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Tetsuya Higashiyama - One of the best experts on this subject based on the ideXlab platform.
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Pollen Tube Guidance by Attractant Molecules: LUREs
Cell Structure and Function, 2020Co-Authors: Satohiro Okuda, Tetsuya HigashiyamaAbstract:Sexual reproduction in flowering plants requires Pollen-Tube guidance, which is thought to be mediated by chemoattractants derived from target ovules. To date, however, no convincing evidence has been reported of a particular molecule being the true attractant. Emerging data indicate that two synergid cells, which are on either side of the egg cell, emit a diffusible, species-specific signal to attract the Pollen Tube at the last step of Pollen-Tube guidance. Recently, it was demonstrated that LUREs (LURE1 and LURE2), cysteine-rich polypeptides secreted from the synergid cell, are the key molecules in Pollen-Tube guidance. In this review, we summarize the mechanism of Pollen-Tube guidance, with special focus on gametophytic guidance and the attractants.
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Chemical signaling for Pollen Tube guidance at a glance.
Journal of Cell Science, 2018Co-Authors: Yoko Mizuta, Tetsuya HigashiyamaAbstract:ABSTRACT Pollen Tube guidance is a unique navigating system that is required for the successful sexual reproduction of plants. As plant sperm cells are non-motile and egg cells are embedded deep inside the female tissues, a Pollen Tube delivers the two sperm cells that it contains by growing towards the ovule, in which the egg cell resides. Pollen Tube growth towards the ovule is precisely controlled and divided into two stages, preovular and ovular guidance. In this Cell Science at a Glance article and accompanying poster, we provide a comprehensive overview of Pollen Tube guidance and highlight some of the attractant peptides used during ovular guidance. We further discuss the precise one-to-one guidance system that exists in multi-ovular plants. The Pollen Tube-blocking system, which is mediated by male–female crosstalk communication, to avoid attraction of multiple Pollen Tubes, is also reviewed.
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structural basis for receptor recognition of Pollen Tube attraction peptides
Nature Communications, 2017Co-Authors: Xiaoxiao Zhang, Hidenori Takeuchi, Tetsuya Higashiyama, Takuya Nagae, Heqiao Zhang, Jijie ChaiAbstract:Transportation of the immobile sperms directed by Pollen Tubes to the ovule-enclosed female gametophytes is important for plant sexual reproduction. The defensin-like (DEFL) cysteine-rich peptides (CRPs) LUREs play an essential role in Pollen Tube attraction to the ovule, though their receptors still remain controversial. Here we provide several lines of biochemical evidence showing that the extracellular domain of the leucine-rich repeat receptor kinase (LRR-RK) PRK6 from Arabidopsis thaliana directly interacts with AtLURE1 peptides. Structural study reveals that a C-terminal loop of the LRR domain (AtPRK6LRR) is responsible for recognition of AtLURE1.2, mediated by a set of residues largely conserved among PRK6 homologs from Arabidopsis lyrata and Capsella rubella, supported by in vitro mutagenesis and semi-in-vivo Pollen Tube growth assays. Our study provides evidence showing that PRK6 functions as a receptor of the LURE peptides in A. thaliana and reveals a unique ligand recognition mechanism of LRR-RKs. The cysteine-rich peptides LUREs play an essential role in Pollen Tube attraction to the ovule for plant sexual reproduction. Here Zhang et al. show that PRK6 functions as a receptor of the LUREs in Arabidopsis thaliana and reveal the ligand recognition mechanism.
