| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
|
First published online October 13, 2006; 10.1104/pp.106.088344 Plant Physiology 142:1412-1426 (2006) © 2006 American Society of Plant Biologists Developmentally Controlled Farnesylation Modulates AtNAP1;1 Function in Cell Proliferation and Cell Expansion during Arabidopsis Leaf Development1Institute of Plant Sciences, ETH Zürich, 8092 Zurich, Switzerland
In multicellular organisms, organogenesis requires tight control and coordination of cell proliferation, cell expansion, and cell differentiation. We have identified Arabidopsis (Arabidopsis thaliana) nucleosome assembly protein 1 (AtNAP1;1) as a component of a regulatory mechanism that connects cell proliferation to cell growth and expansion during Arabidopsis leaf development. Molecular, biochemical, and kinetic studies of AtNAP1;1 gain- or loss-of-function mutants indicate that AtNAP1;1 promotes cell proliferation or cell expansion in a developmental context and as a function of the farnesylation status of the protein. AtNAP1;1 was farnesylated and localized to the nucleus during the cell proliferation phase of leaf development when it promotes cell division. Later in leaf development, nonfarnesylated AtNAP1;1 accumulates in the cytoplasm when it promotes cell expansion. Ectopic expression of nonfarnesylated AtNAP1;1, which localized to the cytoplasm, disrupts this developmental program by promoting unscheduled cell expansion during the proliferation phase.
Genetic analysis of eukaryotic protein prenyl transferases showed that modification of target proteins by farnesyl or geranylgeranyl is critical for control of development, growth, and signaling. Prenyl transferases covalently attach a 15-carbon farnesyl diphosphate (FPP) or the 20-carbon geranylgeranyl diphosphate (GGPP) isoprenoids to a Cys acceptor, which is part of a C-terminal CaaX box motif in the substrate proteins. Protein farnesyl transferase (PFT) and geranylgeranyl transferase (PGGT-I) share a common  -subunit but have distinct  -subunits. Specificity of PFT and PGGT-I is determined by the -subunits of each enzyme through sequence-specific recognition of the C-terminal CaaX box motif in substrate proteins (Yalovsky et al., 1999 ; Sinensky, 2000). Specific inhibitors of PFT or PGGT-I inhibit progression of the cell cycle in plant and animal cells, indicating that prenylation is required for the function of proteins involved in regulating cell division (Morehead et al., 1995; Qian et al., 1996; Tamanoi et al., 2001). For example, Ras, LKB1, CENP, or TC10, which are involved in cell proliferation and differentiation or cytoskeletal functions, are prenylated proteins. Prenylation modulates their function by facilitating membrane association as well as protein-protein interaction (Tamanoi et al., 2001; Hussein and Taylor, 2002; Martin and St Johnston, 2003; Elam et al., 2005). Protein prenylation is conserved in animals and plants (Yalovsky et al., 1999), but, unlike mice in which PFT is essential for early embryonic proliferation (Mijimolle et al., 2005), loss of Arabidopsis (Arabidopsis thaliana) PFT (era1) or PFT/PGGT-I (plp) gene functions is not lethal, although the mutants are affected in their development (Yalovsky et al., 2000a; Running et al., 2004; Mijimolle et al., 2005). This could be due to the specific types of proteins that are prenylated in plants, because most plant candidate protein prenyl transferase protein substrates differ from those identified in yeast (Saccharomyces cerevisiae) and animals (Galichet and Gruissem, 2003).
Among plant candidate PFT protein substrates, nucleosome assembly protein 1 (NAP1) is conserved among eukaryotes and has been identified in soybean (Glycine max), pea (Pisum sativum), rice (Oryza sativa), and tobacco (Nicotiana tabacum) BY2 cells, human, yeast, murine, and Drosophila melanogaster cells (Ishimi et al., 1984 Arabidopsis has four NAP1-related genes whose function is currently not known. We investigated Arabidopsis nucleosome assembly protein 1 (AtNAP1;1), which has a predicted CaaX motif, to understand the function of the protein and the potential role of its farnesylation during Arabidopsis development. Characterization of gain- and loss-of-function mutants demonstrated that AtNAP1;1 contributes to the regulation of cell proliferation and cell expansion. The developmental function of AtNAP1;1 appears to be regulated by the differential farnesylation of the protein during specific stages of leaf development.
