BURSTING POLLEN is required to organize the pollen germination plaque and pollen tube tip in Arabidopsis thaliana

Abstract

Summary Pollen germination may occur via the so‐called germination pores or directly through the pollen wall at the site of contact with the stigma. In this study, we addressed what processes take place during pollen hydration (i.e. before tube emergence), in a species with extra‐poral pollen germination, Arabidopsis thaliana. A T‐DNA mutant population was screened by segregation distortion analysis. Histological and electron microscopy techniques were applied to examine the wild‐type and mutant phenotypes. Within 1 h of the start of pollen hydration, an intine‐like structure consisting of cellulose, callose and at least partly de‐esterified pectin was formed at the pollen wall. Subsequently, this ‘germination plaque’ gradually extended and opened up to provide passage for the cytoplasm into the emerging pollen tube. BURSTING POLLEN (BUP) was identified as a gene essential for the correct organization of this plaque and the tip of the pollen tube. BUP encodes a novel Golgi‐located glycosyltransferase related to the glycosyltransferase 4 (GT4) subfamily which is conserved throughout the plant kingdom. Extra‐poral pollen germination involves the development of a germination plaque and BUP defines the correct plastic‐elastic properties of this plaque and the pollen tube tip by affecting pectin synthesis or delivery.

KNS4/UPEX1: A Type II Arabinogalactan β-(1,3)-Galactosyltransferase Required for Pollen Exine Development

“…Intine forms beneath the exine, and two rounds of mitotic cell division produce two sperm cells surrounded by an AGP-containing wall (Coimbra et al, 2007). The intine in mature pollen grains consists mainly of cellulose, noncellulosic polysaccharides, and pectin (van Aelst and van Went, 1992;Ariizumi and Toriyama, 2011), whereas an intine-like structure ("germination plaque") produced upon pollen germination consists of cellulose, callose, and partly demethylesterified pectin (Hoedemaekers et al, 2015), with the pollen tube wall also including AGPs (NguemaOna et al, 2012).AGPs are a class of Hyp-rich glycoproteins found ubiquitously in plant cell walls, secretions, and at the plasma membrane (Nguema-Ona et al, 2012). Most members of this family of proteins are defined by a Hyp-rich protein backbone decorated by type II AGs, that is, a galactan backbone of b-(1,3)-linked-D-galactopyranose residues, with branches (between one and three residues long) of b-(1,6)-linked-D-galactopyranose, as well as other terminal monosaccharides such as Fuc, GlcA, and rhamnose, among others (Ellis et al, 2010).…”

“…Intine forms beneath the exine, and two rounds of mitotic cell division produce two sperm cells surrounded by an AGP-containing wall (Coimbra et al, 2007). The intine in mature pollen grains consists mainly of cellulose, noncellulosic polysaccharides, and pectin (van Aelst and van Went, 1992;Ariizumi and Toriyama, 2011), whereas an intine-like structure ("germination plaque") produced upon pollen germination consists of cellulose, callose, and partly demethylesterified pectin (Hoedemaekers et al, 2015), with the pollen tube wall also including AGPs (NguemaOna et al, 2012).…”

Exocyst subunit SEC3A marks the germination site and is essential for pollen germination in Arabidopsis thaliana

“…Following hydration, plaque formation starts and is completed within 1 h, by then the pollen tube has emerged39. Polar deposition of callose, cellulose and pectin is observed in the incipient bulge of germinating pollen grains5740. The phenotypes of sec3 mutant and the localization pattern of SEC3A prompted us to look into the cell wall deposition at the germination site.…”

“…In Arabidopsis, once a desiccated, pollen grain contacts a papilla cell on the stigmatic surface, it became hydrated within a short period of time. The presence of a Ca 2+ gradient beneath the potential germination site12, the reorganization of F-actin cytoskeleton34, and the massive deposition of callose, pectin, and cellulose at the germination plaque567 are key events taking place before tube emergence. Until now, it is not yet clear how the the germination site is established.…”

“…These included proteins involved in cell wall material synthesis and modification. For example, BUP encodes a novel Golgi-located glycosyltransferase, the bup is affected during pollen germination and pollen tube growth by affecting pectin synthesis or delivery7. Pollen grains from homozygous plants mutated in PECTIN METHYLESTERASE48 gene developed multiple germinating sites due to the presence of more abundant highly methylesterified pectin in the intine wall10.…”