Journal of Experimental Botany, Vol. 54, No. 391, pp. 2201-2214,
October 1, 2003
© 2003 Oxford University Press
Plant DNA helicases: the long unwinding road*
Received 18 February 2003; Accepted 16 June 2003
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Plant Molecular Biology, International Centre for Genetic Engineering and Biotechnology, Aruna Asaf Ali Marg, New Delhi-110067, India
* This paper is dedicated to Professor Arturo Falaschi on the occasion of his 70th birthday. Fax: +91 11 26162316. E-mail: narendra{at}icgeb.res.in
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Abstract |
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 Top Abstract IntroductionThe historical perspective of...Assays and direction of...Plant DNA helicasesInhibitors of plant DNA...Functions of plant DNA...Concluding remarksReferences |
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DNA helicases are molecular motor proteins that use the energy of nucleoside 5'-triphosphate (NTP) hydrolysis to open transiently the energetically stable duplex DNA into single strands and thereby play essential roles in nearly all DNA metabolic transactions. After the discovery of the first prokaryotic DNA helicase from E. coli in 1976 and the first eukaryotic one from the lily plant in 1978, many more have been isolated and characterized including at least eight from plants. All the DNA helicases share some common properties, including nucleic acid binding, NTP binding and hydrolysis and unwinding of duplex DNA in the 3' to 5' or 5' to 3' direction. In plants, DNA helicases are mainly present in nuclei, mitochondria and chloroplasts. The in vivo role of many DNA helicases has not been well investigated in eukaryotic systems including plants. However, through indirect evidence, the involvement of plant DNA helicases has been suggested at least in the following biological processes: DNA recombination, DNA replication, translation initiation, rDNA transcription and in the early stages of pre-rRNA processing, double-strand break repair, maintenance of telomeric length, nucleotide excision repair, cell division/proliferation during flower development, maintenance of genomic methylation patterns, the plant cell cycle, and in the maintenance of the basic activities of cells. A recently discovered Helitron insertion in the maize genome has suggested the possible role of plant DNA helicase(s) in a new class of rolling-circle transposons. All these reflect that plant DNA helicases may play an important role in plant growth and development and thus have important biotechnological applications. In this review, an up-to-date knowledge of plant DNA helicases is summarized. In addition, the historical perspective, biochemical assay and polarity, inhibitors and functions of plant DNA helicases have also been covered.
Key words: Chloroplast DNA helicase, DEAD-box protein, helicase inhibitors, helicase motifs, plant DNA helicase, RNA helicase, replication, unwinding enzyme.
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Introduction |
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TopAbstractIntroductionThe historical perspective of...Assays and direction of...Plant DNA helicasesInhibitors of plant DNA...Functions of plant DNA...Concluding remarksReferences |
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Despite the energetically stable genomes of all living organisms including plants, the duplex DNA has partially to unwind for a very short time to create a single-stranded (ss) DNA template, which is required for most of their important cellular functions, including replication, repair, recombination, and transcription. Helicases are protein motors that use the energy of NTP hydrolysis to dissociate the hydrogen bonding between the nucleic acid duplexes and also to disrupt other non-covalent interactions between complementary base pairs (Kornberg and Baker, 1991; Matson et al., 1994; Tuteja and Tuteja, 1996; Lohman et al., 1998). Similarly, RNA helicases represent a large family of proteins that are involved in the modulation of RNA structure and thereby influence RNA synthesis, splicing, replication, translation initiation, editing, rRNA processing, ribosome assembly, nuclear mRNA export, and mRNA stabilization and degradation (Aubourg et al., 1999; Koonin, 1991; Tuteja, 2000; Linder and Stutz, 2001; Luking et al., 1998; Tanner and Linder, 2001). All the helicases share at least three common biochemical properties: (i) nucleic acid binding, (ii) NTP/dNTP binding and hydrolysis, and (iii) NTP/dNTP hydrolysis-dependent unwinding of duplex nucleic acids (Hall and Matson, 1999). Therefore, all the helicases described to date also have intrinsic DNA- or RNA-dependent NTPase activity (Kornberg and Baker, 1991; Lohman, 1992, 1993). These enzymes usually act in concert with other enzymes or proteins in DNA metabolic activity.
