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PubMed2001

Molecular chaperones involved in chloroplast protein import.

Transport of cytoplasmically synthesized precursor proteins into chloroplasts, like the protein transport systems of mitochondria and the endoplasmic reticulum, appears to require the action of molecular chaperones. These molecules are likely to be the sites of the ATP hydrolysis required for precursor proteins to bind to and be translocated across the two membranes of the chloroplast envelope. Over the past decade, several different chaperones have been identified, based mainly on their association with precursor proteins and/or components of the chloroplast import complex, as putative factors mediating chloroplast protein import. These factors include cytoplasmic, chloroplast envelope-associated and stromal members of the Hsp70 family of chaperones, as well as stromal Hsp100 and Hsp60 chaperones and a cytoplasmic 14-3-3 protein. While many of the findings regarding the action of chaperones during chloroplast protein import parallel those seen for mitochondrial and endoplasmic reticulum protein transport, the chloroplast import system also has unique aspects, including its hypothesized use of an Hsp100 chaperone to drive translocation into the organelle interior. Many questions concerning the specific functions of chaperones during protein import into chloroplasts still remain that future studies, both biochemical and genetic, will need to address.

Chloroplast Proteins↗

PubMed2002

Development of a GFP reporter gene for Chlamydomonas reinhardtii chloroplast.

Reporter genes have been successfully used in chloroplasts of higher plants, and high levels of recombinant protein expression have been reported. Reporter genes have also been used in the chloroplast of Chlamydomonas reinhardtii, but in most cases the amounts of protein produced appeared to be very low. We hypothesized that the inability to achieve high levels of recombinant protein expression in the C. reinhardtii chloroplast was due to the codon bias seen in the C. reinhardtii chloroplast genome. To test this hypothesis, we synthesized a gene encoding green fluorescent protein (GFP) de novo, optimizing its codon usage to reflect that of major C. reinhardtii chloroplast-encoded proteins. We monitored the accumulation of GFP in C. reinhardtii chloroplasts transformed with the codon-optimized GFP cassette (GFPct), under the control of the C. reinhardtii rbcL 5'- and 3'-UTRs. We compared this expression with the accumulation of GFP in C. reinhardtii transformed with a non-optimized GFP cassette (GFPncb), also under the control of the rbcL 5'- and 3'-UTRs. We demonstrate that C. reinhardtii chloroplasts transformed with the GFPct cassette accumulate approximately 80-fold more GFP than GFPncb-transformed strains. We further demonstrate that expression from the GFPct cassette, under control of the rbcL 5'- and 3'-UTRs, is sufficiently robust to report differences in protein synthesis based on subtle changes in environmental conditions, showing the utility of the GFPct gene as a reporter of C. reinhardtii chloroplast gene expression.

Amino Acid Sequence↗

PubMed2005

Complete nucleotide sequence of the chloroplast genome from the Tasmanian blue gum, Eucalyptus globulus (Myrtaceae).

The complete nucleotide sequence of the chloroplast genome of the hardwood species Eucalyptus globulus is presented and compared with chloroplast genomes of tree and non-tree angiosperms and two softwood tree species. The 160,286 bp genome is similar in gene order to that of Nicotiana, with an inverted repeat (IR) (26,393 bp) separated by a large single copy (LSC) region of 89,012 bp and a small single copy region of 18,488 bp. There are 128 genes (112 individual gene species and 16 genes duplicated in the inverted repeat) coding for 30 transfer RNAs, 4 ribosomal RNAs and 78 proteins. One pseudogene (psi-infA) and one pseudo-ycf (psi-ycf15) were identified. The chloroplast genome of E. globulus is essentially co-linear with that of another hardwood tree species, Populus trichocarpa, except that the latter lacks rps16 and rpl32, and the IR has expanded in Populus to include rps19 (part of the LSC in E. globulus). Since the chloroplast genome of E. globulus is not significantly different from other tree and non-tree angiosperm taxa, a comparison of hardwood and softwood chloroplasts becomes, in essence, a comparison of angiosperm and gymnosperm chloroplasts. When compared with E. globulus, Pinus chloroplasts have a very small IR, two extra tRNAs and four additional photosynthetic genes, lack any functional ndh genes and have a significantly different genome arrangement. There does not appear to be any correlation between plant habit and chloroplast genome composition and arrangement.

