Herkogamy and Its Effects on Mating Patterns in Arabidopsis thaliana

Yonghai Luo,Alex Widmer,Hector Candela

doi:10.1371/journal.pone.0057902

Abstract

The evolution of mating systems, which exhibit an extraordinary diversity in flowering plants, is of central interest in plant biology. Herkogamy, the spatial separation of sexual organs within flowers, is a widespread floral mechanism that is thought to be an adaptive trait reducing self-pollination in hermaphroditic plants. In contrast with previous studies of herkogamy that focused on plants with relatively large floral displays, we here characterized herkogamy in Arabidopsis thaliana, a model plant with a strong selfing syndrome. Developmental features, reproductive consequences, and genetic architecture of herkogamy were exploited using naturally variable A. thaliana accessions, under both greenhouse and natural conditions. Our results demonstrate that the degree of herkogamy can strongly influence the mating patterns of A. thaliana: approach herkogamy can effectively promote outcrossing, no herkogamy is also capable of enhancing the opportunity for outcrossing, and reverse herkogamy facilitates efficient self-pollination. In addition, we found that the expression of herkogamy in A. thaliana was environment-dependent and regulated by multiple quantitative trait loci. This study reveals how minor modifications in floral morphology may cause dramatic changes in plant mating patterns, provides new insights into the function of herkogamy, and suggests the way for dissecting the genetic basis of this important character in a model plant.

Highlights

Plant mating systems are highly diverse and have profound effects on reproductive success under variable ecological conditions
To assess the effects of approach herkogamy on mating patterns in BRA and SIM under natural conditions, we conducted field experiments in which we grew BRA and SIM together with 13 control accessions that exhibit reverse herkogamy (Table S1). Because both BRA and SIM were originally collected at high altitudes, we considered whether the expression of approach herkogamy in these two accessions was related to climatic conditions at different altitudes, and grew one experimental population at high altitude and one at low altitude
Natural genetic variation in outcrossing in A. thaliana Given that A. thaliana is generally considered to be a highly selfing plant, the outcrossing rates detected in our experimental populations were surprisingly high and variable

Summary

Introduction

Plant mating systems are highly diverse and have profound effects on reproductive success under variable ecological conditions. A number of studies have reported evidence for a monotonically increasing relationship between the degree of herkogamy and outcrossing rate across diverse plant species, including Nicotiana [8], Clarkia [9], Turnera [10], Mimulus [11], Aquilegia [12], and Datura [13], there are exceptions (e.g., Narcissus, [14,15]). These self-compatible plant species are commonly with relatively large floral displays and, in these cases, the role of herkogamy in promoting outcrossing may be complex. To clarify the role of herkogamy in promoting outcrossing, ideally it requires a highly selfing species with phenotypic variation in herkogamy and with a small floral display

Methods

Results

Conclusion