ABCG26-Mediated Polyketide Trafficking and Hydroxycinnamoyl Spermidines Contribute to Pollen Wall Exine Formation in Arabidopsis

• Published in: The Plant cell Vol. 26; no. 11; pp. 4483 - 4498
• Main Authors: Quilichini, Teagen D., Samuels, A. Lacey, Douglas, Carl J.
• Format: Journal Article
• Language: English
• Published: United States American Society of Plant Biologists 01.11.2014
• Subjects: Anthers; Apoptosis; Arabidopsis; Arabidopsis - cytology; Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; ATP Binding Cassette Transporter, Sub-Family G; ATP-Binding Cassette Transporters - genetics; ATP-Binding Cassette Transporters - metabolism; Biological Transport; Biopolymers - metabolism; Biosynthesis; Carotenoids - metabolism; exine; Fluorescence; Gene Expression Regulation, Plant; genetic techniques and protocols; image analysis; Inclusion bodies; Microscopy; Microspores; Microsporocytes; Models, Biological; Mutation; Pollen; Pollen - cytology; Pollen - genetics; Pollen - growth & development; Pollen - metabolism; Polyketide Synthases - genetics; Polyketide Synthases - metabolism; Polyketides; Polyketides - metabolism; Spermidine - metabolism; Vacuoles; Vacuoles - metabolism
• ISSN: 1040-4651; 1532-298X; 1532-298X
• DOI: 10.1105/tpc.114.130484

Pollen grains are encased by a multilayered, multifunctional wall. The sporopollenin and pollen coat constituents of the outer pollen wall (exine) are contributed by surrounding sporophytic tapetal cells. Because the biosynthesis and development of the exine occurs in the innermost cell layers of the anther, direct observations of this process are difficult. The objective of this study was to investigate the transport and assembly of exine components from tapetal cells to microspores in the intact anthers of Arabidopsis thaliana. Intrinsically fluorescent components of developing tapetum and microspores were imaged in intact, live anthers using two-photon microscopy. Mutants of ABCG26, which encodes an ATP binding cassette transporter required for exine formation, accumulated large fluorescent vacuoles in tapetal cells, with corresponding loss of fluorescence on microspores. These vacuolar inclusions were not observed in tapetal cells of double mutants of abcg26 and genes encoding the proposed sporopollenin polyketide biosynthetic metabolon (ACYT COENZYMEA SYNTHETASE5, POLYKETIDE SYNTH ASE A [PKSA], PKSB, and TETRAKETIDE α-PYRONE REDUCTASE1), providing a genetic link between transport by ABCG26 and polyketide biosynthesis. Genetic analysis also showed that hydroxycinnamoyl spermidines, known components of the pollen coat, were exported from tapeta prior to programmed cell death in the absence of polyketides, raising the possibility that they are incorporated into the exine prior to pollen coat deposition. We propose a model where ABCG26-exported polyketides traffic from tapetal cells to form the sporopollenin backbone, in coordination with the trafficking of additional constituents, prior to tapetum programmed cell death.