Arabidopsis FIM5 decorates apical actin filaments and regulates their organization in the pollen tube.

Meng Zhang,Xiaolu Qu,Shanjin Huang,Ruihui Zhang

doi:10.1093/jxb/erw160

Abstract

The actin cytoskeleton is increasingly recognized as a major regulator of pollen tube growth. Actin filaments have distinct distribution patterns and dynamic properties within different regions of the pollen tube. Apical actin filaments are highly dynamic and crucial for pollen tube growth. However, how apical actin filaments are generated and properly constructed remains an open question. Here we showed that Arabidopsis fimbrin5 (FIM5) decorates filamentous structures throughout the entire tube but is apically concentrated. Apical actin structures are disorganized to different degrees in the pollen tubes of fim5 loss-of-function mutants. Further observations suggest that apical actin structures are not constructed properly because apical actin filaments cannot be maintained at the cortex of fim5 pollen tubes. Actin filaments appeared to be more curved in fim5 pollen tubes and this was confirmed by measurements showing that the convolutedness and the rate of change of convolutedness of actin filaments was significantly increased in fim5 pollen tubes. This suggests that the rigidity of the actin filaments may be compromised in fim5 pollen tubes. Further, the apical cell wall composition is altered, implying that tip-directed vesicle trafficking events are impaired in fim5 pollen tubes. Thus, we found that FIM5 decorates apical actin filaments and regulates their organization in order to drive polarized pollen tube growth.

Highlights

Pollen tube growth is an essential step during flowering plant reproduction (Lord and Russell, 2002; Berger et al, 2008; McCormick, 2013) and a central question in plant reproductive biology is how the growth of the pollen tube is precisely regulated (Franklin-Tong, 1999; Hepler et al, 2001)
We noted that FIM5 concentrates at the pollen tube tip (Fig. 1A, B) which implies that FIM5 may play an even more prominent role in regulating apical filament organization than its defined role in organizing shank-oriented actin bundles (Wu et al, 2010)
Consistent with the notion that apical actin filaments are less dynamic in fim5 pollen tubes, we found that actin filament elongation and depolymerization rates and severing frequency were decreased in fim5 pollen tubes compared with WT pollen tubes (Fig. 4C)

Summary

Introduction

Pollen tube growth is an essential step during flowering plant reproduction (Lord and Russell, 2002; Berger et al, 2008; McCormick, 2013) and a central question in plant reproductive biology is how the growth of the pollen tube is precisely regulated (Franklin-Tong, 1999; Hepler et al, 2001). The precise organization and function of apical actin structures are not well understood, it is assumed that the apical actin structure is crucial for vesicle fusion and consequent apical cell wall patterning (Lee et al, 2008; Kroeger et al, 2009; Cheung et al, 2010; Zhang et al, 2010b; Bou Daher and Geitmann, 2011; Qin and Yang, 2011; Hepler et al, 2013; Wang et al, 2013; Rounds et al, 2014). How pollen tubes generate and maintain distinct actin structures using the same building blocks within the common cytoplasm remains an open question

Methods

Results

Conclusion