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Plant trichomes and a single gene GLABRA1 contribute to insect community composition on field-grown Arabidopsis thaliana


Sato, Yasuhiro; Shimizu-Inatsugi, Rie; Yamazaki, Misako; Shimizu, Kentaro K; Nagano, Atsushi J (2019). Plant trichomes and a single gene GLABRA1 contribute to insect community composition on field-grown Arabidopsis thaliana. BMC Plant Biology, 19:163.

Abstract

BACKGROUND:
Genetic variation in plants alters insect abundance and community structure in the field; however, little is known about the importance of a single gene among diverse plant genotypes. In this context, Arabidopsis trichomes provide an excellent system to discern the roles of natural variation and a key gene, GLABRA1, in shaping insect communities. In this study, we transplanted two independent glabrous mutants (gl1-1 and gl1-2) and 17 natural accessions of Arabidopsis thaliana to two localities in Switzerland and Japan.
RESULTS:
Fifteen insect species inhabited the plant accessions, with the insect community composition significantly attributed to variations among plant accessions. The total abundance of leaf-chewing herbivores was negatively correlated with trichome density at both field sites, while glucosinolates had variable effects on leaf chewers between the sites. Interestingly, there was a parallel tendency for the abundance of leaf chewers to be higher on gl1-1 and gl1-2 than on their different parental accessions, Ler-1 and Col-0, respectively. Furthermore, the loss of function in the GLABRA1 gene significantly decreased the resistance of plants to the two predominant chewers; flea beetles and turnip sawflies.
CONCLUSIONS:
Overall, our results indicate that insect community composition significantly varies among A. thaliana accessions across two distant field sites, with GLABRA1 playing a key role in altering the abundance of leaf-chewing herbivores. Given that such a trichome variation is widely observed in Brassicaceae plants, the present study exemplifies the community-wide effect of a single plant gene on crucifer-feeding insects in the field.

Abstract

BACKGROUND:
Genetic variation in plants alters insect abundance and community structure in the field; however, little is known about the importance of a single gene among diverse plant genotypes. In this context, Arabidopsis trichomes provide an excellent system to discern the roles of natural variation and a key gene, GLABRA1, in shaping insect communities. In this study, we transplanted two independent glabrous mutants (gl1-1 and gl1-2) and 17 natural accessions of Arabidopsis thaliana to two localities in Switzerland and Japan.
RESULTS:
Fifteen insect species inhabited the plant accessions, with the insect community composition significantly attributed to variations among plant accessions. The total abundance of leaf-chewing herbivores was negatively correlated with trichome density at both field sites, while glucosinolates had variable effects on leaf chewers between the sites. Interestingly, there was a parallel tendency for the abundance of leaf chewers to be higher on gl1-1 and gl1-2 than on their different parental accessions, Ler-1 and Col-0, respectively. Furthermore, the loss of function in the GLABRA1 gene significantly decreased the resistance of plants to the two predominant chewers; flea beetles and turnip sawflies.
CONCLUSIONS:
Overall, our results indicate that insect community composition significantly varies among A. thaliana accessions across two distant field sites, with GLABRA1 playing a key role in altering the abundance of leaf-chewing herbivores. Given that such a trichome variation is widely observed in Brassicaceae plants, the present study exemplifies the community-wide effect of a single plant gene on crucifer-feeding insects in the field.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Institute of Evolutionary Biology and Environmental Studies
08 Research Priority Programs > Global Change and Biodiversity
Dewey Decimal Classification:570 Life sciences; biology
590 Animals (Zoology)
Uncontrolled Keywords:Brassicaceae, Community genetics, GL1, Herbivory, In natura, Plant-insect interaction
Language:English
Date:1 December 2019
Deposited On:02 May 2019 10:34
Last Modified:23 May 2019 16:02
Publisher:BioMed Central
ISSN:1471-2229
OA Status:Gold
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1186/s12870-019-1705-2

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Download PDF  'Plant trichomes and a single gene GLABRA1 contribute to insect community composition on field-grown Arabidopsis thaliana'.
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Content: Supplemental Material
Filetype: Image (PNG) (The first and second principal component (PC1 and PC2) summarizing the total amount (nmol/mg flesh weight) of C3-, C4-, C5-, C7- and C8-Aliphatic glucosinolates for 17 accessions of A. thaliana (compiled from Chan et al.).)
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Download PDF  'Plant trichomes and a single gene GLABRA1 contribute to insect community composition on field-grown Arabidopsis thaliana'.
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Filetype: Image (PNG) (Cumulative number of each insect species in Zurich, Switzerland (left chart) and Otsu, Japan (right chart) throughout the experiments. See Table 2 for the name of the arthropod species.)
Size: 327kB
Content: Supplemental Material
Filetype: Other (Likelihood ratio tests for estimating broad-sense heritability H2. Likelihood ratio, LR-χ2, was tested by comparing the models with and without a random effect of the accession ID.)
Size: 11kB
Content: Supplemental Material
Filetype: Other (ffects of trichome density, the first and second principal component (PC1 and PC2) of aliphatic glucosinolates (GSLs), presence of flowering stems and initial plant sizes on insect abundance and community composition for 17 natural accessions of Arabidops)
Size: 14kB
Filetype: Other (Effects of trichome density, presence of flowering stem and initial plant size on insect abundance and community composition in a comparison between glabrous mutants and their parental accessions.)
Size: 11kB