Male–female communication triggers calcium signatures during fertilization in Arabidopsis

Denninger, Philipp; Bleckmann, Andrea; Lausser, Andreas; Vogler, Frank; Ott, Thomas; Ehrhardt, David W.; Frommer, Wolf B.; Sprunck, Stefanie; Dresselhaus, Thomas; Grossmann, Guido

doi:10.1038/ncomms5645

Title: Male–female communication triggers calcium signatures during fertilization in Arabidopsis

Journal Article · Thu Aug 21 20:00:00 EDT 2014 · Nature Communications

DOI: https://doi.org/10.1038/ncomms5645 · OSTI ID:1623955

Denninger, Philipp ^[1]; Bleckmann, Andrea ^[2]; Lausser, Andreas ^[2]; Vogler, Frank ^[2]; Ott, Thomas ^[3]; Ehrhardt, David W. ^[4]; Frommer, Wolf B. ^[4]; Sprunck, Stefanie ^[2]; Dresselhaus, Thomas ^[2]; Grossmann, Guido ^[5]

Univ. Regensburg (Germany). Biochemie-Zentrum Regensburg. Cell Biology and Plant Biology; Univ. Heidelberg (Germany). Centre for Organismal Studies (COS). Cell Networks-Cluster of Excellence; DOE/OSTI
Univ. Regensburg (Germany). Biochemie-Zentrum Regensburg. Cell Biology and Plant Biology
Ludwig Maximilians Univ. Munchen (Germany). Inst. of Genetics
Carnegie Inst. of Science, Stanford, CA (United States). Dept. of Plant Biology
Univ. Heidelberg (Germany). Centre for Organismal Studies (COS). Cell Networks-Cluster of Excellence; Carnegie Inst. of Science, Stanford, CA (United States). Dept. of Plant Biology

Cell–cell communication and interaction is critical during fertilization and triggers free cytosolic calcium ([Ca2 þ ]cyto) as a key signal for egg activation and a polyspermy block in animal oocytes. Fertilization in flowering plants is more complex, involving interaction of a pollen tube with egg adjoining synergid cells, culminating in release of two sperm cells and their fusion with the egg and central cell, respectively. Here, we report the occurrence and role of [Ca2 þ ]cyto signals during the entire double fertilization process in Arabidopsis. [Ca2 þ ]cyto oscillations are initiated in synergid cells after physical contact with the pollen tube apex. In egg and central cells, a short [Ca2 þ ]cyto transient is associated with pollen tube burst and sperm cell arrival. A second extended [Ca2 þ ]cyto transient solely in the egg cell is correlated with successful fertilization. Thus, each female cell type involved in double fertilization displays a characteristic [Ca2 þ ]cyto signature differing by timing and behaviour from [Ca2 þ ]cyto waves reported in mammals.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Carnegie Inst. of Washington, Washington, DC (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: FG02-04ER15542

OSTI ID:: 1623955

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 5; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (119)

