Male gametophyte development in flowering plants: A story of quarantine and sacrifice

Abstract

Over 160 years ago, scientists made the first microscopic observations of angiosperm pollen. Unlike in animals, male meiosis in angiosperms produces a haploid microspore that undergoes one asymmetric division to form a vegetative cell and a generative cell. These two cells have distinct fates: the vegetative cell exits the cell cycle and elongates to form a tip-growing pollen tube; the generative cell divides once more in the pollen grain or within the growing pollen tube to form a pair of sperm cells. The concept that male germ cells are less active than the vegetative cell came from biochemical analyses and pollen structure anatomy early in the last century and is supported by the pollen transcriptome data of the last decade. However, the mechanism of how and when the transcriptional repression in male germ cells occurs is still not fully understood. In this review, we provide a brief account of the cytological and metabolic differentiation between the vegetative cell and male germ cells, with emphasis on the role of temporary callose walls, dynamic nuclear pore density, transcription repression, and histone variants. We further discuss the intercellular movement of small interfering RNA (siRNA) derived from transposable elements (TEs) and reexamine the function of TE expression in male germ cells.

Introduction

Male gametophyte (pollen) development of angiosperms (flowering plants) takes place in the anthers of a flower and can be divided into two phases — microsporogenesis and microgametogenesis. During microsporogenesis, each diploid pollen mother cell (PMC) undergoes meiotic divisions, giving rise to four haploid microspores in tetrad arrangement. Following the release of microspores from tetrads, pollen development enters microgametogenesis. The released microspores experience size enlargement and nuclear polarization, then undergo an asymmetrical division (pollen mitosis I, PMI), generating a larger vegetative cell and a smaller generative cell, engulfed in the vegetative cell. The generative cell completes a second division (pollen mitosis II, PMII) to produce two sperm cells. The vegetative cell acts as the companion cell of male germ cells (generative and sperm cells) to support their development and to transport sperm cells for double fertilization via pollen tubes. Common model plants such as Arabidopsis, rice, and maize shed tricellular pollen consisting of two sperm cells and one vegetative cell. However, in the natural world, about 70 % of flowering plants such as tomato, Lilium, and Medicago disperse pollen at the bicellular stage containing one generative cell and one vegetative cell (Brewbaker, 1967; Williams et al., 2014) (Fig. 1). The development of angiosperm male germ cells occurs in a relatively closed space, making it a unique system for developmental biology. Extensive research has been conducted to understand cell fate determination, cell differentiation, and cell cycle. Particularly in recent years, the combination of reproductive mutants, cell sorting, and high-throughput sequencing has been providing a more complete view of pollen development. Accumulating evidence suggests the reprogramming of gene expression involves histone variants, small RNA, and DNA methylation. Transposable elements (TE) reactivation in the vegetative cell has been proposed to generate siRNA that moves to the sperm cells to inhibit TE expression across generations. Many excellent reviews have summarized this progress from the perspectives of evolution (Hackenberg and Twell, 2019; Hisanaga et al., 2019), germ cell formation (Berger and Twell, 2011; Borg et al., 2009; Chang et al., 2011; Schmidt et al., 2015; Twell, 2011), cellular processes (Borg and Berger, 2015; Hafidh et al., 2016), transcriptome (Rutley and Twell, 2015; Schmidt et al., 2012), and small RNA (Borges et al., 2011; Wu and Zheng, 2019). Here, we focus on the functional differentiation between the vegetative cell and germ cells, and how metabolic and transcription repression occurs in the germ cells. We also discuss the current model of TE silencing in germ cells via vegetative-cell-derived TE-siRNAs.