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gametophytic Pollen Tube guidance attractant peptides gametic controls and receptors
Plant Physiology, 2017Co-Authors: Tetsuya Higashiyama, Weicai YangAbstract:Pollen Tube guidance in flowering plants is a unique and critical process for successful sexual reproduction. The Pollen Tube that grows from Pollen, which is the male gametophyte, precisely navigates to the embryo sac, which is the female gametophyte, within the pistil. Recent advances have clarified the molecular framework of gametophytic Pollen Tube guidance. Multiple species-specific attractant peptides are secreted from synergid cells, the proper development and function of which are regulated by female gametes. Multiple receptor-like kinases on the Pollen Tube tip are involved in sensing species-specific attractant peptides. In this Update article, recent progress in our understanding of the mechanism of gametophytic Pollen Tube guidance is reviewed, including attraction by synergid cells, control of Pollen Tube guidance by female gametes, and directional growth of the Pollen Tube by directional cue sensing. Future directions in the study of Pollen Tube guidance also are discussed.
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tip localized receptors control Pollen Tube growth and lure sensing in arabidopsis
Nature, 2016Co-Authors: Hidenori Takeuchi, Tetsuya HigashiyamaAbstract:Pollen-specific receptor-like kinase 6 (PRK6), which signals through the guanine nucleotide-exchange factors ROPGEFs, is required for sensing of the LURE1 attractant peptide in Arabidopsis thaliana, and functions together with other PRK family kinases; when introduced into the Pollen Tubes of the related species Capsella rubella, PRK6 could confer responsiveness to AtLURE1. In flowering plants, the female gametophyte secretes chemoattractant peptides to guide Pollen Tube growth so that it delivers the immobile sperm to the ovule-enclosed female gametophyte. Two papers published in this issue of Nature report the identification of male Pollen Tube cell-surface receptors for one of these female attractants, LURE1, in the model plant Arabidopsis thaliana. Wei-Cai Yang and colleagues show that LURE1 is perceived by a receptor-like kinase complex, the heteromer MDIS1–MIK. Tetsuya Higashiyama and Hidenori Takeuchi report that Pollen-specific receptor-like kinase 6 (PRK6) is required for sensing LURE1, and PRK6 acts together with other PRK family receptors. Both groups demonstrate that by engineering Pollen Tubes of the sister species Capsella rubella to express a component of the A. thaliana receptors — either MDIS1 or PRK6 — the reproductive isolation barrier between the two species is partially broken down. Directional control of tip-growing cells is essential for proper tissue organization and cell-to-cell communication in animals and plants1,2. In the sexual reproduction of flowering plants, the tip growth of the male gametophyte, the Pollen Tube, is precisely guided by female cues to achieve fertilization3. Several female-secreted peptides have recently been identified as species-specific attractants that directly control the direction of Pollen Tube growth4,5,6. However, the method by which Pollen Tubes precisely and promptly respond to the guidance signal from their own species is unknown. Here we show that tip-localized Pollen-specific receptor-like kinase 6 (PRK6) with an extracellular leucine-rich repeat domain is an essential receptor for sensing of the LURE1 attractant peptide in Arabidopsis thaliana under semi-in-vivo conditions, and is important for ovule targeting in the pistil. PRK6 interacted with Pollen-expressed ROPGEFs (Rho of plant guanine nucleotide-exchange factors), which are important for Pollen Tube growth through activation of the signalling switch Rho GTPase ROP1 (refs 7, 8). PRK6 conferred responsiveness to AtLURE1 in Pollen Tubes of the related species Capsella rubella. Furthermore, our genetic and physiological data suggest that PRK6 signalling through ROPGEFs and sensing of AtLURE1 are achieved in cooperation with the other PRK family receptors, PRK1, PRK3 and PRK8. Notably, the tip-focused PRK6 accumulated asymmetrically towards an external AtLURE1 source before reorientation of Pollen Tube tip growth. These results demonstrate that PRK6 acts as a key membrane receptor for external AtLURE1 attractants, and recruits the core tip-growth machinery, including ROP signalling proteins. This work provides insights into the orchestration of efficient Pollen Tube growth and species-specific Pollen Tube attraction by multiple receptors during male–female communication.
Ravishankar Palanivelu - One of the best experts on this subject based on the ideXlab platform.