Pollen tube entry into the synergid cell of Arabidopsis is observed at a site distinct from the filiform apparatus Leshem, Yehoram; Johnson, Cameron; Sundaresan, Venkatesan Plant Reproduction, Vol. 26, Issue 2 https://doi.org/10.1007/s00497-013-0211-1	journal	February 2013
External application of gametophyte-specific ZmPMEI1 induces pollen tube burst in maize Woriedh, Mayada; Wolf, Sebastian; Márton, Mihaela L. Plant Reproduction, Vol. 26, Issue 3 https://doi.org/10.1007/s00497-013-0221-z	journal	July 2013
Biochemistry of calcium oscillations Uhlén, Per; Fritz, Nicolas Biochemical and Biophysical Research Communications, Vol. 396, Issue 1 https://doi.org/10.1016/j.bbrc.2010.02.117	journal	May 2010
Troponin C-based biosensors: A new family of genetically encoded indicators for in vivo calcium imaging in the nervous system Garaschuk, O.; Griesbeck, O.; Konnerth, A. Cell Calcium, Vol. 42, Issue 4-5 https://doi.org/10.1016/j.ceca.2007.02.011	journal	October 2007
Gamete Fusion Is Required to Block Multiple Pollen Tubes from Entering an Arabidopsis Ovule Beale, Kristin M.; Leydon, Alexander R.; Johnson, Mark A. Current Biology, Vol. 22, Issue 12 https://doi.org/10.1016/j.cub.2012.04.041	journal	June 2012
Plant Reproduction: Teaching a New Language of Love Johnson, Mark A. Current Biology, Vol. 22, Issue 13 https://doi.org/10.1016/j.cub.2012.06.003	journal	July 2012
A Calcium Dialog Mediated by the FERONIA Signal Transduction Pathway Controls Plant Sperm Delivery Ngo, Quy A.; Vogler, Hannes; Lituiev, Dmytro S. Developmental Cell, Vol. 29, Issue 4 https://doi.org/10.1016/j.devcel.2014.04.008	journal	May 2014
Calcium Spiking in Plant Root Hairs Responding to Rhizobium Nodulation Signals Ehrhardt, David W.; Wais, Rebecca; Long, Sharon R. Cell, Vol. 85, Issue 5 https://doi.org/10.1016/s0092-8674(00)81234-9	journal	May 1996
Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis Duan, Qiaohong; Kita, Daniel; Johnson, Eric A. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4129	journal	January 2014
Live imaging of calcium spikes during double fertilization in Arabidopsis Hamamura, Yuki; Nishimaki, Moe; Takeuchi, Hidenori Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5722	journal	August 2014
Improved calcium imaging in transgenic mice expressing a troponin C–based biosensor Heim, Nicola; Garaschuk, Olga; Friedrich, Michael W. Nature Methods, Vol. 4, Issue 2 https://doi.org/10.1038/nmeth1009	journal	January 2007
Regulation of cell death: the calcium–apoptosis link Orrenius, Sten; Zhivotovsky, Boris; Nicotera, Pierluigi Nature Reviews Molecular Cell Biology, Vol. 4, Issue 7 https://doi.org/10.1038/nrm1150	journal	July 2003
Early cytological events after induction of cell division in egg cells and zygote development following in vitro fertilization with angiosperm gametes Kranz, Erhard; Wiegen, Petra; Lorz, Horst The Plant Journal, Vol. 8, Issue 1 https://doi.org/10.1046/j.1365-313x.1995.08010009.x	journal	July 1995
Expanded dynamic range of fluorescent indicators for Ca2+ by circularly permuted yellow fluorescent proteins Nagai, T.; Yamada, S.; Tominaga, T. Proceedings of the National Academy of Sciences, Vol. 101, Issue 29 https://doi.org/10.1073/pnas.0400417101	journal	July 2004
A plant plasma membrane Ca2+ pump is required for normal pollen tube growth and fertilization Schiott, M.; Romanowsky, S. M.; Baekgaard, L. Proceedings of the National Academy of Sciences, Vol. 101, Issue 25 https://doi.org/10.1073/pnas.0401542101	journal	June 2004
Calcium influx-mediated signaling is required for complete mouse egg activation Miao, Y. -L.; Stein, P.; Jefferson, W. N. Proceedings of the National Academy of Sciences, Vol. 109, Issue 11 https://doi.org/10.1073/pnas.1112333109	journal	February 2012
