Trichome production and spatiotemporal variation in herbivory in the perennial herb Arabidopsis lyrata

Allocation theory suggests that the optimal level of resistance against herbivores should vary with the risk of herbivory if allocation to resistance is costly. The perennial herb Arabidopsis lyrata has a genetically based polymorphism for trichome production and occurs in a glabrous and a trichome-producing form. Leaf trichomes (hairs) can protect plants against insect herbivores, and may increase tolerance to drought and UV-radiation. To examine the functional significance of trichome production, we documented the frequency of glabrous plants and damage by insect herbivores in 30 A. lyrata populations in Sweden and Norway. The proportion of glabrous plants ranged from 0.10 to 0.71 (median=0.44) in polymorphic populations; 7 of 12 populations in Norway and 14 of 18 populations in Sweden were monomorphic glabrous, i.e. with fewer than 5% trichome-producing plants. The mean proportion of the leaf area removed by herbivores varied substantially among populations and years. With few exceptions, glabrous plants were more damaged than trichome-producing plants in polymorphic populations. The intensity of herbivory quantified as the mean damage to glabrous plants tended to be higher in polymorphic populations than in populations monomorphic for the glabrous morph and was higher in Sweden than in Norway. In Norway, both the magnitude of herbivore damage and the frequency of trichome-producing plants tended to decrease with increasing altitude. The results indicate that leaf trichomes contribute to resistance against herbivorous insects in A. lyrata , and suggest that herbivore-mediated selection contributes to the maintenance of the polymorphism in trichome production.     

Population structure in Arabidopsis lyrata: evidence for divergent selection on trichome production

Leaf trichomes may serve several biological functions including protection against herbivores, drought, and UV radiation; and their adaptive value can be expected to vary among environments. The perennial, self-incompatible herb Arabidopsis lyrata is polymorphic for trichome production, and occurs in a glabrous and a trichome-producing form. Controlled crosses indicate that the polymorphism is governed by a single gene, with trichome production being dominant. We examined the hypothesis that trichome production is subject to divergent selection (i.e., directional selection favoring different phenotypes in different populations) by comparing patterns of variation at the locus coding for glabrousness and at eight putatively neutral isozyme loci in Swedish populations of A. lyrata. The genetic diversity (He) and allele number at isozyme loci tended to increase with population size and decreased with latitude of origin, whereas genetic diversity at the locus coding for glabrousness did not vary with population size and increased with latitude of origin. The degree of genetic differentiation at the glabrousness locus was much higher than that at isozyme loci. Genetic identity at isozyme loci was negatively related to geographic distance, suggesting isolation by distance. In contrast, there was no significant correlation between genetic identity at the glabrousness locus and at isozyme loci. The results are consistent with the hypothesis that divergent selection contributes to population differentiation in trichome production in A. lyrata.     

Cost of trichome production and resistance to a specialist insect herbivore in <Emphasis Type="Italic">Arabidopsis lyrata</Emphasis>

Theory predicts that trade-offs between resistance to herbivory and other traits positively affecting fitness can maintain genetic variation in resistance within plant populations. In the perennial herb Arabidopsis lyrata, trichome production is a resistance trait that exhibits both qualitative and quantitative variation. Using a paternal half-sib design, we conducted two greenhouse experiments to ask whether trichomes confer resistance to oviposition and leaf herbivory by the specialist moth Plutella xylostella, and to examine potential genetic constraints on evolution of increased resistance and trichome density. In addition, we examined whether trichome production is induced by insect herbivory. We found strong positive genetic and phenotypic correlations between leaf trichome density and resistance to leaf herbivory, demonstrating that the production of leaf trichomes increases resistance to leaf damage by P. xylostella. Also resistance to oviposition tended to increase with increasing leaf trichome density, but genetic and phenotypic correlations were not statistically significant. Trichome density and resistance to leaf herbivory were negatively correlated genetically with plant size in the absence of herbivores, but not in the presence of herbivores. There was no evidence of increased trichome production after leaf damage by P. xylostella. The results suggest that trichome production and resistance to leaf herbivory are associated with a cost and that the direction of selection on resistance and trichome density depends on the intensity of herbivory.     

Ontogenetics of QTL: the genetic architecture of trichome density over time in Arabidopsis thaliana

Although much is known about the molecular genetic basis of trichome development in Arabidopsis thaliana, less is known about the underlying genetic basis of continuous variation in a trait known to be of adaptive importance: trichome density. The density of leaf trichomes is known to be a major determinant of herbivore damage in natural populations of A. thaliana and herbivores are a significant selective force on genetic variation for trichome density. A number of developmental changes occur during ontogeny in A. thaliana, including changes in trichome density. I used multiple interval mapping (MIM) analysis to identify QTL responsible for trichome density on both juvenile leaves and adult leaves in replicate, independent trials and asked whether those QTL changed with ontogeny. In both juvenile and adult leaves, I detected a single major QTL on chromosome 2 that explained much of the genetic variance. Although additional QTL were detected, there were no consistent differences in the genetic architecture of trichome density measured on juvenile and adult leaves. The finding of a single QTL of major effect for a trait of known adaptive importance suggests that genes of major effect may play an important role in adaptation.     

Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana

The annual plant Arabidopsis thaliana is widely used as a model system in molecular genetics, but little is known about populations in the field. In this experimental field study of natural populations of Arabidopsis, I tested the assumption that plant resistance has fitness costs. Models of the evolution of resistance assume a cost, which is envisioned as a reduction in fitness in the absence of natural enemies, such as insect herbivores and pathogens. The presumed basis of this cost is the diversion of limiting resources away from present and future growth and reproduction. Recent failures to detect allocation costs of resistance to herbivores have raised questions about whether costs exist and, thus, about the appropriateness of theories that postulate such costs. I found genetic variation for two traits commonly thought to function as resistance characters: trichome density and total glucosinolate concentration. Under field conditions, these characters both reduced damage by the natural assemblage of herbivores and exhibited significant fitness costs.     

Interactive effects of jasmonic acid, salicylic acid, and gibberellin on induction of trichomes in Arabidopsis

Leaf trichomes protect plants from attack by insect herbivores and are often induced following damage. Hormonal regulation of this plant induction response has not been previously studied. In a series of experiments, we addressed the effects of artificial damage, jasmonic acid, salicylic acid, and gibberellin on induction of trichomes in Arabidopsis. Artificial damage and jasmonic acid caused significant increases in trichome production of leaves. The jar1-1 mutant exhibited normal trichome induction following treatment with jasmonic acid, suggesting that adenylation of jasmonic acid is not necessary. Salicylic acid had a negative effect on trichome production and consistently reduced the effect of jasmonic acid, suggesting negative cross-talk between the jasmonate and salicylate-dependent defense pathways. Interestingly, the effect of salicylic acid persisted in the nim1-1 mutant, suggesting that the Npr1/Nim1 gene is not downstream of salicylic acid in the negative regulation of trichome production. Last, we found that gibberellin and jasmonic acid had a synergistic effect on the induction of trichomes, suggesting important interactions between these two compounds.     

Genetic basis of trichome production in Arabidopsis lyrata

Leaf trichomes may protect plants against herbivorous insects, and may increase tolerance to drought and UV-radiation. The perennial herb Arabidopsis lyrata (Brassicaceae) is polymorphic for trichome production and occurs in a glabrous and trichome-producing form. In addition, there is quantitative variation in trichome density among trichome-producing plants. To examine the genetic basis of glabrousness, we conducted controlled crosses with plants originating from two natural populations in Sweden (one polymorphic for trichome-production, and one consisting of glabrous plants only). In addition, we estimated the heritability of trichome number from parent-offspring regressions for plants originating from the polymorphic population. Crosses between glabrous plants resulted in glabrous offspring only, whereas crosses between glabrous and trichome-producing plants, and crosses between trichome-producing individuals, resulted in either all trichome-producing offspring or both phenotypes. In segregating crosses between trichome-producing plants, the ratio of glabrous:trichome-producing offspring did not deviate significantly from 1:3, while in segregating crosses between glabrous and trichome-producing individuals the ratio did in most cases not deviate from 1:1. Within- and between-population crosses gave similar results. The heritability of trichome number estimated from regression of offspring on mid-parent was high (h2 +/- SE, 0.65 +/- 0.15). The results suggest that glabrousness is inherited in a simple Mendelian fashion, with the allele coding for trichome production being dominant over that for glabrousness. They further indicate that glabrousness is due to a mutation at the same locus in both populations.     

No trade-off between trichome production and tolerance to leaf and inflorescence damage in a natural population of Arabidopsis lyrata

Aims Early models of plant defense conceived resistance and tolerance to herbivore damage as mutually exclusive strategies. Support for this idea has been equivocal and studies on these two strategies are still needed to understand the evolution of defenses in natural populations. In Arabidopsis lyrata, the production of trichomes, a documented resistance trait, has been associated with a fitness cost in the absence of herbivores. We examined whether trichome production is also associated with reduced tolerance to simulated herbivore damage.Methods We conducted a field experiment in a natural Swedish population of A. lyrata where we inflicted leaf (0 vs. 50% of the area of each leaf removed) and inflorescence damage (0 vs. 50% of inflorescences removed) to trichome-producing and glabrous plants in a factorial design. We examined the response (survival, growth and reproduction) of the plants to the imposed damage over 2 years.Important findings Trichome-producing plants were not less tolerant than glabrous plants to simulated herbivore damage (no significant morph × leaf damage or morph × inflorescence damage interactions). Inflorescence and leaf damage had independent negative effects on the performance of damaged plants. Leaf damage reduced rosette size the year of damage, but effects on reproductive output in the year of damage, and on survival and reproductive performance the following year were weak and not statistically significant. Inflorescence damage significantly reduced the number of flowers, fruits and seeds the year of damage, but not in the following year. Irrespective of morph, the study population was more tolerant to leaf than to inflorescence damage. The results indicated no trade-off between trichome production and tolerance, suggesting that these two defense mechanisms have the potential to evolve independently in this A. lyrata population.     