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the role of lorelei in Pollen Tube reception at the interface of the synergid cell and Pollen Tube requires the modified eight cysteine motif and the receptor like kinase feronia
The Plant Cell, 2016Co-Authors: Claudia Alejandra Castro, Yanbing Wang, Jennifer Ashley Noble, Nathaniel Donaldson Ponvert, Mark G R Bundy, Chelsea Rae Hoel, Elena D Shpak, Ravishankar PalaniveluAbstract:In angiosperms, Pollen Tube reception by the female gametophyte is required for sperm release and double fertilization. In Arabidopsis thaliana lorelei (lre) mutants, Pollen Tube reception fails in most female gametophytes, which thus remain unfertilized. LRE encodes a putative glycosylphosphatidylinositol (GPI)-anchored surface protein with a modified eight-cysteine motif (M8CM). LRE fused to citrine yellow fluorescent protein (LRE-cYFP) remains functional and localizes to the synergid plasma membrane-rich filiform apparatus, the first point of contact between the Pollen Tube and the female gametophyte. Structure-function analysis using LRE-cYFP showed that the role of LRE in Pollen Tube reception requires the M8CM, but not the domains required for GPI anchor addition. Consistently, LRE-cYFP-TM, where GPI anchor addition domains were replaced with a single-pass transmembrane domain, fully complemented the Pollen Tube reception defect in lre-7 female gametophytes. Ectopically expressed and delivered LRE-cYFP from Pollen Tubes could non-cell-autonomously complement the Pollen Tube reception defect in lre female gametophytes, only if they expressed FERONIA. Additionally, Pollen Tube-expressing LRE variants lacking domains critical for GPI anchor addition also rescued lre female gametophyte function. Therefore, LRE and FERONIA jointly function in Pollen Tube reception at the interface of the synergid cell and Pollen Tube.
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Pollen Tube discharge completes the process of synergid degeneration that is initiated by Pollen Tube - synergid interaction in Arabidopsis
Plant Physiology, 2015Co-Authors: Alexander R. Leydon, Mark A Johnson, Tatsuya Tsukamoto, Damayanthi Dunatunga, Ravishankar PalaniveluAbstract:In flowering plant reproduction, Pollen Tube reception is the signaling system that results in Pollen Tube discharge, synergid degeneration, and successful delivery of male gametes (two sperm cells) to the site where they can fuse with female gametes (egg cell and central cell). Some molecules required for this complex and essential signaling exchange have been identified; however, fundamental questions about the nature of the interactions between the Pollen Tube and the synergid cells remain to be clarified. Here, we monitor Pollen Tube arrival, Pollen Tube discharge, and synergid degeneration in Arabidopsis (Arabidopsis thaliana) wild type and in male and female gametophytic mutants that disrupt development and function of the gametophytes. By combining assays used previously to study these interactions and an assay that facilitates simultaneous analysis of Pollen Tube discharge and synergid degeneration, we find that synergid degeneration could be initiated without Pollen Tube discharge. Our data support the hypothesis that Pollen Tube-synergid contact, or signaling via secreted molecules, initiates receptive synergid degeneration. We also find that when Pollen Tubes successfully burst, they always discharge into a degenerated synergid. In addition to this Pollen Tube-dependent promotion of synergid degeneration, we also show that a basal developmental pathway mediates synergid degeneration in the absence of pollination. Our results are consistent with the model that a complex set of interactions between the Pollen Tube and synergid cells promote receptive synergid degeneration.
