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1 Department of Integrated Genetics, National Institute of Genetics, Mishima 411-8540, Japan
2 Department of Botany, Graduate School of Science, Kyoto University, Sakyo-ku, 606-8502, Kyoto, Japan
3 Department of Plant Biology, University of Geneva, Science III, 30 Quai Ernest-Ansermet, CH-1211, Geneva 4, Switzerland
4 Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, CH-4058 Basel, Switzerland
5 Gregor Mendel Institute of Molecular Plant Biology, Austrian Academy of Sciences, Dr. Bohr-Gasse 3, AT-1030, Vienna
6 Adjunct Division of Applied Genetics, National Institute of Genetics, Mishima 411-8540, Japan
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Abstract |
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 Top Abstract IntroductionResultsDiscussionExperimental proceduresReferences |
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Introduction |
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TopAbstractIntroductionResultsDiscussionExperimental proceduresReferences |
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CAF-1 was originally purified from human cell nuclear extracts as an activity that facilitates the nucleosome assembly of newly synthesized DNA (Kaufman et al. 1995; Smith & Stillman 1989). CAF-1 is a histone binding protein complex conserved in various organisms from yeasts to human and higher plants (Kamakaka et al. 1996; Kaufman et al. 1995, 1997; Murzina et al. 1999; Kaya et al. 2001), and it is expected to be involved in, at least, de novo nucleosome assembly during DNA replication in living cells (Krude 1995; Verreault et al. 1996; Shibahara & Stillman 1999).
In Arabidopsis, fas1 and fas2 are the only viable loss-of-function mutants of the CAF-1 p150 and p60 subunits in multicellular organisms. These mutants exhibit essentially the same morphological abnormalities including fasciation, reduced root growth, and disorganization of meristems (Leyser & Furner 1992; Kaya et al. 2001). Importantly, the extent of these abnormalities varies between individual plants and tends to increase with time. In addition, the expression of WUSCHEL and SCARECROW in meristems is disturbed, and particularly, the pattern of misexpression of SCR is unique, with a wide range of variation between individual plants and even between neighboring roots of the same plant (Kaya et al. 2001). However, information on the relation of cause and effect among loss of CAF-1 activity, the stochastic occurrence of the fas phenotype, and disturbances in gene expression is still lacking.
In higher plants, loci in heterochromatin are marked by DNA methylation, histone H3 methylation at lysine 9 (K9), their specific localization in condensed heterochromatin, or the presence of short interfering RNA (Mette et al. 2000; Morel et al. 2000; Miura et al. 2001; Gendrel et al. 2002; Soppe et al. 2002; Lippman et al. 2003). They are thereby kept transcriptionally silent in a wild-type background irrespective of the developmental state of the cells. In order to clarify the implications of CAF-1 in the maintenance of chromatin states in higher eukaryotes, we investigated the TGS defects in fas mutants by different approaches. We obtained multiple evidence that TGS of various endogenous genes and the silent GUS transgene is released in a low incident and in an accidental, stochastic manner in fas mutants.
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Results |
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Many transposon-derived sequences are widely dispersed in the genomes of higher plants, although their roles in genome integrity and regulation of gene expression remain unknown. Endogenous CACTA family transposons are heavily methylated and transcriptionally silenced in wild-type plants (Miura et al. 2001). However, CACTA is transcriptionally active and transposed in decrease in DNA methylation 1 (ddm1) mutants, accompanied by reduced cytosine methylation and the dispersion of the CACTA loci away from the chromocenters (Miura et al. 2001; Soppe et al. 2002).
In order to examine the expression of CACTA in fas mutants, fas2-2, originally in Nossen background, was crossed four times into Columbia (Col) background (hereafter referred to as fas2 (Col)), that has potentially active CACTA members (Miura et al. 2001, 2004). This fas2 (Col) allele is supposed to be a null mutant of the single-copy gene for the CAF-1 p60 subunit in Arabidopsis. The mutation of fas2-2 causes a frame-shift and deletes most of the protein if translated, leaving only one WD-40 repeat intact (Kaya et al. 2001). In addition, the fas2-2 phenotype is indistinguishable from that of a FAS1-deletion line that completely lacks the largest subunit of CAF-1 (Kaya et al. 2000).
