The CDK Inhibitor SIAMESE Targets Both CDKA;1 and CDKB1 Complexes to Establish Endoreplication in Trichomes

Abstract

Endoreplication, also known as endoreduplication, is a modified cell cycle in which DNA is replicated without subsequent cell division. Endoreplication plays important roles in both normal plant development and in stress responses. The SIAMESE (SIM) gene of Arabidopsis (Arabidopsis thaliana) encodes a cyclin-dependent kinase (CDK) inhibitor that plays a central role in establishing endoreplication, and is the founding member of the SIAMESE-RELATED (SMR) family of plant-specific CDK inhibitor genes. However, there has been conflicting evidence regarding which specific cyclin/CDK complexes are inhibited by SIM in vivo. In this work, we use genetic evidence to show that SIM likely inhibits both CDKA;1-and CDKB1-containing CDK complexes in vivo, thus promoting endoreplication in developing Arabidopsis trichomes. We also show that SIM interacts with CYCA2;3, a binding partner of CDKB1;1, via SIM motif A, which we previously identified as a CDK-binding motif. By contrast, SIM motif C, which has been indicated as a cyclin binding motif in other contexts, appears to be relatively unimportant for interaction between SIM and CYCA2;3. Together with earlier results, our work suggests that SIM and other SMRs likely have a multivalent interaction with CYC/CDK complexes.

Phytohormone-Based Regulation of Trichome Development

“…The development of trichomes may involve an endoreduplication cycle. Usually, the cell cycle in eukaryotes involves four phases: G1, S, G2, and M. D -type cyclin (CYCD) and cyclin-dependent kinase (CDKA) complexes play important roles in regulating G1→S and G2→M transitions ( Ishida et al, 2008 ; Wang et al, 2020 ). Trichome initiation occurs at the G1→S and G2→M stages, and regulation of the endoreduplication cycle may be a promising way to modulate multicellular trichomes ( Schnittger et al, 2002a , b ).…”

“…Trichome initiation occurs at the G1→S and G2→M stages, and regulation of the endoreduplication cycle may be a promising way to modulate multicellular trichomes ( Schnittger et al, 2002a , b ). Methyl jasmonate (MeJA) may specifically delay the switch from G1→S and prolong the G1 phase ( Noir et al, 2013 ; Wang et al, 2020 ; Figure 3 ). Therefore, MeJA may regulate trichome development by modulating endoreduplication.…”

Transcriptomic Analysis of Radish (Raphanus sativus L.) Spontaneous Tumor

“…The activity of CDK-cyclin complexes at all phases of the plant cell cycle depends on other proteins: CDKDs, activators of CDK, which interact with CYCPs acting in the nutritional control of cell cycle [ 26 , 27 ], and inhibitors of CDK— SIAMESE-RELATED (SMR) [ 28 ] and Kip-related proteins (KRPs) [ 29 ]. In turn, the stability of KRPs depends on the F-box protein FBL17 [ 30 ].…”

Connections between the Cell Cycle and the DNA Damage Response in Plants

“…In this scheme, under normal growth, Rep-MYBs upon CDK phosphorylation are degraded via the ubiquitin-proteasome system, while, in response to DNA damage, they accumulate to high levels. It appears that if the Rep-MYBs are not transcriptionally regulated in response to DNA damage, the SOG1-targeting of CKIs, resulting in the inhibition of CDK phosphorylation activity [108], might contribute to the stabilization of the Rep-MYBs, allowing them to ensure a high repression level of a subset of G2/M genes, thus, leading to the blockage of the cell cycle [86,109] (Figure 2).…”

“…Similarly, the induction of CKI regulators is to be noticed. Indeed, members of the plant CKI families, the SMR and KRP, have been largely characterized to block cell cycle progression through the negative regulation of CDK/CYC complexes and induction of the endocycle [28,48,108,134]. Despite this substantial functional redundancy, some SIM/SMRs (i.e., SIM, SMR1, SMR2, and SMR11 [28,135] and KRPs [51][52][53]124,136,137] are clearly dedicated to developmental and cell size control processes while others appear to exhibit a specialisation in stress response, and in particular to DNA damage stress.…”