AtNAP1;1 Is a Farnesylated Protein
The presence of the CKQQ motif at the C-terminal end of AtNAP1;1 suggested that the protein is a substrate of PFT. To test if AtNAP1;1 can be prenylated by PFT, we incubated the purified protein with recombinant Arabidopsis PFT and [3H]FPP. AtNAP1;1 was labeled strongly in the presence of both PFT and [3H]FPP but not with PGGT-I using either [3H]FPP or [3H]GGPP (Fig. 1A
). AtNAP1;1 was also labeled weakly by PFT using [3H]GGPP, because the enzyme is somewhat promiscuous for GGPP (Trueblood et al., 1993
To substantiate that AtNAP1;1 is a substrate for PFT, protein extracts from wild-type or era1-1 flowers were tested as a source for the enzyme (Fig. 1B). AtNAP1;1 but not AtNAP1;1C369S was labeled in the presence of protein extracts from wild-type flowers, confirming that the protein extract had PFT activity and that AtNAP1;1 could be correctly farnesylated at the Cys acceptor in the CKQQ prenylation motif. The protein extract from era1-1 flowers was unable to farnesylate AtNAP1;1, confirming the lack of PFT activity in the mutant and establishing that AtNAP1;1 is a substrate of PFT. To confirm that AtNAP1;1 is also farnesylated in vivo, we expressed green fluorescent protein (GFP)-AtNAP1;1 and GFP-AtNAP1;1C369S in tobacco BY-2 cells under control of the cauliflower mosaic virus (CaMV) 35S promoter. Soluble proteins from cells labeled with [3H]mevalonic acid were extracted and separated on SDS-polyacrylamide gels, which were then used either for immunoblot analysis with a polyclonal NAP1 antibody or for fluorography to detect labeled GFP-AtNAP1;1 (Fig. 1C). GFP-AtNAP1;1 and GFP-AtNAP1;1C369S were expressed to a similar level in BY-2 cells. A labeled protein corresponding to the size of GFP-AtNAP1;1 was detected only in extracts from cells expressing GFP-AtNAP1;1 but not in cells expressing GFP-AtNAP1;1C369S or in control BY-2 cells. Together, these results establish that AtNAP1;1 is efficiently farnesylated in vivo as well.
Most farnesylated proteins in yeast and animal cells are targeted to the plasma membrane (Sinensky, 2000
To obtain further insights into the potential role of farnesylation for AtNAP1;1 subcellular localization, GFP-AtNAP1;1 and GFP-AtNAP1;1C369S were stably expressed in transgenic tobacco BY-2 cells (Fig. 2B). GFP-AtNAP1;1 was localized in both the cytoplasm and the nucleoplasm of interphase cells. During mitosis, GFP-AtNAP1;1 was colocalized with the phragmoplast in telophase. Localization of GFP-AtNAP1;1C369S was similar (data not shown). Together, we conclude that the farnesylation status of AtNAP1;1 has no immediate role in the subcellular localization of the protein during the cell cycle.
We examined the physiological role of AtNAP1;1 farnesylation by functional complementation assays using the yeast nap1 mutant strain DK213. This mutant has a reduced growth rate at 37°C and a delay in mitosis, resulting in cells that are elongated and form clumps (Kellogg et al., 1995
Cell Proliferation Is Reduced in Atnap1;1 Leaves
To gain further insight into AtNAP1;1 function, we identified two independent Atnap1;1 mutant alleles in the SALK T-DNA insertion collection (SALK_013610 and SALK_095311; Alonso et al., 2003
Homozygous Atnap1;1-1 and Atnap1;1-2 plants were enlarged compared to wild type early in development but then became reduced in size (Fig. 4, C and D). In contrast, Atnap1;2 and Atnap1;3 plants had no obvious phenotype (data not shown). Interestingly, by day 7, Atnap1;1-1 and Atnap1;1-2 leaves had more than twice as many cells compared to wild type (Fig. 4E). Similarly, 9-d-old Atnap1;1-1 and Atnap1;1-2 cotyledons were enlarged with more cells (data not shown). Between day 7 and 15, cell proliferation slowed in mutant leaves, while cell number continued to increase in wild-type leaves, therefore resulting in approximately 17% fewer cells in mature mutant leaves (Fig. 4E). In contrast, cell size was not significantly different in the two mutant lines compared to wild type during leaf development (data not shown). Together, these results suggest that loss of AtNAP1;1 function alters the normal cell proliferation during leaf development.
To examine the effects of AtNAP1;1 gain of function and the potential role of AtNAP1;1 farnesylation in vivo, we generated Arabidopsis transgenic plants in which the AtNAP1;1 or AtNAP1;1C369S cDNA were expressed under the control of the constitutive CaMV 35S promoter. Nine AtNAP1;1 and 11 AtNAP1;1C369S T1 hygromycin-resistant plants with single T-DNA insertions were selected for further analysis. Six independent T3 homozygous AtNAP1;1 and seven AtNAP1;1C369S lines were analyzed by western blot using the anti-NAP1 antibody. Except one AtNAP1;1 line, all transgenic lines highly expressed the transgene (Fig. 5A ) without any detectable change in the RNA levels expressed from the endogenous members of the AtNAP1 gene family (Fig. 5B). Lines AtNAP1;1 3.5.3 (AtNAP1;1-OE) and AtNAP1;1C369S 2.2.5 (AtNAP1;1C369S-OE) had similar levels of transgene expression and were therefore selected for a full analysis (Fig. 5A, lanes 7 and 10). There was no difference in germination and in the timing of leaf primordia initiation between AtNAP1;1-OE, AtNAP1;1C369S-OE, and wild-type lines. Plants expressing AtNAP1;1 developed smaller leaves and cotyledons, whereas these organs were enlarged in plants expressing AtNAP1;1C369S (Fig. 5C). In contrast, there was no difference in petal size, indicating that AtNAP1;1 overexpression preferentially affected the development of vegetative organs. Because the difference in leaf size was the most striking phenotype, we analyzed leaf development in more detail in the two gain-of-function mutants.
