AOBPreview originally published online on July 24, 2006
Annals of Botany 2007 99(1):9-17; doi:10.1093/aob/mcl159
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INVITED REVIEW |
Conserved Features of Germination and Polarized Cell Growth: A Few Insights from a Pollen–Fern Spore Comparison
Molecular Cell and Developmental Biology, University of Texas, Austin, TX 78751, USA
* For correspondence. E-mail sroux{at}uts.cc.utexas.edu
Received: 18 April 2006 Returned for revision: 10 May 2006 Accepted: 12 June 2006 Published electronically: 24 July 2006
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONCALCIUM IN POLARIZED GROWTHNITRIC OXIDE IN GROWTHGENE EXPRESSION PATTERNSCONCLUSIONS AND IMPLICATIONSACKNOWLEDGEMENTSLITERATURE CITED |
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BACKGROUND: The germination of both pollen and fern spores results in the emergence of a cell—pollen tube from pollen, rhizoid from spore—that grows in a polar fashion, primarily at its apical end. In both of these tip-growing cells, the delivery of secretory vesicles to the growing end is guided in part by a calcium gradient, with calcium entering at the tip where it is most highly concentrated. The similarities between the two systems extend beyond tip-focused calcium gradients to encompass signalling pathways and elements including calmodulin, nitric oxide, annexins and Rop-GTPases.
SCOPE AND AIMS: This review is limited to those pathways and elements that function similarly in fern and pollen systems based on currently available evidence. The aim is to illustrate the common mechanisms by which tip growth occurs, facilitate further investigations into this area, and examine the implications for the evolutionarily conserved control of tip growth.
CONCLUSIONS: The interplay of calcium, nitric oxide and other effectors in both pollen and fern spores suggests certain signalling pathways became important regulators of germination and growth early in the evolution of land plants. Both large- and small-scale comparative genomic methods have shown to be promising in their ability to find new and relevant comparisons for further research. Cross-species comparisons may serve to speed up this process by highlighting both basic pathways and system-specific deviations.
Key words: Annexin, calcium, tip-growth, nitric oxide, secretion, Rop-GTPase, F-actin, Arabidopsis thaliana, Ceratopteris richardii, Dryopteris, Anemia, Nicotiana
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONCALCIUM IN POLARIZED GROWTHNITRIC OXIDE IN GROWTHGENE EXPRESSION PATTERNSCONCLUSIONS AND IMPLICATIONSACKNOWLEDGEMENTSLITERATURE CITED |
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Polar growth and development are important processes for all multicellular organisms, and are especially crucial to non-motile organisms like most plants and fungi. The best-studied examples of polar growth in plant cells are tip growth of rhizoids, root hairs and pollen tubes. In these instances, a single cell grows directionally from one end, and, in the case of pollen tubes, the growth is quite rapid. In recent years, reports have appeared describing the details of polarized growth of fern rhizoids and of pollen tubes from angiosperms. Superficially, the two systems share some common features that make them good candidates for comparison; both are dry, dormant stages of a plant's life cycle and in both the first emerging cell exhibits polar tip growth.
The functionality of the spore and the pollen grain are closely related as well. It seems most likely that the evolution of seed plants and transition to predominantly sporophytic life stages would co-opt the tip growing system for sperm delivery to the female gametophyte/ovaries. Indeed, the pollen grain is simply a reduced form of the male gametophyte, so one could imagine a situation whereby over evolutionary time the gametophyte stage atrophies to become dependent upon the sporophyte, an inverse of what still occurs today in predominantly gametophytic plants such as mosses. The reduction of the prothallus to cell divisions resulting only in generative nuclei would transform a free-living gametophyte to modern pollen. In fact, the sperm cells result from complete cell divisions and are internalized to the pollen tube by being engulfed into the main cell, much as sperm cells on the prothallus of Ceratopteris richardii gametophytes are produced through independent cell divisions occurring within a formed cavity.
