Ipl1/Aurora B kinase coordinates synaptonemal complex disassembly with cell cycle progression and crossover formation in budding yeast meiosis

Abstract

Several protein kinases collaborate to orchestrate and integrate cellular and chromosomal events at the G2/M transition in both mitotic and meiotic cells. During the G2/M transition in meiosis, this includes the completion of crossover recombination, spindle formation, and synaptonemal complex (SC) breakdown. We identified Ipl1/ Aurora B kinase as the main regulator of SC disassembly. Mutants lacking Ipl1 or its kinase activity assemble SCs with normal timing, but fail to dissociate the central element component Zip1, as well as its binding partner, Smt3/SUMO, from chromosomes in a timely fashion. Moreover, lack of Ipl1 activity causes delayed SC disassembly in a cdc5 as well as a CDC5-inducible ndt80 mutant. Crossover levels in the ipl1 mutant are similar to those observed in wild type, indicating that full SC disassembly is not a prerequisite for joint molecule resolution and subsequent crossover formation. Moreover, expression of meiosis I and meiosis II-specific B-type cyclins occur normally in ipl1 mutants, despite delayed formation of anaphase I spindles. These observations suggest that Ipl1 coordinates changes to meiotic chromosome structure with resolution of crossovers and cell cycle progression at the end of meiotic prophase.

Genetic Requirements and Meiotic Function of Phosphorylation of the Yeast Axial Element Protein Red

“…It was proposed then that phosphorylated Red1 interacts with the FHA domain of Mek1 to recruit Mek1 to DSB sites where Mek1 is activated to prevent DMC1-independent DSB repair (52). Although the identity of the kinase involved in the phosphorylation of Red1 remained unknown and the importance of Red1 phosphorylation for meiosis had not been demonstrated, it still was proposed that phosphorylated Red1 plays important roles in meiosis (21,25,36). In the present study, we provide strong evidence suggesting that the phosphorylation of Red1 is not required for its function in meiosis.…”

Meiotic Chromosome Interactions: Nonhomologous Centromere (Un)Coupling and Homologous Synapsis

“…Zip1 is also the (potential) substrate of at least three different kinases, namely, the ATR-like serine/threonine kinase Mec1, the aurora B kinase Ipl1, and the cyclin-dependent kinase Cdc28 [8,[15][16][17]. Mec1-dependent phosphorylation of Zip1 triggers disengagement of NCCs (see later).…”

“…Mec1-dependent phosphorylation of Zip1 triggers disengagement of NCCs (see later). Ipl1 activity on the other hand promotes timely disassembly, as measured by the immunofluorescence staining pattern of Zip1, of SC [16]. In simple model, phosphorylation by these kinases may modulate Zip1's ability to self-interact (e.g., [8]) and/or Zip1's (and/or its associated protein's) interaction with other axis-associated proteins (e.g., [16]), thereby destabilizing Zip1-mediated meiotic chromosome interactions.…”

“…Ipl1 activity on the other hand promotes timely disassembly, as measured by the immunofluorescence staining pattern of Zip1, of SC [16]. In simple model, phosphorylation by these kinases may modulate Zip1's ability to self-interact (e.g., [8]) and/or Zip1's (and/or its associated protein's) interaction with other axis-associated proteins (e.g., [16]), thereby destabilizing Zip1-mediated meiotic chromosome interactions. The polo-like kinase Cdc5 is required for SC disassembly [18][19][20]; the contribution of its kinase activity in this process is unclear, but appears distinct from that of Ipl1 [16].…”

“…In simple model, phosphorylation by these kinases may modulate Zip1's ability to self-interact (e.g., [8]) and/or Zip1's (and/or its associated protein's) interaction with other axis-associated proteins (e.g., [16]), thereby destabilizing Zip1-mediated meiotic chromosome interactions. The polo-like kinase Cdc5 is required for SC disassembly [18][19][20]; the contribution of its kinase activity in this process is unclear, but appears distinct from that of Ipl1 [16]. By contrast, inhibition of the Cdc28 kinase activity prevents normal CE formation; however, CE formation is probably independent of Cdc28-dependent phosphorylation of Zip1 [17].…”