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Plant Physiology 139:1576-1585 (2005) © 2005 American Society of Plant Biologists Nuclear Actin-Related Proteins as Epigenetic Regulators of Development1Department of Genetics, University of Georgia, Athens, Georgia 30602
Complex regulatory networks control cell fate and the development of organs and tissues in multicellular organisms. But what mechanisms initiate the necessary global changes in patterns of gene expression? What regulates the regulators of organismal development? The nuclear actin-related proteins (ARPs) participate in macromolecular chromatin-remodeling machines that regulate the transcription of developmentally important genes. In Arabidopsis (Arabidopsis thaliana), ARP4, ARP6, and ARP7, which are predominantly localized in the nucleus, participate in the regulation of several pathways affecting cell proliferation and organ development. The diverse plant phenotypes resulting from deficiencies in these nuclear ARPs include reduced cell size or numbers, photoperiod-dependent and -independent early flowering, delayed floral senescence, altered leaf, stem, and flower organ morphology, embryo lethality, and an assortment of male and female reproductive defects. A working hypothesis emerging from these and other plant and animal data is that diverse isoforms of nuclear ARP-containing chromatin-modifying complexes exert epigenetic control over global regulators of multicellular development. In support of this hypothesis, we herein examine nuclear ARP phylogeny, the chromatin-remodeling activities of ARP-containing complexes that lead to epigenetic control of gene expression, the expanding developmental roles assigned to several putative plant ARP-containing complexes, as well as the evidence that a large number of ARP complex isoforms may have evolved in concert with the significant demands of multicellular development.
The ARPs share limited sequence identity (15%–60%) with conventional actins, but they appear to maintain the actin fold, a nucleotide-binding pocket and hinge region that enables a conformational change in actin. Eight to 10 ancient classes of ARPs are found in most eukaryotes that have been examined, and all appear to participate in protein complexes (McKinney et al., 2002
Nuclear ARPs act as essential subunits of macromolecular machines that remodel chromatin structure, and their only demonstrated functions are within such complexes. Specifically, ARP-containing complexes are involved in nucleosome phasing and movement, histone acetylation, and exchange of histone subunit isovariants within nucleosomes. The chromatin-modifying activities of these complexes can serve the basal regulatory function of reinforcing or alleviating the nucleosomal suppression of transcription that affects most genes (Yuan et al., 2005
The majority of genes encoding the nuclear ARPs evolved from a common ancestral actin gene prior to the divergence of the four eukaryotic kingdoms, yet the nuclear ARP proteins share 15% to 40% amino acid sequence identity with conventional actin (Blessing et al., 2004  ). Because the initial characterization of the entire family of ARPs was performed in yeast, most nuclear ARPs in other organisms are named relative to the yeast nuclear ARPs (Arp4, 5, 6, 7, 8, and 9; Poch and Winsor, 1997). The increasing numbers in this ARP nomenclature represent increasing divergence from conventional actin, with ARP4 being most closely related (approximately 40% amino acid identity to actin) and ARP9 the most divergent (approximately 15% identity; McKinney et al., 2002; Kandasamy et al., 2004). While the nuclear ARPs share the backbone of actin sequence and are predicted to retain the actin fold, they contain several, sometimes large, insertions and small deletions that distinguish each ARP clade. The phylogenetic relationships of the yeast nuclear ARPs to those in humans, Arabidopsis, and rice (Oryza sativa) are illustrated in Figure 1. Humans contain clear homologs of yeast ARP4 (HsaBAF53), Arp5 (HsARP5), Arp6 (HsARP6x), and Arp8 (HsARP8). Arabidopsis and rice ARP4, ARP5, ARP6, and ARP9 are clear plant homologs of ARP4 (Baf53), Arp5, Arp6, and Arp8, respectively, in animals and yeast. Thus, these four clades of ARPs (labeled in Fig. 1) certainly predate the divergence of the three kingdoms represented from a common ancestor. We have shown that Arabidopsis ARP4, ARP6, and ARP7 are localized to the interphase nucleus (Kandasamy et al., 2003; Deal et al., 2005), and by their phylogenetic position in the sequence tree the plant homologs of yeast ARP5, ARP8, and ARP9 are predicted to encode nuclear ARPs (Kandasamy et al., 2004). The six phylogenetically paired sets of plant ARP proteins from Arabidopsis and rice are 52% to 87% identical at the amino acid sequence level. Because these two angiosperms have not shared a common ancestor for 200 million years, it is likely that homologs to these six ARPs are reasonably well conserved and may be universally present in all higher plants (McKinney et al., 2002; Kandasamy et al., 2004). The phylogenetic relationships of Arabidopsis ARP7 and ARP8 to ARPs in other eukaryotic kingdoms are not clear, and hence, have an orphaned status (Blessing et al., 2004).
