Molecular Plant Advance Access originally published online on October 3, 2008
Molecular Plant 2008 1(6):888-898; doi:10.1093/mp/ssn060
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Arabidopsis Mutants and the Network of Microtubule-Associated Functions
Department of Cell and Developmental Biology, John Innes Centre, 1 Colney Lane, Norwich NR4 7UH, UK
1 To whom correspondence should be addressed. E-mail Henrik.Buschmann{at}bbsrc.ac.uk, fax 0044 1603 450022, tel. 0044 1603 450135.
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Abstract |
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In early eukaryotes, the microtubule system was engaged in mitosis, intracellular transport, and flagellum-based motility. In the plant lineage, the evolution of a multicellular body involved the conservation of some core functions, the loss of others, and the elaboration of new microtubule functions associated with the multicellular plant habit. This diversification is reflected by the presence of both conserved (animal/fungi-like) and novel (plant-like) sequences encoding microtubule-related functions in the Arabidopsis genome. The collection of microtubule mutants has grown rapidly over recent years. These mutants present a wide range of phenotypes, consistent with the hypothesis of a functional diversification of the microtubule system. In this review, we focus on mutant analysis and, in particular, discuss double mutant analysis as a valuable tool for pinpointing pathways of gene function. A future challenge will be to define the complete network of genetic and physical interactions of microtubule function in plants. In addition to reviewing recent progress in the functional analysis of the ‘MAPome’, we present an online database of Arabidopsis mutants impaired in microtubule functions.
Key Words: cell division • cell morphogenesis • cytoskeleton • genetics • development • Arabidopsis
Received for publication July 21, 2008. Accepted for publication August 22, 2008.
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INTRODUCTION |
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TOPAbstractINTRODUCTIONCONCLUSION AND OUTLOOKSUPPLEMENTARY DATAFUNDING |
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Plants Have Evolved Several New Functions for Microtubules
Microtubules are rod-like cytoplasmic polymers assembled from dimers of
and β tubulin and are found in all eukaryotic kingdoms. In vivo, microtubules show dynamic instability based on alternating phases of polymerization and catastrophic depolymerization. This enables microtubules to quickly re-arrange into arrays of various functions. In ‘primitive’ unicellular eukaryotes, microtubules are used for chromosome separation in mitosis and are employed for the regulation of intracellular transport and flagellum-based motility (Margulis et al., 2006). During the evolution of algae and land plants, important functional adjustments to this ‘basal’ microtubule system were achieved. For example, higher plants have lost the flagellum and basal bodies but have critically reorganized the arrangement of interphase microtubules. The interphase array of cortical microtubules found in plant cells is an array of mainly parallel microtubules that underlies the plasma membrane (reviewed by (Ehrhardt and Shaw, 2006; Pastuglia and Bouchez, 2007; Lucas and Shaw, 2008). This cortical array functions in cell wall assembly (Roudier et al., 2005; Paredez et al., 2006) and has an important role in determining the direction of cell and organ growth. In most cases, cell elongation occurs in a direction perpendicular to the alignment of cortical microtubules. Animal and fungal cells possess no structure that resembles the cortical array seen in higher plant cells. In contrast, various groups of protozoa show dense configurations of cortical microtubules. Whereas cortical microtubules are nucleated from dispersed sites in the cortex of higher plants, protozoa (such as trypanosomatid parasites) nucleate cortical microtubules from apically located basal bodies that also carry the flagellum (Gull, 1999). The cortical array seen in such organisms may therefore stem from convergent evolution. Plant cell division employs further plant-specific microtubule arrays. In contrast to animals, plant cells do not divide by constriction but by assembling a new cross-wall (the so-called cell plate) that grows out centrifugally from the remnants of the anaphase spindle until the cortex is reached. Growth of the new cross-wall is facilitated by phragmoplast microtubules that serve as tracks for motor proteins (kinesins) delivering new cell-wall material to the growing cell plate. At an early stage, the plant phragmoplast resembles the midbody—the spindle remnant that is involved in the final abscission of animal daughter cells after the actin-based contractile ring has almost cleaved the cells apart. The major difference is that, in plants, this column-shaped structure opens out into a centrifugally growing ring. Similarities exist in the membrane trafficking processes involved in cytokinesis (Jürgens, 2005; Konopka et al., 2006). Also, the microtubule-associated protein MAP65, which cross-bridges microtubules at particular stages of plant cell division, is related to PRC1, Ase1p, Feo, and SPD1, which perform homologous functions in animals, yeast, flies, and Caenorhabditis elegans, respectively (Mao et al., 2005; Barr and Gruneberg, 2007). In plants, the plane of cell division is determined before mitosis by a structure that is termed the preprophase band (PPB) (reviewed by Lloyd and Buschmann, 2007; Van Damme et al., 2007). In cells approaching division, cortical microtubules bunch up to form the PPB, which encircles the cell in the position at which the new cross-wall will insert after mitosis. However, microtubules of the PPB depolymerize at nuclear envelope breakdown when microtubules gain access to the chromosomes, which are then separated on the bipolar spindle. The main function of the PPB is therefore to deposit a mark at the cell's cortex that serves to memorize the plane of division and to attract the outgrowing phragmoplast and cell plate. The PPB appears to be present only in mosses and vascular plants (Gunning et al., 1978).
