Abstract

The highly resistant biopolymer, sporopollenin, gives the outer wall (exine) of spores and pollen grains their unparalleled strength, shielding these structures from terrestrial stresses. Despite a limited understanding of the composition of sporopollenin, it appears that the synthesis of sporopollenin occurs in the tapetum and requires the transport of one or more sporopollenin constituents to the surface of developing microspores. Here, we describe ABCG26, a member of the ATP-binding cassette (ABC) transporter superfamily, which is required for pollen exine formation in Arabidopsis (Arabidopsis thaliana). abcg26 mutants are severely reduced in fertility, with most siliques failing to produce seeds by self-fertilization and mature anthers failing to release pollen. Transmission electron microscopy analyses revealed an absence of an exine wall on abcg26-1 mutant microspores. Phenotypic abnormalities in pollen wall formation were first apparent in early uninucleate microspores as a lack of exine formation and sporopollenin deposition. Additionally, the highest levels of ABCG26 mRNA were in the tapetum, during early pollen wall formation, sporopollenin biosynthesis, and sporopollenin deposition. Accumulations resembling the trilamellar lipidic coils in the abcg11 and abcg12 mutants defective in cuticular wax export were observed in the anther locules of abcg26 mutants. A yellow fluorescent protein-ABCG26 protein was localized to the endoplasmic reticulum and plasma membrane. Our results show that ABCG26 plays a critical role in exine formation and pollen development and are consistent with a model by which ABCG26 transports sporopollenin precursors across the tapetum plasma membrane into the locule for polymerization on developing microspore walls.

Highlights

  • The highly resistant biopolymer, sporopollenin, gives the outer wall of spores and pollen grains their unparalleled strength, shielding these structures from terrestrial stresses

  • Since ACYL-COA SYNTHETASE5 (ACOS5) is preferentially expressed in the tapetum and encodes an acylCoA synthetase required for sporopollenin biosynthesis, this gene was used for coexpression analysis to identify potential Arabidopsis transporters on the PRIMe database

  • The Arabidopsis ABCG26 gene At3g13220 shows a high coefficient of coexpression in the tissue and development version 1 data set (r2 = 0.95), along with several other genes involved in sporopollenin biosynthesis

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Summary

Introduction

The highly resistant biopolymer, sporopollenin, gives the outer wall (exine) of spores and pollen grains their unparalleled strength, shielding these structures from terrestrial stresses. Our results show that ABCG26 plays a critical role in exine formation and pollen development and are consistent with a model by which ABCG26 transports sporopollenin precursors across the tapetum plasma membrane into the locule for polymerization on developing microspore walls. After the release of microspores from callose-encased tetrads in stage 8, the sporopollenin-based exine wall forms by the deposition of sporopollenin generated in the tapetum, producing the sculptured baculae and tecta of the exine. The sporophytic tapetum, a single cell layer encasing the anther locule, plays key functions in pollen development. It supplies nutrients, structural components, and enzymes essential to the survival and development of microspores (Blackmore et al, 2007). In Arabidopsis, rice (Oryza sativa), wheat (Triticum aestivum), and other plants with secretory tapeta, the spatial separation of the tapetum from developing microspores requires the movement of substances, including sporopollenin components, from the tapetum to the developing microspore

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