Combining QTL mapping with transcriptome and metabolome profiling reveals a possible role for ABA signaling in resistance against the cabbage whitefly in cabbage

Colette Broekgaarden*, Koen T.B. Pelgrom, Johan Bucher, Nicole M. van Dam, Katharine Grosser, Corné M.J. Pieterse, Martijn van Kaauwen, Greet Steenhuis, Roeland E. Voorrips, Martin de Vos, Ben Vosman, Anja Worrich, Saskia C.M. van Wees

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Whiteflies are among the world's most significant agricultural pests and chemical insecticides are extensively used to reduce crop damage to acceptable levels. However, nearly all insecticides pose a threat to the environment and alternative control methods, such as breeding of crop varieties that are inherently insect-resistant, are needed. Previously, a strong source of plant-age dependent resistance to the cabbage whitefly (Aleyrodes proletella) has been identified in the modern white cabbage (Brassica oleracea var. capitata) variety Rivera. However, nothing is known about the molecular mechanisms or the genes involved in this resistance. In the present study, a multidisciplinary approach combining transcriptome and metabolome profiling with genetic mapping was used to identify the molecular players of whitefly resistance in cabbage. Transcriptome profiles of young (susceptible) and older (resistant) Rivera plants were analyzed using RNA sequencing. While many genes involved in general processes were differentially expressed between both ages, several defense-related processes were overrepresented in the transcriptome profile of older plants. Hormone measurements revealed that jasmonic acid (JA) levels decreased upon whitefly infestation at both plant ages. Interestingly, abscisic acid (ABA) levels showed contrasting effects in response to whitefly infestation: ABA levels were reduced in young plants but induced in older plants upon whitefly feeding. Auxin levels were significantly lower in older plants compared with young plants, independent of whitefly presence, while glucosinolate levels were higher. Additionally, whitefly performance was monitored in an F2 population derived from a cross between Rivera and the susceptible white cabbage variety Christmas Drumhead. Significant QTL intervals were mapped on chromosome 2 and 9 for oviposition rate and whitefly adult survival, respectively. Several genes that were higher expressed in older plants and located in the identified QTL intervals were orthologous to Arabidopsis genes that have been related to ABA signaling, suggesting a role for ABA in the regulation of resistance towards whiteflies. Our results show that combining different omics approaches is a useful strategy to identify candidate genes underlying insect resistance.

Original languageEnglish
Article numbere0206103
JournalPLoS ONE
Volume13
Issue number11
DOIs
Publication statusPublished - 6 Nov 2018

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metabolome
Abscisic Acid
Hemiptera
Metabolome
Brassica
Gene Expression Profiling
Aleyrodidae
cabbage
transcriptome
abscisic acid
quantitative trait loci
Genes
Insecticides
Crops
Glucosinolates
Indoleacetic Acids
plant age
Chromosomes
Transcriptome
genes

Cite this

Broekgaarden, Colette ; Pelgrom, Koen T.B. ; Bucher, Johan ; van Dam, Nicole M. ; Grosser, Katharine ; Pieterse, Corné M.J. ; van Kaauwen, Martijn ; Steenhuis, Greet ; Voorrips, Roeland E. ; de Vos, Martin ; Vosman, Ben ; Worrich, Anja ; van Wees, Saskia C.M. / Combining QTL mapping with transcriptome and metabolome profiling reveals a possible role for ABA signaling in resistance against the cabbage whitefly in cabbage. In: PLoS ONE. 2018 ; Vol. 13, No. 11.
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title = "Combining QTL mapping with transcriptome and metabolome profiling reveals a possible role for ABA signaling in resistance against the cabbage whitefly in cabbage",
abstract = "Whiteflies are among the world's most significant agricultural pests and chemical insecticides are extensively used to reduce crop damage to acceptable levels. However, nearly all insecticides pose a threat to the environment and alternative control methods, such as breeding of crop varieties that are inherently insect-resistant, are needed. Previously, a strong source of plant-age dependent resistance to the cabbage whitefly (Aleyrodes proletella) has been identified in the modern white cabbage (Brassica oleracea var. capitata) variety Rivera. However, nothing is known about the molecular mechanisms or the genes involved in this resistance. In the present study, a multidisciplinary approach combining transcriptome and metabolome profiling with genetic mapping was used to identify the molecular players of whitefly resistance in cabbage. Transcriptome profiles of young (susceptible) and older (resistant) Rivera plants were analyzed using RNA sequencing. While many genes involved in general processes were differentially expressed between both ages, several defense-related processes were overrepresented in the transcriptome profile of older plants. Hormone measurements revealed that jasmonic acid (JA) levels decreased upon whitefly infestation at both plant ages. Interestingly, abscisic acid (ABA) levels showed contrasting effects in response to whitefly infestation: ABA levels were reduced in young plants but induced in older plants upon whitefly feeding. Auxin levels were significantly lower in older plants compared with young plants, independent of whitefly presence, while glucosinolate levels were higher. Additionally, whitefly performance was monitored in an F2 population derived from a cross between Rivera and the susceptible white cabbage variety Christmas Drumhead. Significant QTL intervals were mapped on chromosome 2 and 9 for oviposition rate and whitefly adult survival, respectively. Several genes that were higher expressed in older plants and located in the identified QTL intervals were orthologous to Arabidopsis genes that have been related to ABA signaling, suggesting a role for ABA in the regulation of resistance towards whiteflies. Our results show that combining different omics approaches is a useful strategy to identify candidate genes underlying insect resistance.",
author = "Colette Broekgaarden and Pelgrom, {Koen T.B.} and Johan Bucher and {van Dam}, {Nicole M.} and Katharine Grosser and Pieterse, {Corn{\'e} M.J.} and {van Kaauwen}, Martijn and Greet Steenhuis and Voorrips, {Roeland E.} and {de Vos}, Martin and Ben Vosman and Anja Worrich and {van Wees}, {Saskia C.M.}",
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Combining QTL mapping with transcriptome and metabolome profiling reveals a possible role for ABA signaling in resistance against the cabbage whitefly in cabbage. / Broekgaarden, Colette; Pelgrom, Koen T.B.; Bucher, Johan; van Dam, Nicole M.; Grosser, Katharine; Pieterse, Corné M.J.; van Kaauwen, Martijn; Steenhuis, Greet; Voorrips, Roeland E.; de Vos, Martin; Vosman, Ben; Worrich, Anja; van Wees, Saskia C.M.

