Transcriptional Variation in Glucosinolate Biosynthetic Genes and Inducible Responses to Aphid Herbivory on Field-Grown Arabidopsis thaliana

Recently, increasing attempts have been made to understand how plant genes function in natura. In this context, transcriptional profiles represent plant physiological status in response to environmental stimuli. Herein, we combined high-throughput RNA-Seq with insect survey data on 19 accessions of...

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Main Authors: Yasuhiro Sato, Ayumi Tezuka, Makoto Kashima, Ayumi Deguchi, Rie Shimizu-Inatsugi, Misako Yamazaki, Kentaro K. Shimizu, Atsushi J. Nagano
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-09-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fgene.2019.00787/full
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spelling doaj-91c7d37fe04148dfae42930a4d0453302020-11-25T00:53:23ZengFrontiers Media S.A.Frontiers in Genetics1664-80212019-09-011010.3389/fgene.2019.00787469835Transcriptional Variation in Glucosinolate Biosynthetic Genes and Inducible Responses to Aphid Herbivory on Field-Grown Arabidopsis thalianaYasuhiro Sato0Yasuhiro Sato1Ayumi Tezuka2Makoto Kashima3Ayumi Deguchi4Ayumi Deguchi5Rie Shimizu-Inatsugi6Misako Yamazaki7Kentaro K. Shimizu8Kentaro K. Shimizu9Atsushi J. Nagano10PRESTO, Japan Science and Technology Agency, Kawaguchi, JapanResearch Institute for Food and Agriculture, Ryukoku University, Otsu, JapanResearch Institute for Food and Agriculture, Ryukoku University, Otsu, JapanResearch Institute for Food and Agriculture, Ryukoku University, Otsu, JapanResearch Institute for Food and Agriculture, Ryukoku University, Otsu, JapanGraduate School of Horticulture, Chiba University, Matsudo, JapanDepartment of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, SwitzerlandDepartment of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, SwitzerlandDepartment of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, SwitzerlandKihara Institute for Biological Research, Yokohama City University, Yokohama, JapanDepartment of Plant Life Sciences, Faculty of Agriculture, Ryukoku University, Otsu, JapanRecently, increasing attempts have been made to understand how plant genes function in natura. In this context, transcriptional profiles represent plant physiological status in response to environmental stimuli. Herein, we combined high-throughput RNA-Seq with insect survey data on 19 accessions of Arabidopsis thaliana grown at a field site in Switzerland. We found that genes with the gene ontology (GO) annotations of “glucosinolate biosynthetic process” and “response to insects” were most significantly enriched, and the expression of these genes was highly variable among plant accessions. Nearly half of the total expression variation in the glucosinolate biosynthetic genes (AOPs, ESM1, ESP, and TGG1) was explained by among-accession variation. Of these genes, the expression level of AOP3 differed among Col-0 accession individuals depending on the abundance of the mustard aphid (Lipaphis erysimi). We also found that the expression of the major cis-jasmone activated gene CYP81D11 was positively correlated with the number of flea beetles (Phyllotreta striolata and Phyllotreta atra). Combined with the field RNA-Seq data, bioassays confirmed that AOP3 was up-regulated in response to attack by mustard aphids. The combined results from RNA-Seq and our ecological survey illustrate the feasibility of using field transcriptomics to detect an inducible defense, providing a first step towards an in natura understanding of biotic interactions involving phenotypic plasticity.https://www.frontiersin.org/article/10.3389/fgene.2019.00787/fullAOP3in naturaLipaphis erysimiRNA-Seqplant–insect interaction
collection DOAJ
language English
format Article
sources DOAJ
author Yasuhiro Sato
Yasuhiro Sato
Ayumi Tezuka
Makoto Kashima
Ayumi Deguchi
Ayumi Deguchi
Rie Shimizu-Inatsugi
Misako Yamazaki
Kentaro K. Shimizu
Kentaro K. Shimizu
Atsushi J. Nagano
spellingShingle Yasuhiro Sato
Yasuhiro Sato
Ayumi Tezuka
Makoto Kashima
Ayumi Deguchi
Ayumi Deguchi
Rie Shimizu-Inatsugi
Misako Yamazaki
Kentaro K. Shimizu
Kentaro K. Shimizu
Atsushi J. Nagano
Transcriptional Variation in Glucosinolate Biosynthetic Genes and Inducible Responses to Aphid Herbivory on Field-Grown Arabidopsis thaliana
Frontiers in Genetics
AOP3
in natura
Lipaphis erysimi
RNA-Seq
plant–insect interaction
author_facet Yasuhiro Sato
Yasuhiro Sato
Ayumi Tezuka
Makoto Kashima
Ayumi Deguchi
Ayumi Deguchi
Rie Shimizu-Inatsugi
Misako Yamazaki
Kentaro K. Shimizu
Kentaro K. Shimizu
Atsushi J. Nagano
author_sort Yasuhiro Sato
title Transcriptional Variation in Glucosinolate Biosynthetic Genes and Inducible Responses to Aphid Herbivory on Field-Grown Arabidopsis thaliana
title_short Transcriptional Variation in Glucosinolate Biosynthetic Genes and Inducible Responses to Aphid Herbivory on Field-Grown Arabidopsis thaliana
title_full Transcriptional Variation in Glucosinolate Biosynthetic Genes and Inducible Responses to Aphid Herbivory on Field-Grown Arabidopsis thaliana
title_fullStr Transcriptional Variation in Glucosinolate Biosynthetic Genes and Inducible Responses to Aphid Herbivory on Field-Grown Arabidopsis thaliana
title_full_unstemmed Transcriptional Variation in Glucosinolate Biosynthetic Genes and Inducible Responses to Aphid Herbivory on Field-Grown Arabidopsis thaliana
title_sort transcriptional variation in glucosinolate biosynthetic genes and inducible responses to aphid herbivory on field-grown arabidopsis thaliana
publisher Frontiers Media S.A.
series Frontiers in Genetics
issn 1664-8021
publishDate 2019-09-01
description Recently, increasing attempts have been made to understand how plant genes function in natura. In this context, transcriptional profiles represent plant physiological status in response to environmental stimuli. Herein, we combined high-throughput RNA-Seq with insect survey data on 19 accessions of Arabidopsis thaliana grown at a field site in Switzerland. We found that genes with the gene ontology (GO) annotations of “glucosinolate biosynthetic process” and “response to insects” were most significantly enriched, and the expression of these genes was highly variable among plant accessions. Nearly half of the total expression variation in the glucosinolate biosynthetic genes (AOPs, ESM1, ESP, and TGG1) was explained by among-accession variation. Of these genes, the expression level of AOP3 differed among Col-0 accession individuals depending on the abundance of the mustard aphid (Lipaphis erysimi). We also found that the expression of the major cis-jasmone activated gene CYP81D11 was positively correlated with the number of flea beetles (Phyllotreta striolata and Phyllotreta atra). Combined with the field RNA-Seq data, bioassays confirmed that AOP3 was up-regulated in response to attack by mustard aphids. The combined results from RNA-Seq and our ecological survey illustrate the feasibility of using field transcriptomics to detect an inducible defense, providing a first step towards an in natura understanding of biotic interactions involving phenotypic plasticity.
topic AOP3
in natura
Lipaphis erysimi
RNA-Seq
plant–insect interaction
url https://www.frontiersin.org/article/10.3389/fgene.2019.00787/full
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