Differential Levels of Insect Herbivory in the Field Associated with Genotypic Variation in Glucosinolates in Arabidopsis thaliana

Bidart‐Bouzat, M. Gabriela; Kliebenstein, Daniel J.

doi:10.1007/s10886-008-9498-z

Cited by 124 publications

(123 citation statements)

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“…A selective sweep may have increased the frequency of the derived AOP and MAM haplotypes, causing extended LD (Palaisa et al 2004). This possibility is supported by the observation that the 3-hydroxypropyl GSL-accumulating accessions display the highest fitness in an environment with predominantly specialist insect herbivores that have evolved to overcome GSL defenses (Bidart-Bouzat and Kliebenstein 2008). Further, A. thaliana accessions possessing the 4C GSL-associated haplotype at the MAM locus showed the second-highest fitness in the same experiment (BidartBouzat and Kliebenstein 2008).…”

Section: Discussionmentioning

confidence: 93%

“…Indolic GSL are a critical determinant of resistance to pathogens and insects and additionally act as oviposition deterrents (Kim and Jander 2007;de Vos et al 2008;Bednarek et al 2009;Clay et al 2009). Aliphatic GSL influence fitness of A. thaliana and related cruciferous species via their contribution to defense against herbivory (Mauricio 1998;Bidart-Bouzat and Kliebenstein 2008;Lankau and Kliebenstein 2009). Interestingly, the relationship between fitness and GSL is not linear and displays hallmarks of fluctuating and/ or balancing selection.…”

Section: N Atural Phenotypic Variation Within a Species Ormentioning

confidence: 99%

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Understanding the Evolution of Defense Metabolites in Arabidopsis thaliana Using Genome-wide Association Mapping

Chan¹,

Rowe²,

2010

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With the improvement and decline in cost of high-throughput genotyping and phenotyping technologies, genome-wide association (GWA) studies are fast becoming a preferred approach for dissecting complex quantitative traits. Glucosinolate (GSL) secondary metabolites within Arabidopsis spp. can serve as a model system to understand the genomic architecture of quantitative traits. GSLs are key defenses against insects in the wild and the relatively large number of cloned quantitative trait locus (QTL) controlling GSL traits allows comparison of GWA to previous QTL analyses. To better understand the specieswide genomic architecture controlling plant-insect interactions and the relative strengths of GWA and QTL studies, we conducted a GWA mapping study using 96 A. thaliana accessions, 43 GSL phenotypes, and $230,000 SNPs. Our GWA analysis identified the two major polymorphic loci controlling GSL variation (AOP and MAM) in natural populations within large blocks of positive associations encompassing dozens of genes. These blocks of positive associations showed extended linkage disequilibrium (LD) that we hypothesize to have arisen from balancing or fluctuating selective sweeps at both the AOP and MAM loci. These potential sweep blocks are likely linked with the formation of new defensive chemistries that alter plant fitness in natural environments. Interestingly, this GWA analysis did not identify the majority of previously identified QTL even though these polymorphisms were present in the GWA population. This may be partly explained by a nonrandom distribution of phenotypic variation across population subgroups that links population structure and GSL variation, suggesting that natural selection can hinder the detection of phenotype-genotype associations in natural populations. N ATURAL phenotypic variation within a species or population is largely quantitative, polygenic, and controlled by the interaction of environmental and genetic factors (Fisher 1930;Falconer and Mackay 1996;Lynch and Walsh 1998). Advances in both highthroughput genotyping and phenotyping has enabled the use of intraspecific natural variation to identify the molecular and genetic bases of complex traits such as disease resistance, growth and development and correspondingly provide a preliminary view of the ecological and evolutionary consequences of this variation. While quantitative trait locus (QTL) mapping has been the standard approach to studying complex traits in the past, its application to self-incompatible and longgeneration species has been limited by the labor and time required to generate and genotype mapping populations (Liu 1998;Lynch and Walsh 1998;Mauricio 2001). As such, the molecular basis of most quantitative traits remains unknown.Genome-wide association (GWA) mapping has become a popular alternative to QTL mapping in recent years for studying natural genetic variation. GWA identifies association between phenotypes and genotypes, at a genome-wide level, using ''unrelated'' individuals that have been simultaneously genoty...

