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

Kawagoe T, Shimizu KK, Kakutani T, Kudoh H - PLoS ONE (2011)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Faculty of Science, Kobe University, Kobe, Japan. kawagoe.t@ecology.kyoto-u.ac.jp

ABSTRACT
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.

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Trichome variation in a natural population of A. halleri subsp. gemmifera.(A) Hairy plant. (B) Glabrous plant. (C) Flowering stems of a hairy and a glabrous plants. (D) Phaedon brassicae larvae foraging on flowers and flower buds.
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pone-0022184-g001: Trichome variation in a natural population of A. halleri subsp. gemmifera.(A) Hairy plant. (B) Glabrous plant. (C) Flowering stems of a hairy and a glabrous plants. (D) Phaedon brassicae larvae foraging on flowers and flower buds.

Mentions: In the present study, we examined fitness consequences and genetic basis of within-population variation in trichome production in Arabidopsis halleri subsp. gemmifera (Brassicaceae). In one natural population in Japan, nearly half of the plants develop trichomes on the surface of their leaves and flowering stems (referred to as hairy plants, Figure 1), whereas the other half completely lack trichomes (referred to as glabrous plants). This system provides a unique opportunity to study the genetic basis and ecological consequences of distinct morphological variation for the following reasons. First, previous studies in various species have shown that trichomes represent a defense trait against insect herbivores [21]–[23], including in A. thaliana [24], [25], A. lyrata [26]–[29] and other Brassicaceae species [30]. However, the detailed knowledge of ecological factors that allow the coexistence of distinct trichome phenotypes within a population is still limited. In particular, relative fitness for different phenotypes needs to be examined across multiple environmental conditions. Second, we are able to adopt a candidate gene approach because A. halleri subsp. gemmifera is a close relative of the model plant species A. thaliana [31], [32]. The molecular genetics of trichome development in A. thaliana is well understood, and genes involved in trichome production have been identified [33], [34]. As a candidate gene, we focused on a homologue of GLABROUS1 (GL1), which encodes a MYB-family transcription factor involved in the initiation of trichome development in A. thaliana [35]. GL1 has been found to be responsible for the glabrous phenotype in another population of A. halleri subsp. gemmifera [36]. GL1 polymorphisms have also been shown to be associated with trichome variation in natural populations of A. thaliana and A. lyrata [28], [37]. Furthermore, while most of trichome genes show pleiotropic effects on root hair development, GL1 is involved in the development of trichomes but not of root hair [33], [34]. Thus, GL1 is the most promising candidate for trichome variation in Arabidopsis relatives.


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

Kawagoe T, Shimizu KK, Kakutani T, Kudoh H - PLoS ONE (2011)

Trichome variation in a natural population of A. halleri subsp. gemmifera.(A) Hairy plant. (B) Glabrous plant. (C) Flowering stems of a hairy and a glabrous plants. (D) Phaedon brassicae larvae foraging on flowers and flower buds.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3139618&req=5

pone-0022184-g001: Trichome variation in a natural population of A. halleri subsp. gemmifera.(A) Hairy plant. (B) Glabrous plant. (C) Flowering stems of a hairy and a glabrous plants. (D) Phaedon brassicae larvae foraging on flowers and flower buds.
Mentions: In the present study, we examined fitness consequences and genetic basis of within-population variation in trichome production in Arabidopsis halleri subsp. gemmifera (Brassicaceae). In one natural population in Japan, nearly half of the plants develop trichomes on the surface of their leaves and flowering stems (referred to as hairy plants, Figure 1), whereas the other half completely lack trichomes (referred to as glabrous plants). This system provides a unique opportunity to study the genetic basis and ecological consequences of distinct morphological variation for the following reasons. First, previous studies in various species have shown that trichomes represent a defense trait against insect herbivores [21]–[23], including in A. thaliana [24], [25], A. lyrata [26]–[29] and other Brassicaceae species [30]. However, the detailed knowledge of ecological factors that allow the coexistence of distinct trichome phenotypes within a population is still limited. In particular, relative fitness for different phenotypes needs to be examined across multiple environmental conditions. Second, we are able to adopt a candidate gene approach because A. halleri subsp. gemmifera is a close relative of the model plant species A. thaliana [31], [32]. The molecular genetics of trichome development in A. thaliana is well understood, and genes involved in trichome production have been identified [33], [34]. As a candidate gene, we focused on a homologue of GLABROUS1 (GL1), which encodes a MYB-family transcription factor involved in the initiation of trichome development in A. thaliana [35]. GL1 has been found to be responsible for the glabrous phenotype in another population of A. halleri subsp. gemmifera [36]. GL1 polymorphisms have also been shown to be associated with trichome variation in natural populations of A. thaliana and A. lyrata [28], [37]. Furthermore, while most of trichome genes show pleiotropic effects on root hair development, GL1 is involved in the development of trichomes but not of root hair [33], [34]. Thus, GL1 is the most promising candidate for trichome variation in Arabidopsis relatives.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Faculty of Science, Kobe University, Kobe, Japan. kawagoe.t@ecology.kyoto-u.ac.jp

ABSTRACT
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.

Show MeSH
Related in: MedlinePlus