As shown in the RT-PCR analysis in Fig. 1A, strong signals for CACTA transcripts were detected in all three young seedlings of ddm1 (lanes 4–6), whereas a much weaker signal for CACTA transcripts was seen in only one of the three young seedlings of fas 2 (Col) (lanes 7–9). The varied expression of CACTA found in fas plants was not due to differing numbers of CACTA elements in the genome of individual fas2 (Col) plants, since we confirmed that fas2 (Col) had the same number of all five members of the CACTA family (homozygous for each) located in the same genomic regions as in wild-type Col plants (Miura et al. 2004). De-repression of CACTA was also observed in a mutant of another subunit of CAF-1, fas1-1 (Col) (originally isolated in ecotype Enkheim but backcrossed four times into the Col background) (data not shown).
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Transcripts of CACTA are detected in a small population of cells in fas mutants
To further analyze the defects in CACTA gene silencing in fas2 (Col) plants, in situ RNA hybridization was performed with sections of shoot apical meristems (SAM) and leaf primordia, as shown in Fig. 2. In all ddm1 sections, clear and strong signals were observed in all cells of SAM and leaf primordia (Fig. 2B), whereas no signal was detected among more than 50 wild-type plants (Fig. 2A). In contrast to ddm1, weak but distinct signals for CACTA transcripts were seen in small clusters of cells in fas2 (Col) plants (Fig. 2C,D), and in some cases, the CACTA signal was restricted to either a single or a couple of cells (Fig. 2E and its serial sections in Fig. 2L–P). In most cases, the signals were observed in adjacent cells of the same SAM or the same leaf primordium in serial sections (Fig. 2G–K), strongly suggesting that the weak signals in fas2 (Col) plants were specific to CACTA transcripts in the sectors. Importantly, signals were not observed in all fas2 (Col) plants, and only 11.2% of fas2 (Col) plants (eight of 71 five-day-old plants) were positive for the signal in one or more sections. Furthermore, the sizes and sites of the cell clusters expressing CACTA signals were not constant and varied between plants. These observations indicate that transcriptional activation of CACTA was weak and infrequent, and occurred in a stochastic manner. This explains why the CACTA transcripts were not detected in all of the young fas2 (Col) plants in Fig. 1.
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A MULE DNA transposon, AtMu1, on chromosome 4 and a hypothetical gene, T5L23.26, at a heterochromatin knob of chromosome 4 are methylated at cytosine residues and transcriptionally silenced in a wild-type background (Gendrel et al. 2002; Lippman et al. 2003). We investigated whether these silent genes at different chromosomal locations (Fig. 3A) were released simultaneously or independently in the fas mutants. As shown in the RT-PCR analyses in Fig. 3B, CACTA, AtMu1, and T5L23.26 were transcribed in all ddm1 plants (lanes 12–23), whereas some, but not all, young fas2 (Col) plants expressed either one or two genes in random combinations (lanes 24–36). Therefore, it is suggested that the two genes, AtMu1 and T5L23.26, were transcriptionally released in a similar stochastic manner as CACTA, and that the three genes at different chromosomal loci were de-repressed independently and randomly in fas plants.
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The silent GUS transgene is de-repressed in a stochastic manner in fas mutants
Transgenes in higher plants are often repressed by either post-transcriptional gene silencing (PTGS) or TGS. In the transgenic Arabidopsis line L5, a GUS transgene is transcriptionally silenced (Morel et al. 2000; Probst et al. 2004). To investigate the effects of mutations in CAF-1 on the GUS transgene silencing, we crossed fas and morpheus molecule 1 (mom1) plants, which are defective in TGS without affecting DNA methylation (Amedeo et al. 2000), with the L5 line.
