CYCLIN-DEPENDENT KINASE G1 Is Associated with the Spliceosome to Regulate<i>CALLOSE SYNTHASE5</i>Splicing and Pollen Wall Formation in<i>Arabidopsis</i>

Huang, Xueyong; Niu, Jin; Sun, Ming-Xi; Zhu, Jun; Gao, Jufang; Yang, Jun; Zhou, Qing; Yang, Zhong‐Nan

doi:10.1105/tpc.112.107896

Cited by 68 publications

(74 citation statements)

References 61 publications

(95 reference statements)

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“…The large isoform of CDK11 (the mammalian homolog) promotes pre-mRNA splicing through its interaction with CyclinL (33), and a similar function has been proposed for CyclinL in plants (21), where it is required for the correct splicing of disease resistance transcripts. Indeed, CDKG1 was found to be associated with the spliceosome and regulates the splicing of a gene involved in pollen cell wall formation (34), indicating a general role in regulating several different aspects of pollen development.…”

Section: Discussionmentioning

confidence: 99%

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

Zheng

Nibau

Phillips

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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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...

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Section: Discussionmentioning

confidence: 99%

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

Zheng

Nibau

Phillips

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…Therefore, these results show that ARF17 directly regulates CalS5 expression in callose synthesis. Recently, Huang et al (2013) showed that CDKG1 can interact with the splicing factor to regulate CalS5 splicing and pollen wall formation. In addition, CalS5 expression is also decreased in rpg1 and npu mutants (Chang et al, 2012;Sun et al, 2013), indicating that CalS5 expression is regulated at multiple levels.…”

Section: Discussionmentioning

confidence: 99%

“…CALLOSE SYNTHASE5 (CalS5) is the major enzyme responsible for the biosynthesis of the callose peripheral of the tetrad (Dong et al, 2005;Nishikawa et al, 2005). Mutation of Cals5 and abnormal CalS5 pre-mRNA splicing resulted in defective peripheral callose deposition and primexine formation (Dong et al, 2005;Nishikawa et al, 2005;Huang et al, 2013). Besides CalS5, four membrane-associated proteins have also been reported to be involved in primexine formation: DEFECTIVE EXINE FORMATION1 (DEX1; Paxson-Sowders et al, 1997, 2001, NO EXINE FOR-MATION1 (NEF1; Ariizumi et al, 2004), RUPTURED POLLEN GRAIN1 (RPG1; Guan et al, 2008;Sun et al, 2013), and NO PRIMEXINE AND PLASMA MEM-BRANE UNDULATION (NPU; Chang et al, 2012).…”

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confidence: 99%

AUXIN RESPONSE FACTOR17 Is Essential for Pollen Wall Pattern Formation in Arabidopsis

et al. 2013

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In angiosperms, pollen wall pattern formation is determined by primexine deposition on the microspores. Here, we show that AUXIN RESPONSE FACTOR17 (ARF17) is essential for primexine formation and pollen development in Arabidopsis (Arabidopsis thaliana). The arf17 mutant exhibited a male-sterile phenotype with normal vegetative growth. ARF17 was expressed in microsporocytes and microgametophytes from meiosis to the bicellular microspore stage. Transmission electron microscopy analysis showed that primexine was absent in the arf17 mutant, which leads to pollen wall-patterning defects and pollen degradation. Callose deposition was also significantly reduced in the arf17 mutant, and the expression of CALLOSE SYNTHASE5 (CalS5), the major gene for callose biosynthesis, was approximately 10% that of the wild type. Chromatin immunoprecipitation and electrophoretic mobility shift assays showed that ARF17 can directly bind to the CalS5 promoter. As indicated by the expression of DR5-driven green fluorescent protein, which is an synthetic auxin response reporter, auxin signaling appeared to be specifically impaired in arf17 anthers. Taken together, our results suggest that ARF17 is essential for pollen wall patterning in Arabidopsis by modulating primexine formation at least partially through direct regulation of CalS5 gene expression.

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“…A knockout mutant of CDKG1 exhibited a low panicle seed setting rate, and further work indicated that the sixth intron of the CDKG1 pre-mRNA was altered in the cdkg1 mutant. 47 Consistent with mammalian CRK7, a GFP-CDKG1 fusion protein was found to co-localize with spliceosomal components, and it was proposed to couple splicing with transcription (a cyclin-dependent protein kinase, CDKC2, colocalizes with and modulates the distribution of spliceosomal components in Arabidopsis). The regulation of GSLs in higher plants includes both transcriptional and post-translational modifications such as phosphorylation and direct translocation.…”

Section: Callose Biosynthesis During Male Reproductive Development Inmentioning

confidence: 80%

Callose synthesis during reproductive development in monocotyledonous and dicotyledonous plants

Xiao

Han

2015

Plant Signaling & Behavior

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Callose, a linear b-1,3-glucan molecule, plays important roles in a variety of processes in angiosperms, including development and the response to biotic and abiotic stress. Despite the importance of callose deposition, our understanding of the roles of callose in rice reproductive development and the regulation of callose biosynthesis is limited. GLUCAN SYNTHASE-LIKE genes encode callose synthases (GSLs), which function in the production of callose at diverse sites in plants. Studies have shown that callose participated in plant reproductive development, and that the timely deposition and degradation of callose were essential for normal male gametophyte development. In this mini-review, we described conserved sequences found in GSL family proteins from monocotyledonous (Oryza sativa and Zea mays) and dicotyledonous (Arabidopsis thaliana and Glycine max) plants. We also describe the latest findings on callose biosynthesis and deposition during reproductive development and discuss future challenges in unraveling the mechanism of callose synthesis and deposition in higher plants.

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CYCLIN-DEPENDENT KINASE G1 Is Associated with the Spliceosome to RegulateCALLOSE SYNTHASE5Splicing and Pollen Wall Formation inArabidopsis

Cited by 68 publications

References 61 publications

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

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

AUXIN RESPONSE FACTOR17 Is Essential for Pollen Wall Pattern Formation in Arabidopsis

Callose synthesis during reproductive development in monocotyledonous and dicotyledonous plants

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