Fertilization Recovery after Defective Sperm Cell Release in Arabidopsis

Ryushiro D Kasahara,David Twell,Tetsuya Higashiyama,Daisuke Maruyama,Yuki Hamamura,Takashi Sakakibara

doi:10.1016/j.cub.2012.03.069

Ryushiro D Kasahara, David Twell + Show 4 more

Open Access

https://doi.org/10.1016/j.cub.2012.03.069

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Journal: Current Biology	Publication Date: May 17, 2012
Citations: 116	License type: cc-by

Affiliation: University of Leicester, Nagoya University

Abstract

In animal fertilization, multiple sperms typically arrive at an egg cell to "win the race" for fertilization. However, in flowering plants, only one of many pollen tubes, conveying plant sperm cells, usually arrives at each ovule that harbors an egg cell. Plant fertilization has thus been thought to depend on the fertility of a single pollen tube. Here we report a fertilization recovery phenomenon in flowering plants that actively rescues the failure of fertilization of the first mutant pollen tube by attracting a second, functional pollen tube. Wild-type (WT) ovules of Arabidopsis thaliana frequently (∼80%) accepted two pollen tubes when entered by mutant pollen defective in gamete fertility. In typical flowering plants, two synergid cells on the side of the egg cell attract pollen tubes, one of which degenerates upon pollen tube discharge. By semi-in vitro live-cell imaging we observed that fertilization was rescued when the second synergid cell accepted a WT pollen tube. Our results suggest that flowering plants precisely control the number of pollen tubes that arrive at each ovule and employ a fertilization recovery mechanism to maximize the likelihood of successful seed set.

Highlights

We investigated duo pollen 1 [14], duo3-1 [13], and generative cell specific 1 [10] mutants because they have defective male gametes leading to failure of fertilization
We conclude that the recovery of fertilization is limited to the second pollen tube, indicating that there is no third chance for fertilization in two-synergid celled plants
Overall, we have unveiled a fertilization recovery system that allows plants to restore ovule fertility after initial failure of fertilization within the ovule. Further investigation of this phenomenon could advance the understanding of how natural populations of sympatric species are maintained

Summary

Introduction

We observed that 50.0% 6 4.9% (mean 6 SD, n = 12 pistils) of developing seeds (Figure 1E) were fertilized by single pollen tube insertions, which would result from fertilization by pollen carrying the WT allele. Our data indicated that undeveloped seeds penetrated by two pollen tubes arise when first and second pollen tubes each carrying duo3-2 fail to fertilize.

Results

Conclusion