Investigations into similarities between tip growth of fern spores and pollen are of practical interest beyond evolutionary implications because these systems must organize and affect polar growth within a relatively short time frame and with limited resources. Fern spores are somewhat more complex in that they typically undergo several cell divisions and differentiation before rhizoid emergence, yet they exhibit polar growth before emergence of the photosynthetically capable prothallus. Pollen is more limited in its resources, being smaller and dependent upon the stigma and style to achieve full growth potential. However, both systems are capable of germination and directed tip growth in vitro so clearly both systems must contain the necessary elements to carry out such growth. The compact nature and limited initial behaviour of these two systems makes them elegant models for the study of directed tip growth.
This review is not meant to be an exhaustive examination of tip-growth mechanisms, but rather, the goal is to focus on comparisons between these systems to highlight the common mechanisms by which tip growth occurs, facilitate further investigations into this area, and examine the implications for the evolutionarily conserved control of tip growth. It is hoped to illustrate that, beyond conservation of individual proteins or pathways, examination of disparate plant systems will reveal the conservation of complex and interconnected signalling systems.
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CALCIUM IN POLARIZED GROWTH |
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TOPABSTRACTINTRODUCTIONCALCIUM IN POLARIZED GROWTHNITRIC OXIDE IN GROWTHGENE EXPRESSION PATTERNSCONCLUSIONS AND IMPLICATIONSACKNOWLEDGEMENTSLITERATURE CITED |
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Calcium is involved in a vast array of biological processes in diverse organisms from bacteria to mammals. The localization, frequency, duration and intensity of calcium signals are believed to encode the information required for regulating a multitude of cellular activities. In the case of spores of the fern Ceratopteris richardii, calcium can function in the establishment of growth polarity. Unlike some other fern spores that have been examined, C. richardii spores align their initial rhizoid growth with the gravity vector (Edwards and Roux, 1998). The occurrence of a calcium current that flows into the bottom and out the top of the spore coincides with the period during which gravity determines the direction of cell polarization (Chatterjee et al., 2000), and the direction of this current is rapidly responsive to changes in orientation (Stout et al., 2003). This calcium movement subsides after about 24 h, but its direction predicts the direction or orientation of subsequent gravity-directed cellular processes, namely nuclear migration, asymmetric cell division and primary rhizoid emergence. Inhibition of this current by the calcium channel blocker nifedipine results in suppressing the ability of the emerging rhizoids to orient relative to gravity (Chatterjee et al., 2000). This implies a role for calcium in organizing the fern spore for asymmetric development.
Calcium is clearly involved in the early stages of pollen germination and pollen tube growth, as has been very well documented in the literature (for a comprehensive review of ions in pollen, see Holdaway-Clarke and Hepler, 2003). The polarized growth of emerging pollen tubes is crucial to proper fertilization, although, rather than gravity, pollen uses positional signals from the stigma and style as initial growth guides. Calcium is required in the growth media for proper spore rhizoid and pollen tube elongation, but pollen also requires exogenous calcium for germination to occur at all. Chemical inhibition of calcium channels will block the germination of pollen (Bednarska, 1989; Malhó et al., 1994; Franklin-Tong et al., 2002; Wang et al., 2004), certain calmodulin-binding proteins are necessary for germination (Golovkin and Reddy, 2003), and cation influx is predictive of the aperture where the pollen tube will emerge (Weisenseel et al., 1975). A strong uptake of calcium at the site where polarized growth begins has also been observed in algal zygotes (Berger and Brownlee, 1993; Pu and Robinson, 1998) and root hairs (Wymer et al., 1997). In the case of C. richardii fern spores, which only have a single point of exit through the spore coat, the early site of calcium uptake predicts the direction of post-emergent rhizoid growth (Chatterjee et al., 2000). The channels involved in germination and tube growth in pollen appear to at least be of the same class (Wang et al., 2004), most probably stretch-activated calcium channels as indicated by patch clamping and the inhibition of pollen tube ends by venom (Dutta and Robinson, 2004). The importance of general calcium homeostasis is also indicated by the requirement of the plasma membrane calcium pump ACA9 for proper germination and fertilization to occur (Schiøtt et al., 2004).