Base Sequence↗

PubMed1987

Use of nuclear mutants in the analysis of chloroplast development.

Although a wide range of mutations in the nuclear genome also affect chloroplast biogenesis, their pleiotropic nature often limits their use in studying nuclear genes that regulate or facilitate chloroplast development. However, many mutations that cause a high-chlorophyll-fluorescent (hcf) phenotype exhibit limited pleiotrophy, causing the loss of functionally related sets of chloroplast polypeptides. Several hcf mutations are described that result in the loss of one specific protein complex from the thylakoid membrane. Chloroplast and cytosolic mRNAs coding for component polypeptides of the missing complex are unaffected in the mutants, suggesting that each mutation disrupts some process in the synthesis and assembly of the missing complex. Another hcf mutation causes both the loss of three protein complexes and grossly abnormal thylakoid membrane structures. The primary effect of this mutation might be in the assembly of thylakoid membranes or in the stable accumulation of the three protein complexes. Two other hcf mutations are more pleiotropic. Hcf*-38 causes a quantitative reduction of many chloroplast proteins and a reduction of some chloroplast RNAs, including several splicing intermediates. Hcf*-7 causes a major reduction of all chloroplast-encoded proteins examined. The range of pleiotropic effects of hcf mutations indicates that the mutations identify nuclear genes whose products are involved in a number of different steps in chloroplast development. Because some of the mutations described have been generated by transposon insertions, they can be cloned using the transposon to identify the mutant allele.

Cell Nucleus↗

PubMed1986

Chloroplast gene expression in nuclear, photosynthetic mutants of maize.

To assess possible roles of nuclear genes in chloroplast biogenesis, five photosynthetic mutants of maize with nuclear lesions were characterized with respect to their chloroplast proteins and chloroplast RNAs. Each mutant is deficient in a characteristic set of polypeptides. The high sensitivity and resolution of immunoblot analysis revealed that in no case are polypeptides completely missing. Mutants deficient in the cytochrome f/b6 or photosystem I complex show a coordinate reduction of all of the core subunits of these complexes such that the correct stoichiometries are maintained. RNA transcripts encoding most of the affected plastid-encoded proteins were analyzed on Northern blots. In general, chloroplast RNAs in mutant seedlings were not altered in size or abundance, even when the corresponding protein was barely detectable. Therefore, in most cases the nuclear lesions act within the chloroplast at a post-transcriptional level to prevent expression of chloroplast-encoded polypeptides. One mutant, hcf-38, does show striking alterations in the abundance and size of many chloroplast transcripts. The hcf-38 locus might therefore encode a product that functions in chloroplast transcription or RNA processing.

Cell Nucleus↗

PubMed1990

Three distinct ribonucleoproteins from tobacco chloroplasts: each contains a unique amino terminal acidic domain and two ribonucleoprotein consensus motifs.

Chloroplasts contain their own genetic system. Eighteen different split genes have been found among approximately 130 chloroplast genes from higher plants. However, little is known about the chloroplast splicing system. Mammalian heterogeneous nuclear ribonucleoproteins (hnRNP proteins) have been shown to be involved in splicing. We applied a purification procedure developed for HeLa cell hnRNP proteins, which uses a single-stranded DNA (ssDNA) affinity column, directly to the tobacco chloroplast lysate to isolate their chloroplast counterparts. Four proteins (mol. wt approximately 30 kd) bound strongly to the column. The amino-terminal sequences of three of them were determined and their cDNA clones were isolated from a tobacco leaf cDNA library. Sequence analysis of these clones revealed that all three proteins contain two ribonucleoprotein consensus sequences (RNP-CS), confirming their ribonucleoprotein (RNP) nature. The presence of putative transit peptides in their predicted protein sequences, and an in vitro import experiment confirmed they are located in the chloroplast. This is the first report of organellar proteins containing RNP-CS. In addition, these three chloroplast proteins have a very acidic amino-terminal domain, a novel feature among RNP proteins identified so far. They are expressed both in leaves and roots; their mRNA levels showed different light modulation in mature leaves. The three proteins might be involved in splicing and/or processing of chloroplast RNAs.

Amino Acid Sequence↗

PubMed1991

Light regulated translational activators: identification of chloroplast gene specific mRNA binding proteins.

