The RCC1 family protein SAB1 negatively regulates ABI5 through multidimensional mechanisms during postgermination in Arabidopsis

Abstract

Summary Abscisic acid‐insensitive 5 (ABI5) is an essential and conserved plant basic leucine zipper transcription factor whose level controls seed germination and postgerminative development. It has been demonstrated that activity of ABI5 is transcriptionally and post‐translationally regulated. However, transcriptional regulation of ABI5 is not fully understood. Here, we identified SAB1 (Sensitive to ABA 1) as a novel negative regulator of ABI5 that simultaneously regulates its stability, promoter binding activity and histone methylation‐mediated gene silencing of ABI5. SAB1 encodes a Regulator of Chromatin Condensation 1 (RCC1) family protein and is expressed in an opposite pattern to that of ABI5 during early seedling growth in response to abscisic acid (ABA). SAB1 mutation results in enhanced ABA sensitivity and acts upstream of ABI5. SAB1 physically interacts with ABI5 at phosphoamino acid Ser‐145, and reduces the phosphorylation of ABI5 and the protein stability. SAB1 reduces ABI5 binding activity to its own promoter, leading to reduced transcriptional level of ABI5. SAB1 inactivates ABI5 transcription by increasing the level of histone H3K27me2 in the ABI5 promoter. Our findings have identified SAB1 as a crucial new component of ABA signaling which modulates early development of plant by precisely controlling ABI5 activity through multiple mechanisms.

ABI5 modulates seed germination via feedback regulation of the expression of the PYR/PYL/RCAR ABA receptor genes

“…For example, recent studies have shown that the regulator of chromatin condensation 1 (RCC1) family protein SAB1 functions as a negative regulator of ABI5 via multiple pathways. SAB1 can reduce the phosphorylation and protein stability of ABI5 by interacting with ABI5, and SAB1 also reduces the binding of ABI5 to its own promoter and increases the histone H3K27me2 level in the ABI5 promoter, leading to a reduction in the transcription of ABI5 (Ji et al ., 2019). These multiple regulatory mechanisms reveal the complexity of the ABA signaling pathway, which still needs to be further studied.…”

The Transcription Factor INDUCER OF CBF EXPRESSION1 Interacts with ABSCISIC ACID INSENSITIVE5 and DELLA Proteins to Fine-Tune Abscisic Acid Signaling during Seed Germination in Arabidopsis

“…By contrast, the small ubiquitin-related modifier E3 ligase SAP AND MIZ1 negately regulates ABA signaling via sumoylation of ABI5 (Miura et al, 2009). Moreover, several negative regulators of ABI5 facilitate its degradation and/or decrease ABA signaling to promote seed germination, such as KEEP ON GOING, ABI Five Binding Protein, PROTEIN PHOSPHATASE6, SENSITIVE TO ABA1, DWD HYPERSENSITIVE TO ABA1, and DWD HYPERSENSITIVE TO ABA2 (Stone et al, 2006;Garcia et al, 2008;Lee et al, 2010;Liu and Stone, 2010;Dai et al, 2013;Lynch et al, 2017;Ji et al, 2019).…”

Regulator of Chromosome Condensation 1-Domain Protein DEK47 Functions on the Intron Splicing of Mitochondrial Nad2 and Seed Development in Maize

“…The human RCC1 protein is involved in mitosis, nucleo-cytoplasmic transport, and nuclear-envelope assembly as a signal for chromosome position ( Hetzer et al, 2002 ). In A. thaliana , four RCC1-domain proteins (UVR8, RUG3, TCF1, and SAB1) have been characterized ( Brown et al, 2005 ; Kuhn et al, 2011 ; Ji et al, 2015 , 2019 ). In maize, 31 putative RCC1-like proteins are identified; however, none of which have been characterized at the molecular level.…”

“…In animals, RCC1-domain proteins have been shown to mediate diverse biological processes, such as interaction with proteins and lipids, and enzyme inhibition ( Hadjebi et al, 2008 ). In Arabidopsis thaliana , 24 putative RCC1 family proteins have been identified, among which four [UVR8, RCC1/UVR8/GEF-like 3 (RUG3), tolerant to chilling and freezing 1 (TCF1), sensitive to ABA 1 (SAB1)] have been characterized ( Brown et al, 2005 ; Kuhn et al, 2011 ; Ji et al, 2015 , 2019 ). UVR8, dual-targeted to cytosol and nucleus, is involved in UV-protective responses for plant survival in sunlight ( Brown et al, 2005 ; Rizzini et al, 2011 ).…”

“…TCF1 localized in the nucleus is required for modulating lignin biosynthesis to promote freezing tolerance and cold acclimation ( Ji et al, 2015 ). SAB1 that is dual-localized in cytoplasm and nucleus negatively regulates ABI5 in ABA signaling ( Ji et al, 2019 ). In maize, 31 RCC1-domain proteins have been identified, but none have been characterized thus far.…”