There is abundant documentation on the role for calcium in tip growth. A variety of imaging and measuring methods have repeatedly shown that growing pollen tubes have a high concentration of calcium and calcium influx at their tips (Malhó et al., 1994, 1995; Malhó and Trewavas, 1996; Pierson et al., 1996; Franklin-Tong et al., 1997, 2002; Holdaway-Clarke et al., 1997; Messerli and Robinson, 1997; Camacho et al., 2000; Snowman et al., 2000; Camacho and Malhó, 2003; Lazzaro et al., 2005). Scheuerlein and colleagues previously used fura-2 to visualize the accumulation of Ca2+ at the growing tip of fern rhizoids (Fig. 1A; R. Scheuerlein, M. Poenie, G.B. Clark, et al., University of Texas at Austin, Austin, USA, unpubl. res.).
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Beyond the simple establishment of the tip-associated calcium concentrations, research on this topic has also given us information on the impact of the ion on growth control (for reviews, see Battey and Blackbourn, 1993; Franklin-Tong, 1999; Feijó et al., 2004; Hepler, 2005). As a brief summary, pharmacological inhibition of calcium channels inhibits the emergence of pollen tubes, just as it inhibits the emergence of rhizoids. In pollen, the tip accumulation of calcium dissipates after cessation of growth, manipulation of calcium sources and ionophores can redirect tube growth, and waves of calcium accumulation are correlated with pulses in growth. The actual effectors of these tip-associated calcium events are still being decoded, but certain other cellular processes have been connected to tip-specific growth that are good candidates.
Parton et al. (2001) demonstrated a dynamic change of the membrane stain FM4-64, indicative of vesicle movements, at the tips of lily pollen tubes that cycled in time with tip growth. The inverted cone shape of the movement matches that seen in samples fixed for micrographs (Miller et al., 1996). Their data support the notion of vesicle delivery to the tip of polarly growing cells. Plant annexins are a family of proteins with a number of tie-ins to tip growth, the first being the association with Golgi-mediated vesicle secretion (Clark et al., 1992; Carroll et al., 1998; Clark et al., 2005). Plant annexins also bind to phospholipids in a calcium-dependent manner (Blackbourn et al., 1992; Calvert et al., 1996) and some have been demonstrated to exhibit calcium channel activity (Hofmann et al., 2000) and Ca2+-dependent phophodiesterase activity (Calvert et al., 1996). These properties make them highly attractive candidates for the intersection and integration of many of the processes associated with tip-growth.
Annexins are expressed in pollen tubes and fern rhizoids and have been localized to the tips of both systems (Blackbourn et al., 1992; Clark et al., 1995) (Fig. 1B and D). Blackbourn et al. (1992) also demonstrated the ability of maize annexins to bind specifically to pollen tube tip-associated vesicles, concluding from their studies that their annexins can satisfy the requirements to be involved in the process of pollen tube tip-growth. The association of annexins with dynamic cytoskeletal elements further strengthens this hypothesis because it has been observed that F-actin is important for tip growth. In Fucus, F-actin patches form at locations predictive of rhizoid emergence (Alessa and Kropf, 1999; Hable and Kropf, 2000). F-actin and microfibril organization in actively growing pollen tubes shows consistent patterning (Miller et al., 1996; Kost et al., 1998). Although rings of actin can be observed at the extreme tip of tubes (Kost et al., 1998; Lovy-Wheeler et al., 2005), clearly defined microfibrils do not occur there. The actin in this region is likely to be short and fragmented, becoming more so when Ca2+ levels peak. While Blackbourn et al. (1992) showed no binding affinity of their maize annexins for animal F-actin, actin binding has been observed for other plant annexins (Calvert et al., 1996). Importantly, plant annexins were shown to bind to plant F-actin, but not G-actin (Hu et al., 2000). This has implications for modulations of actin-association as the short actin fibres grow and fragment with the cycling of Ca2+ levels. The ability to bind both F-actin and membrane vesicles in a calcium-dependent manner, coupled with their tip-localization, quite literally positions annexins as a potentially important intermediary in the tip-signalling/tip-growth process.
