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 cells. 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 cells. 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 (SCF(FBL17)) 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 SCF(FBL17) as an essential male germ cell proliferation complex that promotes twin sperm cell production and double fertilization in flowering plants.

Control of Cell Proliferation, Organ Growth, and DNA Damage Response Operate Independently of Dephosphorylation of the Arabidopsis Cdk1 Homolog CDKA;1

“…However, all ICK/KRPs tested so far in overexpression studies can block both M and S phases (Verkest et al, 2005b), and at least KRP6 and KRP7 appear to be degraded at the G1/S transition point mediated by a CRL (cullin-RING ligase)-FBL17 complex (Kim et al, 2008;Gusti et al, 2009). By contrast, SIM expression appears to be compatible with DNA replication and preferentially represses M phase (Churchman et al, 2006;Peres et al, 2007).…”

An EAR-Dependent Regulatory Module Promotes Male Germ Cell Division and Sperm Fertility in Arabidopsis

“…For male germline development, a regulatory framework for cell cycle progression and gamete specification has been established Borg and Twell, 2010;Twell, 2011). Timely progression of the generative cell cycle requires the control of cyclin-dependent kinase activity by the F-box protein FBL17, which targets cyclin-dependent kinase inhibitory proteins for degradation (Kim et al, 2008;Gusti et al, 2009). In parallel, the male germline-specific MYB transcription factor DUO POLLEN1 (DUO1) integrates division of the generative cell with differentiation of the sperm cells (Rotman et al, 2005;Brownfield et al, 2009a;Borg et al, 2011).…”

Combinatorial interactions between LBD10 and LBD27 are essential for male gametophyte development in Arabidopsis

“…Degradation of cell cycle inhibitors by SCF FBL17 E3 ubiquitin ligase has been shown to control twin sperm-cell production. 16 Recent studies have demonstrated that degradation of repressors by SCFs through the ubiquitin-proteasome pathway plays a key role in plant hormone auxin, jasmonate, gibberellin, ethylene and abscisic acid signaling. 17,18 Circadian clock and photomorphogenesis are also regulated by proteasome-mediated protein degradation.…”