In the L5 wild-type background, no staining was observed in most cases (Fig. 4A), with the exception of a very few single GUS-positive cells in some seedlings (Fig. 4D). GUS was expressed uniformly in large sectors throughout the plant body in all mom1 homozygotes (Fig. 4B), consistent with previous reports (Amedeo et al. 2000; Takeda et al. 2004). In fas2-2 homozygotes, activation of GUS was also observed, but in contrast to mom1, sectors of GUS-positive cells in fas2-2 plants were much smaller in size (Fig. 4C,E,F). The frequency of GUS-positive cells and sectors varied among fas2-2 plants (see Fig. 4E,F). However, no correlation between the frequency of GUS-positive cells and the severity of the morphological phenotype was observed (data not shown). Similar reactivations of the silent GUS transgene have been observed in fas1-1, fas1-2, and fas2-1 mutants (data not shown). Therefore, it is not likely that this mode of interference with TGS is caused by only a partial loss of CAF-1 activity. It was excluded that this stochastic de-repression of GUS in fas plants is due to crossing different ecotypes, since L5 (Col) crossed with various wild-type plants did not show such staining patterns (data not shown).
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A single or a couple of GUS-positive cells in the cotyledons was frequently observed in the fas mutants (Fig. 4H,N), but they are rare in the wild-type plants. Cell divisions are not frequent in cotyledons after germination (Stoynova-Bakalova et al. 2004), but endoreduplication occurs in mature cotyledons (Melaragno et al. 1993). Therefore, such a de-repression of silent GUS might occur during endoreduplication and/or postmitotically in mature cotyledons. Alternatively, the lack of CAF-1 during mitosis might provoke intermediate and vulnerable chromatin states from which GUS is subsequently more easily and sporadically de-repressed without mitotic events.
Guard cells of stomata in leaves are produced by a series of asymmetric and symmetric cell divisions (Nadeau & Sack 2003). Interestingly, only one guard cell within a single stomatal complex was clearly stained in some cases (Fig. 4K) whereas in other cases both guard cells derived from the same precursor cell were stained (Fig. 4L,M). GUS staining in only one of the two guard cells is not easily explained. We suggest that chromatin states can be accidentally changed in only one daughter strand through DNA replication during the last symmetric cell division of a guard mother cell. Alternatively, the mutations in FAS may also affect the stability of the silent states even postmitotically, although CAF-1 contributes to the stable propagation of chromatin states primarily during DNA replication.
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Discussion |
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In this study, we showed that endogenous silent genes located at different chromosomal sites were activated randomly and non-concomitantly with each other. Histological analyses of the silent CACTA transposons and the silent transgene GUS showed that these silent genes were de-repressed in a stochastic manner in the fas mutants. The stochastic nature of the TGS defects in fas mutants are distinct from other TGS mutants in which TGS is uniformly released in all cells. These observations are reminiscent of previous findings in cac budding yeast cells, which have deletions in genes encoding the subunits of CAF-1 and exhibit an increased rate of switching from transcriptionally inactive to transcriptionally active states for the silent genes at telomere and HML locus (Monson et al. 1997; Enomoto & Berman 1998).
In higher plants, loci at heterochromatin are marked and maintained by specific epigenetic modifications including DNA cytosine methylation, histone modifications, their specific localization in condensed heterochromatin, or the presence of short interfering RNA (Mette et al. 2000; Morel et al. 2000; Miura et al. 2001; Gendrel et al. 2002; Soppe et al. 2002; Lippman et al. 2003). It is interesting to investigate whether the accidental transition from transcriptionally inactive states to active states in fas mutants is preceded and triggered by changes in these epigenetic marks. However, the gross level of DNA methylation (Supplementary Fig. S1) and the formation of chromocenters (Takeda et al. 2004) are not changed in fas mutants. Stochastic release of TGS in fas mutants might be caused mainly by disturbance of speed or efficiency of nucleosome formation during DNA replication. Given that epigenetic states are accidentally erased and altered, fas mutants might accumulate unexpected transitions of transcriptional states in the course of development, and they might carry these altered states into subsequent generations. Indeed, among siblings of fas2 (Col) mutants, the number of plants showing ectopic expression of CACTA increased with time (Fig. 1), and the expression of SCR::GFP was disturbed more severely in older roots than in younger roots (Kaya et al. 2001). These suggest a progressive effect of the fas mutation at least during growth. However, whether transitions of transcriptional states are inherited to the next generation is an interesting question to be resolved.