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three myb transcription factors control Pollen Tube differentiation required for sperm release
Current Biology, 2013Co-Authors: Alexander R. Leydon, Ravishankar Palanivelu, Kristin M Beale, Karolina Woroniecka, Elizabeth Castner, Jefferson Chen, Casie Horgan, Mark A JohnsonAbstract:Summary In flowering plants, immotile sperm cells develop within the Pollen grain and are delivered to female gametes by a Pollen Tube [1, 2]. Upon arrival at the female gametophyte, the Pollen Tube stops growing and releases sperm cells for successful fertilization [3]. Several female signaling components essential for Pollen Tube reception have been identified [4–11]); however, male components remain unknown. We show that the expression of three closely related MYB transcription factors is induced in Pollen Tubes by growth in the pistil. Pollen Tubes lacking these three transcriptional regulators fail to stop growing in synergids, specialized cells flanking the egg cell that attract Pollen Tubes [12–16] and degenerate upon Pollen Tube arrival [17, 18]. myb triple-mutant Pollen Tubes also fail to release their sperm cargo. We define a suite of Pollen Tube-expressed genes regulated by these critical MYBs and identify transporters, carbohydrate-active enzymes, and small peptides as candidate molecular mediators of Pollen Tube-female interactions necessary for flowering plant reproduction. Our data indicate that de novo transcription in the Pollen Tube nucleus during growth in the pistil leads to Pollen Tube differentiation required for release of sperm cells.
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pathfinding in angiosperm reproduction Pollen Tube guidance by pistils ensures successful double fertilization
Wiley Interdisciplinary Reviews-Developmental Biology, 2012Co-Authors: Ravishankar Palanivelu, Tatsuya TsukamotoAbstract:Sexual reproduction in flowering plants is unique in multiple ways. Distinct multicellulargametophytescontaineitherapairofimmotile,haploidmalegametes (sperm cells) or a pair of female gametes (haploid egg cell and homodiploid central cell). After pollination, the Pollen Tube, a cellular extension of the male gametophyte, transports both male gametes at its growing tip and delivers them to the female gametes to affect double fertilization. The Pollen Tube travels a long path and sustains its growth over a considerable amount of time in the female reproductive organ (pistil) before it reaches the ovule, which houses the female gametophyte. The pistil facilitates the Pollen Tube’s journey by providing multiple, stage-specific, nutritional, and guidance cues along its path. The Pollen Tube interacts with seven different pistil cell types prior to completing its journey. Consequently, the Pollen Tube has a dynamic gene expression program allowing it to continuously reset and be receptive to multiple pistil signals as it migrates through the pistil. Here, we review the studies, including several significant recent advances, that led to a better understanding of the multitude of cues generated by the pistil tissues to assist the Pollen Tube in delivering the sperm cells to the female gametophyte. We also highlight the outstanding questions, draw attention to opportunities created by recent advances and point to approaches that could be undertaken to unravel the molecular mechanisms underlying Pollen Tube‐pistil
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a microsystem based assay for studying Pollen Tube guidance in plant reproduction
Journal of Micromechanics and Microengineering, 2011Co-Authors: Ali K Yetisen, Ravishankar Palanivelu, Linan Jiang, J R Cooper, Yitshak ZoharAbstract:We present a novel microsystem-based assay to assess and quantify Pollen Tube behavior in response to pistil tissues. During plant reproduction, signals from female tissues (pistils) guide the sperm-carrying Pollen Tube to the egg cell to achieve fertilization and initiate seed development. Existing Pollen Tube guidance bioassays are performed in an isotropically diffusive environment (for example, a semi in vivo assay in petri dishes) instead of anisotropically diffusive conditions required to characterize guidance signal gradients. Lack of a sensitive Pollen Tube guidance bioassay has therefore compounded the difficulties of identifying and characterizing the guidance signals that are likely produced in minute quantities by the ovules. We therefore developed a novel microsystem-based assay that mimics the in vivo micro-environment of ovule fertilization by Pollen Tubes in the model research plant Arabidopsis thaliana. In this microdevice, the Pollen Tube growth rate, length and ovule targeting frequencies were similar to those obtained using a semi in vivo plate assay. As a direct measure of the microdevice's utility in monitoring Pollen Tube guidance, we demonstrated that in this device, Pollen Tubes preferentially enter chambers with unfertilized ovules, suggesting that the Pollen Tubes sense the concentration gradient and respond to the chemoattractants secreted by unfertilized ovules.
Ueli Grossniklaus - One of the best experts on this subject based on the ideXlab platform.