Apart from cell expansion being associated with the cortical array and cell division with the PPB and phragmoplast, further plant-specific microtubule functions have been recently described. Such functions include trichome branching (Oppenheimer et al., 1997) and root hair tip growth (Sakai et al., 2008), pathogen response (Riemann et al., 2002; Kragler et al., 2003; Caillaud et al., 2008; Hardham et al., 2008), and salt stress (Shoji et al., 2006; Wang et al., 2007).
The Genome for Microtubule-Associated Functions May Contain Several Hundred Genes
Given that higher plants show a combination of old (e.g. chromosome separation through spindle microtubules) and derived microtubule functions (e.g. cytokinesis using PPB and phragmoplast), one might expect to find a combination of old and novel genes encoding microtubule-related functions in the genome of the model plant Arabidopsis. Indeed, the small gene families encoding -, β- and 
-tubulins as well as genes coding for the tubulin-folding machinery are highly conserved. The Arabidopsis genome further encodes various microtubule-associated proteins (MAPs) with homologs in animals and yeast, like the MAP65/PRC1 family with nine group members (Smertenko et al., 2000; Mollinari et al., 2002) involved in microtubule bundling (Chan et al., 1999). Another example is provided by the End-Binding1 (EB1) family of plus tip proteins with three members (Tirnauer and Bierer, 2000; Mathur et al., 2003). The kinesin-related motor proteins represent a larger diversification. Arabidopsis possesses at least 61 genes encoding kinesin motor-domains, many of which are predicted to contain additional functional domains like armadillo-repeats, actin-binding regions as well as calmodulin-binding sites (Reddy and Day, 2001). And, as perhaps anticipated from the diversification of microtubule function, plants possess several protein families with microtubule-associated functions that are not related to prototype MAPs known from animals and fungi. These include the MAP70 family (five members) (Korolev et al., 2005), the TORTIFOLIA1/SPIRAL2 family (six members) (Buschmann et al., 2004; Shoji et al., 2004), and AIR9 (encoded by a single copy gene) (Buschmann et al., 2006).
There is therefore a core of ‘classical’ MAPs that are either homologous to ones found in other eukaryotes, plus novel MAPs that have been functionally identified in plants. However, the microtubule proteome is likely to be much larger, for, in addition to proteins that conform to the classical definition of binding firmly to microtubules in vitro, there will be proteins that are part of MAP complexes (or at least transiently associate with them), the machinery involved in tubulin folding and tubulin itself. With this definition in mind, we estimate, based on published similarity searches (Gardiner and Marc, 2003), our own database searches (Buschmann, unpublished data), forward proteomic (Korolev et al., 2005), and mutant screens (see Supplemental Table 1), that the microtubule proteome of Arabidopsis is composed of a conservative minimum of 200 proteins and is likely to contain many more.
Mutants with Defects in Microtubule Function Show Cell Type-Specific, Stage-Specific, or Ubiquitous Phenotypes
Forward and reverse genetic strategies have supplied us with various Arabidopsis mutants showing defects in microtubule function. This allows microtubule function to be tested in a wide range of cell and tissue types (Figure 1). The number of available mutants is growing rapidly, currently comprising about 40 mutant loci. Supplemental Table 1 presents all Arabidopsis microtubule function mutants known to the authors at the date of submission. This table is also found online on the World Wide Web (www.jic.ac.uk/staff/clive-lloyd/henrik-buschmann/microtubulemutants) and our intention is to update it frequently.