All of the nuclear ARPs that have been examined to date are constituents of either ATP-dependent nucleosome-remodeling (NR) complexes, histone acetyltransferase (HAT) complexes, or histone variant exchange (HVE) complexes, all of which are involved in the modification of chromatin structure (Olave et al., 2002 ; Mizuguchi et al., 2004). The ATP-dependent NR and HVE complexes all contain a DNA-dependent ATPase and use the energy of ATP hydrolysis to drive the repositioning of nucleosomes on DNA or the exchange of one histone type for another within nucleosomes. The NR and HVE complexes share other similar subunits, and there are mechanistic arguments that all NR complexes can carry out HVE activities (Flaus and Owen-Hughes, 2004). In contrast, the HAT complexes transfer an acetyl group onto histone N-terminal tails within nucleosomes, thereby altering chromatin structure indirectly, but they do not contain a DNA-dependent ATPase. The modifications that HAT and related complexes perform on the termini of histone polypeptides generate a histone code that can be decoded to define active and inactive regions of chromatin (Margueron et al., 2005). Surprisingly, the majority of the well-characterized chromatin-modifying complexes include monomeric actin as a subunit in addition to one or more ARPs (Olave et al., 2002).
A number of important themes have emerged regarding the biochemical functions of the ARPs and actins in NR, HVE, and HAT complexes, but no single function stands out as universally conserved in all complexes (Blessing et al., 2004
The activities of several nuclear ARP-containing chromatin-remodeling complexes are known. In yeast, for example, ARP4 is an essential gene and ARP4 protein is a component of the NUA4 (nucleosomal acetyltransferase of H4, HAT), the INO80 (inositol requiring) NR, and the SWR1 HVE complexes (Galarneau et al., 2000
In addition to ARP4, the yeast INO80 NR complex also contains ARP5, ARP8, monomeric actin, and seven other subunits as shown in Table I. The loss-of-function mutations for the Ino80 subunit, a DNA-dependent ATPase, are defective in transcribing the genes involved in inositol biosynthesis and are hypersensitive to DNA-damaging agents (Ebbert et al., 1999
For some time, our knowledge of ARP6 function was limited to the observation that this protein was localized to the nucleus in both yeast and Drosophila. However, two groups have recently isolated the yeast SWR1 complex and found that it contains not only ARP6, but also ARP4, actin, and 10 other subunits as listed in Table I (Krogan et al., 2004 ; Mizuguchi et al., 2004). This complex carries out a new class of chromatin-remodeling activity: the exchange of one histone variant for another within the nucleosome. The SWR1 HVE complex replaces histone H2A with the variant H2A.Z at specific chromosomal locations (Krogan et al., 2004; Mizuguchi et al., 2004). The H2A.Z histone variant is conserved among eukaryotes, and thus the HVE activity of ARP6-containing complexes is probably ancient and present in most eukaryotes. Histone H2A.Z-containing nucleosomes act partly to antagonize the spread of silent heterochromatin into euchromatic regions, but they also have important heterochromatic functions (Meneghini et al., 2003; Dryhurst et al., 2004).