Costs of glandular trichomes in Datura wrightii: a three-year study

Models accounting for genetic variation for resistance to herbivores within plant populations often postulate a balance between the costs of that resistance and its benefits. The production of glandular trichomes by Datura wrightii was shown to be costly in a previous one-year study because plants producing glandular trichomes (sticky plants), a factor conferring resistance to some insect herbivores, also produced 45% fewer seeds than plants producing nonglandular trichomes (velvety plants) when grown in a common garden. Because sticky plants tended to be larger than velvety plants but produced fewer seed capsules, we postulated an allocation trade-off in which velvety plants are more reproduction-dominated whereas sticky plants are more growth-dominated. If a greater commitment to vegetative growth eventually allows sticky plants to compensate for reduced seed production, we would expect a reduction or elimination of the cost of resistance over time in this perennial plant. We monitored growth, survival, and seed production of plants from defined crosses of local populations for three years in a common garden when exposed to and protected from herbivores, and with and without supplemental water. The majority of plants exposed to herbivores had died by the end of the study. We used standard life-table methods to determine the net reproductive rate (R0) and the finite rate of increase (lambda) of plants of each trichome type. After three years, when plants were protected from herbivores, sticky plants were 187-245% larger than velvety plants, depending upon irrigation treatment, but sticky plants continued to be less efficient in producing seeds per unit of canopy volume. Even though the total seed production of sticky plants eventually equaled that of velvety plants, the advantage of earlier reproduction by velvety plants increased lambda by 55-230% over that of sticky plants, depending upon herbivore and irrigation treatment. Exposure to herbivores reduced lambda by 69-83%, depending upon plant type and irrigation treatment, whereas supplemental irrigation increased lambda by 29-175%, depending upon plant type and exposure to herbivores. Although there was a large allocation trade-off between growth and reproduction, the benefits of such a trade-off did not emerge before most plants were killed by herbivores. The cost of producing glandular trichomes strictly for herbivore resistance continued to exceed its benefits, and in the absence of other, unmeasured benefits from the suite of life-history characters associated with glandular trichome production, natural selection is expected to eliminate this costly resistance trait from D. wrightii populations.     

Variation in trichome density and resistance against a specialist insect herbivore in natural populations of Arabidopsis thaliana

Abstract.  1. The annual herb Arabidopsis thaliana is a prime model organism of plant molecular genetics, and is currently used to explore the molecular basis of resistance to herbivores. However, both the magnitude and the causes of variation in resistance among natural populations of A. thaliana are poorly known. The hypotheses (a) that resistance to a specialist herbivore, the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), is positively related to the density of leaf trichomes, and (b) that oviposition preference by female moths is positively correlated to larval performance on different populations and maternal lines of the host plant were examined.
2. Variation in leaf trichome density and resistance to P. xylostella within and among six natural populations of A. thaliana in Sweden was quantified . Resistance was quantified by examining the number of eggs laid on plants exposed to ovipositing female moths and by monitoring larval development on plants of different origin.
3. Trichome density varied significantly among populations; for 4-week-old plants (exposed to ovipositing moths), it also varied significantly among maternal families within populations. The rate of oviposition varied significantly both among populations and among families within populations. This variation could partly be explained by a negative relationship between trichome density and egg number, and a positive relationship between plant size and egg number. Time to pupation, pupal mass, and time to adult eclosion did not vary among populations or maternal lines of the host plant, and offspring performance was not related to P. xylostella oviposition preference . The results indicate that A. thaliana populations may respond to selection for increased resistance to P. xylostella , and suggest that trichome production contributes to resistance against this specialist herbivore.     