AtNAP1;1 Gain of Function Modulates Cell Number and Size during Leaf Development
A change in organ size can reflect an alteration in cell size or number or both. To address these possibilities, we performed a kinematic analysis of the first leaf using the method reported by De Veylder and colleagues (De Veylder et al., 2001
The kinematic analysis of leaf development revealed that ectopic expression of wild-type and mutant NAP1 resulted in alterations of cell size and number in the first leaf. Interestingly, ectopic expression of AtNAP1;1C369S primarily increased cell size, but the comparable size of mature AtNAP1;1C369S-OE and wild-type first leaves suggested that a compensatory mechanism corrects for the increased cell size in AtNAP1;1C369S-OE. Such compensation was not apparent in AtNAP1;1-OE plants, suggesting that the farnesylation of AtNAP1;1 has a profound effect on the function of the protein in this mechanism.
Cell proliferation, expansion, and differentiation are closely linked during leaf development (Beemster et al., 2005
We next examined the effects of ectopic AtNAP1;1 and AtNAP1;1C369S expression on leaf structure and cell differentiation. Dicotyledonous leaves have a distinct tissue organization with specific cell types between the adaxial and abaxial leaf surfaces. The palisade layer below the adaxial epidermis consists of tightly packed elongated cells arranged with their long axes perpendicular to the leaf surface. The spongy mesophyll cells between the palisade cell layer and the abaxial epidermis are smaller and more rounded (Donnelly et al., 1999
To begin to understand how ectopic AtNAP1;1 expression may modulate cell proliferation, expansion, and differentiation at the molecular level, we analyzed the accumulation of mRNAs for cell cycle and cell expansion-related genes during leaf development. qRT-PCR revealed that the CycB1;1 mRNA level was increased in AtNAP1;1-OE leaves at day 9 but was not significantly changed in AtNAP1;1C369S-OE leaves compared to wild type (Fig. 6G, top). No difference was found in the expression of CycD1;1 and CycD1;3 genes (data not shown). EXP5 represents a member of the gene family for expansin proteins that induce extension of the plant cell wall. The mRNA of this gene was strongly increased in leaves expressing AtNAP1;1C369S, consistent with the increased cell size (Fig. 6G, bottom). Interestingly, EXP5 mRNA also accumulated to higher levels in leaves expressing AtNAP1;1 despite their smaller cell size, suggesting that EXP5 function is not entirely restricted to cell elongation.
Given the effects of ectopic AtNAP1;1 or AtNAP1;1C369S expression at the cellular and molecular levels, we next asked whether posttranslational farnesylation of AtNAP1;1 was altered during leaf development, which in turn could modulate the function of AtNAP1;1 to affect cell proliferation, expansion, and differentiation. For this work, we also took advantage of the era1-1 mutant, which lacks PFT activity (Yalovsky et al., 2000a
Because era1-1 lacks PFT activity, NAP1;1 is not farnesylated in this mutant (Fig. 1, A and B) or modified by PGGT-I, which is somewhat promiscuous for the CaaX motif (Trueblood et al., 1993 ; Lane and Beese, 2006). Interestingly, AtNAP1 proteins accumulated to significantly higher levels in the era1-1 first leaf early in development (Fig. 7A, lanes 5 and 6) and remained at higher levels in older leaves (Fig. 7A, lanes 7 and 8) as wild type at comparable stages. This result suggests that the lack of AtNAP1 farnesylation in era1-1 may affect the regulation of NAP1 gene expression. Alternatively, nonfarnesylated NAP1;1 may be more stable in era1-1.
Subcellular analysis of AtNAP1;1 expressed in BY-2 tobacco cells had revealed that the protein was located in the cytoplasm or the nucleus depending on stage of the cell cycle, but this was not depending on farnesylation (Fig. 2). Considering the opposing effects of ectopically expressed AtNAP1;1 and AtNAP1;1C369S on cell proliferation and expansion (Fig. 6), it was still possible that the farnesylation status of NAP1;1 during leaf development (Fig. 7B) was important to direct the subcellular localization of the protein. We therefore analyzed the subcellular localization of AtNAP1 proteins during development of the first leaf. In leaves from control and AtNAP1;1-OE lines, the AtNAP1 proteins detected by the antibody were found exclusively in the nuclear fraction on day 9, whereas they were equally distributed between the nuclear and cytoplasmic fractions on day 15 (Fig. 7C). In contrast, AtNAP1 proteins were equally distributed between the nucleus and the cytoplasm in leaves of AtNAP1;1C369S expressing lines at both 9 and 15 d. A parallel analysis of the first leaf of era1-1 showed that AtNAP1 proteins were found both in the nucleus and cytoplasm at day 11, whereas they were exclusively present in the cytoplasm after 17 d (Fig. 7D). Together, we conclude that farnesylation of AtNAP1;1 directs the protein to the nucleus early in leaf development, perhaps in concert with other localization mechanisms. The results also suggest that farnesylation and nuclear localization of AtNAP1;1 facilitate cell proliferation during early leaf development.
The analysis of mutants has provided significant new insights into leaf development during the last several years. Typically, leaf growth is tightly regulated by the control of cell number, cell size, and differentiation. The genetic and biochemical networks that integrate these cellular processes, however, are still largely unknown. Our analysis established that AtNAP1;1 function is required for correct cell proliferation control during Arabidopsis leaf development and that this function is dependent on the temporal farnesylation of the protein.
