CDKF;1 and CDKD Protein Kinases Regulate Phosphorylation of Serine Residues in the C-Terminal Domain of <i>Arabidopsis</i> RNA Polymerase II

Hajheidari, Mohsen; Farrona, Sara; Huettel, Bruno; Koncz, Zsuzsa; Koncz, Csaba

doi:10.1105/tpc.112.096834

Cited by 75 publications

(84 citation statements)

References 78 publications

(144 reference statements)

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“…The difference between CDKD;2 and CAK1 (or CDK7) was further shown by the discovery that CDKD;2 phosphorylates Ser-5 and Ser-2 of the Pol II CTD (Hajheidari et al, 2012). In this study, we found that cdkd;2 displayed an earlyflowering phenotype ( Figures 4C and 4D), whereas cdkc;1 and cdkc;2 exhibited a later-flowering phenotype (Cui et al, 2007).…”

Section: Discussionsupporting

confidence: 55%

Phosphorylation of SPT5 by CDKD;2 Is Required for VIP5 Recruitment and Normal Flowering in Arabidopsis thaliana

Tian

Wang

et al. 2017

Plant Cell

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The elongation factor suppressor of Ty 5 homolog (Spt5) is a regulator of transcription and histone methylation. In humans, phosphorylation of SPT5 by P-TEFb, a protein kinase composed of Cyclin-dependent kinase 9 (CDK9) and cyclin T, interacts with the RNA polymerase II-associated factor1 (PAF1) complex. However, the mechanism of SPT5 phosphorylation is not well understood in plants. Here, we examine the function of SPT5 in Arabidopsis thaliana and find that spt5 mutant flowers early under long-day and short-day conditions. SPT5 interacts with the CDK-activating kinase 4 (CAK4; CDKD;2) and is specifically phosphorylated by CDKD;2 at threonines. The phosphorylated SPT5 binds VERNALIZATION INDEPENDENCE5 (VIP5), a subunit of the PAF1 complex. Genetic analysis showed that VIP5 acts downstream of SPT5 and CDKD;2. Loss of SPT5 or CDKD;2 function results in early flowering because of decreased amounts of FLOWERING LOCUS C (FLC) transcript. Importantly, CDKD;2 and SPT5 are required for the deposition of VIP5 and the enhancement of trimethylation of histone 3 lysine 4 in the chromatin of the FLC locus. Together, our results provide insight into the mechanism by which the Arabidopsis elongation factor SPT5 recruits the PAF1 complex via the posttranslational modification of proteins and suggest that the phosphorylation of SPT5 by CDKD;2 enables it to recruit VIP5 to regulate chromatin and transcription in Arabidopsis.

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Section: Discussionsupporting

confidence: 55%

Phosphorylation of SPT5 by CDKD;2 Is Required for VIP5 Recruitment and Normal Flowering in Arabidopsis thaliana

Tian

Wang

et al. 2017

Plant Cell

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“…P-TEFb phosphorylates the C-terminal domain (CTD) of Pol II at the Ser 2 site within the heptad repeats (26,29). This Ser 2 posttranslational modification orchestrates the interplay between transcriptional elongation and processing of mRNA (32)(33)(34)(35). This amino acid change in cdkc;2-3 is within the activation loop, known to be important for substrate binding, but not involved in interaction with the cyclin component of P-TEFb (Fig.…”

Section: Significancementioning

confidence: 99%

Antisense-mediated FLC transcriptional repression requires the P-TEFb transcription elongation factor

