Cytoplasmic Ca2+ changes dynamically during the interaction of the pollen tube with synergid cells

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.

[1]  T. Higashiyama,et al.  Attraction of tip-growing pollen tubes by the female gametophyte. , 2011, Current opinion in plant biology.

[2]  U. Grossniklaus,et al.  She's the boss: signaling in pollen tube reception. , 2011, Current opinion in plant biology.

[3]  E. Lord,et al.  REVIEW: PART OF A SPECIAL ISSUE ON SEXUAL PLANT REPRODUCTION Pollen tube growth and guidance: roles of small, secreted proteins , 2011 .

[4]  A. Miyawaki,et al.  Live-Cell Imaging Reveals the Dynamics of Two Sperm Cells during Double Fertilization in Arabidopsis thaliana , 2011, Current Biology.

[5]  T. Dresselhaus,et al.  Female gametophyte-controlled pollen tube guidance. , 2010, Biochemical Society transactions.

[6]  Christian von Mering,et al.  Arabidopsis Female Gametophyte Gene Expression Map Reveals Similarities between Plant and Animal Gametes , 2010, Current Biology.

[7]  T. Dresselhaus,et al.  Micropylar pollen tube guidance and burst: adapted from defense mechanisms? , 2009, Current opinion in plant biology.

[8]  J. Schroeder,et al.  Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge , 2009, Development.

[9]  Hiroo Fukuda,et al.  ANXUR1 and 2, Sister Genes to FERONIA/SIRENE, Are Male Factors for Coordinated Fertilization , 2009, Current Biology.

[10]  A. Miyawaki,et al.  Fine-Tuning of the Cytoplasmic Ca2+ Concentration Is Essential for Pollen Tube Growth1[W] , 2009, Plant Physiology.

[11]  T. Kuroiwa,et al.  Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells , 2009, Nature.

[12]  A. Cheung,et al.  Structural and signaling networks for the polar cell growth machinery in pollen tubes. , 2008, Annual review of plant biology.

[13]  G. N. Drews,et al.  Development and function of the synergid cell , 2008, Sexual Plant Reproduction.

[14]  T. Higashiyama,et al.  Gametophytic pollen tube guidance , 2008, Sexual Plant Reproduction.

[15]  S. McCormick,et al.  Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. , 2007, The Plant journal : for cell and molecular biology.

[16]  Justin O Borevitz,et al.  Genome-Wide Expression Profiling of the Arabidopsis Female Gametophyte Identifies Families of Small, Secreted Proteins , 2007, PLoS genetics.

[17]  G. N. Drews,et al.  MYB98 Positively Regulates a Battery of Synergid-Expressed Genes Encoding Filiform Apparatus–Localized Proteins[W] , 2007, The Plant Cell Online.

[18]  Joshua G. Steffen,et al.  Identification of genes expressed in the Arabidopsis female gametophyte. , 2007, The Plant journal : for cell and molecular biology.

[19]  F. Berger,et al.  Distinct Dynamics of HISTONE3 Variants between the Two Fertilization Products in Plants , 2007, Current Biology.

[20]  G. Copenhaver,et al.  Synergid Cell Death in Arabidopsis Is Triggered following Direct Interaction with the Pollen Tube1[W][OA] , 2007, Plant Physiology.

[21]  T. Kuroiwa,et al.  Species Preferentiality of the Pollen Tube Attractant Derived from the Synergid Cell of Torenia fournieri1 , 2006, Plant Physiology.

[22]  Ravishankar Palanivelu,et al.  Distinct short-range ovule signals attract or repel Arabidopsis thaliana pollen tubes in vitro , 2006, BMC Plant Biology.

[23]  C. Dumas,et al.  Fertilization in plants: is calcium a key player? , 2006, Seminars in cell & developmental biology.

[24]  G. N. Drews,et al.  MYB98 Is Required for Pollen Tube Guidance and Synergid Cell Differentiation in Arabidopsisw⃞ , 2005, The Plant Cell Online.

[25]  A. Miyawaki,et al.  Ca2+ Dynamics in a Pollen Grain and Papilla Cell during Pollination of Arabidopsis1 , 2004, Plant Physiology.

[26]  A. Trewavas,et al.  Fluctuations in the pollen tube tip-focused calcium gradient are not reflected in nuclear calcium level: a comparative analysis using recombinant yellow cameleon calcium reporter , 2004, Sexual Plant Reproduction.

[27]  A. Miyawaki,et al.  Expanded dynamic range of fluorescent indicators for Ca(2+) by circularly permuted yellow fluorescent proteins. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[28]  M. Schiøtt,et al.  A plant plasma membrane Ca2+ pump is required for normal pollen tube growth and fertilization. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[29]  T. Kuroiwa,et al.  Pollen Tube Attraction by the Synergid Cell , 2001, Science.

[30]  K. Shimizu,et al.  Attractive and repulsive interactions between female and male gametophytes in Arabidopsis pollen tube guidance. , 2000, Development.

[31]  R. Tsien,et al.  Cameleon calcium indicator reports cytoplasmic calcium dynamics in Arabidopsis guard cells. , 1999, The Plant journal : for cell and molecular biology.

[32]  T. Kuroiwa,et al.  Guidance in Vitro of the Pollen Tube to the Naked Embryo Sac of Torenia fournieri , 1998, Plant Cell.

[33]  R. Tsien,et al.  Fluorescent indicators for Ca2+based on green fluorescent proteins and calmodulin , 1997, Nature.

[34]  J. Dangl,et al.  Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions. , 1996, The Plant cell.

[35]  D. Ehrhardt,et al.  Calcium Spiking in Plant Root Hairs Responding to Rhizobium Nodulation Signals , 1996, Cell.

[36]  C. Lamb,et al.  Calcium-mediated apoptosis in a plant hypersensitive disease resistance response , 1996, Current Biology.

[37]  D. Callaham,et al.  Tip-localized calcium entry fluctuates during pollen tube growth. , 1996, Developmental biology.

[38]  T. Bisseling,et al.  Symbiotic Nitrogen Fixation. , 1995, The Plant cell.

[39]  D. Callaham,et al.  Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: effect of BAPTA-type buffers and hypertonic media. , 1994, The Plant cell.

[40]  Elizabeth E. Hood,et al.  NewAgrobacterium helper plasmids for gene transfer to plants , 1993, Transgenic Research.

[41]  B. J. Reger,et al.  The dynamics of calcium distribution in the synergid cells of wheat after pollination , 1992, Sexual Plant Reproduction.

[42]  B. J. Reger,et al.  Calcium in the synergid cells and other regions of pearl millet ovaries , 1992, Sexual Plant Reproduction.

[43]  R. Pressey,et al.  Chemotropic responses by pearl millet pollen tubes , 1992, Sexual Plant Reproduction.

[44]  B. J. Reger,et al.  Relatively high calcium is localized in synergid cells of wheat ovaries , 1990, Sexual Plant Reproduction.

[45]  J. P. Mascarenhas,et al.  Chemotropic Response of Antirrhinum majus Pollen to Calcium , 1962, Nature.

[46]  T. Higashiyama,et al.  Pollen tube guidance by attractant molecules: LUREs. , 2010, Cell structure and function.

[47]  B. J. Reger,et al.  Prepollination degeneration in mature synergids of pearl millet: an examination using antimonate fixation to localize calcium , 2004, Sexual Plant Reproduction.

[48]  J F Harper,et al.  Diversity and regulation of plant Ca2+ pumps: insights from expression in yeast. , 2000, Annual review of plant physiology and plant molecular biology.