Models for the role of CAF-1 in the maintenance of epigenetic states
How CAF-1 contributes to the maintenance of chromatin states in living cells is an important issue (Ridgway & Almouzni 2000; van Nocker 2003). CAF-1 is known to be involved in de novo nucleosome assembly (Verreault 2000; Krude & Keller 2001; Mello & Almouzni 2001). The CAF-1-mediated system is the only nucleosome assembly pathway coupled to DNA replication so far known (Hoek & Stillman 2003), and there are no equivalent genes or activities that could compensate for the loss of CAF-1 in Arabidopsis (Kaya et al. 2001). Therefore, we postulate that rapid nucleosome formation would be disturbed, at least locally, in the absence of CAF-1, leaving replicated DNA naked and easily accessible for a longer period of time. Such a situation would increase the probability that DNA-binding proteins are accidentally targeted to the newly synthesized DNA, causing accidental transition of transcriptional states with or without misplaced modifications of chromatin (Fig. 5A).
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Alternatively, CAF-1 might play a role in the maintenance of epigenetic marks via recruitment of some chromatin components. A specific interaction between CAF-1 p150 and heterochromatin protein 1 (HP1) in mouse and human has been reported (Murzina et al. 1999; Quivy et al. 2004), suggesting that CAF-1 plays a key role in pooling and delivering HP1 to heterochromatic sites at replication foci during DNA replication (Quivy et al. 2004). CAF-1 can also associate with methyl-CpG binding protein1 (MBD1), and this association is required for H3-K9 methylation by SETDB1 during DNA replication (Sarraf & Stancheva 2004). If Arabidopsis CAF-1 would bind to functional homologs of HP1 or MBD1, the recruitment of these chromatin components or related activities by CAF-1 at the silent chromatin loci would be disrupted in fas mutants, resulting in the release of TGS (Fig. 5C).
Recently, bru1 mutants (also reported as tsk or mgo3) have also been shown to exhibit phenotypic similarities to fas mutants (Guyomarc’h et al. 2004; Suzuki et al. 2004; Takeda et al. 2004). These include variable degrees of developmental abnormalities, accompanied by misregulation of meristematic genes, and in particular, the stochastic release of TGS. However, the molecular function of BRU1 and the link between BRU1 and CAF-1 is still unknown. Future analysis of BRU1 would provide yet another clue for understanding the mechanisms of epigenetic maintenance.
A link between the loss of CAF-1 function and a stochastic occurrence of variegated phenotypes in fas mutants
Multilayer devices must ensure the maintenance of chromatin states in the development of multicellular organisms, and we propose that CAF-1 contributes to this process. Indeed, the most prominent feature of fas mutants is the stochastic occurrence of the various pleiotropic phenotypes (Leyser & Furner 1992; Kaya et al. 2001), which appear to be reinforced by additional mutations in either one of two anti-silencing function1 (ASF1) orthologues in Arabidopsis, AtASF1a and AtASF1b (our unpublished observation). ASF1 is a histone H3-H4 binding protein known to facilitate CAF-1-dependent nucleosome assembly probably via its interaction with the second largest subunit of CAF-1 (Tyler et al. 1999, 2001). In higher eukaryotes, many developmental genes in euchromatic regions are also repressed by compaction into a heterochromatin-like structure and are kept silent throughout the course of development unless required. We predict that, in fas mutants, the expression states of many genes involved in various developmental phases are unstable, and even developmentally silent genes are de-repressed accidentally, thereby causing the stochastic occurrence of varied morphological alterations. Future analysis to link morphological phenotypes and the aberrant expression of the genes responsible for the phenotypes will be important for understanding the physiological roles of CAF-1 in multicellular organisms.
