A Tug-of-War Model Explains the Saltatory Sperm Cell Movement in Arabidopsis thaliana Pollen Tubes by Kinesins With Calponin Homology Domain.

Saskia Schattner,Eva Höppe,Fabian Munder,Wilhelm J Walter,Jan Schattner

doi:10.3389/fpls.2020.601282

Abstract

Upon pollination, two sperm cells are transported inside the growing pollen tube toward the apex. One sperm cell fertilizes the egg cell to form the zygote, while the other fuses with the two polar nuclei to form the triploid endosperm. In Arabidopsis thaliana, the transport of the two sperm cells is characterized by sequential forward and backward movements with intermediate pauses. Until now, it is under debate which components of the plant cytoskeleton govern this mechanism. The sperm cells are interconnected and linked to the vegetative nucleus via a cytoplasmic projection, thus forming the male germ unit. This led to the common hypothesis that the vegetative nucleus is actively transported via myosin motors along actin cables while pulling along the sperm cells as passive cargo. In this study, however, we show that upon occasional germ unit disassembly, the sperm cells are transported independently and still follow the same bidirectional movement pattern. Moreover, we found that the net movement of sperm cells results from a combination of both longer and faster runs toward the pollen tube apex. We propose that the observed saltatory movement can be explained by the function of kinesins with calponin homology domain (KCH). This subgroup of the kinesin-14 family actively links actin filaments and microtubules. Based on KCH's specific properties derived from in vitro experiments, we built a tug-of-war model that could reproduce the characteristic sperm cell movement in pollen tubes.

Highlights

A major step in the evolution of land plants was the shift from a gametophyte-dominant to a sporophyte-dominant life cycle in flowering plants which represent more than 90% of all land plants today
We found a net movement of the sperm cells from the pollen grain toward the tube apex in all observed pollen
We found that sperm cells are transported in Arabidopsis thaliana pollen tubes in a saltatory manner

Summary

Introduction

A major step in the evolution of land plants was the shift from a gametophyte-dominant to a sporophyte-dominant life cycle in flowering plants which represent more than 90% of all land plants today. The sperm cells have to be transported toward the ovary through the female tissue to fertilize the egg cell and the central cell of the megagametophyte This challenge is met by the displacement of self-propelling sperm cells by pollen-mediated transport of the male gametes. In most flowering plants including the model plant Arabidopsis thaliana, the sperm cells travel together and are interconnected with each other as well as with the vegetative nucleus by a cytoplasmic projection (Lalanne and Twell, 2002) This complex which is composed of the two sperm cells and the vegetative nucleus is called the male germ unit (Jensen and Fisher, 1970; Russell and Cass, 1981). During transport through the pollen tube, the sperm cells do not move continuously in the direction of the apex but perform saltatory back and forth movements (Hamamura et al, 2011)

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