Organ development is tightly coordinated at the cellular level by cell division, expansion, and differentiation such that each organ reaches its appropriate size relative to the size of the organism. In determinate plant organs, particularly leaves, final organ cell number is regulated by the initial number of cells recruited into the primodium, the timing of cell division, and the rate of proliferation. After mitotic activity ceases, cell differentiation and expansion establish the regular pattern of tissue layers in the leaf blade (Donnelly et al., 1999
The reduced leaf growth in Atnap1;1 is the consequence of a decreased rate of cell division. In contrast, ectopic AtNAP1;1 expression in Arabidopsis increased cell proliferation but did not affect the time window of cell cycle activity during leaf development. Because the effect of either loss or gain of AtNAP1;1 function appears to be restricted primarily to the phase of cell proliferation, we suggest that AtNAP1;1 functions as a stage-specific positive regulator of cell proliferation. The high AtNAP1 protein level that we detected in leaves during the cell proliferation phase is also consistent with a role of AtNAP1 in the control of cell division. In humans, HsNAP1L1 gene is expressed in all tissues but its expression is increased in proliferating cells. Moreover, the HsNAP1L1 protein level increases in cultured T-lymphocytes induced to proliferate (Simon et al., 1994
How does AtNAP1;1 influence cell proliferation rate? Our analysis has revealed that AtNAP1;1 overexpression increases the expression of CYCB1;1, which functions in late G2 and M phases (Donnelly et al., 1999
Following the cell division phase, cell enlargement and cellular differentiation contribute to the final size and shape of leaves. It has been long recognized that a correlation exists between DNA endoreplication and leaf cell expansion, suggesting that DNA ploidy level may determine cell size (Melaragno et al., 1993
The possibility that AtNAP1;1 can both negatively or positively influence cell growth and expansion dependent on its farnesylation status is also consistent with the result that ectopic expression of AtNAP1;1 reduced normal cell growth during the cell proliferation phase of leaf development. It must be noted, however, that increased cell division can also inhibit cell growth (Fleming, 2002
In plants, protein farnesylation has been shown to affect protein function and subcellular localization (Zhu et al., 1993 If the farnesylation-dependent localization of AtNAP1;1 is altered during leaf development, as was the case during the cell proliferation phase in AtNAP1;1C369S-OE plants, this results in premature cell expansion. It is possible that unscheduled accumulation of AtNAP1;1 may allow the protein to engage interactions with other proteins that control cell growth and expansion in the context of the cell cycle but independent of AtNAP1;1. These interactions could occur in the nucleus or the cytoplasm, but it is currently unknown if they require NtNAP1;1 to be farnesylated. Also, these interactions do not easily explain how the different subcellular localizations of AtNAP1;1 could exert effects on cell proliferation or cell growth and expansion. Additional experiments will be necessary to identify proteins that specifically interact with NAP1;1 during different leaf development phases.
It is reasonable to expect that the farnesylation status of AtNAP1;1 may allow the protein to engage in different protein complexes, which exert specific functions during leaf development. In yeast, NAP1 was shown to specifically interact with a set of proteins, including histones, Clb2, Gin4, Nbp1, and p300/CREB-binding proteins (Ishimi et al., 1987
Plant Material and Growth Conditions Arabidopsis (Arabidopsis thaliana) plants used in our study were all derived from the Columbia (Col-0) accession line. Seeds of Atnap1;1-1 (SALK_013610), Atnap1;1-2 (SALK_095311), and Atnap1;2 (SALK_002892) mutants were obtained from the SALK T-DNA insertion collection (http://signal.salk.edu) and Atnap1;3 (SAIL_373_H11) mutant seeds from the Syngenta Arabidopsis insertion library. Seeds were surface sterilized using 5% bleach and germinated on Murashige and Skoog medium. After 2 weeks, the seedlings were transferred to soil and grown in Conviron chambers with a 16-/8-light/-dark cycle at 23°C in 70% humidity.
The Arabidopsis AtNAP1;1 cDNA (At4g26110) was amplified by PCR using the primer NAP1-For (5'-ATGAGCAACGACAAGGATAGCTTC-3'), together with either NAP1-Rev1 (5'-GTCGACTTACTGTTGCTTGCATTCGGG-3', for the wild-type version of the CaaX box, CKQQ) or NAP1-Rev2 (5'-GTCGACTTACTGTTGCTTGCTTTCGGG-3', for the C369S version, SKQQ). The wild-type and the mS PCR fragments were cloned in the pCR 2.1-TOPO cloning vector (Stratagene) and subsequently in the pRSETa vector for protein expression in Escherichia coli. Recombinant proteins were purified on nickel-nitrilotriacetic acid agarose talon superflow metal affinity resin (CLONTECH). Polyclonal anti-AtNAP1;1 was produced by injecting the purified AtNAP1;1 in mouse.