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NITRIC OXIDE IN GROWTH |
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TOPABSTRACTINTRODUCTIONCALCIUM IN POLARIZED GROWTHNITRIC OXIDE IN GROWTHGENE EXPRESSION PATTERNSCONCLUSIONS AND IMPLICATIONSACKNOWLEDGEMENTSLITERATURE CITED |
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Nitric oxide (NO), like calcium, is implicated in regulating diverse cellular processes in organisms from every kingdom. There is a connection between the two signalling pathways, since an increase in cytosolic calcium can lead to an activation of NO synthase activity (in some cases through the mediation of calmodulin) and subsequent increase in NO production (Corpas et al., 2004; Lamotte et al., 2004; Vandelle et al., 2006), and NO production, in turn, can induce the release of Ca2+ from internal stores (Sokolovski et al., 2004; Vadelle et al., 2006). There are diverse modes of NO production in plants (Shapiro et al., 2005), and not all of these are regulated by calcium, but certainly the NO and calcium signalling pathways are intimately intertwined.
The involvement of NO in pollen tube growth was first documented by Prado et al. (2004). They set up a gradient of NO in a medium in which pollen was growing by allowing the NO donor s-nitrosoacetylpenicillamine (SNAP) to diffuse into the medium from a glass micropipette tip. As growing pollen tubes approached the higher concentrations of NO near the tip, their growth rate was reduced and they reoriented sharply away from the source. This response was blocked by NO scavengers. Enhanced sensitivity was seen by treatment with sildenafil citrate, an inhibitor of the animal phosphodiesterases PDE5 and PDE6, suggesting a connection to cGMP signalling.
More recently, Morris and Poterfield (2004) reported that NO can play a signalling role influencing gravity-directed cell polarity in germinating C. richardii spores. Using many of the same NO-pathway agonists and antagonists as used by Prado et al. (2004), they showed that both agonists and antagonists could disrupt the ability of gravity to direct the growth of the rhizoids. However, the most dramatic block of the ability of gravity to direct rhizoid growth was obtained with LY83583, an inhibitor of guanyl cyclase, which is typically activated by NO. Treatment with 100 µm LY83583 completely randomized the orientation of emerging rhizoids, making their orientation statistically indistinguishable from that of spores grown on a clinostat, which randomizes the position of the spores relative to the gravity vector by rotating them continuously at 1 rpm (Morris and Poterfield, 2004).
Together these results strongly suggested that the direction and rate of growth of pollen tubes and rhizoids can be regulated by NO and by a downstream product of NO stimulation, cGMP. Conservation of a signalling role for NO in fern spores and pollen is not surprising, given that enzymatic NO production has been discovered in animals, plants, protozoa, yeasts and bacteria. Torreilles (2001) has summarized the published data that point to the conclusion that ‘NO is one of the earliest and most widespread signalling molecules in living organisms’. Examples of NO (Hutchings et al., 2000; Lee et al., 2006) and Ca2+ (see review by Shemarova and Nesterov, 2005) as signalling molecules in prokaryotes indicate that the NO system is likely to be as ancient as the Ca2+ one.
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GENE EXPRESSION PATTERNS |
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TOPABSTRACTINTRODUCTIONCALCIUM IN POLARIZED GROWTHNITRIC OXIDE IN GROWTHGENE EXPRESSION PATTERNSCONCLUSIONS AND IMPLICATIONSACKNOWLEDGEMENTSLITERATURE CITED |
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The conservation of the regulatory processes involved in tip-growth imply that similar genes, or at least gene functions, are being expressed during the early stages when fern spores and pollen are preparing to initiate their polarized growth. The advent of the microarray makes large-scale gene comparisons possible, and further, cross-system comparisons have a chance of uncovering hidden but crucial players common to the systems being investigated. Even so, a critical review of the many genes in common between any two systems requires the weeding out of so-called housekeeping genes from those believed to have more specific functions. This can be accomplished in part by limiting analyses to genes found exclusively in certain tissues or time points. In the case of germinating pollen and spores, those processes involved with the establishment and execution of polarized growth of most concern, so most of the common elements found in sporophyte tissues can be excluded.