In conclusion, we observed in fas mutants that a lack of CAF-1 releases TGS of these genes in a stochastic manner at different times and sites. Therefore, we conclude that CAF-1 ensures the fidelity of the stable propagation of silent chromatin states through the growth and development of higher plants.
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Experimental procedures |
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TopAbstractIntroductionResultsDiscussionExperimental proceduresReferences |
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Plants were grown at 22 °C under constant light as previously described (Kaya et al. 2001). The mutants, ddm1-1, fas, and mom1, were also as previously described (Vongs et al. 1993; Amedeo et al. 2000; Kaya et al. 2001). fas1-1 (originally in Enkheim background) and fas2-2 (originally in Nossen background) were backcrossed four times with Columbia.
RT-PCR
Total RNA was prepared using Concert Plant RNA (Invitrogen). Aliquots of total RNA treated with DNase I were reverse transcribed with oligo (dT) primer and Superscript II reverse transcriptase (Invitrogen), and the cDNA was amplified using Takara EX taq DNA polymerase (Takara). PCR conditions were as follows: for CACTA, 40 cycles (96 °C, 30 s; 55 °C, 30 s; 72 °C, 100 s) with primers SP15 and SP40 (Kato et al. 2003); for AtMu1, 35 cycles (94 °C, 30 s; 60 °C, 30 s; 72 °C, 2 min) with primers AtMu1F and AtMu1R (Lippman et al. 2003); for T5L23.26, 35 cycles (94 °C, 30 s; 58 °C, 30 s; 72 °C, 2 min) with primers T5L23.26F and T5L23.26R(Gendrel et al. 2002); for AP2 as a control, 32 cycles (96 °C, 30 s; 55 °C, 30 s; 72 °C, 1 min) with primers AP2A and AP2R.
In situ RNA hybridization
In situ RNA hybridization was performed basically as described (Kaya et al. 2001). The fragment of CACTA element was amplified by RT-PCR using primers SP15 and SP40 (Kato et al. 2003), and transcribed using a DIG RNA Labelling Kit (Roche) after subcloning. The probes were used for hybridization after confirming their quality and quantity by agarose gel electrophoresis. Tissue sections (8 µ thick) treated with protease K were hybridized in buffer (50% formamide, 5xSSC) at 58 °C for 12 h. After washing with 0.1 x SSC at 65 °C, the slides were processed for detection of the DIG antigen. This involved blocking with DIG-blocking reagent (Roche), followed by incubation with alkaline phosphatase-conjugated anti-DIG Fab fragments (Roche). Immunological detection was performed by incubation in a NBT/BCIP solution (Roche).
Histochemical detection of GUS expression
The L5 line has one transgenic locus, 35S-GUS, with more than two copies of the gene, and the GUS locus was silenced at the transcriptional level (Morel et al. 2000; Probst et al. 2004). GUS expression analysis was performed basically as previously described (Kaya et al. 2001). Plants were incubated in reaction buffer containing potassium ferrocyanide and potassium ferricyanide to minimize diffusion artifacts and to enable observation of clear clonal sectors.
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Acknowledgements |
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Footnotes |
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These authors (Tatsuya Ono and Hidetaka Kaya) contributed equally to this work. 
Communicated by: Masao Tasaka aPresent address: Department of Cell Signaling, Genome & Drug Research Center, Tokyo University of Science, Noda, Chiba 278-8510, Japan
bPresent address: Bioscience and Biotechnology Center, Nagoya University, Chikusa, Nagoya 464-8601, Japan
* Correspondence: E-mail: kshibaha{at}lab.nig.ac.jp |
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Received: 26 August 2005
Accepted: 8 November 2005
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A. Kirik, A. Pecinka, E. Wendeler, and B. Reiss The Chromatin Assembly Factor Subunit FASCIATA1 Is Involved in Homologous Recombination in Plants PLANT CELL, October 1, 2006; 18(10): 2431 - 2442. [Abstract] [Full Text] [PDF]
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