Genetic analysis has revealed a set of nuclear-encoded factors that regulate chloroplast mRNA translation by interacting with the 5' leaders of chloroplastic mRNAs. We have identified and isolated proteins that bind specifically to the 5' leader of the chloroplastic psbA mRNA, encoding the photosystem II reaction center protein D1. Binding of these proteins protects a 36 base RNA fragment containing a stem-loop located upstream of the ribosome binding site. Binding of these proteins to the psbA mRNA correlates with the level of translation of psbA mRNA observed in light- and dark-grown wild type cells and in a mutant that lacks D1 synthesis in the dark. The accumulation of at least one of these psbA mRNA-binding proteins is dependent upon chloroplast development, while its mRNA-binding activity appears to be light modulated in developed chloroplasts. These nuclear encoded proteins are prime candidates for regulators of chloroplast protein synthesis and may play an important role in coordinating nuclear-chloroplast gene expression as well as provide a mechanism for regulating chloroplast gene expression during development in higher plants.

Animals↗

PubMed2000

Protein translocation within chloroplast is similar in Euglena and higher plants.

It is currently thought that chloroplasts of higher plants were derived from endosymbiont oxygenic photosynthetic bacteria (primary endosymbiosis), while Euglena, a photosynthetic protista, gained chloroplasts by secondary endosymbiosis (i.e., incorporation of a photosynthetic eukaryote into heterotrophic eukaryotic host). To examine if the protein transport inside chloroplasts is similar between these organisms, we carried out heterologous protein import experiments with Euglena precursor proteins and spinach chloroplasts. The precursor of a 30-kDa subunit of the oxygen-evolving complex (OEC30) from the thylakoid lumen of Euglena chloroplasts contained the N-terminal signal, stroma targeting, and thylakoid transfer domains. Truncated preOEC30s lacking the N-terminal domain were post-translationally imported into spinach chloroplasts, transported into the thylakoid lumen, and processed to a mature protein. These results showed that protein translocations within chloroplasts in Euglena and higher plants are similar and supported the hypothesis that Euglena chloroplasts are derived from the ancestral Chlorophyta.

Adenosine Triphosphate↗

PubMed1994

Protein substitution in chloroplast ribosome evolution. A eukaryotic cytosolic protein has replaced its organelle homologue (L23) in spinach.

The chloroplast translational system differs from the eubacterial ones in containing several ribosomal proteins (RPs) that have no apparent homologues in eubacteria, and in having their RP genes distributed in two cellular genome compartments. The genes maintained in the organelle genome encode mainly ribosome assembly proteins. The discovery in spinach and related plants (Caryophyllidae) of a disrupted chloroplast gene encoding the ribosome assembly protein L23 raised speculations about the transfer of the functional rpl23 gene to the nucleus or the evolutionary loss of L23 protein requirement. To solve this problem, we overexpressed in E. coli the intact rpl23 gene from corn (Zea mays), purified the protein and raised antibodies. Based on immunoanalysis, we show that a prokaryotic-type L23 protein is absent in spinach. Concomittantly we have isolated a new protein from spinach chloroplast 50 S ribosomal subunits and determined its amino acid sequence. The data revealed an unexpectedly high sequence identity to the eukaryotic family of cytosolic L23 proteins (reported from yeast, trypanosome and rat), with conservation of a peptide motif responsible for the specific interaction of these proteins with domain III of 26 S and 23 S rRNA. We propose that the prokaryotic-type L23 protein in the chloroplast ribosomes of Caryophyllidae has been replaced by a homologue of the eukaryotic cytosolic L23 family. These results represent the first case of a protein (gene) substitution in chloroplast ribosome evolution, and open a new view on how the nuclear genome could progressively exert stronger control over the chloroplast translational system. We also describe experiments on the incorporation of chloroplast L23 into E. coli ribosomes, its effect on cell growth, and an unexpected immuno cross-reaction between two chloroplast RP families.

Amino Acid Sequence↗

PubMed1996

Mitochondrial and chloroplast targeting sequences in tandem modify protein import specificity in plant organelles.

