CDKG1 protein kinase is essential for synapsis and male meiosis at high ambient temperature in Arabidopsis thaliana

Abstract

The Arabidopsis cyclin-dependent kinase G (CDKG) gene defines a clade of cyclin-dependent protein kinases related to CDK10 and CDK11, as well as to the enigmatic Ph1-related kinases that are implicated in controlling homeologous chromosome pairing in wheat. Here we demonstrate that the CDKG1/CYCLINL complex is essential for synapsis and recombination during male meiosis. A transfer-DNA insertional mutation in the cdkg1 gene leads to a temperature-sensitive failure of meiosis in late Zygotene/Pachytene that is associated with defective formation of the synaptonemal complex, reduced bivalent formation and crossing over, and aneuploid gametes. An aphenotypic insertion in the cyclin L gene, a cognate cyclin for CDKG, strongly enhances the phenotype of cdkg1-1 mutants, indicating that this cdk-cyclin complex is essential for male meiosis. Since CYCLINL, CDKG, and their mammalian homologs have been previously shown to affect mRNA processing, particularly alternative splicing, our observations also suggest a mechanism to explain the widespread phenomenon of thermal sensitivity in male meiosis. R eplication and segregation of DNA underpins the reproduction of all cells. In organisms that undergo sexual reproduction, the nucleus carries two copies of each chromosome (or homologs) that replicate and recognize each other before the meiotic reduction division. This process allows the homologs to pair and exchange genetic material before segregation. A proteinaceous structure, known as the synaptonemal complex (SC), forms along the length of each set of paired chromosomes and subsequently forms physical connections between the homologs. Recombination between the homologs involves first the formation of DNA double-strand breaks (DSBs) that are either repaired as noncrossover or crossover (CO) products. Chiasmata, the cytological manifestation of COs, provide a physical connection between the homologs that persists after the SC is disassembled.Many of the proteins involved in meiotic recombination and homologous chromosome synapsis have been identified. At the leptotene stage of prophase I, the chromosome axes are elaborated along the conjoined bases of the sister chromatids. Concomitantly, Spo11-dependent DSBs form and are processed at the axes where the recombination machinery is assembled. This enables the alignment of homologous chromosomes and is dependent on the strand-exchange proteins Rad51 and DMC1. During zygotene, the SC starts to form between the homologs through the polymerization of the central element protein ZYP1 which brings the homologous chromosomes into close apposition. SC formation is complete by pachytene, during which the final stages of recombination are complete. The SC breaks down at the end of pachytene, and the chromosomes condense further during diplotene/diakinesis. At metaphase the bivalents held together by chiasmata are arranged at the metaphase plate, and the first meiotic division occurs.Although many of the structural proteins involved in the progression of meiotic prophase have been identi...

Short periods of high temperature during meiosis prevent normal meiotic progression and reduce grain number in hexaploid wheat (Triticum aestivum L.)

“…However, in maize and rice am1 mutants, meiosis arrests prematurely during leptotene, leading the authors to suggest the presence of a meiotic checkpoint at leptotene/zygotene (Che et al 2011; Pawlowski et al 2009). Moreover, Zheng et al (2014) suggest that in Arabidopsis, the cyclin dependent kinase CDKG1 could be part of a checkpoint mechanism that detects recombination defects and leads to meiotic arrest. Interestingly, CDKG1 is essential for the completion of chromosome synapsis at high ambient temperature.…”

Meiosis evolves: adaptation to external and internal environments

“…The importance of mitigating temperature effects on SC stability is highlighted by the identification of genes in both plants and animals that are required to stabilize meiosis only at elevated temperatures. In A. thaliana , mutation of a protein kinase (CDKG1) causes SC failures at elevated, but normally well‐tolerated temperatures, but has no effect at lower temperatures (Zheng et al ., ). The failures in the mutant are similar to those seen in wild‐type plants at higher growth temperatures (Loidl, ; Higgins et al ., ; Zheng et al ., ), suggesting that mutation of CDKG1 does not qualitatively alter the nature of meiotic failure, but rather shifts the tolerance threshold.…”

The Arabidopsis Cdk1/Cdk2 homolog CDKA ;1 controls chromosome axis assembly during plant meiosis

“…A function of CDKA;1 in meiosis is supported by the analysis of weak loss-of-function mutants, which are completely sterile (Dissmeyer et al, , 2009). Next to CDKA;1, CDKG has been implicated in meiosis by controlling synapsis at ambient but not low temperatures (Zheng et al, 2014). However, CDKG, which is related to human Cdk10, is likely involved in transcriptional and posttranscriptional control of gene expression and presumably does not control structural components of chromosomes directly (Doonan & Kitsios, 2009;Tank & Thaker, 2011;Huang et al, 2013;Zabicki et al, 2013).…”