A cell becomes and maintains a polar state through non-uniform distribution of its sensing apparatus, secondary messengers and/or effectors. The non-uniform distribution of these elements can occur at several steps in the gene expression process. The control points could be through localization of mRNA or proteins via directed transport, by limiting regions of response, and through control of element stability.
A vast amount of research has been done in the area of message and protein localization using Drosophila and Xenopus oocytes, which are especially suited to these investigations due to their large size. In these systems it has been shown that not only are proteins differentially localized in a developing embryo, but localization of the RNA messages themselves can lead to localized protein distribution. A recent summary by Shav-Tal and Singer (2005) covers examples of RNA localization from several different organisms and Okita and Choi (2002) specifically discuss the topic in plants.
Of the eight genes found by Salmi et al. (2005) to be expressed in common between C. richardii spores and Arabidopsis pollen and seeds (Fig. 2), one has sequence similarity to an RNA localization Mago nashi-like gene (AT1G02140). The Mago nashi protein is a component of the exon–exon junction complex (Le Hir et al., 2001) that is also vital to the localization of oskar mRNAs (Newmark and Boswell, 1994) and the establishment of Drosophila polarity (Micklem et al., 1997). The Mago nashi genes are remarkably conserved across diverse species (Swidzinski et al., 2001). In the context of pollen, Johnson et al. (2004) have isolated a hapless mutant with pollen tube growth defects that maps to AtMago. The continued importance of RNA localization even after initial polarity establishment is not surprising, but it remains to be elucidated what effects manipulation of Mago nashi may have on the polarized development of C. richardii spores.
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Directed transport within a cell is also a method by which a cell can create domains within its internal environment. Of key importance for a polarly growing cell is not only localization of the appropriate sensing and responding elements to the growing tip, but also the delivery of basic growth materials. Vesicle delivery to the growing cell tip can accomplish both functions through delivery of plasma membrane proteins as well as cell wall materials. Relevant to this point, there is a synaptobrevin gene (AT2G32670) in the three-system comparison (Fig. 2). Synaptobrevins provide specificity to the SNAP- and SNARE-type protein targeting systems, so this particular member of the family may be functioning specifically in pollen and spore vesicle trafficking, a critical activity given the vesicle arrangements and movements that occur at pollen tube tips.
The distribution of signalling molecules is another way a single cell may establish polarity. As discussed in the above commentary on calcium in pollen tubes and rhizoids, ion concentrations can be locally regulated, with implications for local activation of calcium-related effectors, signalling pathways and responses. Salmi et al. (2005) provided a cursory glance at the genes expressed commonly between just Arabidopsis pollen and C. richardii fern spores. A more detailed examination of the 33 genes encoding proteins of known function (Table 1) reveals a few of particular interest to calcium signalling, Calmodulin-2 (CaM-2, AT2G27030) and No Pollen Germination 1 (NPG1, AT2G43040). Calmodulins are well-characterized small calcium-binding proteins that modulate the activities of other effectors. This is directly related to NPG1, a pollen-specific and tube-localized protein capable of binding to CaM-2 in a calcium-dependent manner (Golovkin and Reddy, 2003). As the name implies, npg1 pollen is incapable of germination, though not due to any observable changes in development or morphology. It would be of great interest to investigate the role of NPG1 in germinating C. richardii spores, as any similarities or differences would help to elucidate the role NPG1 has to play in the process of localized calcium signalling. Due to the obvious difficulties associated with analysing mutants that are arrested in their growth, it also remains to be seen if NPG1 continues to function at later stages of pollen tube growth.
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Protein stability also has a potential role in polarity. A less-expected player in the pollen-spore gene comparison (Table 1) is COP9, since this functional complex was originally isolated as a constitutively photomorphogenic mutant. However, the COP9 signalosome (CSN) is a protein complex involved in ubiquitin-mediated protein degradation processes and is implicated as an important regulator of a number of developmental events (for reviews, see Serino and Deng 2003; Wei and Deng, 2003). COP9 and the CSN, then, may have important regulatory and polarity-related roles.