Nitrocellulose membranes were first blocked overnight at 4°C with 5% nonfat milk and subsequently incubated for 2 h at room temperature with the AtNAP1 antibody (diluted 1:5,000), washed with Tris-buffered saline containing Tween 20, and incubated 2 h with 5,000-fold diluted goat anti-mouse secondary antibody conjugated with horseradish peroxidase for detection with an ECL kit (Amersham Pharmacia Biotech). Immunodetection using polyclonal antibodies raised against MSI1 was carried out as described (Köhler et al., 2003
In vitro prenylation assay was performed as previously described (Yalovsky et al., 2000
AtNAP1;1, AtNAP1;1C369S, and ScNAP1 genes were directionally cloned in pJR1133 vector, containing the URA3 marker. The resulting plasmids were used to transform the yeast (Saccharomyces cerevisiae) strain DK213 (MATa clb3::TRP1 clb4::HIS3
Wild AtNAP1;1 and AtNAP1;1C369S cDNA were cloned in pGFP-MRC (Rodriguez-Concepcion et al., 1999
AtNAP1;1 and AtNAP1;1C369S cDNA were cloned in the modified vector pCAMBIA 1380 containing a CaMV 35S promoter (kindly provided by L. Gomez-Gomez). The constructs were introduced into Agrobacterium tumefaciens strain LBA4404. These strains were used to transform Arabidopsis Col-0 plants by floral dip (Clough and Bent, 1998
RNA was extracted using Qiagen RNeasy columns according to the manufacturer's instructions. For RT-PCR analysis, 5 µg total RNA was treated with DNase I and DNA-free RNA was transcribed using an oligo(dT) primer and Moloney murine leukemia virus reverse transcriptase (CLONTECH). Aliquots of the generated cDNA, which equaled 50 ng total RNA, were used as template for qRT-PCR. Specific primers (temperature, melting, 58°C–63°C) were designed to generate PCR products between 150 and 350 bp. CycB1;1 (At3g11520) forward primer (5'-CCTCAACCAGTTAGAGGTGATCC-3') and reverse primer (5'-GTTTCCAATGTCGCCAAGAG-3'), AtExp5 (At3g29030) forward primer (5'-GCTCATGCCACTTTTTACGG-3') and reverse primer (5'-TCTCCAGTCCATAACCTTGG-3') were used and qRT-PCR of GAPDHA (At3g26650) with forward primer (5'-CTCCCTTGGAAGGAGCTAGG-3') and reverse primer (5'-TTCTTGGCACCAGCTTCAAT-3') was performed for standardization. qRT-PCR reactions were monitored using an ABI Prism 7700 Sequence Detection system with the SYBR green PCR Mastermix (Applied Biosystem).
After removal of the leaf petioles, leaf blades were chopped with a razor blade and ploidy analysis was carried out as described (Köhler et al., 2003
Histological analyses were performed with samples in Technovit 7100 resin according to the manufacturer's instructions (Kulzer & Co.). For transverse sections, tissue samples were cut at the center of the first leaf. For longitudinal sections, tissue samples were cut halfway between themed rib and leaf margin.
Nuclei were isolated from harvested first leaves as described (Köhler et al., 2003
We are grateful to Johannes Fütterer for tobacco BY-2 cell transformation and GFP fluorescence analysis, to Joanna Wyrzykowska, Gerrit T.S. Beemster, and Andrew J. Fleming for helpful discussions and for critical reading of the manuscript. We thank Marzanna Gontarczyk for help with the histological preparations and Chantal Ebel for useful discussions. We thank D.R. Kellog for the DK213 yeast strain, Syngenta for the Atnap1;3 T-DNA line, the Salk Institute Genomic Analysis Laboratory for providing the sequence-indexed Arabidopsis T-DNA Atnap1;1-1, Atnap1;1-2, and Atnap1;2 insertion mutants, and Arabidopsis Biological Resource Center for providing us the seeds. Received August 15, 2006; accepted September 27, 2006; published October 13, 2006.
1 This work was supported by the Swiss Federal Institute of Technology Zurich. 
2 Present address: Division of Clinical Chemistry and Biochemistry, Department of Pediatrics, University Children's Hospital, 8032 Zurich, Switzerland. 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: Wilhelm Gruissem (wgruissem{at}ethz.ch). www.plantphysiol.org/cgi/doi/10.1104/pp.106.088344 * Corresponding author; e-mail wgruissem{at}ethz.ch; fax 41–44–632–1079.
Abu-Daya A, Steer WM, Trollope AF, Friedeberg CE, Patient RK, Thorne AW, Guille MJ (2005) Zygotic nucleosome assembly protein-like 1 has a specific, non-cell autonomous role in hematopoiesis. Blood 106: 514–520 Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653–657 Altman R, Kellogg D (1997) Control of mitotic events by Nap1 and the Gin4 kinase. J Cell Biol 138: 119–130 Asahara H, Tartare-Deckert S, Nakagawa T, Ikehara T, Hirose F, Hunter T, Ito T, Montminy M (2002) Dual roles of p300 in chromatin assembly and transcriptional activation in cooperation with nucleosome assembly protein 1 in vitro. Mol Cell Biol 22: 2974–2983 Autran D, Jonak C, Belcram K, Beemster GT, Kronenberger J, Grandjean O, Inze D, Traas J (2002) Cell numbers and leaf development in Arabidopsis: a functional analysis