The Arabidopsis ROCK‐N‐ROLLERS gene encodes a homolog of the yeast ATP‐dependent DNA helicase MER3 and is required for normal meiotic crossover formation

Abstract

SummaryRecent studies in Saccharomyces cerevisiae have unveiled that meiotic recombination crossovers are formed by two genetically distinct pathways: a major interference-sensitive pathway and a minor interferenceinsensitive pathway. Several proteins, including the MSH4/MSH5 heterodimer and the MER3 DNA helicase, are indispensable for the interference-sensitive pathway. MSH4 homologs have been identified in mice and Arabidopsis and shown to be required for normal levels of crossovers, suggesting that the function of MSH4 may be conserved among major eukaryotic kingdoms. However, it is not known whether an MER3-like function is also required for meiosis in animals and plants. We have identified an Arabidopsis gene that encodes a putative MER3 homolog and is preferentially expressed in meiocytes. T-DNA insertional mutants of this gene exhibit defects in fertility and meiosis. Detailed cytological studies indicate that the mutants are defective in homolog synapsis and crossover formation, resulting in a reduction of bivalents and in the formation of univalents at late prophase I. We have named this gene ROCK-N-ROLLERS (RCK) to reflect the mutant phenotype of chromosomes undergoing the meiotic 'dance' either in pairs or individually. Our results demonstrate that an MER3-like function is required for meiotic crossover in plants and provide further support for the idea that Arabidopsis, like the budding yeast, possesses both interference-sensitive and insensitive pathways for crossover formation.

Replication Protein A2c Coupled with Replication Protein A1c Regulates Crossover Formation during Meiosis in Rice

“…There was a slight but significant reduction in COs in ZYP1 RNAi and an increased number of COs in zep1 (Higgins et al, 2005;Osman et al, 2006;Wang et al, 2010). However, zep1 zip4 and zep1 mer3 double mutants exhibited much lower numbers of COs than zip4 and mer3 single mutants (Chen et al, 2005;Mercier et al, 2005;Wang et al, 2009;Shen et al, 2012). Recently, a homolog of yeast Zip3, Human Enhancer of Invasion10 (HEI10), was identified in both Arabidopsis and rice.…”

“…Os-MER3 is the rice homolog of MER3, a member of the ZMM proteins that is essential for class I CO formation in diverse species (Chen et al, 2005;Mercier et al, 2005;Wang et al, 2009). To further investigate the function of RPA2c on CO formation, we performed dual immunostaining using RPA2c and MER3 antibodies.…”

Functional conservation of the meiotic genes SDS and RCK in male meiosis in the monocot rice

“…However, because the crossovers in the RCK-RNAi plants were not completely randomly distributed, the existence of a minor interference-insensitive pathway in rice, as that in Arabidopsis, needs further investigation. Phenotype of RCK-RNAi cells indicated that they were defective in the interference-sensitive pathway of meiotic recombination, similar to the phenotype of the Arabidopsis rck mutants [30]. Therefore, the functions of SDS and RCK are largely conserved in Arabidopsis and rice, which represent eudicots and monocots, respectively.…”

“…A mutation in the Arabidopsis ASY1 gene encoding an HOP1 homolog also causes a reduction in chiasmata number [54,55]. In addition, Arabidopsis sds mutant also shows greatly reduced frequency of meiotic recombination [20], and some other mutants defective in meiotic recombination including atspo11-1, atrand51, atxrcc3 and rck [8,30,56,57] are unable to achieve normal SC formation, indicating that normal levels of recombination are needed for proper SC formation. Because SDS could potentially regulate gene expression indirectly, we tested whether rice SDS can affect RCK expression and found that the level of RCK transcript was not influenced when SDS expression was suppressed (Figure 8), suggesting that, though SDS and RCK function in two closely coupled processes of synapsis and recombination, they are not regulated by each other in rice.…”

“…Recent studies showed that a MER3 homolog in Arabidopsis, named as either ROCK-N-ROLLERS (RCK) or AtMER3, is also necessary for crossover formation [30,31]. RCK is preferentially expressed in the developing anthers and T-DNA insertional rck knockout mutants show defects in homolog synapsis and crossover formation; consequently, rck late prophase I meiocytes contain lesser than five bivalents and some univalents [30].…”