A computer-assisted amino acid sequence analysis of helicases from many different organisms has revealed seven short conserved motifs (I, Ia, II, III, IV, V, and VI), called ‘helicase motifs’ (Gorbalenya et al., 1988, 1989; Gorbalenya and Koonin, 1993; Tanner and Linder, 2001). With this discovery, the helicases have been classified into three superfamilies (SF) namely SF1, SF2, and SF3 based on the extent of similarity and the organization of these conserved motifs. High sequence conservation has been maintained in this large group of helicases, suggesting that the motifs containing helicase genes evolved from a common ancestor. These seven motifs of SF1 and SF2 are usually clustered in a region of 200–700 amino acids and can be called a core-region. These conserved motifs are separated by stretches of low sequence, but high length, conservation. It has been suggested that the divergent regions are responsible for individual protein function, whereas the highly conserved domains are involved in ATP-binding and hydrolysis or binding and unwinding of nucleic acids. Because of the sequence of motif II (DEAD or DEAH or DEXH), the helicase family is also called the DEAD-box protein family. From the post-sequencing-genome era of Arabidopsis it is now known that the DEAD-box helicase family contains more than 55 members in Arabidopsis. Recently, a new motif upstream of motif I, called the ‘Q motif’ has been discovered, which is suggested to regulate ATP binding and hydrolysis in yeast eIF-4A (Tanner et al., 2003).
The mechanism of DNA unwinding by helicases is not well understood. However, on the basis of study with various helicases, two distinct models have been suggested: namely ‘active rolling’ (SenGupta and Borowiec, 1992; Wong and Lohman, 1992; Lohman, 1992) and ‘inchworm’ (Yarranton and Gefter, 1979; Lohman, 1992; Lohman and Bjornson, 1996), which have been described previously (Tuteja, 2000).
In plants, helicases must be playing an important role in growth and development, which is the result of controlled cell proliferation. In green plant cells, helicases are present in all the three organelles: nucleus, mitochondrion and chloroplast, which contain their own genomes (Gagliardi et al., 1999; Pham et al., 2000; Tuteja et al., 1996, 2001a). This review provides an up-to-date progress of research on plant DNA helicases. Furthermore, the historical background of helicases (mainly plant) and biochemical assay and polarity, inhibitors and functions of plant DNA helicases have also been covered. Reviews are cited wherever possible.
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The historical perspective of plant helicases |
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TopAbstractIntroductionThe historical perspective of...Assays and direction of...Plant DNA helicasesInhibitors of plant DNA...Functions of plant DNA...Concluding remarksReferences |
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DNA helicase was first discovered in E. coli in 1976 and classified as ‘DNA unwinding enzyme’ (Abdel-Monem et al., 1976). Nearly 100 DNA helicases have been isolated from different organisms including bacteria, bacteriophages, viruses, yeasts, cow, frog, Drosophila, mouse, humans, and plants (Ilyina et al, 1992; Lohman, 1992, 1993; Matson et al., 1994; Tuteja and Tuteja, 1996; Tuteja, 1997). E. coli contains at least 13 different DNA helicases (Lohman, 1992; Matson et al., 1994) and, similarly, several have been isolated from humans, calf thymus, yeasts, and viruses (Matson et al., 1994; Borowiec, 1996; Tuteja and Tuteja, 1996). The first plant DNA helicase was discovered in 1978 from lily which, interestingly, happened to be the first report from any eukaryotic system (Hotta and Stern, 1978). Since then, almost a quarter century has passed, but the progress in plant helicase research has been slow. The major milestones in the discovery of plant DNA helicases are summarized in Table 1.
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Assays and direction of unwinding |
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TopAbstractIntroductionThe historical perspective of...Assays and direction of...Plant DNA helicasesInhibitors of plant DNA...Functions of plant DNA...Concluding remarksReferences |
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The most accepted and direct assay for measuring helicase activity in vitro was developed almost simultaneously by the Nossal and the Richardson groups (Venkateson et al., 1982; Matson et al., 1983), which utilized gel electrophoresis. An unwinding reaction catalysed by helicase is shown in Fig. 1A. This method relies on measurement of the release of a 32P-labelled oligonucleotide annealed to a longer single-stranded (ss) DNA molecule by the action of active DNA helicase, which can be monitored by polyacrylamide or agarose gel electrophoresis followed by autoradiography. A radioactive label within the DNA permits direct visualization and quantitation of the results. One unit of unwinding activity is usually defined as the amount of DNA helicase required for unwinding a certain percentage of the partially duplex substrate in 30 min at 37 °C (Tuteja, 1997, 2000).