Wang

Raitskin

et al. 2014

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

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The functional significance of noncoding transcripts is currently a major question in biology. We have been studying the function of a set of antisense transcripts called COOLAIR that encompass the whole transcription unit of the Arabidopsis floral repressor FLOWERING LOCUS C (FLC). Alternative polyadenylation of COOL-AIR transcripts correlates with different FLC sense expression states. Suppressor mutagenesis aimed at understanding the importance of this sense-antisense transcriptional circuitry has identified a role for Arabidopsis cyclin-dependent kinase C (CDKC;2) in FLC repression. CDKC;2 functions in an Arabidopsis positive transcription elongation factor b (P-TEFb) complex and influences global RNA polymerase II (Pol II) Ser 2 phosphorylation levels. CDKC;2 activity directly promotes COOLAIR transcription but does not affect an FLC transgene missing the COOLAIR promoter. In the endogenous gene context, however, the reduction of COOLAIR transcription by cdkc;2 disrupts a COOLAIR-mediated repression mechanism that increases FLC expression. This disruption then feeds back to indirectly increase COOLAIR expression. This tight interconnection between sense and antisense transcription, together with differential promoter sensitivity to P-TEFb, is central to quantitative regulation of this important floral repressor gene.lncRNA | autonomous pathway | transcriptional regulation | chromatin silencing W e are investigating the role of specific antisense transcripts in gene regulation through our analysis of the regulation of expression of Arabidopsis thaliana FLOWERING LOCUS C (FLC), an important regulator of flowering time (1, 2). Multiple genetic pathways have been defined that regulate FLC expression; some function in parallel whereas others function antagonistically. FRIGIDA (FRI) up-regulates FLC expression, causing plants to overwinter vegetatively (3). FRI function is antagonized by vernalization, a process through which prolonged cold epigenetically silences FLC (4-7). Acting in parallel with vernalization to repress FLC expression is the autonomous pathway. The autonomous pathway was initially characterized through mutations specifically affecting flowering time but has subsequently been shown to regulate many other targets in the A. thaliana genome (8-10). The autonomous pathway is composed of a number of factors: RNA-binding proteins FCA (11), FPA (12), and FLK (13, 14), RNA 3′ processing factors FY (15-17), CstF64, and CstF77 (18), a histone 3 lysine 4 (H3K4) demethylase FLD (19,20), a homolog of MSI1 (multicopy suppressor of ira1) FVE (21), and a homeodomain protein LUMINIDEPENDENS (LD) (22). These factors link alternative processing of a set of antisense transcripts produced at the FLC locus, collectively termed COOLAIR, with chromatin modifications in the FLC gene body (8). FCA, FY, and FPA promote proximal polyadenylation of COOLAIR transcripts (18), FLD-dependent H3K4me2 demethylation across the body of the gene, and low FLC transcription (23). Their loss results in distal polyadenylation in COOLAI...

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“…CDKA and CDKB are direct regulators of cell cycle transitions (Boudolf et al, 2004;Iwakawa et al, 2006). CDKD and CDKF are CDK activation kinases, which regulate the activities of other CDKs (Shimotohno et al, 2004;Umeda et al, 2005;Hajheidari et al, 2012). CDKC and CDKE are related to the transcriptional regulation of RNA polymerase II (Barrôco et al, 2003;Wang and Chen, 2004;Cui et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2013

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Arabidopsis thaliana CYCLIN-DEPEDENT KINASE G1 (CDKG1) belongs to the family of cyclin-dependent protein kinases that were originally characterized as cell cycle regulators in eukaryotes. Here, we report that CDKG1 regulates pre-mRNA splicing of CALLOSE SYNTHASE5 (CalS5) and, therefore, pollen wall formation. The knockout mutant cdkg1 exhibits reduced male fertility with impaired callose synthesis and abnormal pollen wall formation. The sixth intron in CalS5 pre-mRNA, a rare type of intron with a GC 59 splice site, is abnormally spliced in cdkg1. RNA immunoprecipitation analysis suggests that CDKG1 is associated with this intron. CDKG1 contains N-terminal Ser/Arg (RS) motifs and interacts with splicing factor Arginine/SerineRich Zinc Knuckle-Containing Protein33 (RSZ33) through its RS region to regulate proper splicing. CDKG1 and RS-containing Zinc Finger Protein22 (SRZ22), a splicing factor interacting with RSZ33 and U1 small nuclear ribonucleoprotein particle (snRNP) component U1-70k, colocalize in nuclear speckles and reside in the same complex. We propose that CDKG1 is recruited to U1 snRNP through RSZ33 to facilitate the splicing of the sixth intron of CalS5.

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CDKF;1 and CDKD Protein Kinases Regulate Phosphorylation of Serine Residues in the C-Terminal Domain of Arabidopsis RNA Polymerase II

Cited by 75 publications

References 78 publications

Phosphorylation of SPT5 by CDKD;2 Is Required for VIP5 Recruitment and Normal Flowering in Arabidopsis thaliana

Phosphorylation of SPT5 by CDKD;2 Is Required for VIP5 Recruitment and Normal Flowering in Arabidopsis thaliana

Antisense-mediated FLC transcriptional repression requires the P-TEFb transcription elongation factor

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

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