Yeast SWI/SNF and RSC are two related ATP-dependent NR complexes containing 11 and 15 subunits, respectively, including ARP7 and ARP9. Table I shows the composition of the yeast SWI/SNF complex. Unlike the complexes described above, neither SWI/SNF nor RSC contain monomeric actin. The SWI/SNF complex was identified independently in genetic screens for genes involved in mating-type switching and Suc fermentation, and the RSC complex was later isolated based on homology to SWI/SNF complex components. Yeast strains lacking ARP7 or ARP9 show typical swi/snf– phenotypes, indicating that these proteins play an essential role in the function of SWI/SNF. In addition to the swi/snf– phenotype, mutations in ARP7 or ARP9 also lead to other transcriptional defects not related to SWI/SNF function, indicating that RSC plays a role in transcriptional regulation as well (Cairns et al., 1998 In summary, nuclear ARP functions are believed to be central to the activity of the majority of the known chromatin-remodeling complexes and to NR, HAT, and HVE complexes in particular. The six yeast nuclear ARPs (ARP4–9) are all found in these three classes of complexes. Thus, the subunit compositions of the yeast NR, HAT, and HVE complexes, such as those examples presented in Table I, are likely to be predictive of the basic subunit compositions of ARP-containing complexes in other kingdoms.
During the last few years, chromatin remodeling has been directly linked to numerous pathways of plant development (Wagner, 2003 ; Gendrel and Colot, 2005). Although it is known that ARPs are essential components of all SWI/SNF and most other chromatin-modifying complexes in yeast, there were until recently no data directly linking ARP functions to plant development. Therefore, it was exciting to find that knocking down or knocking out the Arabidopsis nuclear ARPs ARP4, ARP6, and ARP7 was associated with defects in several developmental pathways. A sampling of the developmental abnormalities associated with deficiencies in these three ARPs is illustrated in Figure 2. Reduction in ARP4 expression produces phenotypes affecting numerous aspects of plant growth and development (Kandasamy et al., 2005a). For example, the leaky arp4-1-deficient mutant allele is partially male sterile. Anthers retain a small, immature heart shape and make a small number of mature pollen grains (Fig. 2I), reducing the efficiency of selfpollination. Targeting the distinct 3' untranslated region of Arabidopsis ARP4 transcripts with RNA interference generates an epiallelic series with strong, moderate, or weak ARP4 deficiency phenotypes (Fig. 2). Strong lines with barely detectable ARP4 protein levels have smaller than normal cotyledons, leaves, inflorescence stems, flowers, and fruits (Fig. 2, C, D, and J). Under long-day but not short-day growth conditions, the strong RNAi lines flower a week early with only six rosette leaves compared to 12 leaves for wild type (Fig. 2G), suggesting a defect in the photoperiod-dependent flowering pathway. The plants with strong epialleles also show an extreme delay in floral organ senescence and abscission, with 20 or more flowers retaining their petals and sepals (Fig. 2H), whereas a wild-type inflorescence seldom retains these floral organs on more than six flowers.
ARP7 is an essential protein whose knockdown results in aberrant cell expansion and retarded plant development (Kandasamy et al., 2005b ). Knocking out the expression of Arabidopsis ARP7 protein in the homozygous arp7-1 T-DNA mutant produces morphologically abnormal embryos that are arrested early in development (torpedo stage, Fig. 2B). Moreover, knocking down the expression of ARP7 protein levels with RNA interference produces an epiallelic series of plant lines with dosage-dependant, heritable defects in multiple developmental pathways. ARP7-defective plants are severely to moderately dwarfed, with highly retarded roots having reduced elongation zones at their tips (Fig. 2F). Moreover, the dwarf plants contain fewer rosette leaves that were small and severely curled as compared to wild type. These smaller leaves have a similar number of cells to wild type, but the cells are about one-half the size of wild-type cells (Fig. 2E; Kandasamy et al., 2005b). ARP7-deficient plants show a significant decrease in fertility due to defects in pistil and anther development, and poor pollen production. Silenced lines also show delayed abscission of the petal and sepals (Fig. 2H).