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Despite the functional diversity among helicases, they all exhibit specific polarity, which is the intrinsic property of all the helicases. It is defined as the direction of helicase movement on initially bound ssDNA or ssRNA template (i.e. 3' to 5' or 5' to 3') with respect to the polarity of the sugar-phosphate backbone (Fig. 1B). The polarity of unwinding is usually determined by using DNA or RNA substrate consisting of a linear ss-template with duplex ends (Fig. 1B). The enzyme reaction shown in Fig. 1A has 3' to 5' polarity and in Fig. 1B has 3' to 5' as well as 5' to 3' polarity shown by two different helicases. Mostly, unidirectionality is an intrinsic characteristic of all the DNA and RNA helicases of cellular as well as of viral origin. However, an interesting exception is provided by the eukaryotic translation initiation factors eIF-4A or eIF-4F in combination with eIF-4B, which unwinds duplex RNA in a bi-directional manner (Rozen et al., 1990). Unwinding in the 5' to 3' direction by eIF-4F in conjunction with eIF-4B was stimulated by the presence of the RNA 5' cap structure, whereas unwinding in the 3' to 5' direction is completely cap-independent (Rozen et al., 1990). For the helicases, which are involved in DNA replication, the polarity of the reaction is strongly indicative of helicase placement on the leading (a 3' to 5' polarity) or lagging (5' to 3' polarity) strand.
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Plant DNA helicases |
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TopAbstractIntroductionThe historical perspective of...Assays and direction of...Plant DNA helicasesInhibitors of plant DNA...Functions of plant DNA...Concluding remarksReferences |
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Little is known about DNA helicases from plant systems. Hotta and Stern (1978) discovered the existence of the first eukaryotic DNA helicase from the lily plant, but, unfortunately, this helicase was only partially purified and this work was not followed up. The first plant DNA helicase purified to homogeneity and characterized biochemically was reported in 1996 (Tuteja et al., 1996) and the cloning of the first plant DNA helicase cDNA encoding biochemically active protein was reported in 2000 (Pham et al., 2000). A list of biochemically active DNA helicases reported so far from plant cells is shown in Table 2 and is described briefly below.
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Lily DNA helicase
The first plant DNA unwinding protein (‘U-protein’) was only partially purified from meiotic cells of Lilium and shown to be present at a high level during the meiotic prophase of lily cells (Table 2) (Hotta and Stern, 1978). Lily helicase required a 3'-OH terminus for both binding and unwinding of duplex DNA. This protein was different from bacterial U-protein I and II, which can also unwind DNA-RNA duplexes, whereas the lily U-protein did not show such activity.
Chloroplast DNA helicases
Eleven years after the first report of the plant DNA helicase, a second plant DNA helicase was reported, also in a partially purified form, from chloroplasts of the SB-1 cell line of Glycine max (Table 2) (Cannon and Heinhorst, 1990). Later on, two more chloroplast DNA helicases were purified and characterized from pea (Tuteja et al., 1996; Tuteja and Phan, 1998). These have been covered in detail previously (Tuteja, 2000). The properties and the differences between the chloroplast DNA helicases are summarized in Table 3.
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Pea nuclear DNA helicases
So far only a few nuclear DNA helicases in a biochemically active and purified form have been reported from plants (Table 2). The first plant nuclear DNA helicase, named PDH45, is a protein encoded by cDNA PDH45 of pea, which was over-expressed and purified from a bacterial system (Pham et al., 2000). PDH45 is a unique member of a DEAD-box protein family, containing DESD and SRT conserved motifs instead of DEAD/H and SAT (Gorbalenya et al., 1989; Tanner and Linder, 2001). The amino acid sequence of PDH45 shows 86% similarity with the tobacco translation initiation factor-4A3 (eIF-4A) (Pham et al., 2000). PDH45 is also homologous to the DEAD-box helicase from Arabidopsis thaliana (At3g19760) that is orthologous to FAL1 in yeast, which is involved in the biogenesis of ribosomes (Kressler et al., 1997; Tanner and Linder, 2001). eIF-4A was previously reported as an RNA helicase and it plays a key role in unwinding inhibitory secondary structures (present in the 5' UTRs of many proteins) during translation initiation of mRNAs (Pause et al., 1994). PDH45 also has RNA helicase activity and the antibody against it inhibits in vitro protein synthesis (Pham et al., 2000). Another most striking property of PDH45 is that it physically interacts and stimulates pea topoisomerase I activity. Topo isomerases are ubiquitously present and play a major role in cellular DNA metabolism including replication, repair, transcription, and recombination, by resolving the topological constraints imposed on DNA during these processes (Wang et al., 1990). It is possible that both types of enzymes may function in concert, as topoisomerases probably relieve helicase-induced DNA torsional tension. The overall properties of PDH45 suggested that it could be an important multifunctional protein involved in protein synthesis, maintaining the basic activities of the cell, and in the up-regulation of topoisomerase I activity (Pham et al., 2000).