Protein targeting to plant mitochondria and chloroplasts is usually very specific and involves targeting sequences located at the amino terminus of the precursor. We challenged the system by using combinations of mitochondrial and chloroplast targeting sequences attached to reporter genes. The sequences coding for the presequence of the mitochondrial F1-ATPase beta-subunit and the transit peptide of the chloroplast chlorophyll a/b-binding protein, both from Nicotiana plumbaginifolia, were fused together in both combinations, then linked to the reporter genes, chloramphenicol acetyl transferase (CAT) and beta-glucuronidase (GUS), and introduced into tobacco. Analysis of CAT and GUS activities and proteins in the subcellular fractions revealed that the chloroplast transit peptide alone was not sufficient to target the reporter proteins to chloroplasts. However, when the mitochondrial beta-presequence was inserted downstream of the chloroplast sequence, import of CAT and GUS into chloroplasts was observed. Using the reciprocal system, the mitochondrial presequence alone was able to direct transport of CAT and, to a lesser extent, GUS to mitochondria; the GUS targeting to mitochondria was increased when the chloroplast targeting sequence was linked downstream of the mitochondrial presequence. Immunodetection experiments using subcellular fractions confirmed the results observed by enzymatic assays. These results indicate the importance of the amino-terminal position of the targeting sequence in determining protein import specificity and are considered within the hypothesis of a co-translational protein import.

Amino Acid Sequence↗

PubMed1996

Regulation of gene expression in chloroplasts of higher plants.

Chloroplasts contain their own genetic system which has a number of prokaryotic as well as some eukaryotic features. Most chloroplast genes of higher plants are organized in clusters and are cotranscribed as polycistronic pre-RNAs which are generally processes into many shorter overlapping RNA species, each of which accumulates of steady-state RNA levels. This indicates that posttranscriptional RNA processing of primary transcripts is an important step in the control of chloroplast gene expression. Chloroplast RNA processing steps include RNA cleavage/trimming, RNA splicing, ENA editing and RNA stabilization. Several chloroplast genes are interrupted by introns and therefore require processing for gene function. In tobacco chloroplasts, 18 genes contain introns, six for tRNA genes and 12 for protein-encoding genes. A number of specific proteins and RNA factors are believed to be involved in splicing and maturation of pre-RNAs in chloroplasts. Processing enzymes and RNA-binding proteins which could be involved in posttranscriptional steps have been identified in the last several years. Our current knowledge of the regulation of gene expression in chloroplasts of higher plants is overviewed and further studies on this matter are also considered.

Chloroplasts↗

PubMed1990

Optimization of delivery of foreign DNA into higher-plant chloroplasts.

We report here an efficient and highly reproducible delivery system, using an improved biolistic transformation device, that facilitates transient expression of beta-glucuronidase (GUS) in chloroplasts of cultured tobacco suspension cells. Cultured tobacco cells collected on filter papers were bombarded with tungsten particles coated with pUC118 or pBI101.3 (negative controls), pBI505 (positive nuclear control) or a chloroplast expression vector (pHD203-GUS), and were assayed for GUS activity. No GUS activity was detected in cells bombarded with pUC118 or pBI101.3. Cells bombarded with pBI505 showed high levels of expression with blue color being distributed evenly throughout the whole cytosol of the transformants. pHD203-GUS was expressed exclusively in chloroplasts. We base this conclusion on: i) the procaryotic nature of the promoter used in the chloroplast expression vector; ii) delayed GUS staining; iii) localization of blue color within subcellular compartments corresponding to plastids in both shape and size; and iv) confirmation of organelle-specific expression of pHD203-GUS using PEG-mediated protoplast transformation. Chloroplast transformation efficiencies increased dramatically (about 200-fold) using an improved helium-driven biolistic device, as compared to the more commonly used gun powder charge-driven device. Using GUS as a reporter gene and the improved biolistic device, optimal bombardment conditions were established, consistently producing several hundred transient chloroplast transformants per Petri plate. Chloroplast transformation efficiency was found to be increased further (20-fold) with supplemental osmoticum (0.55 M sorbitol and 0.55 M mannitol) in the bombardment and incubation medium. This system provides a highly effective mechanism for introducing and expressing plasmid DNA within higher-plant chloroplasts, and the fact that GUS functions as an effective marker gene now makes many genetic studies possible which were not possible before.

Bacterial Proteins↗

PubMed1988

The chloroplast genome of the green alga Chlamydomonas moewusii: localization of protein-coding genes and transcriptionally active regions.