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Assuming that microtubule function in higher plants is diverse, is there such a thing as a typical microtubule phenotype? No, but it is interesting that a number of separate phenotypes have been reported repeatedly and for independent mutants. A range of frequently reported phenotypes is presented in Table 1. In a given mutant, one or several of such phenotypes may be displayed. Some mutants have broad phenotypes with defects visible in almost every organ and cell type. For example, kiesel mutants, which are defective in the single copy gene that codes for the tubulin-folding cofactor A, are stunted plants that show a severe loss in cell anisotropy and defects in karyo- and cytokinesis (Kirik et al., 2002b). Other microtubule function mutants show phenotypes that appear to be specific for a certain cell type (e.g. the trichome-branching mutant zwichel), a certain type of organ or tissue (spr1 mutants show obvious defects in epidermal and cortical cells but the stele appeared to be normal), or a developmental stage (in tor1 plants, leaf twisting is strong in primary leaves, but weak in rosette leaves, unpublished results). Such observations support the notion that microtubule function in plants is diverse and that the microtubule system may be specialized in certain cell or tissue types. In cases in which microtubule-related functions are encoded by gene families, organ- or stage-specific mutant phenotypes may reflect gene expression patterns. However, the fact that certain mutant phenotypes show no overlap at all (e.g. tor1 and zwichel) suggests the presence of distinct genetic pathways of microtubule function.
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Microscopy of Mutants Helps to Identify Protein Function
When a novel MAP is identified in, for example, a mutant screen, then its molecular or sub-cellular function may not be immediately clear. In such cases, the microscopic analysis of microtubule arrays in mutant and wild-type background often provides important clues concerning protein function. We provide two examples in which the analysis of microtubule arrays in a mutant background has helped to identify protein function.
Proteins required for wild-type orientation of cortical microtubules
Arabidopsis helical growth mutants show striking left- or right-handed organ torsions. A thorough investigation by Furutani et al. (2000) provided the first link between helical organ growth of Arabidopsis mutants and microtubules. The authors showed that in the right-handed spiral1 (spr1) mutant, helical root growth is linked with left-handed helical cortical microtubule orientations. Cloning of SPR1 revealed a novel protein of unknown function specific to plants. GFP-tagging of SPR1 (also termed SKU6) suggested that this novel gene encodes for a protein that associates with microtubules plus-ends (Nakajima et al., 2004; Sedbrook et al., 2004). tor1 mutants show similar right-handed helical organ torsions; however, the additive phenotype of tor1/spr1 double mutants suggests that the two loci represent independent genetic pathways (Furutani et al., 2000). Cloning and analyses of TOR1 (also termed SPIRAL2) showed that this plant-specific protein binds directly to microtubules (Buschmann et al., 2004; Shoji et al., 2004). tor1 mutants exhibit aberrant microtubules in hypocotyls, including a pronounced shift towards left-handed helical microtubule orientations. The results suggest that SPR1 and TOR1 proteins function in orienting microtubules and that they are required to prevent the formation of left-handed helical arrays. The analysis of tor1, spr1, and further helical growth mutants (Ishida et al., 2007) supported the earlier notion that plant cortical microtubule arrays show an intrinsic asymmetry (Liang, 1996). However, the molecular basis of this asymmetry is not known.
The analysis of microtubule orientations in hypocotyls of tor1 had to be based on a thorough description of microtubule orientations in the wild-type. Interestingly, it was found that, in hypocotyls growing at maximum rate, only a fraction of the cells exhibited transverse microtubule arrays and that most cells showed oblique arrays (Buschmann et al., 2004). This is very different from roots, where fast growing cells show strictly transverse microtubule arrays (Sugimoto et al., 2000; Sedbrook and Kaloriti, 2008). Recently, strikingly oblique microtubule orientations were also reported for elongating sunflower hypocotyls (Hejnowicz, 2005). This study based on fixed cells suggested that microtubules change their orientation in a rotating fashion. A recent study based on time-lapse microscopy by Chan et al. (2007) supports the notion that growing Arabidopsis hypocotyls show varying array orientations and that this may be based on rotating fields of microtubules.
