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The relationship between structurally different pyrrolizidine alkaloids and western flower thrips resistance in F(2) hybrids of Jacobaea vulgaris and Jacobaea aquatica.

Cheng D, Kirk H, Vrieling K, Mulder PP, Klinkhamer PG - J. Chem. Ecol. (2011)

Bottom Line: Among 37 individual PAs that were derived from four structural groups (senecionine-, jacobine-, erucifoline- and otosenine-like PAs), the N-oxides of jacobine, jaconine, and jacoline were negatively correlated with feeding damage caused by WFT, and the tertiary amines of jacobine, jaconine, jacoline, and other PAs did not relate to feeding damage.Multiple regression tests suggested that jacobine-like PAs play a greater role in WFT resistance than PAs from other structural groups.We found no evidence for synergistic effects of different PAs on WFT resistance.

View Article: PubMed Central - PubMed

Affiliation: Plant Ecology & Phytochemistry, Institute of Biology, Leiden University, the Netherlands. d.d.cheng@biology.leidenuniv.nl

ABSTRACT
Segregating plant hybrids often have more ecological and molecular variability compared to parental species, and are therefore useful for studying relationships between different traits, and the adaptive significance of trait variation. Hybrid systems have been used to study the relationship between the expression of plant defense compounds and herbivore susceptibility. We conducted a western flower thrips (WFT) bioassay using a hybrid family and investigated the relationship between WFT resistance and pyrrolizidine alkaloid (PA) variation. The hybrid family consisted of two parental (Jacobaea vulgaris and Jacobaea aquatica) genotypes, two F(1) genotypes, and 94 F(2) hybrid lines. The J. aquatica genotype was more susceptible to thrips attack than the J. vulgaris genotype, the two F(1) hybrids were as susceptible as J. aquatica, and susceptibility to WFT differed among F(2) hybrid lines: 69 F(2) lines were equally susceptible compared to J. aquatica, 10 F(2) lines were more susceptible than J. aquatica and 15 F(2) lines were as resistant as J. vulgaris or were intermediate to the two parental genotypes. Among 37 individual PAs that were derived from four structural groups (senecionine-, jacobine-, erucifoline- and otosenine-like PAs), the N-oxides of jacobine, jaconine, and jacoline were negatively correlated with feeding damage caused by WFT, and the tertiary amines of jacobine, jaconine, jacoline, and other PAs did not relate to feeding damage. Total PA concentration was negatively correlated with feeding damage. Among the four PA groups, only the total concentration of the jacobine-like PAs was negatively correlated with feeding damage. Multiple regression tests suggested that jacobine-like PAs play a greater role in WFT resistance than PAs from other structural groups. We found no evidence for synergistic effects of different PAs on WFT resistance. The relationship between PA variation and WFT feeding damage in the Jacobaea hybrids suggests a role for PAs in resistance to generalist insects.

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Principal component analysis (PCA) of the pyrrolizidine alkaloid (PA) profiles of F2 hybrids of Jacobaea aquatica and Jacobaea vulgaris. PCA was performed on the log-transformed genotypic mean concentrations of all individual PAs excluding six minor PAs that did not have normally distributed concentrations (see Table 2). One dot represents one of 94 F2 hybrid genotypes. Size of each dot represents mean WFT feeding damage for that genotype. The genotypic mean concentrations are the average value of the three to six replicates from the same genotype
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Fig3: Principal component analysis (PCA) of the pyrrolizidine alkaloid (PA) profiles of F2 hybrids of Jacobaea aquatica and Jacobaea vulgaris. PCA was performed on the log-transformed genotypic mean concentrations of all individual PAs excluding six minor PAs that did not have normally distributed concentrations (see Table 2). One dot represents one of 94 F2 hybrid genotypes. Size of each dot represents mean WFT feeding damage for that genotype. The genotypic mean concentrations are the average value of the three to six replicates from the same genotype