Null alleles lacking ARP6 protein (arp6-1, arp6-2) display defects during several stages of Arabidopsis development (Choi et al., 2005
In plants, the mechanisms by which ARP-containing chromatin-remodeling complexes are targeted to specific genes are poorly understood, but there are several examples of the subunits of these complexes acting as high-level regulators of cell proliferation and development. The control of flowering time in Arabidopsis is the most thoroughly studied plant developmental pathway regulated by changes in chromatin structure, as summarized in Figure 3 (He and Amasino, 2005
FLC and a few other related transcription factors appear to be the primary global regulators of flowering time that integrate signals from the various information pathways. Thus, the flowering-time signaling pathway in Arabidopsis is relevant to dissecting subsets of ARP4 and ARP6 functions. The photoperiod-independent early flowering of ARP6 knockout mutants is associated with reduced expression of FLC as well as MADS AFFECTING FLOWERING 4 and MADS AFFECTING FLOWERING 5 (Deal et al., 2005 ). Consistent with the reduced expression of FLC, the downstream targets of FLC, FT, and SOC are increased in expression in arp6 mutants. In addition, arp6 mutations suppress the FLC-mediated late flowering of a dominant FRIGIDA allele, indicating that ARP6 is required for the activation of FLC expression to levels that inhibit flowering (Choi et al., 2005; Deal et al., 2005). Finally, strong overexpression of ARP6 resulted in no abnormal plant phenotypes, consistent with ARP6 activity being limited by other components of a chromatin-modifying complex. Thus, FLC expression appears to be directly controlled by chromatin remodeling that is dependent upon the normal expression of ARP6.
PHOTOPERIOD-INDEPENDENT EARLY FLOWERING1 and ARP6 encode the closest Arabidopsis homologs of two subunits in the yeast SWR1 complex. The photoperiod-independent early flowering1 and arp6 mutants have many of the same diverse developmental phenotypes, suggesting they participate in the same chromatin-remodeling complex(es) (Noh and Amasino, 2003 In summary, there are abundant examples of chromatin remodeling being required for normal plant development. Deficiencies in Arabidopsis ARP4, ARP6, and ARP7 each result in multiple distinct developmental abnormalities including defects in cell expansion and proliferation, dwarfing, and/or alterations in the shape of every vegetative and reproductive organ, and alterations in the timing of developmental pathways such as flowering and floral senescence. The defects observed are consistent with their roles in chromatin-remodeling complexes effecting epigenetic changes in the expression of global regulators like FLC. The possible roles of putative plant nuclear ARPs, ARP5, ARP8, and ARP9 in plant development are as yet unknown.
There is substantial evidence that diverse isoforms of ARP-containing chromatin-modifying complexes exist with the potential to exert epigenetic control over development. To define what is meant by isoforms of chromatin complexes, consider the ARP-containing SWI/SNF, SWR1, and INO80 complexes. All three complexes contain 12 to 13 different protein subunits, summarized in Table I. Protein isovariants are classically defined as closely related polypeptides with altered sequences encoded by different gene family members. In plants and animals, divergent gene families encode multiple isovariants of several subunits in each complex. Substituting a single subunit with a different isovariant would generate a new complex isoform with the potential to recognize a new target gene or carry out a slightly different chromatin-modifying reaction (i.e. different phasing of nucleosomes or different histone modifications). Sequentially substituting three different isovariants of, for example, the Snf2 DNA-dependent ATPase subunit of a SWI/SNF complex would generate three isoforms of the complex. By extension, substituting three different isovariants of two different subunits has the potential to generate nine isoforms, and so on. Besides being derived from gene families, protein isovariants could be generated from single genes by alternate splicing or polyadenylation site selection, alternate initiation and termination of translation, and posttranslational protein modifications.
Direct and indirect support for the existence of multiple isoforms of chromatin-remodeling complexes can be found in the plant and animal literature and from further examination of their complex genomes. Several human and mouse chromatin-remodeling complexes were first isolated as mixtures of isoforms. For example, the purified mammalian BAF or SWI/SNF complex was shown to have a basic composition of about nine to 12 proteins, but it existed in several isoforms. Isoforms purified from various organs varied in their Baf60 subunit and Swi2/Snf2 subunit compositions (Wang et al., 1996 Evidence for large numbers of isoforms of ARP-containing complexes in plants comes indirectly from the existence of small gene families encoding subunit isovariants, which we will discuss briefly in the context of the Arabidopsis genome. The three yeast complexes SWI/SNF, SWR1, and INO80 collectively contain all the yeast nuclear ARPs: ARP4, ARP5, ARP6, ARP7, ARP8, and