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cytoplasmic ca2 changes dynamically during the interaction of the Pollen Tube with synergid cells
Development, 2012Co-Authors: Megumi Iwano, Ueli Grossniklaus, Tetsuyuki Entani, Hiroshi Shiba, Takeharu Nagai, Atsushi Miyawaki, Akira Isogai, Seiji TakayamaAbstract:The directional growth of the Pollen Tube from the stigma to the embryo sac in the ovules is regulated by Pollen-pistil interactions based on intercellular communication. Although Pollen Tube growth is regulated by the cytoplasmic Ca2+ concentration ([Ca2+]cyt), it is not known whether [Ca2+]cyt is involved in Pollen Tube guidance and reception. Using Arabidopsis expressing the GFP-based Ca2+-sensor yellow cameleon 3.60 (YC3.60) in Pollen Tubes and synergid cells, we monitored Ca2+ dynamics in these cells during Pollen Tube guidance and reception under semi-in vivo fertilization conditions. In the Pollen Tube growing towards the micropyle, Pollen Tubes initiated turning within 150 μm of the micropylar opening; the [Ca2+]cyt in these Pollen Tube tips was higher than in those not growing towards an ovule in assays with myb98 mutant ovules, in which Pollen Tube guidance is disrupted. These results suggest that attractants secreted from the ovules affect Ca2+ dynamics in the Pollen Tube. [Ca2+]cyt in synergid cells did not change when the Pollen Tube grew towards the micropyle or entered the ovule. Upon Pollen Tube arrival at the synergid cell, however, [Ca2+]cyt oscillation began at the micropylar pole of the synergid, spreading towards the chalazal pole. Finally, [Ca2+]cyt in the synergid cell reached a maximum at Pollen Tube rupture. These results suggest that signals from the Pollen Tube induce Ca2+ oscillations in synergid cells, and that this Ca2+ oscillation is involved in the interaction between the Pollen Tube and synergid cell.
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she s the boss signaling in Pollen Tube reception
Current Opinion in Plant Biology, 2011Co-Authors: Sharon A Kessler, Ueli GrossniklausAbstract:In angiosperms, the sperm cells are carried within the Pollen Tubes (male gametophytes) to the female gametophyte so that double fertilization can occur. The female gametophyte exerts control over the male, with specialized cells known as synergids guiding the Pollen Tubes and controlling their behavior when they enter the female gametophyte so that the sperm cells can be delivered to the egg and central cell. Upon Pollen Tube arrival at the ovule, signal transduction cascades mediated by receptor-like kinases are initiated in both the synergid and the tip of the Pollen Tube, leading to synergid cell death and Pollen Tube rupture. In this review, we discuss the role of these receptors and of newly discovered members of the Pollen Tube reception pathway.
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disruption of the Pollen expressed feronia homologs anxur1 and anxur2 triggers Pollen Tube discharge
Development, 2009Co-Authors: Aurelien Boissondernier, Konstantinos Kritsas, Monica A Grobei, Miloslawa Jaciubek, Julian I Schroeder, Ueli GrossniklausAbstract:The precise delivery of male to female gametes during reproduction in eukaryotes requires complex signal exchanges and a flawless communication between male and female tissues. In angiosperms, molecular mechanisms have recently been revealed that are crucial for the dialog between male (Pollen Tube) and female gametophytes required for successful sperm delivery. When Pollen Tubes reach the female gametophyte, they arrest growth, burst and discharge their sperm cells. These processes are under the control of the female gametophyte via the receptor-like serine-threonine kinase (RLK) FERONIA (FER). However, the male signaling components that control the sperm delivery remain elusive. Here, we show that ANXUR1 and ANXUR2 (ANX1, ANX2), which encode the closest homologs of the FER-RLK in Arabidopsis, are preferentially expressed in Pollen. Moreover, ANX1-YFP and ANX2-YFP fusion proteins display polar localization to the plasma membrane at the tip of the Pollen Tube. Finally, genetic analyses demonstrate that ANX1 and ANX2 function redundantly to control the timing of Pollen Tube discharge as anx1 anx2 double-mutant Pollen Tubes cease their growth and burst in vitro and fail to reach the female gametophytes in vivo. We propose that ANX-RLKs constitutively inhibit Pollen Tube rupture and sperm discharge at the tip of growing Pollen Tubes to sustain their growth within maternal tissues until they reach the female gametophytes. Upon arrival, the female FER-dependent signaling cascade is activated to mediate Pollen Tube reception and fertilization, while male ANX-dependent signaling is deactivated, enabling the Pollen Tube to rupture and deliver its sperm cells to effect fertilization.