Kinesins are required to establish the division site
Of the two principal eukaryotic motor proteins, dynein and kinesin, plants seem to have retained only kinesin, since the Arabidopsis genome is devoid of the force-producing dynein heavy chain subunits. Prototype kinesins migrate along microtubules based on cycles of ATP hydrolysis and nucleotide exchange. Kinesins with binding domains for cargo allow the asymmetric sub-cellular distribution of specific cargo, like protein complexes or vesicles. Other kinesins, such as the tetravalent kinesin-5 members, cross-link microtubules and slide them apart in opposite directions (Asada et al., 1997; Barroso et al., 2000). However, binding of kinesins to microtubules and cargo needs to be confirmed experimentally and cannot be deduced from sequence homology only. Recent research using Arabidopsis mutants has uncovered multiple functions for kinesins in cells undergoing division. Several kinesins are required for phragmoplast growth and cytokinesis (Strompen et al., 2002; Tanaka et al., 2004; Lee et al., 2007) whereas others are required for spindle organization and chromosome separation (Marcus et al., 2003; Ambrose et al., 2005; Bannigan et al., 2007).
Two recent papers describe a class of so-called phragmoplast-orienting kinesins (pok) that are required for division plane alignment: pok mutants are characterized by intact but irregularly placed cross-walls. The quantitative analysis of PPB and phragmoplast orientation suggested that phragmoplast guidance is defective in pok mutants. Because pok mutants form PPBs, it appears that POK kinesins are specifically required for the establishment of the PPB memory (Müller et al., 2006). The only protein known to memorize the former PPB site is TANGLED1. tan1 mutants have a phenotype comparable to pok in that phragmplast guidance is impaired (Walker et al., 2007). Importantly, it was possible to show that TAN1 is not localized to PPB sites in pok background. This suggests that POK kinesins function upstream of TAN1 and raises the possibility that POK motors may transport TAN1 to PPB sites. Live-cell imaging of GFP-tagged POK kinesin is required to support this intriguing model. Another unresolved question is how the TAN1-decorated PPB memory communicates with the phragmoplast to ensure that the cell plate ‘lands’ correctly at the predicted site.
Mutants Can Be Employed to Identify Genetic Pathways of Microtubule Function
Genes and proteins do not function in isolation, but through a multitude of genetic and physical interactions. Double mutant analyses provide a powerful means of analysing genetic interactions. Microtubule phenotypes of Arabidopsis mutants are reproducible in the sense that most phenotypes have been observed repeatedly—but for independent loci. Geneticists might conclude that the affected genes act in the same pathway and may therefore aim to conduct a double mutant analysis to support this idea (Box1). For example, picture two metabolic enzymes that act on subsequent steps in a reaction chain. If both enzymes are knocked out in a double mutant, one would expect the double mutant's phenotype to be identical to the single knockouts. If, instead, the phenotype of the double mutant is additive (in some cases, multiplicative, depending on scale), it is concluded that the two enzymes act on independent genetic pathways (Mani et al., 2008). It is important to note that this conclusion is valid only for combinations of null or near null mutants. Situations in which the double mutant phenotype is non-additive lead to seemingly non-Mendelian segregation ratios in the F2 population. The genetic interaction that is indicated through this segregation behaviour is often described by the word epistatis. The term epistasis, in its original meaning as it was coined by Bateson (1909), describes an interaction of two loci where the first locus masks the phenotypic manifestation of a second (Box1). For a discussion of the original and derived meanings of the term epistasis, see Phillips (1998). Double mutant analyses may employ phenotypically similar mutants; however, one may also combine mutants with highly dissimilar phenotypes. If the phenotypes of two mutants are different from one another or do only partially overlap, epistatic interactions may be used to answer questions relating to the order of gene action (Avery and Wasserman, 1992).
