The F-Box Protein ZYGO1 Mediates Bouquet Formation to Promote Homologous Pairing, Synapsis, and Recombination in Rice Meiosis

Abstract

Telomere bouquet formation, a highly conserved meiotic event, plays an important role in homologous pairing and therefore progression of meiosis; however, the underlying molecular mechanism remains largely unknown. Here, we identified ZYGOTENE1 (ZYGO1), a novel F-box protein in rice (Oryza sativa), and verified its essential role in bouquet formation during early meiosis. In zygo1 mutants, zygotene chromosome aggregation and telomere clustering failed to occur. The suppressed telomere clustering in homologous pairing aberration in rice meiosis1 (pair1) zygo1 and rice completion of meiotic recombination (Oscom1) zygo1 double mutants, together with the altered localization of OsSAD1 (a SUN protein associated with the nuclear envelope) in zygo1, showed that ZYGO1 has a significant function in bouquet formation. In addition, the interaction between ZYGO1 and rice SKP1-like protein 1 suggested that ZYGO1 might modulate bouquet formation as a component of the SKP1-Cullin1-F-box complex. Although double-strand break formation and early recombination element installation occurred normally, zygo1 mutants showed defects in full-length pairing and synaptonemal complex assembly. Furthermore, crossover (CO) formation was disturbed, and foci of Human enhancer of invasion 10 were restricted to the partially synapsed chromosome regions, indicating that CO reduction might be caused by the failure of full-length chromosome alignment in zygo1. Therefore, we propose that ZYGO1 mediates bouquet formation to efficiently promote homolog pairing, synapsis, and CO formation in rice meiosis.

Chromatin Organization in Early Land Plants Reveals an Ancestral Association between H3K27me3, Transposons, and Constitutive Heterochromatin

“…In interphase, telomeres often clustered to form a single speckle ( Figure 1C). A similar conformation, called a ''bouquet,'' has been reported in meiotic maize, wheat, and rice cells [27][28][29]. However, in contrast to bouquet conformation described in flowering plants, the telomere gathering in Marchantia nuclei did not display a specific association of telomeres with the nuclear periphery ( Figure 1C).…”

Time-resolved transcriptome of barley anthers and meiocytes reveals robust and largely stable gene expression changes at meiosis entry

“…Several F-box proteins, putatively interacting in the SCF E3 ubiquitin ligase complex, also displayed differential expression throughout prophase I. In rice, mutations in two F-box proteins interacting with the ASK1 equivalent OSK1, MOF and ZYGO1, have also been shown to result in male sterility (He et al , 2016; Zhang et al , 2017). Several genes annotated as SINA E3 ligases also displayed differential expression during prophase I.…”

OsHOP2 regulates the maturation of crossovers by promoting homologous pairing and synapsis in rice meiosis

“…In Arabidopsis pachytene checkpoint 2 (pch2 ) and pollen semisterility 1 (pss1 ) mutants, HEI10 or MutL Homolog 1 (MLH1) foci (marking mature CO sites) were associated only with stretches of SC (Duroc et al, 2014;Lambing et al, 2015). Recently, it was reported that rice ZYGOTENE1 (ZYGO1) promotes homologous pairing, synapsis and CO formation by mediating bouquet formation (Zhang et al, 2017). In these mutants, double-strand break (DSB) formation and early recombination intermediates are successfully established, whereas the intermediates do not mature into COs.…”