A specific role described for CSN in pollen is in self-incompatibility responses, which effectively prevent the fertilization of eggs by genetically identical or closely related pollen. Stone et al. (2003) found that the ARM-repeat-containing protein 1 (ARC1) localized to the CSN after activation of the S receptor kinase. ARC1 exhibited E3 ligase activity, and its activation led to increased ubiquitination of pistil proteins and rejection of self pollen. The expression of COP9 transcripts in the fern spore system, which has no self-incompatibility response, implies broader roles in development for the CSN through the established paradigm of regulated protein degradation.
A review of pollen and rhizoid proteins involved in polarized growth would be incomplete without a discussion of two groups of related proteins that have received growing attention in recent years, the Rops and Rop–GEFs. A BLASTX search (Altschul et al., 1997) of Arabidopsis Rop1 against the C. richardii 20 h EST database revealed a clone with an expect value of 4e–110 (Accession Number CV734863 [GenBank] ). The expression of Rop transcripts in germinating C. richardii spores is related to a key theme of this review because the functions of Rops and their modulating Rop–GEFs are closely associated with growing pollen tips, and their activities are modulated co-ordinately with calcium fluxes. Rop1At localizes specifically to mature pollen and pollen tubes (Li et al., 1998) and injection of antibodies against Rop1 into Arabidopsis pollen tubes disrupts both tube growth (Lin and Yang, 1997) and tip-associated calcium influx (Li et al., 1999). A GFP–Rop1 fusion protein showed localization to pollen tube membranes, with tip swelling associated with stronger GFP signals, and dominant negative mutants have slow-growing tubes (Li et al., 1999). Several Rop–GEFs localize to pollen tube tips. Overexpression of Rop–GEF1 leads to loss of pollen tube polarity with appearance similar to that of the overexpressed GFP-Rop1 (Gu et al., 2006). Phosphorylation may be important to the Rop signalling pathway since hyperphosphorylation through protein phosphatase type 2A (PP2A) inhibitors results in pollen tube and actin network morphologies similar to the genetic overexpressors of Rop1 (Foissner et al., 2002). Two effector targets of Rop1, RIC3 and RIC4, are also capable of modulating F-actin assembly but do so in opposite fashions (Gu et al., 2005). The activation of conflicting pathways by Rop1 implies a role in regulation of the F-actin system. The data point to Rops and their associated proteins being integral to the process of tip-growth in pollen. Given other pollen–fern spore parallels in polarized growth regulation, the question of whether the transcripts encoding the Rop-like protein in C. richardii spores are crucial for the initiation of polarized growth of spore rhizoids seems worthy of investigation.
Another signalling system garnering attention recently is mediated by phospholipase D (PLD) and phosphoinositides. PLD and its associated modulator and effector molecules affect many of the processes relevant to tip growth in pollen tubes. Potock
et al. (2003) and Monteiro et al. (2005) demonstrated that antagonists of phosphatidic acid (PA) production (via PLD hydrolysis of PIP2) halt pollen tube growth, whereas addition of PA could increase pollen tube growth. These growth changes may be tied to changes in calcium concentrations, since IP3, the other messenger product of PLD action, causes elevations in calcium, and suppression of PA causes loss of the strong calcium gradient. Additionally, osmotic stresses in pollen tubes lead to changes in PLD activity, PA accumulation and PIP2 (Zonia and Munnik, 2004), which may have biological relevance to the cyclical rates of pollen tube growth. This system of signalling molecules is also linked to actin modifications. As with Rop1, there are RNAs encoding PLD members present in the germinating spore, so the conservation of these signalling molecules and activities of the PLDs present are worth investigating.