The second plant nuclear DNA helicase, named PDH65, is a homologue of human DNA helicase I and was purified from pea nuclei (Tuteja et al., 2001a). The properties of PDH65 and its differences from other plant nuclear DNA helicases are described in Table 4. PDH65 is also reported as an RNA helicase and both its DNA and RNA unwinding activities are up-regulated after phosphorylation with cdc2 and CK2 protein kinases. By the incorporation of BrUTP into pea root tissue, followed by double immunofluorescence labelling and confocal microscopy, PDH65 was shown to be localized within the dense fibrillar component of pea root nucleoli in the regions around the rDNA transcription sites. These observations suggest that PDH65 might be involved in both the rDNA transcription and in the early stages of pre-rRNA processing (Tuteja et al., 2001a).
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Recently, a third pea nuclear DNA helicase has been isolated, which is present in extremely low amounts and has the highest specific activity among plant DNA helicases (Table 2; Phan et al., 2003). It is a heterodimer of 54 and 66 kDa polypeptides with a native size of 120 kDa and named as PDH120. It unwinds DNA in the 3' to 5' direction and can utilize all the NTPs/dNTPs. The properties of PDH120 and its differences from other plant nuclear DNA helicases are described in Table 4.
Plant Ku DNA helicase
Ku is a multifunctional DNA-binding heterodimer protein composed of 
70 and 80 kDa subunits (Ku70 and Ku80), originally identified as an autoantigen recognized by sera of patients with autoimmune diseases (Mimori et al., 1981; Tuteja and Tuteja, 2000). The Ku70/80 heterodimer is a critical component of the non-homologous end-joining (NHEJ) pathway and of the telomere cap in yeasts and mammals. The existence of Ku or Ku-like proteins in plant nuclei and chloroplasts was first observed by western blotting using pea proteins and anti-human Ku antibodies (Tuteja and Tuteja, 2000; Fig. 2A, B).
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Recently, the cDNAs (AtKu70 and AtKu80) encoding the first plant homologues of human Ku proteins (AtKu70 and AtKu80, respectively) have been reported from Arabidopsis thaliana (Tamura et al., 2002). The deduced amino acid sequences shared only 28.6% and 22.5% identity with the corresponding proteins from human. However, AtKu70 and AtKu80 contained previously defined conserved PHRs (primary homology regions), which have more sequence identity. Both the subunits of plant Ku interact with each other in vivo and form a functional heterodimer, which binds to double-stranded telomeric and non-telomeric DNA sequences, but not to single-stranded (ss) DNA (Tamura et al., 2002). The AtKu70/80 also contained ssDNA-dependent ATPase and ATP-dependent DNA helicase activities (Table 4). However, the DNA helicase activity of the plant Ku is not well characterized compared with human Ku (Tuteja et al., 1994). AtKu proteins have been shown to be localized in the nucleus and cytoplasm and expressed in plant tissues under normal growth conditions (Tamura et al., 2002).
Plant RecQ family of DNA helicases
Members of the RecQ family of DNA helicases are known to be involved in processes linked to DNA replication, DNA recombination and gene silencing. Now all the six cDNAs of different RecQ-like proteins (AtRecQ11, AtRecQ12, AtRecQ13, AtRecQ14A, AtRecQ14B, and AtRecQsim) have been reported from Arabidopsis thaliana (Hartung et al., 2000). These genes are expressed to a different extent in Arabidopsis thaliana, but their products have not yet been characterized biochemically as DNA helicase.
Other most likely candidates of plant DNA helicases
Some most likely candidates of DNA helicases in plants could be nucleolin (Bogre et al., 1996), MCM proteins (Sabelli et al., 1996; Springer et al., 2000), araXPB (Ribeiro et al., 1998) or products of AtXPB1, and the XPB/RAD25 homologue gene from Arabidopsis (Costa et al., 2001), because all of these proteins in other systems have been shown to be DNA helicases.