of the STRUWWELPETER gene. EMBO J 21: 6036–6049[CrossRef][Web of Science][Medline] Beemster GT, De Veylder L, Vercruysse S, West G, Rombaut D, Van Hummelen P, Galichet A, Gruissem W, Inze D, Vuylsteke M (2005) Genome-wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis. Plant Physiol 138: 734–743 Beemster GT, Fiorani F, Inze D (2003) Cell cycle: the key to plant growth control? Trends Plant Sci 8: 154–158[CrossRef][Web of Science][Medline] Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743[CrossRef][Web of Science][Medline] De Veylder L, Beeckman T, Beemster GT, de Almeida Engler J, Ormenese S, Maes S, Naudts M, Van Der Schueren E, Jacqmard A, Engler G, et al (2002) Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa-DPa transcription factor. EMBO J 21: 1360–1368[CrossRef][Web of Science][Medline] De Veylder L, Beeckman T, Beemster GT, Krols L, Terras F, Landrieu I, van der Schueren E, Maes S, Naudts M, Inze D (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13: 1653–1668 Dong A, Zhu Y, Yu Y, Cao K, Sun C, Shen WH (2003) Regulation of biosynthesis and intracellular localization of rice and tobacco homologues of nucleosome assembly protein 1. Planta 216: 561–570[Web of Science][Medline] Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215: 407–419[CrossRef][Web of Science][Medline] Elam C, Hesson L, Vos MD, Eckfeld K, Ellis CA, Bell A, Krex D, Birrer MJ, Latif F, Clark GJ (2005) RRP22 is a farnesylated, nucleolar, Ras-related protein with tumor suppressor potential. Cancer Res 65: 3117–3125 Fleming AJ (2002) The mechanism of leaf morphogenesis. Planta 216: 17–22[CrossRef][Web of Science][Medline] Folkers U, Berger J, Hulskamp M (1997) Cell morphogenesis of trichomes in Arabidopsis: differential control of primary and secondary branching by branch initiation regulators and cell growth. Development 124: 3779–3786[Abstract] Galichet A, Gruissem W (2003) Protein farnesylation in plants: conserved mechanisms but different targets. Curr Opin Plant Biol 6: 530–535[CrossRef][Web of Science][Medline] Hu RJ, Lee MP, Johnson LA, Feinberg AP (1996) A novel human homologue of yeast nucleosome assembly protein, 65 kb centromeric to the p57KIP2 gene, is biallelically expressed in fetal and adult tissues. Hum Mol Genet 5: 1743–1748 Hussein D, Taylor SS (2002) Farnesylation of Cenp-F is required for G2/M progression and degradation after mitosis. J Cell Sci 115: 3403–3414 Ishimi Y, Hirosumi J, Sato W, Sugasawa K, Yokota S, Hanaoka F, Yamada M (1984) Purification and initial characterization of a protein which facilitates assembly of nucleosome-like structure from mammalian cells. Eur J Biochem 142: 431–439[Web of Science][Medline] Ishimi Y, Kikuchi A (1991) Identification and molecular cloning of yeast homolog of nucleosome assembly protein I which facilitates nucleosome assembly in vitro. J Biol Chem 266: 7025–7029 Ishimi Y, Kojima M, Yamada M, Hanaoka F (1987) Binding mode of nucleosome-assembly protein (AP-I) and histones. Eur J Biochem 162: 19–24[Web of Science][Medline] Ito T, Bulger M, Kobayashi R, Kadonaga JT (1996) Drosophila NAP-1 is a core histone chaperone that functions in ATP-facilitated assembly of regularly spaced nucleosomal arrays. Mol Cell Biol 16: 3112–3124[Abstract] Ito T, Ikehara T, Nakagawa T, Kraus WL, Muramatsu M (2000) p300-mediated acetylation facilitates the transfer of histone H2A-H2B dimers from nucleosomes to a histone chaperone. Genes Dev 14: 1899–1907 Jeong ML, Jiang H, Chen HS, Tsai CJ, Harding SA (2004) Metabolic profiling of the sink-to-source transition in developing leaves of quaking aspen. Plant Physiol 136: 3364–3375 Kawase H, Okuwaki M, Miyaji M, Ohba R, Handa H, Ishimi Y, Fujii-Nakata T, Kikuchi A, Nagata K (1996) NAP-I is a functional homologue of TAF-I that is required for replication and transcription of the adenovirus genome in a chromatin-like structure. Genes Cells 1: 1045–1056[Abstract] Kellogg DR, Kikuchi A, Fujii-Nakata T, Turck CW, Murray AW (1995) Members of the NAP/SET family of proteins interact specifically with B-type cyclins. J Cell Biol 130: 661–673 Kellogg DR, Murray AW (1995) NAP1 acts with Clb1 to perform mitotic functions and to suppress polar bud growth in budding yeast. J Cell Biol 130: 675–685 Kho Y, Kim SC, Jiang C, Barma D, Kwon SW, Cheng J, Jaunbergs J, Weinbaum C, Tamanoi F, Falck J, et al (2004) A tagging-via-substrate technology for detection and proteomics of farnesylated proteins. Proc Natl Acad Sci USA 101: 12479–12484 Kim GT, Shoda K, Tsuge T, Cho KH, Uchimiya H, Yokoyama R, Nishitani K, Tsukaya H (2002) The ANGUSTIFOLIA gene of Arabidopsis, a plant CtBP gene, regulates leaf-cell expansion, the arrangement of cortical microtubules in leaf cells and expression of a gene involved in cell-wall formation. EMBO J 21: 1267–1279[CrossRef][Web of Science][Medline] Kim GT, Tsukaya H, Uchimiya