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Section: Discussionmentioning

confidence: 93%

Section: N Atural Phenotypic Variation Within a Species Ormentioning

confidence: 99%

Understanding the Evolution of Defense Metabolites in Arabidopsis thaliana Using Genome-wide Association Mapping

Chan¹,

Rowe²,

2010

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“…This indicates that accessions enriched in butenyls, pentenyls, and their hydroxylated derivatives were protected from herbivores in France. In a field study in Ohio, European accessions enriched in alkenyl GSLs were less protected (32). This disparity suggests herbivore communities vary in their GSL preference.…”

Section: Significancementioning

confidence: 96%

Coselected genes determine adaptive variation in herbivore resistance throughout the native range of Arabidopsis thaliana

Brachi

Meyer

Villoutreix

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

120

176

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The "mustard oil bomb" is a major defense mechanism in the Brassicaceae, which includes crops such as canola and the model plant Arabidopsis thaliana. These plants produce and store blends of amino acid-derived secondary metabolites called glucosinolates. Upon tissue rupture by natural enemies, the myrosinase enzyme hydrolyses glucosinolates, releasing defense molecules. Brassicaceae display extensive variation in the mixture of glucosinolates that they produce. To investigate the genetics underlying natural variation in glucosinolate profiles, we conducted a large genomewide association study of 22 methionine-derived glucosinolates using A. thaliana accessions from across Europe. We found that 36% of among accession variation in overall glucosinolate profile was explained by genetic differentiation at only three known loci from the glucosinolate pathway. Glucosinolate-related SNPs were up to 490-fold enriched in the extreme tail of the genome-wide F ST scan, indicating strong selection on loci controlling this pathway. Glucosinolate profiles displayed a striking longitudinal gradient with alkenyl and hydroxyalkenyl glucosinolates enriched in the West. We detected a significant contribution of glucosinolate loci toward general herbivore resistance and lifetime fitness in common garden experiments conducted in France, where accessions are enriched in hydroxyalkenyls. In addition to demonstrating the adaptive value of glucosinolate profile variation, we also detected long-distance linkage disequilibrium at two underlying loci, GS-OH and GS-ELONG. Locally cooccurring alleles at these loci display epistatic effects on herbivore resistance and fitness in ecologically realistic conditions. Together, our results suggest that natural selection has favored a locally adaptive configuration of physically unlinked loci in Western Europe.Arabidopsis thaliana | glucosinolates | genome-wide association mapping | linkage disequilibrium | adaptation

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“…2008). Bidart‐Bouzat and Kliebenstein (2008) similarly associated intraspecific GS concentrations in 20 natural accessions of Arabidopsis with resistance against insects, but found a positive correlation between total GS concentration and the extent of the damage caused by specialists in field experiments.…”

Section: Introductionmentioning

confidence: 98%

“…2005; Clauss et al. 2006; Bidart‐Bouzat and Kliebenstein 2008; Poelman et al. 2008); several have indicated negative correlations between the constitutive and induced concentrations of GS for defense against lepidopteran generalist insects (Clauss et al.…”

Section: Introductionmentioning

confidence: 99%

Intraspecific variation in defense against a generalist lepidopteran herbivore in populations of Eruca sativa (Mill.)

Ogran

Landau

Hanin

et al. 2016

Ecology and Evolution

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Populations of Eruca sativa (Brassicaceae) from desert and Mediterranean (Med) habitats in Israel differ in their defense against larvae of the generalist Spodoptera littoralis but not the specialist Pieris brassicae. Larvae of the generalist insect feeding on plants of the Med population gained significantly less weight than those feeding on the desert plants, and exogenous application of methyl jasmonate (MJ) on leaves of the Med plants significantly reduced the level of damage created by the generalist larvae. However, MJ treatment significantly induced resistance in plants of the desert population, whereas the generalist larvae caused similar damage to MJ‐induced and noninduced plants. Analyses of glucosinolates and expression of genes in their synthesis pathway indicated that defense in plants of the Med population against the generalist insect is governed by the accumulation of glucosinolates. In plants of the desert population, trypsin proteinase inhibitor activity was highly induced in response to herbivory by S. littoralis. Analysis of genes in the defense‐regulating signaling pathways suggested that in response to herbivory, differences between populations in the induced levels of jasmonic acid, ethylene, and salicylic acid mediate the differential defenses against the insect. In addition, expression analysis of myrosinase‐associated protein NSP2 suggested that in plants of the desert population, glucosinolates breakdown products were primarily directed to nitrile production. We suggest that proteinase inhibitors provide an effective defense in the desert plants, in which glucosinolate production is directed to the less toxic nitriles. The ecological role of nitrile production in preventing infestation by specialists is discussed.

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Differential Levels of Insect Herbivory in the Field Associated with Genotypic Variation in Glucosinolates in Arabidopsis thaliana

Cited by 124 publications

References 42 publications

Understanding the Evolution of Defense Metabolites in Arabidopsis thaliana Using Genome-wide Association Mapping

Understanding the Evolution of Defense Metabolites in Arabidopsis thaliana Using Genome-wide Association Mapping

Coselected genes determine adaptive variation in herbivore resistance throughout the native range of Arabidopsis thaliana

Intraspecific variation in defense against a generalist lepidopteran herbivore in populations of Eruca sativa (Mill.)

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