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Inhibitors of plant DNA helicases |
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TopAbstractIntroductionThe historical perspective of...Assays and direction of...Plant DNA helicasesInhibitors of plant DNA...Functions of plant DNA...Concluding remarksReferences |
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Many DNA-binding agents have been shown to modulate DNA and RNA metabolism by binding to the nucleic acid and disrupting the enzymatic machinery that interacts with it (Bachur et al., 1992; George et al., 1992). Since DNA helicases are likely to be the first component of the ‘protein machines’ during replication, recombination and other DNA structural transitions, the effect of DNA helicase inhibitors would be harmful on further DNA processes. Many inhibitors have been reported to inhibit different DNA helicases from different sources, of which nogalamycin and daunorubicin are found to be quasi-universal inhibitors of most of the DNA helicases tested so far (Pham and Tuteja, 2002). In addition to these, the inhibitors which showed inhibition of plant DNA helicases are ethidium bromide, actinomycin C1, cisplatin, and ellipticine (Pham and Tuteja, 2002). The effects of these inhibitors (inhibition constant) on different plant DNA helicases are shown in Table 5. A brief description of these compounds is given below.
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Daunorubicin intercalates into the major groove of DNA, while nogalamycin intercalates into both the major and minor grooves of DNA; nogalose sugar in the minor groove and the positive charged anion group and two hydroxyl groups in the major groove (Egli et al., 1991). Cisplatin, cis-diaminedichloroplatinum (II), is known to form covalent DNA-adducts and thereby blocks the enzymes involved in replication and transcription (Chu, 1994). It forms 1,2d (GpG), 1,2d (ApG), and 1,3d (G-pXpG) intra-strand adduct as well as inter-strand DNA cross-links between two DNA strands (Zamble and Lippard, 1995). Ethidium bromide, a potent inhibitor of DNA synthesis, is a phenathridium compound, which intercalates into DNA (Pham and Tuteja, 2002). Actinomycin C1, a polypeptide containing the properties of an antibiotic, intercalates into double-stranded DNA and thereby inhibits nucleic acid synthesis (see Pham and Tuteja 2002). Ellipticine [5,11-dimehtyl-6H-pyrido-(4,3-b)-carbazole] is a cytotoxic plant alkaloid (Pham and Tuteja, 2002).
One of the interesting findings of inhibitor study on plant DNA helicases is the differential effect of actinomycin C1 and ellipticine on chloroplast and nuclear DNA helicases from pea. The former inhibits only chloroplast DNA helicase and not the nuclear DNA helicase, while the latter inhibits only nuclear DNA helicase and not the chloroplast DNA helicase (Pham and Tuteja, 2002). This differential inhibition suggests that the mechanism of DNA unwinding could be different in both these organelles. The mechanism by which the inhibitors inhibit the unwinding reaction might be through intercalation into the duplex DNA substrate, which results in the formation of a DNA–inhibitor complex. This probably provides a physical block to continued translocation by the helicase, causing the unwinding reaction to be inhibited. The inhibitor study might be useful for a better understanding of the mechanism of plant DNA helicase unwinding and the mechanism by which these agents can disturb genome integrity.
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Functions of plant DNA helicases |
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TopAbstractIntroductionThe historical perspective of...Assays and direction of...Plant DNA helicasesInhibitors of plant DNA...Functions of plant DNA...Concluding remarksReferences |
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The functions of plant DNA helicases have not been well studied. However, indirect evidence suggests their roles in many different pathways. In the following sections, the functions of biochemically active helicases are described first, followed by the probable function of some of the plant DEAD-box and RNA helicases.
Since lily DNA helicase is reported to be prominent during meiotic prophase, a probable role in plant DNA recombination was suggested (Hotta and Stern, 1978). Most of the studies on plant DNA replication have investigated chloroplast DNA (Tuteja and Tewari, 1999) where replication begins by the formation of two D-loops (displacement loop, oriA and oriB), which expand towards each other through unwinding by DNA helicase(s) and form a Cairns replicative forked structure (Fig. 3). The small Cairns forked structure expands bidirectionally by the action of DNA helicase(s) followed by the formation of two daughter molecules (Tuteja and Tewari, 1999). Since chloroplast DNA helicase II prefers replication fork structures, its probable role in chloroplast DNA replication during Cairns fork progression was suggested (Tuteja and Phan, 1998). PDH45 is homologous to eIF-4A and contains multiple activities, therefore it may be involved in both DNA and RNA metabolism, in the initiation of translation, and in maintaining the basic activities of the cell (Pham et al., 2000). Through confocal microscopy, the plant nuclear DNA helicase (PDH65) was shown to be localized within the dense fibrillar component of pea nucleoli in the regions around the rDNA transcription sites (Fig. 4), which suggested that PDH65 may be involved both in rDNA transcription and in the early stages of pre-rRNA processing (Tuteja et al., 2001a).