H (1998) The ROTUNDIFOLIA3 gene of Arabidopsis thaliana encodes a new member of the cytochrome P-450 family that is required for the regulated polar elongation of leaf cells. Genes Dev 12: 2381–2391 Köhler C, Hennig L, Bouveret R, Gheyselinck J, Grossniklaus U, Gruissem W (2003) Arabidopsis MSI1 is a component of the MEA/FIE polycomb group complex and required for seed development. EMBO J 22: 4804–4814[CrossRef][Web of Science][Medline] Lane KT, Beese LS (2006) Thematic review series: lipid posttranslational modifications. Structural biology of protein farnesyltransferase and geranylgeranyltransferase type I. J Lipid Res 47: 681–699 Lankenau S, Barnickel T, Marhold J, Lyko F, Mechler BM, Lankenau DH (2003) Knockout targeting of the Drosophila nap1 gene and examination of DNA repair tracts in the recombination products. Genetics 163: 611–623 Levchenko V, Jackson V (2004) Histone release during transcription: NAP1 forms a complex with H2A and H2B and facilitates a topologically dependent release of H3 and H4 from the nucleosome. Biochemistry 43: 2359–2372[CrossRef][Medline] Martin SG, St Johnston D (2003) A role for Drosophila LKB1 in anterior-posterior axis formation and epithelial polarity. Nature 421: 379–384[CrossRef][Medline] McQuibban GA, Commisso-Cappelli CN, Lewis PN (1998) Assembly, remodeling, and histone binding capabilities of yeast nucleosome assembly protein 1. J Biol Chem 273: 6582–6590 Meijer M, Murray JA (2001) Cell cycle controls and the development of plant form. Curr Opin Plant Biol 4: 44–49[CrossRef][Web of Science][Medline] Melaragno JE, Mehrotra B, Coleman AW (1993) Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5: 1661–1668[Abstract] Mijimolle N, Velasco J, Dubus P, Guerra C, Weinbaum CA, Casey PJ, Campuzano V, Barbacid M (2005) Protein farnesyltransferase in embryogenesis, adult homeostasis, and tumor development. Cancer Cell 7: 313–324[CrossRef][Web of Science][Medline] Miyaji-Yamaguchi M, Kato K, Nakano R, Akashi T, Kikuchi A, Nagata K (2003) Involvement of nucleocytoplasmic shuttling of yeast Nap1 in mitotic progression. Mol Cell Biol 23: 6672–6684 Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 97: 942–947 Morehead TA, Biermann BJ, Crowell DN, Randall SK (1995) Changes in protein isoprenylation during the growth of suspension-cultured tobacco cells. Plant Physiol 109: 277–284[Abstract] Nakagawa T, Bulger M, Muramatsu M, Ito T (2001) Multistep chromatin assembly on supercoiled plasmid DNA by nucleosome assembly protein-1 and ATP-utilizing chromatin assembly and remodeling factor. J Biol Chem 276: 27384–27391 Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. J Exp Bot 52: 1383–1400 Pei ZM, Ghassemian M, Kwak CM, McCourt P, Schroeder JI (1998) Role of farnesyltransferase in ABA regulation of guard cell anion channels and plant water loss. Science 282: 287–290 Pyke P, Lopez-Juez E (1999) Cellular differentiation and leaf morphogenesis in Arabidopsis. CRC Crit Rev Plant Sci 18: 527–546[CrossRef] Qian D, Zhou D, Ju R, Cramer CL, Yang Z (1996) Protein farnesyltransferase in plants: molecular characterization and involvement in cell cycle control. Plant Cell 8: 2381–2394[Abstract] Rehtanz M, Schmidt HM, Warthorst U, Steger G (2004) Direct interaction between nucleosome assembly protein 1 and the papillomavirus E2 proteins involved in activation of transcription. Mol Cell Biol 24: 2153–2168 Rodriguez-Concepcion M, Yalovsky S, Zik M, Fromm H, Gruissem W (1999) The prenylation status of a novel plant calmodulin directs plasma membrane or nuclear localization of the protein. EMBO J 18: 1996–2007[CrossRef][Web of Science][Medline] Rodriguez P, Munroe D, Prawitt D, Chu LL, Bric E, Kim J, Reid LH, Davies C, Nakagama H, Loebbert R, et al (1997) Functional characterization of human nucleosome assembly protein-2 (NAP1L4) suggests a role as a histone chaperone. Genomics 44: 253–265[CrossRef][Web of Science][Medline] Rogner UC, Spyropoulos DD, Le Novere N, Changeux JP, Avner P (2000) Control of neurulation by the nucleosome assembly protein-1-like 2. Nat Genet 25: 431–435[CrossRef][Web of Science][Medline] Rougeulle C, Avner P (1996) Cloning and characterization of a murine brain specific gene Bpx and its human homologue lying within the Xic candidate region. Hum Mol Genet 5: 41–49 Running MP, Lavy M, Sternberg H, Galichet A, Gruissem W, Hake S, Ori N, Yalovsky S (2004) Enlarged meristems and delayed growth in plp mutants result from lack of CaaX prenyltransferases. Proc Natl Acad Sci USA 101: 7815–7820 Scott A, Wyatt S, Tsou PL, Robertson D, Allen NS (1999) Model system for plant cell biology: GFP imaging in living onion epidermal cells. Biotechniques 26: 1125, 1128–1132 Sessions A, Burke E, Presting G, Aux G, McElver J, Patton D, Dietrich B, Ho P, Bacwaden J, Ko C, et al (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell 14: 2985–2994 