Mentions: Data Analysis We used general linear models to determine whether WFT resistance differed according to plant genotype. Feeding damage (dependent variable) was log- transformed to achieve normality, and plant genotype was defined as the independent variable with plant dry mass as covariate. Normal distributions and homogenous variances were confirmed by testing the residuals of the models using Shapiro tests and Bartlett tests respectively. Two models were set up: in the first, J. vulgaris was used as a reference, and in the second, J. aquatica was used. All other genotypes were compared to the reference in the model. Differences between the hybrid and parental genotypes were evaluated by using the regression coefficient matrices of the two models. In each matrix, the estimated coefficient of a hybrid indicated whether it had suffered more or less damage than the reference genotype, and the P value showed whether the difference was significant (Crawley, 2005). This is similar to a post-hoc test of an ANOVA model, however, such a post-hoc test includes all pair-wise comparisons between groups, and we were interested only in testing for differences between hybrid and parental genotypes. The difference between the two parental genotypes was also tested by using the same regression coefficient matrices. WFT resistance of each hybrid genotype was categorized according to these definitions: ND—no difference, leaf damage area of the hybrid was not different from that of both parents; A—additive, damage was intermediate between that of the parents; Ds—susceptible-dominant, damage was similar to that of the susceptible parent; Dr—resistant-dominant, damage was similar to that of the resistant parent, S—susceptible, damage was greater than that of the susceptible parent; R—resistant, damage was less than that of the resistant parent (Supplementary Table 1).For correlation tests and principal components analysis, we included only data from F2 genotypes, since we were interested in using the variation from this segregating generation to search for underlying relationships between WTF resistance and PA expression. We were not able to test for differences in these relationships between the different generations described in this study because only a limited number of genotypes were included from the parental and F1 generations. However, the parental and F1 plants provided reference points for WFT resistance comparison. We used log-transformed genotypic mean values of feeding damage and PA concentrations to carry out correlation analyses. Either Spearman (for six minor PAs that did not have normally distributed concentrations) or Pearson correlation tests were carried out to test the relationship between feeding damage and the concentrations of individual PAs, pooled concentrations of each of the four PA groups and total PA (see details in Table 2 and Fig. 3).Pyrrolizidine alkaloids from within structural groups were closely correlated with each other, and it was not possible, therefore, to investigate the interactions between them. The PAs from different structural groups, however, were generally expressed independently. The sum concentrations of the PAs from the four groups were not correlated with one another (Cheng et al., 2011). We used a multiple-regression model to test for interactions between the effects of different PA structural classes on feeding damage. In this model, feeding damage (represented by log-transformed genotypic mean values) was defined as the dependent variable, and the sum concentrations of each of the four PA structural groups (log-transformed and centered genotypic mean concentrations) were defined as independent variables.The principal component analysis (PCA) was carried out by using log-transformed genotypic mean concentrations of all individual PAs except the six minor PAs that did not have normally distributed concentrations. Compared to the major PAs, these six PAs were present at very low concentrations (on average less than 1% of total PA concentration). Pearson correlation tests were carried out between the first six principle components (PCs) from the PCA and feeding damage. In order to evaluate the contribution of each PA to each PC (in other words the loading), Pearson correlation tests were carried out between individual PAs and the first 3 PCs, since PCs four to six accounted for a low proportion of the total variation and were not correlated with WFT feeding damage. The P-values were adjusted using the sequential Bonferroni method when multiple tests were carried out.All analyses were conducted in R version 2.10.0 (R Development Core Team, 2009)


The relationship between structurally different pyrrolizidine alkaloids and western flower thrips resistance in F(2) hybrids of Jacobaea vulgaris and Jacobaea aquatica.

Cheng D, Kirk H, Vrieling K, Mulder PP, Klinkhamer PG - J. Chem. Ecol. (2011)

Principal component analysis (PCA) of the pyrrolizidine alkaloid (PA) profiles of F2 hybrids of Jacobaea aquatica and Jacobaea vulgaris. PCA was performed on the log-transformed genotypic mean concentrations of all individual PAs excluding six minor PAs that did not have normally distributed concentrations (see Table 2). One dot represents one of 94 F2 hybrid genotypes. Size of each dot represents mean WFT feeding damage for that genotype. The genotypic mean concentrations are the average value of the three to six replicates from the same genotype
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3197926&req=5