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Ku plays a major role in DSB repair in the NHEJ pathway and has been implicated (directly or indirectly) in V(D)J recombination in differentiating lymphocytes, DNA replication, transcription regulation, regulation of heat shock-induced responses, regulation of structure of telomeric termini, and also plays a role in G2 and M phases of the cell cycle (Mimori et al., 1981; Tuteja and Tuteja, 2000). In plants, the transcription of Ku genes (AtKu70 and AtKu80) was shown to be up-regulated in response to the induction of DSBs by DNA-damaging agents (bleomycin and methylmethane sulphonate), which suggested that the plant Ku proteins are also important for DSB repair by the NHEJ pathway (Tamura et al., 2002). Ku has also been shown to be required for telomeric strand maintenance in plants, as the lack of Ku70 resulted in a dramatic deregulation of telomere length control. Furthermore, in contrast to the situation in mammals, chromosome fusions are not associated with a Ku deficiency in Arabidopsis. Riha et al. (2002) reported that Arabidopsis KU70/80 genes are ubiquitously expressed and their products form stable heterodimers in vitro. Plants harbouring a T-DNA insertion in KU70 exhibit no growth or developmental defects under standard growth conditions. However, mutant seedlings are hypersensitive to gamma-irradiation-induced double-strand breaks. Riha et al. (2002) observed that mutants are hypersensitive to methyl methanosulphonate during seed germination, but lose this sensitivity in seedlings, implying that the requirement for NHEJ varies during plant development. They also observed dramatic deregulation of telomere length control in a mutant lacking the Ku70 subunit (Riha et al., 2002). It is known that the telomere elongation is telomerase-dependent and any dysfunction arising from mutations in telomerase or in telomere capping proteins leads to end-to-end chromosome fusions.
The Ku70/80 heterodimer is also found at telomeres, and in mammals it is required to prevent telomere fusion. Riha and Shippen (2003) found that the terminal 3' G overhang was significantly extended in Ku70 mutants and in plants deficient in both Ku70 and the catalytic subunit of telomerase (TERT), implying that Ku is needed for proper maintenance of the telomeric C-rich strand. Consistent with inefficient C-strand maintenance, telomere shortening was accelerated in Ku70 TERT double mutants, and the onset of a terminal sterile phenotype was reached two to three times faster than in TERT single mutants. Unexpectedly, abundant anaphase bridges were found in terminal plants harbouring critically shortened telomeres, indicating that Ku is not required for the formation of end-to-end chromosome fusions in telomerase-deficient Arabidopsis. This finding is in contrast to mammals where chromosome fusions are associated with a Ku deficiency. Together, these findings suggest that Ku70 as a gene in higher eukaryotes is required for maintenance of the telomeric C-rich strand and underscores the complexity and diversity of molecular interactions at telomeres (Riha and Shippen, 2003).
The helicase activity of plant nucleolin has not been demonstrated yet. However, nucleolin is known to be a DNA and RNA helicase in human. It has been implicated directly or indirectly in many metabolic processes such as ribosome biogenesis, cell proliferation and growth, cytoplasmic-nucleolar transport of ribosomal components, replication, signal transduction and many more (Bogre et al., 1996; Tuteja and Tuteja, 1998). The induction of the plant homologue of human nucleolin gene nucMs1 expression is reported to be highest in roots and other meristematic cells of the plant and is tightly linked to cell division and cell proliferation, suggesting a significant role in plant growth and development (Bogre et al., 1996). Furthermore, it has been shown in Medicago sativa that the expression of the nucleolin gene (nucMs1) and the cyclin gene (cycMs4) is induced at the same time in the G1 phase before the onset of DNA synthesis (Bogre et al., 1996) and is linked to cell division. Nucleolin gene expression is also known as a marker for proliferation events during flower development. In pea, nucleolin is shown to be light (phytochrome) regulated (Tong et al., 1997).