A calcium influx is triggered and propagates in the zygote as a wavefront during in vitro fertilization of flowering plants Antoine, A. F.; Faure, J. -E.; Cordeiro, S. Proceedings of the National Academy of Sciences, Vol. 97, Issue 19 https://doi.org/10.1073/pnas.180243697	journal	September 2000
Molecular model for receptor-stimulated calcium spiking. Meyer, T.; Stryer, L. Proceedings of the National Academy of Sciences, Vol. 85, Issue 14 https://doi.org/10.1073/pnas.85.14.5051	journal	July 1988
A free calcium wave traverses the activating egg of the medaka, Oryzias latipes. Gilkey, J. C.; Jaffe, L. F.; Ridgway, E. B. Journal of Cell Biology, Vol. 76, Issue 2 https://doi.org/10.1083/jcb.76.2.448	journal	February 1978
Taking one for the team: self-recognition and cell suicide in pollen Wilkins, K. A.; Poulter, N. S.; Franklin-Tong, V. E. Journal of Experimental Botany, Vol. 65, Issue 5 https://doi.org/10.1093/jxb/ert468	journal	January 2014
Double Fertilization in Arabidopsis thaliana Involves a Polyspermy Block on the Egg but Not the Central Cell Scott, Rod J.; Armstrong, Susan J.; Doughty, James Molecular Plant, Vol. 1, Issue 4 https://doi.org/10.1093/mp/ssn016	journal	July 2008
Male–Female Crosstalk during Pollen Germination, Tube Growth and Guidance, and Double Fertilization Dresselhaus, Thomas; Franklin-Tong, Noni Molecular Plant, Vol. 6, Issue 4 https://doi.org/10.1093/mp/sst061	journal	July 2013
Imaging of the Yellow Cameleon 3.6 Indicator Reveals That Elevations in Cytosolic Ca ²⁺ Follow Oscillating Increases in Growth in Root Hairs of Arabidopsis Monshausen, Gabriele B.; Messerli, Mark A.; Gilroy, Simon Plant Physiology, Vol. 147, Issue 4 https://doi.org/10.1104/pp.108.123638	journal	June 2008
Maternal Control of Male-Gamete Delivery in Arabidopsis Involves a Putative GPI-Anchored Protein Encoded by the LORELEI Gene Capron, Arnaud; Gourgues, Mathieu; Neiva, Lissiene S. The Plant Cell, Vol. 20, Issue 11 https://doi.org/10.1105/tpc.108.061713	journal	November 2008
Control of Pollen Tube Tip Growth by a Rop GTPase–Dependent Pathway That Leads to Tip-Localized Calcium Influx Li, Hai; Lin, Yakang; Heath, Rachel M. The Plant Cell, Vol. 11, Issue 9 https://doi.org/10.1105/tpc.11.9.1731	journal	September 1999
The RootChip: An Integrated Microfluidic Chip for Plant Science Grossmann, Guido; Guo, Woei-Jiun; Ehrhardt, David W. The Plant Cell, Vol. 23, Issue 12 https://doi.org/10.1105/tpc.111.092577	journal	December 2011
Comparative Detection of Calcium Fluctuations in Single Female Sex Cells of Tobacco to Distinguish Calcium Signals Triggered by in vitro Fertilization Peng, Xiong-Bo; Sun, Meng-Xiang; Yang, Hong-Yuan Journal of Integrative Plant Biology, Vol. 51, Issue 8 https://doi.org/10.1111/j.1744-7909.2009.00857.x	journal	August 2009
Micropylar Pollen Tube Guidance by Egg Apparatus 1 of Maize Marton, M. L. Science, Vol. 307, Issue 5709 https://doi.org/10.1126/science.1104954	journal	January 2005
Reprogramming Plant Cells for Endosymbiosis Oldroyd, G. E. D.; Harrison, M. J.; Paszkowski, U. Science, Vol. 324, Issue 5928 https://doi.org/10.1126/science.1171644	journal	May 2009
A Peptide Hormone and Its Receptor Protein Kinase Regulate Plant Cell Expansion Haruta, M.; Sabat, G.; Stecker, K. Science, Vol. 343, Issue 6169 https://doi.org/10.1126/science.1244454	journal	January 2014
An in Vitro System for Adhesion and Fusion of Maize Gametes Faure, J. -E.; Digonnet, C.; Dumas, C. Science, Vol. 263, Issue 5153 https://doi.org/10.1126/science.263.5153.1598	journal	March 1994
The Language of Calcium Signaling Dodd, Antony N.; Kudla, Jörg; Sanders, Dale Annual Review of Plant Biology, Vol. 61, Issue 1 https://doi.org/10.1146/annurev-arplant-070109-104628	journal	June 2010
