Special Issue "Pollen Tube Growth"

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A special issue of Plants (ISSN 2223-7747).

Deadline for manuscript submissions: closed (20 December 2012)

Special Issue Editor

Guest Editor
Prof. Dr. Giampiero Cai

Dipartimento Scienze della Vita, Università di Siena, Via Mattioli 4, 53100 Siena, Italy
Website | E-Mail
Fax: +39 0577 232860
Interests: pollen; pollen tube growth; cytoskeleton; microtubules; kinesin; motor proteins; organelle trafficking; tip-growth; cell wall-cytoskeleton interactions

Special Issue Information

Dear Colleagues,

Pollen and pollen tubes are known to be the vector by which male gametes are delivered to the egg cell for fertilization in higher plants. Consequently, they have a fundamental role in plant reproduction, ensuring gene transfer and propagation of seed plants. In angiosperms, pollen tubes grow within the style of receptive flowers, with which they exchange continuously signals and information that regulate (either negatively or positively) the growth rate of pollen tubes. Signaling between pollen tubes and female reproductive structures is extremely critical to promote and guide pollen tube growth but also to avoid inbreeding and outcrossing through the recognition and rejection of self- or incompatible pollen. Therefore, the pollen tube is a favorite model system for the study of cell-cell interaction and cell guidance in plants. Key genes and molecules involved in pollen tube guidance have been partially identified but a general view of how they orchestrate tube growth is still missing.
Growth of pollen tubes occurs essentially in a limited region, the tip, where a consistent number of secretory vesicles accumulate providing additional material for the cell wall and the plasma membrane. In this region, external signals are perceived, interpreted and used to regulate the growth rate. In recent years, identification of RAC/ROP GTPases, their recruitment to the cell membrane and activation in response to external signals are becoming progressively clear allowing to decipher the mechanism of signal perception, transduction and regulation of diverse cellular processes (such as growing within the female organs and delivering of sperms to the female gametophyte). An important component of the signal transduction mechanism are ion flux, intracellular ion gradients and dynamics, which are critical for the polarization of pollen tubes and for maintaining the growth site at the tube tip. Understanding how these features are generated and how they are related to the signal transduction pathway is an important challenge.
Signaling is interfaced to the dynamics of exocytosis and endocytosis, whose precise balance regulates pollen tube growth at the apex and whose perturbation causes significant changes in the tube morphology. Exo- and endocytosis regulates the assembly and deposition of the cell wall, which is important for pollen tube growth and, more generally, for the global morphogenesis of plants. A number of evidences describe the composition of the pollen tube cell wall, but little is known about the molecular mechanism controlling cell wall deposition. Nevertheless, we are progressively appreciating how callose and cellulose are synthetized, deposited, and designed to be load-bearing and resistant to tensile forces. Secretion, modification and dynamics of pectins are also progressively elucidating but a clear outlook of how the synthesis of cell wall polymers is interplayed is still missing as well as their relationship with the signal transduction pathway. Deposition of cell wall and accumulation of secretory vesicles are both dependent on the dynamics of the cytoskeleton, whose activity is regulated by both motor and non-motor proteins. The precise balance between polymerized and unpolymerized cytoskeletal filaments (coupled to the dynamic interplay between cytoskeleton and motor proteins) supports the continuous supply of secretory vesicles in the tip. Regulation of cytoskeleton activity is likely to be dependent on both signal transduction pathway and ion dynamics.
In view of this amazing interplay between different molecular processes (ranging from ion dynamics to membrane transport), the pollen tube is now considered as an excellent model in which to investigate  the problem of shape generation and the interaction between a mechanical problem and its biological control, which leads to the generation of complex growth processes. This issue is focused on research aimed at improving our current knowledge of the molecular mechanisms governing pollen tube growth, from the perception of extracellular signals to the cytoskeleton-based delivery of cell wall components to the integration of such mechanisms into a global process that determines the shape of the pollen tube, its growth and ultimately fertilization in plants.

Prof. Dr. Giampiero Cai
Guest Editor

Keywords

  • pollen tube growth
  • fertilization in higher plants
  • signal transduction
  • intracellular ion gradients
  • exocytosis and endocytosis
  • cell wall synthesis
  • cytoskeleton dynamics
  • system tip growth model

Published Papers (9 papers)