Fig3: Principal component analysis (PCA) of the pyrrolizidine alkaloid (PA) profiles of F2 hybrids of Jacobaea aquatica and Jacobaea vulgaris. PCA was performed on the log-transformed genotypic mean concentrations of all individual PAs excluding six minor PAs that did not have normally distributed concentrations (see Table 2). One dot represents one of 94 F2 hybrid genotypes. Size of each dot represents mean WFT feeding damage for that genotype. The genotypic mean concentrations are the average value of the three to six replicates from the same genotype
Mentions: Data Analysis We used general linear models to determine whether WFT resistance differed according to plant genotype. Feeding damage (dependent variable) was log- transformed to achieve normality, and plant genotype was defined as the independent variable with plant dry mass as covariate. Normal distributions and homogenous variances were confirmed by testing the residuals of the models using Shapiro tests and Bartlett tests respectively. Two models were set up: in the first, J. vulgaris was used as a reference, and in the second, J. aquatica was used. All other genotypes were compared to the reference in the model. Differences between the hybrid and parental genotypes were evaluated by using the regression coefficient matrices of the two models. In each matrix, the estimated coefficient of a hybrid indicated whether it had suffered more or less damage than the reference genotype, and the P value showed whether the difference was significant (Crawley, 2005). This is similar to a post-hoc test of an ANOVA model, however, such a post-hoc test includes all pair-wise comparisons between groups, and we were interested only in testing for differences between hybrid and parental genotypes. The difference between the two parental genotypes was also tested by using the same regression coefficient matrices. WFT resistance of each hybrid genotype was categorized according to these definitions: ND—no difference, leaf damage area of the hybrid was not different from that of both parents; A—additive, damage was intermediate between that of the parents; Ds—susceptible-dominant, damage was similar to that of the susceptible parent; Dr—resistant-dominant, damage was similar to that of the resistant parent, S—susceptible, damage was greater than that of the susceptible parent; R—resistant, damage was less than that of the resistant parent (Supplementary Table 1).For correlation tests and principal components analysis, we included only data from F2 genotypes, since we were interested in using the variation from this segregating generation to search for underlying relationships between WTF resistance and PA expression. We were not able to test for differences in these relationships between the different generations described in this study because only a limited number of genotypes were included from the parental and F1 generations. However, the parental and F1 plants provided reference points for WFT resistance comparison. We used log-transformed genotypic mean values of feeding damage and PA concentrations to carry out correlation analyses. Either Spearman (for six minor PAs that did not have normally distributed concentrations) or Pearson correlation tests were carried out to test the relationship between feeding damage and the concentrations of individual PAs, pooled concentrations of each of the four PA groups and total PA (see details in Table 2 and Fig. 3).Pyrrolizidine alkaloids from within structural groups were closely correlated with each other, and it was not possible, therefore, to investigate the interactions between them. The PAs from different structural groups, however, were generally expressed independently. The sum concentrations of the PAs from the four groups were not correlated with one another (Cheng et al., 2011). We used a multiple-regression model to test for interactions between the effects of different PA structural classes on feeding damage. In this model, feeding damage (represented by log-transformed genotypic mean values) was defined as the dependent variable, and the sum concentrations of each of the four PA structural groups (log-transformed and centered genotypic mean concentrations) were defined as independent variables.The principal component analysis (PCA) was carried out by using log-transformed genotypic mean concentrations of all individual PAs except the six minor PAs that did not have normally distributed concentrations. Compared to the major PAs, these six PAs were present at very low concentrations (on average less than 1% of total PA concentration). Pearson correlation tests were carried out between the first six principle components (PCs) from the PCA and feeding damage. In order to evaluate the contribution of each PA to each PC (in other words the loading), Pearson correlation tests were carried out between individual PAs and the first 3 PCs, since PCs four to six accounted for a low proportion of the total variation and were not correlated with WFT feeding damage. The P-values were adjusted using the sequential Bonferroni method when multiple tests were carried out.All analyses were conducted in R version 2.10.0 (R Development Core Team, 2009)

Bottom Line: Among 37 individual PAs that were derived from four structural groups (senecionine-, jacobine-, erucifoline- and otosenine-like PAs), the N-oxides of jacobine, jaconine, and jacoline were negatively correlated with feeding damage caused by WFT, and the tertiary amines of jacobine, jaconine, jacoline, and other PAs did not relate to feeding damage.Multiple regression tests suggested that jacobine-like PAs play a greater role in WFT resistance than PAs from other structural groups.We found no evidence for synergistic effects of different PAs on WFT resistance.

View Article: PubMed Central - PubMed

Affiliation: Plant Ecology & Phytochemistry, Institute of Biology, Leiden University, the Netherlands. d.d.cheng@biology.leidenuniv.nl

ABSTRACT
Segregating plant hybrids often have more ecological and molecular variability compared to parental species, and are therefore useful for studying relationships between different traits, and the adaptive significance of trait variation. Hybrid systems have been used to study the relationship between the expression of plant defense compounds and herbivore susceptibility. We conducted a western flower thrips (WFT) bioassay using a hybrid family and investigated the relationship between WFT resistance and pyrrolizidine alkaloid (PA) variation. The hybrid family consisted of two parental (Jacobaea vulgaris and Jacobaea aquatica) genotypes, two F(1) genotypes, and 94 F(2) hybrid lines. The J. aquatica genotype was more susceptible to thrips attack than the J. vulgaris genotype, the two F(1) hybrids were as susceptible as J. aquatica, and susceptibility to WFT differed among F(2) hybrid lines: 69 F(2) lines were equally susceptible compared to J. aquatica, 10 F(2) lines were more susceptible than J. aquatica and 15 F(2) lines were as resistant as J. vulgaris or were intermediate to the two parental genotypes. Among 37 individual PAs that were derived from four structural groups (senecionine-, jacobine-, erucifoline- and otosenine-like PAs), the N-oxides of jacobine, jaconine, and jacoline were negatively correlated with feeding damage caused by WFT, and the tertiary amines of jacobine, jaconine, jacoline, and other PAs did not relate to feeding damage. Total PA concentration was negatively correlated with feeding damage. Among the four PA groups, only the total concentration of the jacobine-like PAs was negatively correlated with feeding damage. Multiple regression tests suggested that jacobine-like PAs play a greater role in WFT resistance than PAs from other structural groups. We found no evidence for synergistic effects of different PAs on WFT resistance. The relationship between PA variation and WFT feeding damage in the Jacobaea hybrids suggests a role for PAs in resistance to generalist insects.

Show MeSH
Related in: MedlinePlus