We have recently reported the map positions of the ribosomal RNA genes and 6 protein-coding genes on the 292 kbp Chlamydomonas moewusii chloroplast genome. In the present study we localized 12 additional protein-coding genes on this green algal genome as well as 5 of these genes on the 196 kbp C. reinhardtii chloroplast genome. The gene mapping data agree with previous reports indicating that these two algal genomes differ tremendously in their global sequence organization and bear little similarity to their land plant counterparts. Among the 18 protein-coding genes examined, atpA and atpF of C. moewusii constitute the unique set of closely linked genes which is shared with land plant chloroplast genomes. The important gene order differences between the C. moewusii and C. reinhardtii chloroplast DNAs led us to speculate that gene grouping into transcription units is less prevalent in green algal chloroplast genomes than in their land plant homologs. To gain an insight into the transcriptional organization of the C. moewusii chloroplast genome, we probed Northern blots of total cellular RNA with clones covering 85% of this genome. Most chloroplast DNA regions were found to produce simple transcript patterns with RNAs less than 3.5 kb in size. This may be interpreted as indicating that Chlamydomonas chloroplast genes are transcribed mainly as monocistronic RNAs or that the RNAs observed are processed forms of unstable polycistronic transcripts.

Biological Evolution↗

PubMed1996

Selection on the codon bias of Chlamydomonas reinhardtii chloroplast genes and the plant psbA gene.

Plant chloroplast genes have a codon use that reflects the genome compositional bias of a high A+T content with the single exception of the highly translated psbA gene which codes for the photosystem II D1 protein. The codon usage of plant psbA corresponds more closely to the limited tRNA population of the chloroplast and is very similar to the codon use observed in the chloroplast genes of the green alga Chlamydomonas reinhardtii. This pattern of codon use may be an adaptation for increased translation efficiency. A correspondence between codon use of plant psbA and Chlamydomonas chloroplast genes and the tRNAs coded by the chloroplast genome, however, is not observed in all synonymous codon groups. It is shown here that the degree of correspondence between codon use and tRNA population in different synonymous groups is correlated with the second codon position composition. Synonymous groups with an A or T at the second codon position have a high representation of codons for which a complementary tRNA is coded by the chloroplast genome. Those with a G or C at the second position have an increased representation of codons that bind a chloroplast tRNA by wobble. It is proposed that the difference between synonymous groups in terms of codon adaptation to the tRNA population in plant psbA and Chlamydomonas chloroplast genes may be the result of differences in second position composition.

Animals↗

PubMed2005

Comparative studies on codon usage pattern of chloroplasts and their host nuclear genes in four plant species.

A detailed comparison was made of codon usage of chloroplast genes with their host (nuclear) genes in the four angiosperm species Oryza sativa, Zea mays, Triticum aestivum and Arabidopsis thaliana. The average GC content of the entire genes, and at the three codon positions individually, was higher in nuclear than in chloroplast genes, suggesting different genomic organization and mutation pressures in nuclear and chloroplast genes. The results of Nc-plots and neutrality plots suggested that nucleotide compositional constraint had a large contribution to codon usage bias of nuclear genes in O. sativa, Z. mays, and T. aestivum, whereas natural selection was likely to be playing a large role in codon usage bias in chloroplast genomes. Correspondence analysis and chi-test showed that regardless of the genomic environment (species) of the host, the codon usage pattern of chloroplast genes differed from nuclear genes of their host species by their AU-richness. All the chloroplast genomes have predominantly A- and/or U-ending codons, whereas nuclear genomes have G-, C- or U-ending codons as their optimal codons. These findings suggest that the chloroplast genome might display particular characteristics of codon usage that are different from its host nuclear genome. However, one feature common to both chloroplast and nuclear genomes in this study was that pyrimidines were found more frequently than purines at the synonymous codon position of optimal codons.

Arabidopsis↗

PubMed2000

The unicellular green alga Chlamydomonas reinhardtii as an experimental system to study chloroplast RNA metabolism.