The TFIIH is a 6-9 subunit complex containing XPB (ERCC3) and XPD (ERCC2) DNA helicases and plays an important role in nucleotide excision repair (NER) in mammals (for details see Tuteja and Tuteja, 2001). In plants, the NER system is still not well characterized (Tuteja et al., 2001b). The molecular evidence for the conservation of the NER pathway came from the cloning of Arabidopsis XPB (araXPB) (Ribeiro et al., 1998) and the lily homologue of human ERCCI (Xu et al., 1998). The araXPB protein shared 50% identity and 70% conserved amino acids with yeast and human homologues. The plant XPB contained all the functional domains found in the other proteins, including the nuclear localization signal, DNA-binding domain and helicase motifs suggesting that it might be playing a role in NER in plant cells (Ribeiro et al., 1998). However, the DNA unwinding activity of plant XPB has not been determined yet. Costa et al. (2001) have suggested the participation of AtXPB1, the XPB/RAD25 homologue gene from Arabidopsis thaliana, in DNA repair and plant development. The MCM proteins, first discovered in minichromosome maintenance mutants in yeast, are known to be involved in initiation and elongation during eukaryotic DNA replication and one of the MCM protein complex (MCM4/6/7) from human is also reported as a DNA helicase (Ishimi, 1997). In the case of plants, the MCM genes/products are reported (Ivanova et al., 1994; Sabelli et al., 1996, 1999; Springer et al., 1995, 2000). The DNA helicase activity of plant MCM proteins has not been yet determined.
DEAD-box proteins are mainly known as RNA helicases or putative helicases but some members are also known as DNA helicases (for details see Aubourg et al., 1999; Tuteja, 2000). By cDNA microarray analysis of 1300 Arabidopsis genes Seki et al. (2001) reported a DEAD-box helicase gene (accession number AB050574 [GenBank] ) as a cold-stress-inducible gene, which suggested that plant helicases might also play an important role in stress tolerance in plants. Recently, two chilling and freezing-stress-inducible DEAD-box helicase genes have been identified using Arabidopsis mutants that were impaired in the cold-regulated expression of CBF and their downstream target genes (Gong et al., 2002). This study suggested that DEAD-box helicases not only act as positive regulators of CBF genes, but are also involved in plant chilling resistance. Previously, a DEAD-box helicase gene (crhC) from cynobacteria was reported to be expressed specifically only under cold-shock conditions (Chamot et al., 1999). These helicases might be removing cold-stabilized secondary structures in cold-shock mRNAs, thereby overcoming the cold-induced blockage of translation initiation under cold-shock conditions (Thieringer et al., 1998). However, until now the biochemical activity of the plant stress-induced helicases has not been reported, they may be RNA helicases or both RNA and DNA helicases.
A few examples of the suggested functions of putative DEAD-box helicases are as follows. Disruption of a putative helicase/RNAse III gene in Arabidopsis causes unregulated cell division in floral meristems (Jacobsen et al., 1999). The tobacco VDL gene (for variegated and distorted leaves) encodes a plastid DEAD-box helicase and is involved in chloroplast differentiation and plant morphogenesis (Wang et al., 2000). Li SC et al. (2001) have shown that VrRHI (Vigna radiata RNA helicase I) may play a role in the viability of mung bean seeds. Dalmay et al. (2001) reported that the SDE3 gene, which encodes a putative helicase, is required for post-transcriptional gene silencing in Arabidopsis. Recently, the DDM1 gene of Arabidopsis was reported to be a homologue of the SW12/SNF2 family of helicases, which is required for the maintenance of genomic methylation patterns in plant and mammals (Bourc’his and Bestor, 2002).