In: PLoS ONE, Vol. 13, No. 11, e0206103, 06.11.2018.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Combining QTL mapping with transcriptome and metabolome profiling reveals a possible role for ABA signaling in resistance against the cabbage whitefly in cabbage

AU - Broekgaarden, Colette

AU - Pelgrom, Koen T.B.

AU - Bucher, Johan

AU - van Dam, Nicole M.

AU - Grosser, Katharine

AU - Pieterse, Corné M.J.

AU - van Kaauwen, Martijn

AU - Steenhuis, Greet

AU - Voorrips, Roeland E.

AU - de Vos, Martin

AU - Vosman, Ben

AU - Worrich, Anja

AU - van Wees, Saskia C.M.

PY - 2018/11/6

Y1 - 2018/11/6

N2 - Whiteflies are among the world's most significant agricultural pests and chemical insecticides are extensively used to reduce crop damage to acceptable levels. However, nearly all insecticides pose a threat to the environment and alternative control methods, such as breeding of crop varieties that are inherently insect-resistant, are needed. Previously, a strong source of plant-age dependent resistance to the cabbage whitefly (Aleyrodes proletella) has been identified in the modern white cabbage (Brassica oleracea var. capitata) variety Rivera. However, nothing is known about the molecular mechanisms or the genes involved in this resistance. In the present study, a multidisciplinary approach combining transcriptome and metabolome profiling with genetic mapping was used to identify the molecular players of whitefly resistance in cabbage. Transcriptome profiles of young (susceptible) and older (resistant) Rivera plants were analyzed using RNA sequencing. While many genes involved in general processes were differentially expressed between both ages, several defense-related processes were overrepresented in the transcriptome profile of older plants. Hormone measurements revealed that jasmonic acid (JA) levels decreased upon whitefly infestation at both plant ages. Interestingly, abscisic acid (ABA) levels showed contrasting effects in response to whitefly infestation: ABA levels were reduced in young plants but induced in older plants upon whitefly feeding. Auxin levels were significantly lower in older plants compared with young plants, independent of whitefly presence, while glucosinolate levels were higher. Additionally, whitefly performance was monitored in an F2 population derived from a cross between Rivera and the susceptible white cabbage variety Christmas Drumhead. Significant QTL intervals were mapped on chromosome 2 and 9 for oviposition rate and whitefly adult survival, respectively. Several genes that were higher expressed in older plants and located in the identified QTL intervals were orthologous to Arabidopsis genes that have been related to ABA signaling, suggesting a role for ABA in the regulation of resistance towards whiteflies. Our results show that combining different omics approaches is a useful strategy to identify candidate genes underlying insect resistance.

AB - Whiteflies are among the world's most significant agricultural pests and chemical insecticides are extensively used to reduce crop damage to acceptable levels. However, nearly all insecticides pose a threat to the environment and alternative control methods, such as breeding of crop varieties that are inherently insect-resistant, are needed. Previously, a strong source of plant-age dependent resistance to the cabbage whitefly (Aleyrodes proletella) has been identified in the modern white cabbage (Brassica oleracea var. capitata) variety Rivera. However, nothing is known about the molecular mechanisms or the genes involved in this resistance. In the present study, a multidisciplinary approach combining transcriptome and metabolome profiling with genetic mapping was used to identify the molecular players of whitefly resistance in cabbage. Transcriptome profiles of young (susceptible) and older (resistant) Rivera plants were analyzed using RNA sequencing. While many genes involved in general processes were differentially expressed between both ages, several defense-related processes were overrepresented in the transcriptome profile of older plants. Hormone measurements revealed that jasmonic acid (JA) levels decreased upon whitefly infestation at both plant ages. Interestingly, abscisic acid (ABA) levels showed contrasting effects in response to whitefly infestation: ABA levels were reduced in young plants but induced in older plants upon whitefly feeding. Auxin levels were significantly lower in older plants compared with young plants, independent of whitefly presence, while glucosinolate levels were higher. Additionally, whitefly performance was monitored in an F2 population derived from a cross between Rivera and the susceptible white cabbage variety Christmas Drumhead. Significant QTL intervals were mapped on chromosome 2 and 9 for oviposition rate and whitefly adult survival, respectively. Several genes that were higher expressed in older plants and located in the identified QTL intervals were orthologous to Arabidopsis genes that have been related to ABA signaling, suggesting a role for ABA in the regulation of resistance towards whiteflies. Our results show that combining different omics approaches is a useful strategy to identify candidate genes underlying insect resistance.

U2 - 10.1371/journal.pone.0206103

DO - 10.1371/journal.pone.0206103

M3 - Article

VL - 13

JO - PLoS ONE

JF - PLoS ONE

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