Trichome production and variation in young plant resistance to the specialist insect herbivore Plutella xylostella among natural populations of Arabidopsis lyrata

The strength of plant‐herbivore interactions varies spatially and through plant ontogeny, which may result in variable selection on plant defense, both among populations and life‐history stages. To test whether populations have diverged in herbivore resistance at an early plant stage, we quantified oviposition preference and larval feeding by Plutella xylostella (L.) (Lepidoptera: Plutellidae) on young (5–6 weeks old) Arabidopsis lyrata (L.) O'Kane & Al‐Shehbaz (Brassicaceae) plants, originating from 12 natural populations, six from Sweden and six from Norway. Arabidopsis lyrata can be trichome‐producing or glabrous, with glabrous plants usually receiving more damage from insect herbivores in natural populations. We used the six populations polymorphic for trichome production to test whether resistance against P. xylostella differs between the glabrous and the trichome‐producing morph among young plants. There was considerable variation among populations in the number of eggs received and the proportion of leaf area consumed by P. xylostella, but not between regions (Sweden vs. Norway) or trichome morphs. Rosette size explained a significant portion of the variation in oviposition and larval feeding. The results demonstrate that among‐population variation in resistance to insect herbivory can be detected among very young individuals of the perennial herb A. lyrata. They further suggest that trichome densities are too low at this plant developmental stage to contribute to resistance, and that the observed among‐population variation in resistance is related to differences in other plant traits.     

Coexistence of trichome variation in a natural plant population: a combined study using ecological and candidate gene approaches

The coexistence of distinct phenotypes within populations has long been investigated in evolutionary ecology. Recent studies have identified the genetic basis of distinct phenotypes, but it is poorly understood how the variation in candidate loci is maintained in natural environments. In this study, we examined fitness consequences and genetic basis of variation in trichome production in a natural population of Arabidopsis halleri subsp. gemmifera. Half of the individuals in the study population produced trichomes while the other half were glabrous, and the leaf beetle Phaedon brassicae imposed intensive damage to both phenotypes. The fitness of hairy and glabrous plants showed no significant differences in the field during two years. A similar result was obtained when sibling hairy and glabrous plants were transplanted at the same field site, whereas a fitness cost of trichome production was detected under a weak herbivory condition. Thus, equivalent fitness of hairy and glabrous plants under natural herbivory allows their coexistence in the contemporary population. The pattern of polymorphism of the candidate trichome gene GLABROUS1 (GL1) showed no evidence of long-term maintenance of trichome variation within the population. Although balancing selection under fluctuating biotic environments is often proposed to explain the maintenance of defense variation, the lack of clear evidence of balancing selection in the study population suggests that other factors such as gene flow and neutral process may have played relatively large roles in shaping trichome variation at least for the single population level.     

植物不同类型表皮毛调控模型研究进展

表皮毛是植物地上部分表皮细胞向外突出延伸的特化毛状结构,不仅可以保护植物免受病虫的危害,还具有一定的经济和药用价值,对其调控的分子机制的阐明有利于植物的分子设计育种和遗传改良。近年来,模式植物拟南芥表皮毛形成的调控模式基本被阐明,其他植物表皮毛的调控机制也取得很大进展。鉴于此,文中综述了拟南芥和棉花(单细胞表皮毛)及番茄和青蒿(多细胞表皮毛)在基因和激素水平上对表皮毛的发育调控,同时简要介绍了其他典型单、双子叶植物表皮毛相关的研究进展,最后,展望了植物表皮毛的研究方向和应用前景。     

Within and between generation phenotypic plasticity in trichome density of Mimulus guttatus

Mimulus guttatus (yellow monkeyflower) frequently produce glandular trichomes, a trait that may resist herbivory. Constitutive production of trichomes is variable both within and among populations of M. guttatus and most of this variation is genetic. This study demonstrates that damage on early leaves can induce increased trichome production on later leaves, a plastic response that is likely adaptive. Moreover, this study shows that this induction can be maternally transmitted, increasing trichome density in progeny before they experience herbivory. This transgenerational response must involve a yet undescribed epigenetic mechanism. These experiments also show genetic variation among plants in the capacity for both within and between plant generation induction. Despite the clear evolutionary importance of variation in constitutive and induced herbivory-resistance traits, few other studies have noted genetic variation in both within a plant species.     

Defensive role of leaf trichomes in resistance to herbivorous insects in Datura stramonium

This study assessed the role of leaf trichome density as a component of resistance to herbivores, in six populations of Datura stramonium. Phenotypic selection on plant resistance was estimated for each population. A common garden experiment was carried out to determine if population differences in leaf trichome density are genetically based. Among population differences in leaf trichome density, relative resistance and fitness were found. Leaf trichome density was strongly positively correlated to resistance across populations. In 5 out of 6 populations, trichome density was related to resistance, and positive directional selection on resistance to herbivores was detected in three populations. Differences among populations in mean leaf trichome density in the common garden suggest genetic differentiation for this character in Datura stramonium. The results are considered in the light of the adaptive role of leaf trichomes as a component of defence to herbivores, and variable selection among populations.