OSD1 Promotes Meiotic Progression via APC/C Inhibition and Forms a Regulatory Network with TDM and CYCA1;2/TAM

Abstract

Cell cycle control is modified at meiosis compared to mitosis, because two divisions follow a single DNA replication event. Cyclin-dependent kinases (CDKs) promote progression through both meiosis and mitosis, and a central regulator of their activity is the APC/C (Anaphase Promoting Complex/Cyclosome) that is especially required for exit from mitosis. We have shown previously that OSD1 is involved in entry into both meiosis I and meiosis II in Arabidopsis thaliana; however, the molecular mechanism by which OSD1 controls these transitions has remained unclear. Here we show that OSD1 promotes meiotic progression through APC/C inhibition. Next, we explored the functional relationships between OSD1 and the genes known to control meiotic cell cycle transitions in Arabidopsis. Like osd1, cyca1;2/tam mutation leads to a premature exit from meiosis after the first division, while tdm mutants perform an aberrant third meiotic division after normal meiosis I and II. Remarkably, while tdm is epistatic to tam, osd1 is epistatic to tdm. We further show that the expression of a non-destructible CYCA1;2/TAM provokes, like tdm, the entry into a third meiotic division. Finally, we show that CYCA1;2/TAM forms an active complex with CDKA;1 that can phosphorylate OSD1 in vitro. We thus propose that a functional network composed of OSD1, CYCA1;2/TAM, and TDM controls three key steps of meiotic progression, in which OSD1 is a meiotic APC/C inhibitor.

Arabidopsis Cell Division Cycle 20.1 Is Required for Normal Meiotic Spindle Assembly and Chromosome Segregation

“…Incorrect attachment triggers the SAC, which creates a "wait signal" until all kinetochores are properly attached to microtubules to prevent chromosome mis-segregation (Zamariola et al, 2014). Persistent incorrect attachment between spindles and kinetochores results in meiotic arrest at metaphase I in animals and delayed meiotic progression in plants (Riehs et al, 2008;Cromer et al, 2012). Studies in multiple organisms estimate that meiotic prophase I occupies ;85% of the meiotic time course (Armstrong et al, 2003;Hamant et al, 2006).…”

“…However, the function of CDC20 in plant meiosis was previously unknown. Additional information for CDC20's role in plant meiosis comes from studies of two Arabidopsis meiotic cell division factors OSD1 and PANS1, which can physically interact with CDC20 in yeast two-hybrid assays (Cromer et al, 2012(Cromer et al, , 2013). These observations indicate a possible role for CDC20 in the degradation of cyclin and cohesin during chromosome segregation, but this hypothesis has yet to be experimentally tested.…”

Cuf2 boosts the transcription of APC/C activator Fzr1 to terminate the meiotic division cycle

“…In mouse and ascidian meioses, proper regulation of Mos-MAPK activity is essential to avoid the entry to meiosis III [19,21,22], although this is unlikely to be a universal mechanism according to studies in other species, including amphibians [23]. In Arabidopsis thaliana, initiation of meiosis II is regulated by a close homologue of fission yeast Mes1 [24]. As yeasts and plants do not appear to have the Mos-MAPK pathway that regulates APC/C, the transcription machinery conducted by meiotic transcription factors including Cuf2 might have developed to enhance the APC/C activity to terminate meiosis in these organisms.…”

BnaC9.SMG7b functions as a positive regulator of number of seeds per silique in rapeseed (Brassica napus L.) by regulating the formation of functional female gametophytes

“…Two key processes are completed during meiosis: one is the chromosome exchange between parents that generates genetic variations in the daughter generations, and one is the two rounds of cell division that produce four haploid gametes. The molecular mechanisms involved in meiotic recombination have been widely investigated (Jones et al, 2003;Hamant et al, 2006;Liu and Makaroff, 2006;Mercier and Grelon, 2008); however, relatively little is known about the control of cell cycle transition underlying meiotic division in plants (Cromer et al, 2012;Wijnker and Schnittger, 2013;Zhao et al, 2014).…”