ARP9 (www.yeastgenome.org). As a case study, the plant chromatin (www.chromdb.org) and The Arabidopsis Information Resource (www.arabidopsis.org) databases were searched for homologs of the subunits of these three yeast complexes. Table I summarizes this preliminary examination of Arabidopsis subunit isovariants. The yeast SWI/SNF, SWR1, and INO80 complexes each contain a single, high-Mr snf2-related ATPase subunit, Snf2, Swr1, and Ino80, respectively. The yeast genome encodes a total of 10 distinct Snf2-related proteins (www.yeastgenome.org), and all 10 ATPases are known to participate in a different chromatin-remodeling complex. By contrast, Arabidopsis encodes 42 genes that can be classified as homologs of these ATPases, with one or more being closely allied with each of the 10 yeast sequences in a protein sequence tree (www.chromdb.org). The Arabidopsis clade encoding the immediate homologs of yeast Snf2 contains four genes (Table I). Because the Snf2-related ATPases are not known to participate in any processes other than chromatin modification and have been found primarily in ARP-containing chromatin-remodeling complexes, it is likely that these four closest relatives of the Snf2-ATPase will participate in different isoforms of the Arabidopsis SWI/SNF complex. A similar analysis shows that in addition to the four Snf2 isovariants, Arabidopsis encodes two, two, four, and two isovariants of yeast Snf12, Swi1, Swi3, and Taf14 subunits, respectively (Table I). If these 14 subunit isovariants from the five Arabidopsis gene families are freely interchangeable in SWI/SNF complexes, 128 isoforms of the Arabidopsis complex (i.e. 4 x 2 x 2 x 4 x 2 = 128) would be generated. Each would have the potential to target different genes or carry out variations in NR complex function.
A recent analysis of mutants in the four Arabidopsis Swi3 (Table I) isovariants provides direct support for the functional significance of four SWI/SNF complex isoforms each with a different Swi3 isovariant (Zhou et al., 2003 Moreover, homologs of several subunit proteins within the yeast SWR1 and INO80 complexes are also encoded by small gene families in Arabidopsis, as shown in Table I. There are 21 subunit isovariants in six families with the potential to produce 1,200 SWR1 isoforms. Similarly, there are 14 isovariants in four families with the potential to produce 84 INO80 isoforms. Thus, Arabidopsis ARP4, ARP5, ARP6, and perhaps ARP7 and ARP8 are each predicted to participate in numerous distinct isoforms of complexes distinguished by their isovariant subunit compositions. Each individual ARP complex with a different isovariant composition might control only one or a few target genes participating in the global regulation of development. It seems reasonable to ask how diverse isoforms of ARP-containing chromatin-remodeling complexes became functionally linked to the macroevolution of multicellular development. One evolutionary view would be that as plants and animals diversified from single-celled protist ancestors, there was a combinatorial expansion in the number of nuclear ARP complex isoforms following an expansion and diversification of the gene families encoding their various subunit isovariants. An increase in chromatin-modifying complex isoforms allowed the natural selection of more specialized control over chromatin dynamics and target gene transcription, which generated more specialized epigenetic control over multicellular development. It is logical to assume that greater target gene specificity and more finely tuned epigenetic control were selective advantages to multicellular organisms.
Eukaryotic genomes encode several ancient classes of nuclear ARPs that participate in macromolecular machines affecting chromatin dynamics. Nuclear ARPs are variously required for assembly, chromatin binding, and/or the enzymatic activities of different complexes. ARP-containing chromatin-modifying complexes carry out NR, chemical modifications of histones, or HVE reactions. These activities exert epigenetic control over cell proliferation and multicellular development along with controlling basal levels of transcription. In Arabidopsis, developmental pathways affecting every plant organ require normal levels of ARP4, ARP6, and/or ARP7 expression, providing strong evidence for this role. Diverse isoforms of ARP complexes may provide the greater target gene specificity and wider variety of chromatin-modifying activities needed for multicellular development, relative to development of single-celled organisms like yeast. Sequence data from this article can be found in the GenBank/EMBL data libraries under locus numbers given in Table I.
We would like to thank Dr. Haini Cai and Gay Gragson for their critical reading of the manuscript. Received October 5, 2005; returned for revision October 6, 2005; accepted October 6, 2005.
1 This work was supported by the National Institutes of Health (grant no. GM 36397–18 to R.B.M. and training grant no. GM 07103–29 to R.B.D.).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Richard B. Meagher (meagher{at}uga.edu). www.plantphysiol.org/cgi/doi/10.1104/pp.105.072447. * Corresponding author; e-mail meagher{at}uga.edu; fax 706–542–1387.
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