Shen HH, Huang AM, Hoheisel J, Tsai SF (2001) Identification and characterization of a SET/NAP protein encoded by a brain-specific gene, MB20. Genomics 71: 21–33[CrossRef][Web of Science][Medline] Shikama N, Chan HM, Krstic-Demonacos M, Smith L, Lee CW, Cairns W, La Thangue NB (2000) Functional interaction between nucleosome assembly proteins and p300/CREB-binding protein family coactivators. Mol Cell Biol 20: 8933–8943 Shimizu Y, Akashi T, Okuda A, Kikuchi A, Fukui K (2000) NBP1 (Nap1 binding protein 1), an essential gene for G2/M transition of Saccharomyces cerevisiae, encodes a protein of distinct sub-nuclear localization. Gene 246: 395–404[CrossRef][Web of Science][Medline] Simon HU, Mills GB, Kozlowski M, Hogg D, Branch D, Ishimi Y, Siminovitch KA (1994) Molecular characterization of hNRP, a cDNA encoding a human nucleosome-assembly-protein-I-related gene product involved in the induction of cell proliferation. Biochem J 297: 389–397[Medline] Sinensky M (2000) Recent advances in the study of prenylated proteins. Biochim Biophys Acta 1484: 93–106[Medline] Suzuki N, Yamaguchi Y, Koizumi N, Sano H (2002) Functional characterization of a heavy metal binding protein CdI19 from Arabidopsis. Plant J 32: 165–173[CrossRef][Web of Science][Medline] Tamanoi F, Kato-Stankiewicz J, Jiang C, Machado I, Thapar N (2001) Farnesylated proteins and cell cycle progression. J Cell Biochem Suppl (Suppl) 37: 64–70[Medline] Trueblood CE, Ohya Y, Rine J (1993) Genetic evidence for in vivo cross-specificity of the CaaX-box protein prenyltransferases farnesyltransferase and geranylgeranyltransferase-I in Saccharomyces cerevisiae. Mol Cell Biol 13: 4260–4275 von Lindern M, van Baal S, Wiegant J, Raap A, Hagemeijer A, Grosveld G (1992) Can, a putative oncogene associated with myeloid leukemogenesis, may be activated by fusion of its 3' half to different genes: characterization of the set gene. Mol Cell Biol 12: 3346–3355 Walter PP, Owen-Hughes TA, Cote J, Workman JL (1995) Stimulation of transcription factor binding and histone displacement by nucleosome assembly protein 1 and nucleoplasmin requires disruption of the histone octamer. Mol Cell Biol 15: 6178–6187[Abstract] Yalovsky S, Kulukian A, Rodriguez-Concepcion M, Young CA, Gruissem W (2000a) Functional requirement of plant farnesyltransferase during development in Arabidopsis. Plant Cell 12: 1267–1278 Yalovsky S, Rodriguez-Concepcion M, Bracha K, Toledo-Ortiz G, Gruissem W (2000b) Prenylation of the floral transcription factor APETALA1 modulates its function. Plant Cell 12: 1257–1266 Yalovsky S, Rodriguez-Concepcion M, Gruissem W (1999) Lipid modifications of proteins: slipping in and out of membranes. Trends Plant Sci 4: 439–445[CrossRef][Web of Science][Medline] Yoon HW, Kim MC, Lee SY, Hwang I, Bahk JD, Hong JC, Ishimi Y, Cho MJ (1995) Molecular cloning and functional characterization of a cDNA encoding nucleosome assembly protein 1 (NAP-1) from soybean. Mol Gen Genet 249: 465–473[CrossRef][Web of Science][Medline] Zhu JK, Bressan RA, Hasegawa PM (1993) Isoprenylation of the plant molecular chaperone ANJ1 facilitates membrane association and function at high temperature. Proc Natl Acad Sci USA 90: 8557–8561 Zimmerman ZA, Kellogg DR (2001) The Sda1 protein is required for passage through start. Mol Biol Cell 12: 201–219 This article has been cited by other articles:
|
|||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| ASPB Publications | PLANT PHYSIOLOGY® | THE PLANT CELL | |
|---|---|---|---|
TOP
ABSTRACT
RESULTS
), AtNAP1-1 (
), or AtNAP1;1C369S (
), and cells were arrested in G2/M and then released in fresh media at the permissive temperature (30°C) or at the restrictive temperature (37°C). A, Cell proliferation was monitored at 37°C by measuring the OD600 nm of the culture over a period of 24 h. B, Nomarski images after 16 h at 30°C. C, Immunoblot analysis of wild-type DK213 yeast cells (1) or DK213 cells expressing ScNAP1 (2), AtNAP1;1 (3), or AtNAP1;1C369S proteins. Protein extracts were separated by SDS-PAGE in 10% gel followed by western blotting.
), AtNAP1;1-OE (
) plants. Twenty individual leaves and 40 palisade mesophyll cells were analyzed in duplicate. A, Average leaf blade area; B, average cell area; C, average number of cells; and D, division rate. E, Quantification of ploidy distribution as mean ± SD of two independent measurements involving different sets of plants. F, Transverse sections through the central part of 9-d-old plastic-embedded first leaves stained with toluidine blue. Scale bars are 50 µm. G, Expression analyses of CYCB1 (top) and EXP5 (bottom) genes by qRT-PCR in AtNAP1;1-OE and AtNAP1;1C369S-OE 9-, 15-, and 25-d-old first leaves. Results of quantification using GAPDH as a reference are relative to wild-type expression level.
clb1 NAP1::LEU2 leu2-3, 112 ura3-52 can1-100 ade2-1 his3-11 