Certainly there are more insights to be gained from further comparative studies of transcript expression patterns in tip growing systems, as pointed out in the review by Feijó et al. (2004). Honys and Twell (2004) have continued to refine their pollen transcriptome data along with other researchers in the field (Becker et al., 2003; Lee and Lee, 2003; Pina et al., 2005). The 3000 different Ceratopteris genes represented on the microarrays analysed so far represent only about 25% of the genes being expressed in germinating spores (Salmi et al., 2005), so clearly more comprehensive microarray analyses are possible in the future. More than simply comparing tip-growth in just two cell types, however, there is the potential to compare diverse systems such as vascular plant root hairs, angio- and gymnosperm pollen tubes, fungal hyphae and fern and algal rhizoids. While there currently exist certain technical and data limitations on such comparisons, they have the benefit of seeing beyond categories of ‘pollen specific’, ‘spore specific’, or even ‘Arabidopsis specific’ to look for ‘tip-growth specific’ genes, revealing common players of interest such as has been found with the Mago nashi or NPG1 genes.
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CONCLUSIONS AND IMPLICATIONS |
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TOPABSTRACTINTRODUCTIONCALCIUM IN POLARIZED GROWTHNITRIC OXIDE IN GROWTHGENE EXPRESSION PATTERNSCONCLUSIONS AND IMPLICATIONSACKNOWLEDGEMENTSLITERATURE CITED |
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Taken in sum, the calcium, annexin, NO and gene expression details all point towards a highly conserved process for tip growth. That various types of plants, and even separate kingdoms like fungi, all carry out this process in such a similar fashion implies that this process developed early on and is an evolutionarily ancient process. Considering the common requirements of these systems, this is not surprising. What is of note is the apparent complexity of the system established for this process. It is not just that there exist small GTPases, or that NO acts as a signalling molecule, or that calcium concentrations are important, but rather that all of these mechanisms interact together to affect the end result of localized tip growth. It appears that evolutionarily ancient organisms established a means of directed growth that was successful enough that diverse modern plant species still use it.
Biologists concern themselves with the ordinary and the extraodinary, by which is meant that phenomena of interest are typically the most common or the most unique. Modern genomic and proteomic methods are speeding up the rates at which new information can be discovered. As an example, Honys and Twell (2003, 2004) refer to their microarray studies in pollen in terms of fold increases and quantum increases in the data pool. Sifting through these data becomes a daunting task needing computers and classification schema. Cross-system and cross-species comparisons have great potential to uncover both the mundane and the extraordinary components of these vast amounts of data. In the case of tip growth, it is believed that further comparisons, either of the large- or of the more traditional small-scale variety, will fill in missing elements in the process (Fig. 3) giving a backbone mechanism of reference.
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Functionality has not been overlooked, however, for a root hair is not a rhizoid is not a pollen tube. Having the basic plan of tip-growth allows for examination of uniqueness to uncover how each cell type can respond to its own specific situations. Here again, the large- and small-scale comparisons become of value for seeing what is different. Already it is possible to separate out unique genes in pollen from that of the rest of the plant, yet still there is an overwhelming number of genes left to sift through, with even more found as genomics improve and more sequence information of other organisms becomes available. System comparison allows the focus to be narrowed from what is occurring in pollen or fern spores, to what is occurring only in pollen or fern spores. It is hoped that alternative model organisms will work with established systems to facilitate the progress of investigations in the modern era of genomics and proteomics.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONCALCIUM IN POLARIZED GROWTHNITRIC OXIDE IN GROWTHGENE EXPRESSION PATTERNSCONCLUSIONS AND IMPLICATIONSACKNOWLEDGEMENTSLITERATURE CITED |
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We thank the members of Dr Vishy Iyer's laboratory for their assistance in preparation and execution of the Ceratopteris EST microarrays reviewed here, and Dr Greg Clark's input to and proofreading of this manuscript. Authors' research reviewed here was supported by NASA grants NAG21586 and NAG10-295.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONCALCIUM IN POLARIZED GROWTHNITRIC OXIDE IN GROWTHGENE EXPRESSION PATTERNSCONCLUSIONS AND IMPLICATIONSACKNOWLEDGEMENTSLITERATURE CITED |
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