltration with 2G4 or 6A10 cDNA elicited strong defense priming of SAR markers following drench application of R. solanacearum on plant roots. In silico and qRT-PCR analyses revealed the presence of 2G5 and 6A10 transcripts in insect salivary glands. This is the first report of whitefly effectors that prime SAR against aboveground and belowground bacterial pathogens.https://www.frontiersin.org/article/10.3389/fevo.2018.00090/fullwhiteflyeffectorNicotiana benthamianaRalstonia solanacearumtransient expression
collection DOAJ
language English
format Article
sources DOAJ
author Hae-Ran Lee
Soohyun Lee
Seyeon Park
Paula J. M. van Kleeff
Robert C. Schuurink
Choong-Min Ryu
Choong-Min Ryu
spellingShingle Hae-Ran Lee
Soohyun Lee
Seyeon Park
Paula J. M. van Kleeff
Robert C. Schuurink
Choong-Min Ryu
Choong-Min Ryu
Transient Expression of Whitefly Effectors in Nicotiana benthamiana Leaves Activates Systemic Immunity Against the Leaf Pathogen Pseudomonas syringae and Soil-Borne Pathogen Ralstonia solanacearum
Frontiers in Ecology and Evolution
whitefly
effector
Nicotiana benthamiana
Ralstonia solanacearum
transient expression
author_facet Hae-Ran Lee
Soohyun Lee
Seyeon Park
Paula J. M. van Kleeff
Robert C. Schuurink
Choong-Min Ryu
Choong-Min Ryu
author_sort Hae-Ran Lee
title Transient Expression of Whitefly Effectors in Nicotiana benthamiana Leaves Activates Systemic Immunity Against the Leaf Pathogen Pseudomonas syringae and Soil-Borne Pathogen Ralstonia solanacearum
title_short Transient Expression of Whitefly Effectors in Nicotiana benthamiana Leaves Activates Systemic Immunity Against the Leaf Pathogen Pseudomonas syringae and Soil-Borne Pathogen Ralstonia solanacearum
title_full Transient Expression of Whitefly Effectors in Nicotiana benthamiana Leaves Activates Systemic Immunity Against the Leaf Pathogen Pseudomonas syringae and Soil-Borne Pathogen Ralstonia solanacearum
title_fullStr Transient Expression of Whitefly Effectors in Nicotiana benthamiana Leaves Activates Systemic Immunity Against the Leaf Pathogen Pseudomonas syringae and Soil-Borne Pathogen Ralstonia solanacearum
title_full_unstemmed Transient Expression of Whitefly Effectors in Nicotiana benthamiana Leaves Activates Systemic Immunity Against the Leaf Pathogen Pseudomonas syringae and Soil-Borne Pathogen Ralstonia solanacearum
title_sort transient expression of whitefly effectors in nicotiana benthamiana leaves activates systemic immunity against the leaf pathogen pseudomonas syringae and soil-borne pathogen ralstonia solanacearum
publisher Frontiers Media S.A.
series Frontiers in Ecology and Evolution
issn 2296-701X
publishDate 2018-07-01
description Infestation of plants with the phloem-feeding whitefly Bemisia tabaci modulates root microbiota and both local and systemic immunity against microbial pathogens. Specifically, aboveground whitefly infestation suppresses pathogen propagation and symptom development caused by the soil-borne pathogens Agrobacterium tumefaciens and Ralstonia solanacearum in the root system through systemic signal transduction. Therefore, we hypothesized that secreted protein(s)/non-protein factors from whitefly saliva (referred to as candidate effectors) might function as insect determinants that activate systemic acquired resistance (SAR) in the host plant. Here, we intensively screened a cDNA library constructed from mRNA from whitefly feeding on Nicotiana benthamiana leaves and selected three candidate effectors 2G4, 2G5, and 6A10, that appear to reduce disease development caused by the aboveground pathogen Pseudomonas syringae pv. tabaci and the soil-borne pathogen R. solanacearum. Transient expression of the three candidate effector cDNAs in leaves primed the expression of SAR marker genes NbPR1a and NbPR2 in local and systemic leaves against P. syringae pv. tabaci, while leaf infiltration with 2G4 or 6A10 cDNA elicited strong defense priming of SAR markers following drench application of R. solanacearum on plant roots. In silico and qRT-PCR analyses revealed the presence of 2G5 and 6A10 transcripts in insect salivary glands. This is the first report of whitefly effectors that prime SAR against aboveground and belowground bacterial pathogens.
topic whitefly
effector
Nicotiana benthamiana
Ralstonia solanacearum
transient expression
url https://www.frontiersin.org/article/10.3389/fevo.2018.00090/full
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