Coordinating Nodule Morphogenesis with Rhizobial Infection in Legumes Oldroyd, Giles E. D.; Downie, J. Allan Annual Review of Plant Biology, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.arplant.59.032607.092839	journal	June 2008
Cytoplasmic Ca2+ changes dynamically during the interaction of the pollen tube with synergid cells Iwano, M.; Ngo, Q. A.; Entani, T. Development, Vol. 139, Issue 22 https://doi.org/10.1242/dev.081208	journal	October 2012
The cell biology of mammalian fertilization Okabe, M. Development, Vol. 140, Issue 22 https://doi.org/10.1242/dev.090613	journal	November 2013
First evidence of a calcium transient in flowering plants at fertilization Digonnet, C.; Aldon, D.; Leduc, N. Development, Vol. 124, Issue 15 https://doi.org/10.1242/dev.124.15.2867	journal	August 1997
The dynamics of calcium oscillations that activate mammalian eggs Swann, Karl; Yu, Yuansong The International Journal of Developmental Biology, Vol. 52, Issue 5-6 https://doi.org/10.1387/ijdb.072530ks	journal	January 2008
Egg activation in physiological polyspermy Iwao, Yasuhiro REPRODUCTION, Vol. 144, Issue 1 https://doi.org/10.1530/rep-12-0104	journal	July 2012
Defensin-Like ZmES4 Mediates Pollen Tube Burst in Maize via Opening of the Potassium Channel KZM1 Amien, Suseno; Kliwer, Irina; Marton, Mihaela L. San Francisco : Public Library Science https://doi.org/10.15488/300	other	January 2010
Pollen Tube Growth and the Intracellular Cytosolic Calcium Gradient Oscillate in Phase while Extracellular Calcium Influx Is Delayed Holdaway-Clarke, Terena L.; Feijo, Jose A.; Hackett, Grant R. The Plant Cell, Vol. 9, Issue 11 https://doi.org/10.2307/3870560	journal	November 1997
Time-lapse Fluorescence Imaging of Arabidopsis Root Growth with Rapid Manipulation of The Root Environment Using The RootChip Grossmann, Guido; Meier, Matthias; Cartwright, Heather N. Journal of Visualized Experiments, Issue 65 https://doi.org/10.3791/4290	journal	July 2012
ANXUR Receptor-Like Kinases Coordinate Cell Wall Integrity with Growth at the Pollen Tube Tip Via NADPH Oxidases Boisson-Dernier, Aurélien; Lituiev, Dmytro S.; Nestorova, Anna ETH Zurich https://doi.org/10.3929/ethz-b-000080801	text	January 2013
Calcium signalling Kaestner, Lars Springer Berlin, Heidelberg https://doi.org/10.1007/978-3-642-34617-0	book	January 2013
Pollen tube entry into the synergid cell of Arabidopsis is observed at a site distinct from the filiform apparatus Leshem, Yehoram; Johnson, Cameron; Sundaresan, Venkatesan Plant Reproduction, Vol. 26, Issue 2 https://doi.org/10.1007/s00497-013-0211-1	journal	February 2013
External application of gametophyte-specific ZmPMEI1 induces pollen tube burst in maize Woriedh, Mayada; Wolf, Sebastian; Márton, Mihaela L. Plant Reproduction, Vol. 26, Issue 3 https://doi.org/10.1007/s00497-013-0221-z	journal	July 2013
Calcium signalling Rink, T. J.; Merritt, J. E. Current Opinion in Cell Biology, Vol. 2, Issue 2 https://doi.org/10.1016/0955-0674(90)90007-2	journal	April 1990
Calcium Spiking in Plant Root Hairs Responding to Rhizobium Nodulation Signals Ehrhardt, David W.; Wais, Rebecca; Long, Sharon R. Cell, Vol. 85, Issue 5 https://doi.org/10.1016/S0092-8674(00)81234-9	journal	May 1996
Biochemistry of calcium oscillations Uhlén, Per; Fritz, Nicolas Biochemical and Biophysical Research Communications, Vol. 396, Issue 1 https://doi.org/10.1016/j.bbrc.2010.02.117	journal	May 2010
Troponin C-based biosensors: A new family of genetically encoded indicators for in vivo calcium imaging in the nervous system Garaschuk, O.; Griesbeck, O.; Konnerth, A. Cell Calcium, Vol. 42, Issue 4-5 https://doi.org/10.1016/j.ceca.2007.02.011	journal	October 2007