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the central cell plays a critical role in Pollen Tube guidance in arabidopsis
The Plant Cell, 2007Co-Authors: Yanhong Chen, Ueli Grossniklaus, Hongju Li, Li Yuan, Rajini Sreenivasan, Ramarmurthy Baskar, Weicai YangAbstract:The sperm cell of flowering plants cannot migrate unaided and must be transported by the Pollen Tube cell of the male gametophyte to achieve successful fertilization. Long-distance Pollen Tube guidance is controlled by the seven-celled female gametophyte, the embryo sac. Previous reports showed that the synergid cell of the embryo sac is essential for Pollen Tube guidance. Here, we report the identification of a central cell guidance (ccg) mutant, which is defective in micropylar Pollen Tube guidance. CCG encodes a nuclear protein with an N-terminal conserved zinc β-ribbon domain that is functionally interchangeable with that of TFIIB in yeast. This suggests that CCG might act as a transcription regulator for Pollen Tube guidance. CCG is expressed in the central cell of the female gametophyte. Expression of CCG in the central cell alone is sufficient to restore the normal Pollen Tube guidance phenotype, demonstrating that the central cell plays a critical role in Pollen Tube guidance.
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the feronia receptor like kinase mediates male female interactions during Pollen Tube reception
Science, 2007Co-Authors: Juanmiguel Escobarrestrepo, Weicai Yang, Sharon A Kessler, Norbert Huck, Valeria Gagliardini, Jacqueline Gheyselinck, Ueli GrossniklausAbstract:In flowering plants, signaling between the male Pollen Tube and the synergid cells of the female gametophyte is required for fertilization. In the Arabidopsis thaliana mutant feronia ( fer ), fertilization is impaired; the Pollen Tube fails to arrest and thus continues to grow inside the female gametophyte. FER encodes a synergid-expressed, plasma membrane–localized receptor-like kinase. We found that the FER protein accumulates asymmetrically in the synergid membrane at the filiform apparatus. Interspecific crosses using Pollen from Arabidopsis lyrata and Cardamine flexuosa on A. thaliana stigmas resulted in a fer -like phenotype that correlates with sequence divergence in the extracellular domain of FER. Our findings show that the female control of Pollen Tube reception is based on a FER -dependent signaling pathway, which may play a role in reproductive isolation barriers.
Tsuneyoshi Kuroiwa - One of the best experts on this subject based on the ideXlab platform.
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Pollen Tube guidance beacons from the female gametophyte
Current Opinion in Plant Biology, 2003Co-Authors: Tetsuya Higashiyama, Haruko Kuroiwa, Tsuneyoshi KuroiwaAbstract:The sperm cell of a flowering plant cannot migrate unaided and it must be transported by the Pollen-Tube cell before successful fertilization can occur. The Pollen Tube is precisely guided to the target female gametophyte, the embryo sac, which contains the egg cell. The mechanism that precisely directs the Pollen Tube through the pistil to the female gametophyte has been studied for more than a century. There has been controversy over whether a diffusible signal attracts the Pollen Tube or whether female tissues define its path. Emerging genetic and physiological data show that the female gametophyte produces at least two directional signals, and that at least one of these signals is diffusible and derived from the two synergid cells.