It has been shown that the RNA binding protein, HUA, and a putative DExH box helicase, HEN (HUA ENHANCER), play important roles in flower and vegetative development in Arabidopsis (Chen and Meyerowitz, 1999; Jack, 2002; Li J et al., 2001; Chen et al., 2002; Cheng et al., 2003). The Arabidopsis floral organ identity gene AGAMOUS (AG) specifies stamen and carpel development as well as floral determinacy. The identities of the four floral organ types in an Arabidopsis flower are specified by the combinatorial activities of the floral homeotic A, B, and C function genes; AGAMOUS is the only known C function gene. The HUA1, HUA2, HEN1, and HEN2 genes encode nuclear proteins that play a role in RNA metabolism and these genes also function redundantly as components of the AG pathway. HEN1 was identified from a sensitized genetic screen in the hua1-1 hua2-1 background that is compromised in floral homeotic C function (Chen et al., 2002). It has been shown that HEN1, like the C function gene AGAMOUS, acts to specify reproductive organ identities and to repress A function. HEN1 also shares AG’s non-homeotic function in controlling floral determinacy. HEN1 may achieve these functions by regulating the expression of AG. hen1 single mutants exhibit pleiotropic phenotypes such as reduced organ size, altered rosette leaf shape and increased number of coflorescences, during most stages of development. Therefore, HEN1, like the A function gene AP2, plays multiple roles in plant development as well as acting in organ identity specification in the flower. HEN1 codes for a novel protein and is expressed throughout the plant (Chen et al., 2002). It has been shown that HEN2, a putative DExH-box helicase, maintains homeotic B and C gene expression in Arabidopsis (Western et al., 2002). Recently it has been reported that strains carrying mutations in three genes, HUA1, HUA2, and HEN4, exhibit floral defects similar to those in agamous mutants: reproductive-to-perianth organ transformation and loss of floral determinacy (Cheng et al., 2003). It has been shown that HUA1 binds AGAMOUS pre-mRNA in vitro and that HEN4, HUA1, and HUA2 act in floral morphogenesis by specifically promoting the processing of AGAMOUS pre-mRNA (Cheng et al., 2003).
A recently discovered Helitron insertion, a DNA helicase-bearing transposable element, in the maize genome has suggested the possible role of plant DNA helicase in a new class of transposon (Lal et al., 2003). Autonomous Helitrons encode a 5' to 3' DNA helicase and are known to transpose by a rolling-circle mode of DNA replication and are, therefore, also called rolling-circle transposons (Kapitonov and Jurka, 2001). Although the maize element lacks sequence information for a DNA helicase, however, it does contain four exons with similarity to a plant DEAD-box helicase (Lal et al., 2003).
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Concluding remarks |
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TopAbstractIntroductionThe historical perspective of...Assays and direction of...Plant DNA helicasesInhibitors of plant DNA...Functions of plant DNA...Concluding remarksReferences |
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The involvement of helicases in almost all DNA and RNA metabolism has several implications of general interest. It is naïve to think of helicases simply as nucleic acid unwinding enzymes. In plants, this field has received relatively poor attention at the biochemical level and this review intends to highlight this important point. The understanding of different functions of plant helicases is of critical importance. Through indirect evidence, the involvement of plant DNA helicases has been suggested in the following biological processes: DNA recombination, DNA replication, translation initiation, rDNA transcription and in the early stages of pre-rRNA processing, double-strand break repair, nucleotide excision repair, the maintenance of telomeric length and basic activities of cells, the plant cell cycle, the maintenance of genomic methylation patterns, and in cell division/proliferation during flower development.
It will be important to understand the detailed energetics of the translocation process and the mechanism of unwinding which is still not well understood. Structural analysis, revealed by electron microscopy, is beginning to provide clues to some of the functions and mechanisms of action of these remarkable proteins in prokaryotes. A better understanding of these proteins in plants will still have to wait for the necessary breakthrough that, hopefully, will be provided by the high-resolution structure of a helicase to be solved by X-ray crystallography. To understand the regulation of DNA helicases from plants, it is crucial to identify and characterize the protein kinases and phosphatases that act on these helicases for their regulation. Translational control has a key role in regulating cell growth. The eIF-4A (a DNA and RNA helicase) of plants needs to be studied in detail in order to understand the control of translation, which is fundamental to the regulation of the cell cycle.
The knowledge gained so far about plant cell DNA helicases has provided the framework for further studies towards elucidating their biological function. Considering the multiplicity of helicases, their tissue specificity, functional diversity and control of activity by phosphorylation/dephosphorylation, it is reasonable to assume that they also play an important role in plant cell division, growth and development. Therefore, this exciting field must be accelerated in plants. Furthermore, in plants, the RNA approach and/or making of transgenic anti-sense plants will help in understanding the detailed role of helicases in plant growth and development and, therefore, will have important biotechnological applications. Overall, the analysis of plant DNA helicases is beginning to expand our understanding of nucleic acid metabolism in plants and is also providing scientists with a dizzying array of tools for plant cellular machinery.
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Acknowledgements |
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I would like to thank Mr Tran Quang Ngoc for his help in preparation of illustrations and Drs Renu Tuteja and SK Sopory for reading and commenting on the manuscript.
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