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Research

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Open AccessArticle The Progamic Phase in High-Mountain Plants: From Pollination to Fertilization in the Cold
Plants 2013, 2(3), 354-370; doi:10.3390/plants2030354
Received: 12 April 2013 / Revised: 24 May 2013 / Accepted: 26 May 2013 / Published: 25 June 2013
Cited by 1 | PDF Full-text (201 KB) | HTML Full-text | XML Full-text
Abstract
In high-mountains, cold spells can occur at any time during the growing season and plants may be covered with snow for several days. This raises the question to what extent sexual processes are impaired by low temperatures. We tested pollen performance and fertilization
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In high-mountains, cold spells can occur at any time during the growing season and plants may be covered with snow for several days. This raises the question to what extent sexual processes are impaired by low temperatures. We tested pollen performance and fertilization capacity of high-mountain species with different elevational distribution in the European Alps (Cerastium uniflorum, Gentianella germanica, Ranunculus glacialis, R. alpestris, Saxifraga bryoides, S. caesia, S. moschata) during simulated cold snaps in the laboratory. Plants were exposed to 0 °C (the temperature below the snow) for 12, 36, 60 and 84 h. In S. caesia, the experiment was verified in situ during a cold snap. Sexual processes coped well with large temperature differences and remained functional at near-freezing temperatures for a few days. During the cooling-down phase a high percentage (67–97%) of pollen grains germinated and grew tubes into the style. At zero degrees, tube growth continued slowly both in the laboratory and in situ below the snow. Fertilization occurred in up to 100% of flowers in the nival species and in G. germanica, but was strongly delayed or absent in the alpine species. During rewarming, fertilization continued. Overall, progamic processes in high-mountain plants appear fairly robust toward weather extremes increasing the probability of successful reproduction. Full article
(This article belongs to the Special Issue Pollen Tube Growth)
Open AccessArticle Growth Media Induces Variation in Cell Wall Associated Gene Expression in Arabidopsis thaliana Pollen Tube
Plants 2013, 2(3), 429-440; doi:10.3390/plants2030429
Received: 28 March 2013 / Revised: 3 June 2013 / Accepted: 18 June 2013 / Published: 25 June 2013
Cited by 2 | PDF Full-text (704 KB) | HTML Full-text | XML Full-text | Supplementary Files
Abstract
The influence of three different pollen germination media on the transcript profile of Arabidopsis pollen tubes has been assessed by real-time PCR on a selection of cell wall related genes, and by a statistical analysis of microarray Arabidopsis pollen tube data sets. The
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The influence of three different pollen germination media on the transcript profile of Arabidopsis pollen tubes has been assessed by real-time PCR on a selection of cell wall related genes, and by a statistical analysis of microarray Arabidopsis pollen tube data sets. The qPCR assays have shown remarkable differences on the transcript levels of specific genes depending upon the formulation of the germination medium used. With the aid of principal component analysis performed on existing microarray data, a subset of genes has been identified that is more prone to produce diverging transcript levels. A functional classification of those genes showed that the clusters with higher number of members were those for hydrolase activity (based in molecular function) and for cell wall (based in cellular component). Taken together, these results may indicate that the nutrient composition of the pollen germination media influences pollen tube metabolism and that caution must be taken when interpreting transcriptomic data of pollen tubes. Full article
(This article belongs to the Special Issue Pollen Tube Growth)
Open AccessArticle Pollen Performance in Clarkia Taxa with Contrasting Mating Systems: Implications for Male Gametophytic Evolution in Selfers and Outcrossers
Plants 2013, 2(2), 248-278; doi:10.3390/plants2020248
Received: 15 February 2013 / Revised: 13 March 2013 / Accepted: 3 April 2013 / Published: 24 April 2013
Cited by 3 | PDF Full-text (1191 KB) | HTML Full-text | XML Full-text
Abstract
We tested three predictions regarding the joint evolution of pollen performance and mating system. First, due to the potential for intense intrasexual competition in outcrossing populations, we predicted that outcrossers would produce faster-growing pollen than their selfing relatives. Second, if elevated competition promotes
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We tested three predictions regarding the joint evolution of pollen performance and mating system. First, due to the potential for intense intrasexual competition in outcrossing populations, we predicted that outcrossers would produce faster-growing pollen than their selfing relatives. Second, if elevated competition promotes stronger selection on traits that improve pollen performance, then, among-plant variation in pollen performance would be lower in outcrossers than in selfers. Third, given successive generations of adaptation to the same maternal genotype in selfers, we predicted that, in selfing populations (but not in outcrossing ones), pollen would perform better following self- than cross-pollinations. We tested these predictions in field populations of two pairs of Clarkia (Onagraceae) sister taxa. Consistent with our predictions, one outcrosser (C. unguiculata) exhibited faster pollen germination and less variation in pollen tube growth rate (PTGR) among pollen donors than its selfing sister species, C. exilis. Contrary to our predictions, the selfing C. xantiana ssp. parviflora exhibited faster PTGR than the outcrossing ssp. xantiana, and these taxa showed similar levels of variation in this trait. Pollen performance following self- vs. cross-pollinations did not differ within either selfing or outcrossing taxa. While these findings suggest that mating system and pollen performance may jointly evolve in Clarkia, other factors clearly contribute to pollen performance in natural populations. Full article
(This article belongs to the Special Issue Pollen Tube Growth)
Open AccessArticle PiSCP1 and PiCDPK2 Localize to Peroxisomes and Are Involved in Pollen Tube Growth in Petunia Inflata
Plants 2013, 2(1), 72-86; doi:10.3390/plants2010072
Received: 6 January 2013 / Revised: 19 February 2013 / Accepted: 26 February 2013 / Published: 4 March 2013
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Abstract
Petunia inflata small CDPK-interacting protein 1 (PiSCP1) was identified as a pollen expressed PiCDPK1 interacting protein using the yeast two hybrid system and the interaction confirmed using pull-down and phosphorylation assays. PiSCP1 is pollen specific and shares amino acid homology with uncharacterized proteins
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Petunia inflata small CDPK-interacting protein 1 (PiSCP1) was identified as a pollen expressed PiCDPK1 interacting protein using the yeast two hybrid system and the interaction confirmed using pull-down and phosphorylation assays. PiSCP1 is pollen specific and shares amino acid homology with uncharacterized proteins from diverse species of higher plants, but no protein of known function. Expression of PiSCP1-GFP in vivo inhibited pollen tube growth and was shown to localize to peroxisomes in growing pollen tubes. As PiCDPK1 is plasma membrane localized, we investigated the localization of a second isoform, PiCDPK2, and show that it co-localizes to peroxisomes with PiSCP1 and that the two proteins interact in the yeast 2 hybrid interaction assay, suggesting that interaction with the latter CDPK isoform is likely the one of biological relevance. Both PiCDPK2 and PiSCP1 affect pollen tube growth, presumably by mediating peroxisome function, however how they do so is currently not clear. Full article
(This article belongs to the Special Issue Pollen Tube Growth)
Open AccessArticle Pollen Tube Growth and Self-Compatibility in Almond
Plants 2013, 2(1), 50-56; doi:10.3390/plants2010050
Received: 5 December 2012 / Revised: 2 January 2013 / Accepted: 28 January 2013 / Published: 4 February 2013
Cited by 2 | PDF Full-text (300 KB) | HTML Full-text | XML Full-text
Abstract
Although pollen tube growth has been an important criterion for self-compatibility evaluation in almond, there is not a clear-cut separation between positive and negative growth of pollen tubes in the different genotypes. The examination of pollen tube growth after selfing almond seedlings has
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Although pollen tube growth has been an important criterion for self-compatibility evaluation in almond, there is not a clear-cut separation between positive and negative growth of pollen tubes in the different genotypes. The examination of pollen tube growth after selfing almond seedlings has allowed establishing different levels of compatibility, but not a clear-cut separation between self-compatible (SC) and self-incompatible (SI) genotypes, related to the presence of pseudo-self-compatibility in almond. Consequently, a relationship between pollen tube growth and self-compatibility in almond may be established for evaluating the seedlings in breeding programs. Full article
(This article belongs to the Special Issue Pollen Tube Growth)