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Pollen Tube attraction by the synergid cell
Science, 2001Co-Authors: Tetsuya Higashiyama, Narie Sasaki, Haruko Kuroiwa, Shizu Yabe, Yoshiki Nishimura, Shinya Miyagishima, Tsuneyoshi KuroiwaAbstract:In flowering plants, guidance of the Pollen Tube to the embryo sac (the haploid female gametophyte) is critical for successful fertilization. The target embryo sac may attract the Pollen Tube as the final step of guidance in the pistil. We show by laser cell ablation that two synergid cells adjacent to the egg cell attract the Pollen Tube. A single synergid cell was sufficient to generate an attraction signal, and two cells enhanced it. After fertilization, the embryo sac no longer attracts the Pollen Tube, despite the persistence of one synergid cell. This cessation of attraction might be involved in blocking polyspermy.
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explosive discharge of Pollen Tube contents in torenia fournieri
Plant Physiology, 2000Co-Authors: Tetsuya Higashiyama, Haruko Kuroiwa, Shigeyuki Kawano, Tsuneyoshi KuroiwaAbstract:When animals copulate, the male organ penetrates the female. Similarly, the Pollen Tube of a flowering plant (the male gametophyte) penetrates the embryo sac (the female gametophyte) and then discharges its contents, which include male gametes. Details of the interaction between the Pollen Tube and
Mark A Johnson - One of the best experts on this subject based on the ideXlab platform.
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Pollen Tube discharge completes the process of synergid degeneration that is initiated by Pollen Tube - synergid interaction in Arabidopsis
Plant Physiology, 2015Co-Authors: Alexander R. Leydon, Mark A Johnson, Tatsuya Tsukamoto, Damayanthi Dunatunga, Ravishankar PalaniveluAbstract:In flowering plant reproduction, Pollen Tube reception is the signaling system that results in Pollen Tube discharge, synergid degeneration, and successful delivery of male gametes (two sperm cells) to the site where they can fuse with female gametes (egg cell and central cell). Some molecules required for this complex and essential signaling exchange have been identified; however, fundamental questions about the nature of the interactions between the Pollen Tube and the synergid cells remain to be clarified. Here, we monitor Pollen Tube arrival, Pollen Tube discharge, and synergid degeneration in Arabidopsis (Arabidopsis thaliana) wild type and in male and female gametophytic mutants that disrupt development and function of the gametophytes. By combining assays used previously to study these interactions and an assay that facilitates simultaneous analysis of Pollen Tube discharge and synergid degeneration, we find that synergid degeneration could be initiated without Pollen Tube discharge. Our data support the hypothesis that Pollen Tube-synergid contact, or signaling via secreted molecules, initiates receptive synergid degeneration. We also find that when Pollen Tubes successfully burst, they always discharge into a degenerated synergid. In addition to this Pollen Tube-dependent promotion of synergid degeneration, we also show that a basal developmental pathway mediates synergid degeneration in the absence of pollination. Our results are consistent with the model that a complex set of interactions between the Pollen Tube and synergid cells promote receptive synergid degeneration.
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Interactions between Pollen Tube and pistil control Pollen Tube identity and sperm release in the Arabidopsis female gametophyte.
Biochemical Society Transactions, 2014Co-Authors: Alexander R. Leydon, Adisorn Chaibang, Mark A JohnsonAbstract:Flowering plants have immotile sperm that develop within the Pollen cytoplasm and are delivered to female gametes by a Pollen Tube, a highly polarized extension of the Pollen cell. In many flowering plant species, including seed crop plants, hundreds of Pollen Tubes grow towards a limited number of ovules. This system should ensure maximal fertilization of ovules and seed production; however, we know very little about how signalling between the critical cells is integrated to orchestrate delivery of two functional sperm to each ovule. Recent studies suggest that the Pollen Tube changes its gene-expression programme in response to growth through pistil tissue and that this differentiation process is critical for Pollen Tube attraction by the female gametophyte and for release of sperm. Interestingly, these two signalling systems, called Pollen Tube guidance and Pollen Tube reception, are also species-preferential. The present review focuses on Arabidopsis Pollen Tube differentiation within the pistil and addresses the idea that Pollen Tube differentiation defines Pollen Tube identity and recognition by female cells. We review recent identification of genes that may control Pollen Tube–female gametophyte recognition and discuss how these may be involved in blocking interspecific hybridization.