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Recent work in budding yeast has gone in new directions in order to determine genetic interactions on a genome-wide scale and may have lessons for plant biology. The studies in yeast became possible through the construction of the genome-wide set of knockout deletion mutants. The majority of the obtained single knockout mutants were able to grow under optimal growth conditions but approximately 18 % of all genes were revealed to be essential (Giaever et al., 2002). In order to uncover genetic interactions between the viable knockout mutations, systematic double mutant analyses were carried out on the basis of synthetic lethality screens. In yeast, double mutants are routinely created through a series of replica-plating steps. In a typical experiment, a set of query mutants of related function is crossed with the genome-wide set of viable deletion mutants and resulting double mutants are screened for survival. Those double mutant combinations that do not support growth are assumed to present a synthetic lethal interaction. Synthetic interactions are genetic interactions in which the double mutant phenotype is different (often more dramatic) from the single mutant or additive phenotype and, in the case of synthetic lethality, does not support survival (Box1). The common interpretation of synthetic lethal interactions is that the knockout of two mutually buffering pathways leads to a shortage of an essential function (cell wall integrity, DNA repair, etc.) beyond which cell survival cannot be sustained (Ooi et al., 2006). Indeed, several case studies in yeast have shown that synthetic lethal interactions mainly point to independent but related pathways. For example, synthetic lethality analyses have shown that microtubule-based functions are buffered by both actin-based and DNA synthesis or DNA repair functions (Tong et al., 2004). The great (but not yet fulfilled) promise of synthetic lethality analyses in yeast is to analyse all possible double mutant combinations and thereby to reveal the complete genome-wide genetic interaction network. Estimates predict about 200,000 genome-wide synthetic lethal interactions, whereas only
1000 single deletion mutants are not viable under normal growth conditions (Boone et al., 2007). Synthetic lethality analysis is an efficient way of assaying synthetic enhancement in single-celled yeast. In contrast to yeast, multicellular organisms like Arabidopsis allow the genetic analysis of cells and tissues that are not directly required for germ cell survival. We are just beginning to understand the genetic interactions involving the microtubule system of Arabidopsis. However, double mutant analyses (e.g. Furutani et al., 2000; Kirik et al., 2007) and the great variety of mutant phenotypes (see Table 1 and Figure 1) suggest the existence of a number of discrete genetic pathways involving microtubules in Arabidopsis. The list of available microtubule mutants (Supplemental Table 1) is designed to serve as a guide to creating double mutants involving microtubule functions. Because mutant crossing in Arabidopsis is currently made by hand, a complete set of double mutants for microtubule-associated functions is probably out of the question. However, suppressor and enhancer screens of known microtubule mutants appear to be powerful methods for uncovering pathways involving microtubule-related functions. Indeed, forward screens on the basis of zwichel and spiral1 mutants have already yielded important new mutants (Krishnakumar and Oppenheimer, 1999; Thitamadee et al., 2002).
The Network of Physical Interactions and Microtubule-Associated Complexes
In certain cases, the observation of a genetic interaction raises the possibility of a physical interaction of the encoded proteins. Most proteins function in protein complexes. For example, based on yeast two-hybrid screens and proteomic analyses, estimates for budding yeast predict about five to ten interactions per protein on average (Grigoriev, 2003; Hart et al., 2006). What microtubule-associated complexes are present in Arabidopsis? There is some evidence for microtubule plus and minus end complexes. EB1, CLASP1, and SPR1 were shown to localize to microtubule plus ends (Chan et al., 2003; Sedbrook et al., 2004; Ambrose et al., 2007; Kirik et al., 2007). MOR1 may also localize to plus ends, as its homolog XMAP215 is known to be involved in the addition of tubulin-dimers to microtubule plus ends (Whittington et al., 2001; Brouhard et al., 2008). In animals, CLASP1 was shown to interact with EB1 physically, but no evidence could be provided for plants so far (Kirik et al., 2007; Akhmanova and Steinmetz, 2008). In a review article, Arabidopsis EB1 and the plant-specific plus-tip protein SPR1 were reported to interact in vitro, genetically and in yeast two-hybrid (Kaloriti et al., 2007), but detailed experimental data have not been published. Data are also sparse concerning the composition of a microtubule nucleating complex at the minus ends of Arabidopsis microtubules. Biochemical data show that -tubulin is present in high molecular weight protein complexes (Drykova et al., 2003) and genetic analyses stress the importance of -tubulin for microtubule assembly (Binarova et al., 2006; Pastuglia et al., 2006). The Arabidopsis -tubulin-containing complex also contains homologs of SPC98 and SPC97, required for microtubule nucleation in yeast. SPC98 from Arabidopsis was shown to facilitate microtubule growth from isolated nuclei (Erhardt et al., 2002; Seltzer et al., 2007).