Review

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Open AccessReview Endocytic Pathways and Recycling in Growing Pollen Tubes
Plants 2013, 2(2), 211-229; doi:10.3390/plants2020211
Received: 15 February 2013 / Revised: 21 March 2013 / Accepted: 26 March 2013 / Published: 3 April 2013
Cited by 13 | PDF Full-text (784 KB) | HTML Full-text | XML Full-text
Abstract
Pollen tube growth is based on transport of secretory vesicles into the apical region where they fuse with a small area of the plasma membrane. The amount of secretion greatly exceeds the quantity of membrane required for growth. Mechanisms of membrane retrieval have
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Pollen tube growth is based on transport of secretory vesicles into the apical region where they fuse with a small area of the plasma membrane. The amount of secretion greatly exceeds the quantity of membrane required for growth. Mechanisms of membrane retrieval have recently been demonstrated and partially characterized using FM (Fei Mao) dyes or charged nanogold. Both these probes reveal that clathrin-dependent and -independent endocytosis occur in pollen tubes and are involved in distinct degradation pathways and membrane recycling. Exocytosis, internalization and sorting of PM proteins/lipids depend on the integrity of the actin cytoskeleton and are involved in actin filament organization. However, some kinds of endocytic and exocytic processes occurring in the central area of the tip still need to be characterized. Analysis of secretion dynamics and data derived from endocytosis highlight the complexity of events occurring in the tip region and suggest a new model of pollen tube growth. Full article
(This article belongs to the Special Issue Pollen Tube Growth)
Open AccessReview Polar Expansion Dynamics in the Plant Kingdom: A Diverse and Multifunctional Journey on the Path to Pollen Tubes
Plants 2013, 2(1), 148-173; doi:10.3390/plants2010148
Received: 28 December 2012 / Revised: 24 February 2013 / Accepted: 1 March 2013 / Published: 18 March 2013
Cited by 6 | PDF Full-text (660 KB) | HTML Full-text | XML Full-text
Abstract
Polar expansion is a widespread phenomenon in plants spanning all taxonomic groups from the Charophycean Green Algae to pollen tubes in Angiosperms and Gymnosperms. Current data strongly suggests that many common features are shared amongst cells displaying polar growth mechanics including changes to
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Polar expansion is a widespread phenomenon in plants spanning all taxonomic groups from the Charophycean Green Algae to pollen tubes in Angiosperms and Gymnosperms. Current data strongly suggests that many common features are shared amongst cells displaying polar growth mechanics including changes to the structural features of localized regions of the cell wall, mobilization of targeted secretion mechanisms, employment of the actin cytoskeleton for directing secretion and in many cases, endocytosis and coordinated interaction of multiple signal transduction mechanisms prompted by external biotic and abiotic cues. The products of polar expansion perform diverse functions including delivery of male gametes to the egg, absorption, anchorage, adhesion and photo-absorption efficacy. A comparative analysis of polar expansion dynamics is provided with special emphasis on those found in early divergent plants. Full article
(This article belongs to the Special Issue Pollen Tube Growth)
Figures