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three myb transcription factors control Pollen Tube differentiation required for sperm release
Current Biology, 2013Co-Authors: Alexander R. Leydon, Ravishankar Palanivelu, Kristin M Beale, Karolina Woroniecka, Elizabeth Castner, Jefferson Chen, Casie Horgan, Mark A JohnsonAbstract:Summary In flowering plants, immotile sperm cells develop within the Pollen grain and are delivered to female gametes by a Pollen Tube [1, 2]. Upon arrival at the female gametophyte, the Pollen Tube stops growing and releases sperm cells for successful fertilization [3]. Several female signaling components essential for Pollen Tube reception have been identified [4–11]); however, male components remain unknown. We show that the expression of three closely related MYB transcription factors is induced in Pollen Tubes by growth in the pistil. Pollen Tubes lacking these three transcriptional regulators fail to stop growing in synergids, specialized cells flanking the egg cell that attract Pollen Tubes [12–16] and degenerate upon Pollen Tube arrival [17, 18]. myb triple-mutant Pollen Tubes also fail to release their sperm cargo. We define a suite of Pollen Tube-expressed genes regulated by these critical MYBs and identify transporters, carbohydrate-active enzymes, and small peptides as candidate molecular mediators of Pollen Tube-female interactions necessary for flowering plant reproduction. Our data indicate that de novo transcription in the Pollen Tube nucleus during growth in the pistil leads to Pollen Tube differentiation required for release of sperm cells.
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Pollen Tube Development
Methods of Molecular Biology, 2010Co-Authors: Mark A Johnson, Benedikt KostAbstract:: Pollen Tubes grow rapidly in a strictly polarized manner as they transport male reproductive cells through female flower tissues to bring about fertilization. Vegetative Pollen Tube cells are an excellent model system to investigate processes underlying directional cell expansion. In this chapter, we describe materials and methods required for (1) the identification of novel factors essential for polarized cell growth through the isolation and analysis of Arabidopsis mutants with defects in Pollen Tube growth and (2) the detailed functional characterization of Pollen Tube proteins based on transient transformation and microscopic analysis of cultured tobacco Pollen Tubes.
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Functional genomics of Pollen Tube-pistil interactions in Arabidopsis.
Biochemical Society Transactions, 2010Co-Authors: Ravishankar Palanivelu, Mark A JohnsonAbstract:The Pollen Tube represents an attractive model system for functional genomic analysis of the cell–cell interactions that mediate guided cellular growth. The Pollen Tube extends through pistil tissues and responds to guidance cues that direct the Tube towards an ovule, where it releases sperm for fertilization. Pollen is readily isolated from anthers, where it is produced, and can be induced to produce a Tube in vitro. Interestingly, Pollen Tube growth is significantly enhanced in pistils, and Pollen Tubes are rendered competent to respond to guidance cues after growth in a pistil. This potentiation of the Pollen Tube by the pistil suggested that Pollen Tubes alter their gene-expression programme in response to their environment. Recently, the transcriptomes of Pollen Tubes grown in vitro or through pistil tissues were determined. Significant changes in the transcriptome were found to accompany growth in vitro and through the pistil tissues. Reverse genetic analysis of Pollen-Tube-induced genes identified a new set of factors critical for Pollen Tube extension and navigation of the pistil environment. Recent advances reviewed in the present paper suggest that functional genomic analysis of Pollen Tubes has the potential to uncover the regulatory networks that shape the genetic architecture of the Pollen Tube as it responds to migratory cues produced by the pistil.