Chloroplasts are typical organelles of photoautotrophic eukaryotic cells which drive a variety of functions, including photosynthesis. For many years the unicellular green alga Chlamydomonas reinhardtii has served as an experimental organism for studying photosynthetic processes. The recent development of molecular tools for this organism together with efficient methods of genetic analysis and the availability of many photosynthesis mutants has now made this alga a powerful model system for the analysis of chloroplast biogenesis. For example, techniques have been developed to transfer recombinant DNA into both the nuclear and the chloroplast genome. This allows both complementation tests and analyses of gene functions in vivo. Moreover, site-specific DNA recombinations in the chloroplast allow targeted gene disruption experiments which enable a "reverse genetics" to be performed. The potential of the algal system for the study of chloroplast biogenesis is illustrated in this review by the description of regulatory systems of gene expression involved in organelle biogenesis. One example concerns the regulation of trans-splicing of chloroplast mRNAs, a process which is controlled by both multiple nuclear- and chloroplast-encoded factors. The second example involves the stabilization of chloroplast mRNAs. The available data lead us predict distinct RNA elements, which interact with trans-acting factors to protect the RNA against nucleolytic attacks.

Animals↗

PubMed2003

The development and evaluation of consensus chloroplast primer pairs that possess highly variable sequence regions in a diverse array of plant taxa.

Although universal or consensus chloroplast primers are available, they are limited by their number and genomic distribution. Therefore, a set of consensus chloroplast primer pairs for simple sequence repeats (ccSSRs) analysis was constructed from tobacco (Nicotiana tabacum L.) chloroplast sequences. These were then tested for their general utility in the genetic analysis of a diverse array of plant taxa. In order to increase the number of ccSSRs beyond that previously reported, the target sequences for SSR motifs was set at A or T ( n >/= 7) mononucleotide repeats. Each SSR sequence motif, along with +/-200-bp flanking sequences from the first of each mononucleotide base repeat, was screened for homologies with chloroplast DNA sequences of other plant species in GenBank databases using BLAST search procedures. Twenty three putative marker loci that possessed conserved flanking sequence spans were selected for consensus primer pair construction using commercially available computer algorithms. All primer pairs produced amplicons after PCR employing genomic DNA from members of the Cucurbitaceae (six species) and Solanaceae (four species). Sixteen, 22 and 19 of the initial 23 primer pairs were successively amplified by PCR using template DNA from species of the Apiaceae (two species), Brassicaceae (one species) and Fabaceae (two species), respectively. Twenty of 23 primer pairs were also functional in three monocot species of the Liliaceae [onion (Allium cepa L.) and garlic (Allium sativum L.)], and the Poaceae [oat (Avena sativa L.)]. Sequence analysis of selected ccSSR fragments suggests that ccSSR length and sequence variation could be useful as a tool for investigating the genetic relationships within a genus or closely related taxa (i.e., tribal level). In order to provide for a marker system having significant coverage of the cucumber chloroplast genome, ccSSR primers were strategically "recombined" and named recombined consensus chloroplast primers (RCCP) for PCR analysis. Successful amplification after extended-length PCR of 16 RCCP primer pairs from cucumber ( Cucumis sativus L.) DNA suggested that the amplicons detected are representative of the cucumber chloroplast genome. These RCCP pairs, therefore, could be useful as an initial molecular tool for investigation of traits related to a chloroplast gene(s) in cucumber, and other closely related species.

Base Sequence↗

PubMed2002

Accumulation response of chloroplasts induced by mechanical stimulation in bryophyte cells.

Chloroplast movement has been studied in many plants but mainly as a model system for light signaling. However, we recently showed that the avoidance response of chloroplasts is also induced by mechanical stimulation in fern protonemal cells. Here we report the discovery of a mechanically induced accumulation response of chloroplasts in bryophytes. When mechanical stimulation was directly applied with a capillary to a part of a cell, chloroplasts moved towards and accumulated at the pressed site within 30 min after the onset of stimulation in all species tested. The accumulation movement of chloroplasts was inhibited by Cremart but not by cytochalasin B in red-light-grown protonemata of Physcomitrella patens (Hedw.) B., S. & G. To determine the contribution of external Ca(2+) to the response, we examined the effects on the accumulation movement of gadolinium (Ga(3+)), an inhibitor of stretch-activated ion channels, and lanthanum (La(3+)), a potent inhibitor of calcium channels. Mechano-relocation of chloroplasts was abolished by these drugs, but no effects were observed on photo-relocation of chloroplasts, irrespective of light colors and intensity. These results suggest that influx of external Ca(2+) through the plasma membrane is essential for the early steps in signaling of mechano-relocation of chloroplasts whose motility system is dependent on microtubules.

Adiantum↗