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BIOCHEMICAL PROCESSES AND MACROMOLECULAR STRUCTURES

CYP704B1 Is a Long-Chain Fatty Acid -Hydroxylase Essential for Sporopollenin Synthesis in Pollen of Arabidopsis^1,[W],[OA]

Department of Molecular Genetics and Cell Biology, University of Chicago, Chicago, Illinois 60637 (A.A.D., J.S., D.P.); Plant Biochemistry Laboratory, Department of Plant Biology and Biotechnology, Faculty of Life Sciences and VKR Research Centre "Pro-Active Plants," University of Copenhagen, DK–1871 Frederiksberg C, Copenhagen, Denmark (M.M., B.L.M.); Institut de Biologie Moléculaire des Plantes, CNRS UPR2357-Université de Strasbourg, Département Réseau Métabolique, F–67083 Strasbourg cedex, France (F.P., M.M.); and Department of Biology, Valparaiso University, Valparaiso, Indiana 46383 (R.S.)

Sporopollenin is the major component of the outer pollen wall (exine). Fatty acid derivatives and phenolics are thought to be its monomeric building blocks, but the precise structure, biosynthetic route, and genetics of sporopollenin are poorly understood. Based on a phenotypic mutant screen in Arabidopsis (Arabidopsis thaliana), we identified a cytochrome P450, designated CYP704B1, as being essential for exine development. CYP704B1 is expressed in the developing anthers. Mutations in CYP704B1 result in impaired pollen walls that lack a normal exine layer and exhibit a characteristic striped surface, termed zebra phenotype. Heterologous expression of CYP704B1 in yeast cells demonstrated that it catalyzes -hydroxylation of long-chain fatty acids, implicating these molecules in sporopollenin synthesis. Recently, an anther-specific cytochrome P450, denoted CYP703A2, that catalyzes in-chain hydroxylation of lauric acid was also shown to be involved in sporopollenin synthesis. This shows that different classes of hydroxylated fatty acids serve as essential compounds for sporopollenin formation. The genetic relationships between CYP704B1, CYP703A2, and another exine gene, MALE STERILITY2, which encodes a fatty acyl reductase, were explored. Mutations in all three genes resulted in pollen with remarkably similar zebra phenotypes, distinct from those of other known exine mutants. The double and triple mutant combinations did not result in the appearance of novel phenotypes or enhancement of single mutant phenotypes. This implies that each of the three genes is required to provide an indispensable subset of fatty acid-derived components within the sporopollenin biosynthesis framework.

² These authors contributed equally to the article.

³ Present address: Department of Microbial Discovery, Novozymes A/S, 2880 Bagsvaerd, Denmark.

⁴ Present address: Chromatin, Inc., Chicago, IL 60616.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Anna A. Dobritsa (dobritsa{at}uchicago.edu).

^[W] The online version of this article contains Web-only data.

^[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.109.144469

^* Corresponding author; e-mail dobritsa{at}uchicago.edu.

Received July 8, 2009; accepted August 18, 2009; published August 21, 2009.

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