Chromatin assembly factor CAF-1 is required for cellular differentiation during plant development

Abstract

Chromatin assembly factor CAF-1 facilitates the formation of nucleosomes on newly replicated DNA in vitro. However, the role of CAF-1 in development is poorly understood because mutants are not available in most multicellular model organisms. Biochemical evidence suggests that FASCIATA1, FASCIATA2 and MSI1 form CAF-1 in Arabidopsis thaliana. Because fasciata mutants are viable, CAF-1 is not essential for cell division in plants. Arabidopsis CAF-1 mutants have defects in shoot apical meristems; in addition, CAF-1 is required to establish seedling architecture, leaf size and trichome differentiation. CAF-1 is needed to restrict branching of trichomes on rosette leaves. Increased trichome branching in CAF-1 mutants is not strictly correlated with increased nuclear DNA content. In addition, fas2 glabra3 double mutants show an additive genetic interaction, demonstrating that CAF-1 acts genetically parallel to the GLABRA3-containing, endoreduplication-coupled trichome branching pathway. However, CAF-1 is often needed to restrict endoreduplication, because seedlings of most CAF-1 mutants have increased ploidy. Notably, in the Landsberg erecta background, loss of CAF-1 does not affect ploidy, demonstrating that loss of CAF-1 can be compensated in some Arabidopsis accessions. These results reveal that the functions of FAS1, FAS2 and MSI1 are not restricted to meristems, but are also needed to control genome replication at multiple steps of development.

E2F RegulatesFASCIATA1, a Chromatin Assembly Gene Whose Loss Switches on the Endocycle and Activates Gene Expression by Changing the Epigenetic Status

“…In our conditions, homozygous fas1-4 plants showed ,3% of the full-length FAS1 mRNA levels and expressed a truncated product that lacks the domains required for interaction with proliferating cell nuclear antigen (PCNA) and other CAF subunits (data not shown). Arabidopsis fas1-4 plants showed phenotypes similar to those previously described for other fas1 alleles (Leyser and Furner, 1992;Kaya et al, 2001;Exner et al, 2006), such as reduced growth, altered floral organ structure, and reduced fertility associated with smaller siliques, among others (Supplemental Fig. S1).…”

“…It has been proposed that these genes are regulated differently in the C24 ecotype, where the fas1-4 mutation was identified, than in the En or Ler ecotypes, the background of the fas1-1 and fas2-1 mutations, respectively. This might well be the case because in the fas1-4 (Col-0 ecotype; Exner et al, 2006; this work) and fas1-2 and fas2-1 (En and Ler ecotypes, respectively; Schö nrock et al, 2006) plants, significant overexpression of G2 checkpoint genes is detected. Interestingly, expression of the Ku70 gene, a component of the G1 checkpoint pathway, was not altered, reinforcing the idea that defects in CAF-1 likely result in activation of a G2 checkpoint.…”

“…In addition, a role for FAS1 in the cell cycle has been proposed, although not experimentally demonstrated (Endo et al, 2006;Exner et al, 2006). Members of the E2F/DP family of transcription factors are among the major regulators controlling the expression of cell cycle genes (Gutierrez, 2005;Inzé and De Veylder, 2006).…”

Multiple Functions of Kip-Related Protein5 Connect Endoreduplication and Cell Elongation

“…Indeed, 75% of KRP5 targets are in heterochromatin regions, suggesting that KRP5 may modulate chromatin organization. Many lines of evidence link chromatin structure and DNA replication: replication timing requires specific chromatin marks (Casas-Delucchi et al, 2012), and recently, the chromatin factor CAF-1 has been implicated not only in the control of meristem structure but also in the control of genome replication at several stages of development (Exner et al, 2006). Another example is that mutations in the genes encoding the two homologous H3K27 monomethyltransferases ATXR5 and ATXR6 lead to the rereplication of specific genomic portions.…”

Impact of nucleosome dynamics and histone modifications on cell proliferation during Arabidopsis development

“…Both fas1 and msi1 mutants possess reduced heterochromatic content and, in general, a less compacted chromatin (Kirik et al, 2006;Schonrock et al, 2006). Also, CAF-1 is necessary to maintain the repressed state of a subset of genes involved in the G2 checkpoint (Endo et al, 2006;Exner et al, 2006;Kirik et al, 2006;Ramirez-Parra and Gutierrez, 2007b). However, instead of a permanent G2 arrest, as it occurs in animal cells, in the absence of CAF-1 plant cells trigger a premature switch to the endoreplication programme (Ramirez-Parra and Gutierrez, 2007b).…”