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Control of plant germline proliferation by SCFFBL17 degradation of cell cycle inhibitors

Abstract

Flowering plants possess a unique reproductive strategy, involving double fertilization by twin sperm cells1. Unlike animal germ lines, the male germ cell lineage in plants only forms after meiosis and involves asymmetric division of haploid microspores, to produce a large, non-germline vegetative cell and a germ cell that undergoes one further division to produce the twin sperm cells2. Although this switch in cell cycle control is critical for sperm cell production and delivery, the underlying molecular mechanisms are unknown. Here we identify a novel F-box protein of Arabidopsis thaliana, designated FBL17 (F-box-like 17), that enables this switch by targeting the degradation of cyclin-dependent kinase A;1 inhibitors specifically in male germ cells. We show that FBL17 is transiently expressed in the male germ line after asymmetric division and forms an SKP1–Cullin1–F-box protein (SCF) E3 ubiquitin ligase complex (SCFFBL17) that targets the cyclin-dependent kinase inhibitors KRP6 and KRP7 for proteasome-dependent degradation. Accordingly, the loss of FBL17 function leads to the stabilization of KRP6 and inhibition of germ cell cycle progression. Our results identify SCFFBL17 as an essential male germ cell proliferation complex that promotes twin sperm cell production and double fertilization in flowering plants.

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Figure 1: FBL17 is required for the single male germline division.
Figure 2: FBL17 is part of an SCF complex and binds to KRP6 and KRP7 that show proteasome-dependent degradation.
Figure 3: FBL17 is required for KRP6 turnover in the male germ line.

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Acknowledgements

We thank K. H. Suh, Y. S. Park and B. H. Kim for technical assistance. This work was supported by MOST (KOSEF) through the National Core Research Center for Systems Bio-Dynamics (to H.G.N.) and the Crop Functional Genomics Research Program (to H.G.N.), by the Biotechnology and Biological Sciences Research Council (to D.T.), by the BK21 research fellowship for Life Science, Kyungpook National University (to S.A.O.), and by a KRF grant from MOHERD (to I.H.).

Author Contributions H.J.K. carried out Y2H analysis, FBL17 protein and molecular analysis, construction of FBL17 and KRP transgenic lines, in vitro degradation assays and wrote the manuscript. S.A.O. characterized fbl17 mutant phenotype and nuclear DNA content analysis. L.B. analysed in vivo expression of FBL17 and KRP by confocal laser scanning microscopy and contributed to manuscript writing. S.H.H. carried out co-immunoprecipitation assay of FBL17. H.R., I.H. and H.J.K. initially isolated fbl17 T-DNA mutant. D.T. and H.G.N. contributed to planning, interpretation and manuscript writing and are considered co-senior authors. All authors discussed the results and commented on the manuscript.

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Correspondence to David Twell or Hong Gil Nam.

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Kim, H., Oh, S., Brownfield, L. et al. Control of plant germline proliferation by SCFFBL17 degradation of cell cycle inhibitors. Nature 455, 1134–1137 (2008). https://doi.org/10.1038/nature07289

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