Open AccessReview Cell Wall Composition, Biosynthesis and Remodeling during Pollen Tube Growth
Plants 2013, 2(1), 107-147; doi:10.3390/plants2010107
Received: 13 December 2012 / Revised: 19 February 2013 / Accepted: 19 February 2013 / Published: 7 March 2013
Cited by 14 | PDF Full-text (1483 KB) | HTML Full-text | XML Full-text
Abstract
The pollen tube is a fast tip-growing cell carrying the two sperm cells to the ovule allowing the double fertilization process and seed setting. To succeed in this process, the spatial and temporal controls of pollen tube growth within the female organ are
[...] Read more.
The pollen tube is a fast tip-growing cell carrying the two sperm cells to the ovule allowing the double fertilization process and seed setting. To succeed in this process, the spatial and temporal controls of pollen tube growth within the female organ are critical. It requires a massive cell wall deposition to promote fast pollen tube elongation and a tight control of the cell wall remodeling to modify the mechanical properties. In addition, during its journey, the pollen tube interacts with the pistil, which plays key roles in pollen tube nutrition, guidance and in the rejection of the self-incompatible pollen. This review focuses on our current knowledge in the biochemistry and localization of the main cell wall polymers including pectin, hemicellulose, cellulose and callose from several pollen tube species. Moreover, based on transcriptomic data and functional genomic studies, the possible enzymes involved in the cell wall remodeling during pollen tube growth and their impact on the cell wall mechanics are also described. Finally, mutant analyses have permitted to gain insight in the function of several genes involved in the pollen tube cell wall biosynthesis and their roles in pollen tube growth are further discussed. Full article
(This article belongs to the Special Issue Pollen Tube Growth)
Figures

Open AccessReview Regulation of Pollen Tube Growth by Transglutaminase
Plants 2013, 2(1), 87-106; doi:10.3390/plants2010087
Received: 5 January 2013 / Revised: 8 February 2013 / Accepted: 27 February 2013 / Published: 6 March 2013
PDF Full-text (621 KB) | HTML Full-text | XML Full-text
Abstract
In pollen tubes, cytoskeleton proteins are involved in many aspects of pollen germination and growth, from the transport of sperm cells to the asymmetrical distribution of organelles to the deposition of cell wall material. These activities are based on the dynamics of the
[...] Read more.
In pollen tubes, cytoskeleton proteins are involved in many aspects of pollen germination and growth, from the transport of sperm cells to the asymmetrical distribution of organelles to the deposition of cell wall material. These activities are based on the dynamics of the cytoskeleton. Changes to both actin filaments and microtubules are triggered by specific proteins, resulting in different organization levels suitable for the different functions of the cytoskeleton. Transglutaminases are enzymes ubiquitous in all plant organs and cell compartments. They catalyze the post-translational conjugation of polyamines to different protein targets, such as the cytoskeleton. Transglutaminases are suggested to have a general role in the interaction between pollen tubes and the extracellular matrix during fertilization and a specific role during the self-incompatibility response. In such processes, the activity of transglutaminases is enhanced, leading to the formation of cross-linked products (including aggregates of tubulin and actin). Consequently, transglutaminases are suggested to act as regulators of cytoskeleton dynamics. The distribution of transglutaminases in pollen tubes is affected by both membrane dynamics and the cytoskeleton. Transglutaminases are also secreted in the extracellular matrix, where they may take part in the assembly and/or strengthening of the pollen tube cell wall. Full article
(This article belongs to the Special Issue Pollen Tube Growth)

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