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Published on September 28, 2007; 10.1104/pp.106.095323

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Received December 28, 2006
Accepted September 25, 2007

The Ubiquitin-Specific Protease Subfamily UBP3/UBP4 Is Essential for Pollen Development and Transmission in Arabidopsis

Jed H. Doelling *, Allison R. Phillips , Gulsum Soyler-Ogretim , Jasen Wise , Jennifer Chandler , Judy Callis , Marisa S. Otegui , and Richard D. Vierstra

Division of Plant and Soil Sciences, West Virginia University, 1090 Agricultural Sciences Building, Morgantown, WV 26506; Department of Genetics, University of Wisconsin-Madison, 425 Henry Mall, Madison, WI 53706; Department of Pathology, West Virginia University, 2335 Health Sciences Center South, Morgantown, WV 26506; Section of Molecular and Cellular Biology, University of California-Davis, Davis, CA 95616; Department of Botany, University of Wisconsin-Madison, 224 Birge Hall, Madison, WI 53706

* Corresponding author; email: jed.doelling{at}mail.wvu.edu.

Deubiquitinating enzymes are essential to the ubiquitin (Ub)/26S proteasome system where they release Ub monomers from the primary translation products of poly-Ub and Ub-extension genes, recycle Ubs from poly-ubiquitinated proteins, and reverse the effects of ubiquitination by releasing bound Ubs from individual targets. The Ub-specific proteases (UBPs) are one large family of deubiquitinating enzymes that bear signature cysteine and histidine motifs. Here, we genetically characterize a UBP subfamily in Arabidopsis thaliana encoded by paralogous UBP3 and UBP4 genes. Whereas homozygous ubp3 and ubp4 single mutants do not display obvious phenotypic abnormalities, double homozygous mutant individuals could not be created due to a defect in pollen development and/or transmission. This pollen defect was rescued with a transgene encoding wild-type UBP3 or UBP4 but not with a transgene encoding an active-site mutant of UBP3, indicating that the deubiquitination activity of UBP3/4 is required. Nuclear DNA staining revealed that ubp3 ubp4 pollen often fail to undergo mitosis II that generates the two sperm cells needed for double fertilization. Substantial changes in vacuolar morphology were also evident in the mutant grains at the time of pollen dehiscence, suggestive of defects in vacuole and endomembrane organization. Even though some ubp3 ubp4 pollen could germinate in vitro, they failed to fertilize wild-type ovules even in the absence of competing wild-type pollen. These studies provide additional evidence that the Ub/26S proteasome system is important for male gametogenesis in plants and suggest that deubiquitination of one or more targets by UBP3/4 is critical for the development of functional pollen.






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