A microtubule-associated complex composed of the HINKEL (NACK1)/STUD1 kinesins and mitogen-activated protein KKK is likely to be present in Arabidopsis. In tobacco suspension cells, this complex is required for normal microtubule dynamics in the cytokinetic phragmoplast. Complex formation signals through the mitogen-activated kinase cascade and inactivates microtubule-bundling by tobacco MAP65-1 (Nishihama et al., 2002; Soyano et al., 2003). This allows phragmoplast expansion. Components of this signalling pathway locate to the phragmoplast midline, indicating a more or less intimate association with microtubule plus ends. Since the genes are conserved and the respective Arabidopsis mutants show obvious cytokinetic defects (Hülskamp et al., 1997; Krysan et al., 2002; Strompen et al., 2002; Yang et al., 2003; Muller et al., 2004; Tanaka et al., 2004), it is likely that a similar microtubule-associated complex and mitogen-activated kinase signalling to the phragmoplast is present in Arabidopsis (reviewed by Sasabe and Machida, 2006). Apart from data concerning plus and minus end complexes, there is good evidence for another, possibly independent microtubule-associated complex containing ZWICHEL/KCBP, ANGUSTIFOLIA1, and KIC (KCBP-interacting Ca2+-binding protein) involved in trichome branching. Yeast two-hybrid analyses indicate that ZWICHEL/KCBP interacts with ANGUSTIFOLIA and KIC, respectively (Folkers et al., 2002; Reddy et al., 2004). Biochemical data suggest that ZWICHEL/KCBP is regulated through calmodulin (Reddy and Day, 2000); however, the in vitro binding of KIC by ZWICHEL/KCBP suggests an additional level of Ca2+ regulation of the complex. Further possible physical interactors of the ZWICHEL/KCBP-containing complex are indicated through genetic suppressors of zwichel (suz) and possibly the FURCA genes (Krishnakumar and Oppenheimer, 1999; Luo and Oppenheimer, 1999). The ZWICHEL/KCBP-containing complex may be specific to plants and has been speculated to function in a microtubule-dependant vesicle trafficking process (Folkers et al., 2002; Smith and Oppenheimer, 2005).
While it seems likely that future research will present other, possibly plant-specific microtubule-associated complexes, we can already predict the existence of complexes that are conserved among eukaryotes. The kinetochore is a large assembly of protein complexes that mediates the attachment of spindle microtubules to the chromosome. Kinetochore attachment to microtubules signals to the mitotic spindle checkpoint. In Xenopus oocytes, the kinesin CENP-E is required for kinetochore capture by microtubules and for chromosome movement into the spindle equator (Kim et al., 2008). CENP-E homologs are encoded by barley and Arabidopsis genomes (At1g59540) and an antibody against barley CENP-E localizes to the outer kinetochore of metaphase chromosomes (ten Hoopen et al., 2002). CENP-E is reported to interact with several proteins of which BUBR1 and CENP-F have homologs in the Arabidopsis genome (Chan et al., 1998; Houben and Schubert, 2003). In Xenopus, BUBR1 kinase activity becomes repressed when CENP-E binds to microtubules, possibly creating a switch that signals to the mitotic spindle checkpoint and allows anaphase progression (Mao et al., 2003; Musacchio and Salmon, 2007). Arabidopsis mutants could be employed to ask whether the CENP-E and BUBR1 homologs have similar functions in plants.
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CONCLUSION AND OUTLOOK |
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TOPAbstractINTRODUCTIONCONCLUSION AND OUTLOOKSUPPLEMENTARY DATAFUNDING |
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We have seen that higher plants have evolved a microtubule system that is functionally diverse and governs most stages of plant development. The network of genetic and physical interactions underlying this functional diversity is likely to be complex. First steps have been taken to unravel such interactions. Genetic suppressor and enhancer screens, proteomic approaches and yeast two-hybrid experiments will contribute to deepen our understanding of interactions involving the microtubule system. One great future challenge is to integrate signalling pathways that target the microtubule system. Such signalling may include phytohormones (Le et al., 2005; Chilley et al., 2006), small GTPase signalling (Fu et al., 2005), cyclin-dependant kinase (Hush et al., 1996; Hemsley et al., 2001; Weingartner et al., 2001) and additional mitogen-activated-protein-kinase signalling (Naoi and Hashimoto, 2004). The set of mutants and phenotypes presented in this review (Supplemental Table 1; updated table at www.jic.ac.uk/staff/clive-lloyd/henrik-buschmann/microtubulemutants) provides a framework to analyze the genetic interactions involving the microtubule system of Arabidopsis.
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SUPPLEMENTARY DATA |
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TOPAbstractINTRODUCTIONCONCLUSION AND OUTLOOKSUPPLEMENTARY DATAFUNDING |
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Supplementary Data are available at Molecular Plant Online.
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TOPAbstractINTRODUCTIONCONCLUSION AND OUTLOOKSUPPLEMENTARY DATAFUNDING |
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This work was supported by a BBSRC grant to C.W.L.
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Acknowledgements |
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We are grateful to Ramon Torres-Ruiz for valuable discussions. No conflict of interest declared.
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