Atypical Regulation of a Green Lineage-Specific B-Type Cyclin-Dependent Kinase

Abstract

Cyclin-dependent kinases (CDKs) are the main regulators of cell cycle progression in eukaryotes. The role and regulation of canonical CDKs, such as the yeast (Saccharomyces cerevisiae) Cdc2 or plant CDKA, have been extensively characterized. However, the function of the plant-specific CDKB is not as well understood. Besides being involved in cell cycle control, Arabidopsis (Arabidopsis thaliana) CDKB would integrate developmental processes to cell cycle progression. We investigated the role of CDKB in Ostreococcus (Ostreococcus tauri), a unicellular green algae with a minimal set of cell cycle genes. In this primitive alga, at the basis of the green lineage, CDKB has integrated two levels of regulations: It is regulated by Tyr phosphorylation like cdc2/CDKA and at the level of synthesis-like B-type CDKs. Furthermore, Ostreococcus CDKB/cyclin B accounts for the main peak of mitotic activity, and CDKB is able to rescue a yeast cdc28 ts mutant. By contrast, Ostreococcus CDKA is not regulated by Tyr phosphorylation, and it exhibits a low and steady-state activity from DNA replication to exit of mitosis. This suggests that from a major role in the control of mitosis in green algae, CDKB has evolved in higher plants to assume other functions outside the cell cycle.Control of cell cycle progression in eukaryotes relies largely on universally conserved heterodimeric kinases belonging to the cyclin-dependent kinase (CDK) family. These kinases phosphorylate, at the key G1/S and G2/M transitions, a variety of substrate required for DNA replication and mitosis, respectively (Murray, 2004). Cyclins are regulatory subunits enabling periodic activation of CDKs. Whereas animals possess several CDKs, in both fission yeast (Schizosaccharomyces pombe) and budding yeast (Saccharomyces cerevisiae) a single CDK, Cdc2/Cdc28, in association to different cyclins, controls cell cycle progression (Arellano and Moreno, 1997;Mendenhall and Hodge, 1998;Endicott et al., 1999;John et al., 2001). Rapid activation of Cdc2 at mitosis entry is achieved by dephosphorylation of T14 and Y15 residues (Lew and Kornbluth, 1996). CDK/ cyclin complexes are also targets of survey mechanisms, which stop or delay cell cycle progression upon failing, such as incomplete DNA replication, DNA damage, or defect of the mitotic spindle (Paulovich et al., 1997;Rhind and Russell, 1998;Lew and Burke, 2003;Lukas et al., 2004;Stark and Taylor, 2004). Inhibitory phosphorylation of T14 and Y15 is largely involved in CDK inhibition upon activation of the DNA integrity checkpoint (Murakami and Nurse, 2000;Donzelli and Draetta, 2003).Higher plants have a considerable number of core cell cycle genes. Arabidopsis (Arabidopsis thaliana) contains nine cell cycle-related CDK genes and about 30 cyclin genes (Vandepoele et al., 2002). Plant cell cycle genes have been classified on the basis of their sequence homology to their animal counterparts and globally perform similar roles: A-type cyclins are involved in S-phase progression and mitosis, and B-type cyclins are mitotic (Breyne...

Requirement of B2-TypeCyclin-Dependent Kinasesfor Meristem Integrity inArabidopsis thaliana

“…Among those, the B-type CDKs appear to be plant specific, and their origin can be traced back to the unicellular green algae Ostreococcus tauri. This member of a lineage that is ancestral to vascular plants has a single B-type CDK, which is regulated in a cell cycle-dependent manner similar to that of Arabidopsis CDKB1s and is able to complement the yeast cdc28 mutant (Corellou et al, 2005;Robbens et al, 2005). This function has been assumed by CDKA;1 in Arabidopsis, but B-type CDKs are still integral parts of the Arabidopsis cell cycle machinery as evidenced by the sharing of interaction partners, such as CYCD4;1, CDK inhibitors, and CKS1 by A-and B-type CDKs (Ferreira et al, 1991; (A) to (J) Wild-type and OE1 root explants were subjected to hormone treatments to assess their regeneration capacity.…”

A Microbial Avenue to Cell Cycle Control in the Plant Superkingdom

“…Chlamydomonas, like all Viridiplantae, has two CDKs suspected of involvement in cell cycle control, CDKA and the plant-specific CDKB (Porceddu et al, 2001;Vandepoele et al, 2002;De Veylder et al, 2007) (see below). Cks1 precipitates active cyclinbound forms of both (De Veylder et al, 1997;Corellou et al, 2005), thus providing a profile of global CDK activity.…”

Light-Dependent Regulation of Cell Division in Ostreococcus: Evidence for a Major Transcriptional Input

“…Interestingly, the expression of genes like Cyclin D, CKS, or Rb (MAT3) does not change significantly under light/dark cycles in Chlamydomonas but it is regulated in Ostreococcus (Bisova et al, 2005). Unlike higher plants and Chlamydomonas, Ostreococcus contains an animal-type CDC25 phosphatase, which has been shown to activate CDKB by dephosphorylation on a conserved Tyr residue (Corellou et al, 2005). Both CDC25 and Wee1 are regulated at the transcriptional level.…”

“…In agreement with this view, different patterns of expression were observed for Ostreococcus core cell cycle genes. Genes like CDKB or cyclin B, which are involved in the control of mitosis entry (Corellou et al, 2005), are expressed from S phase, several hours after genes likely to be involved in earlier stages of cell cycle progression such as D-type cyclin. Interestingly, the expression of genes like Cyclin D, CKS, or Rb (MAT3) does not change significantly under light/dark cycles in Chlamydomonas but it is regulated in Ostreococcus (Bisova et al, 2005).…”

“…The set of the main core cell cycle genes is extremely reduced, most cyclins and CDKs being present as a single copy gene (Robbens et al, 2005). Ostreococcus contains also a canonical CDC25 like not found in higher plants (Khadaroo et al, 2004), as well as a plant-specific B-type CDK (Corellou et al, 2005).…”