Distinct Dynamics of HISTONE3 Variants between the Two Fertilization Products in Plants Ingouff, Mathieu; Hamamura, Yuki; Gourgues, Mathieu Current Biology, Vol. 17, Issue 12 https://doi.org/10.1016/j.cub.2007.05.019	journal	June 2007
Live-Cell Imaging Reveals the Dynamics of Two Sperm Cells during Double Fertilization in Arabidopsis thaliana Hamamura, Yuki; Saito, Chieko; Awai, Chie Current Biology, Vol. 21, Issue 6 https://doi.org/10.1016/j.cub.2011.02.013	journal	March 2011
Gamete Fusion Is Required to Block Multiple Pollen Tubes from Entering an Arabidopsis Ovule Beale, Kristin M.; Leydon, Alexander R.; Johnson, Mark A. Current Biology, Vol. 22, Issue 12 https://doi.org/10.1016/j.cub.2012.04.041	journal	June 2012
Overcoming Hybridization Barriers by the Secretion of the Maize Pollen Tube Attractant ZmEA1 from Arabidopsis Ovules Márton, Mihaela L.; Fastner, Astrid; Uebler, Susanne Current Biology, Vol. 22, Issue 13 https://doi.org/10.1016/j.cub.2012.04.061	journal	July 2012
Ethylene Signaling Is Required for Synergid Degeneration and the Establishment of a Pollen Tube Block Völz, Ronny; Heydlauff, Juliane; Ripper, Dagmar Developmental Cell, Vol. 25, Issue 3 https://doi.org/10.1016/j.devcel.2013.04.001	journal	May 2013
A Calcium Dialog Mediated by the FERONIA Signal Transduction Pathway Controls Plant Sperm Delivery Ngo, Quy A.; Vogler, Hannes; Lituiev, Dmytro S. Developmental Cell, Vol. 29, Issue 4 https://doi.org/10.1016/j.devcel.2014.04.008	journal	May 2014
Fluorescent indicators for Ca2+based on green fluorescent proteins and calmodulin Miyawaki, Atsushi; Llopis, Juan; Heim, Roger Nature, Vol. 388, Issue 6645 https://doi.org/10.1038/42264	journal	August 1997
Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells Okuda, Satohiro; Tsutsui, Hiroki; Shiina, Keiko Nature, Vol. 458, Issue 7236 https://doi.org/10.1038/nature07882	journal	March 2009
Differential contribution of cytoplasmic Ca2+ and Ca2+ influx to gamete fusion and egg activation in maize Antoine, Anne-Frédérique; Faure, Jean-Emmanuel; Dumas, Christian Nature Cell Biology, Vol. 3, Issue 12 https://doi.org/10.1038/ncb1201-1120	journal	November 2001
Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis Duan, Qiaohong; Kita, Daniel; Johnson, Eric A. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4129	journal	January 2014
Live imaging of calcium spikes during double fertilization in Arabidopsis Hamamura, Yuki; Nishimaki, Moe; Takeuchi, Hidenori Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5722	journal	August 2014
Improved calcium imaging in transgenic mice expressing a troponin C–based biosensor Heim, Nicola; Garaschuk, Olga; Friedrich, Michael W. Nature Methods, Vol. 4, Issue 2 https://doi.org/10.1038/nmeth1009	journal	January 2007
Regulation of cell death: the calcium–apoptosis link Orrenius, Sten; Zhivotovsky, Boris; Nicotera, Pierluigi Nature Reviews Molecular Cell Biology, Vol. 4, Issue 7 https://doi.org/10.1038/nrm1150	journal	July 2003
Early cytological events after induction of cell division in egg cells and zygote development following in vitro fertilization with angiosperm gametes Kranz, Erhard; Wiegen, Petra; Lorz, Horst The Plant Journal, Vol. 8, Issue 1 https://doi.org/10.1046/j.1365-313X.1995.08010009.x	journal	July 1995
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana Clough, Steven J.; Bent, Andrew F. The Plant Journal, Vol. 16, Issue 6, p. 735-743 https://doi.org/10.1046/j.1365-313x.1998.00343.x	journal	December 1998
Cell-type-specific calcium responses to drought, salt and cold in the Arabidopsis root Kiegle, Edward; Moore, Catherine A.; Haseloff, Jim The Plant Journal, Vol. 23, Issue 2 https://doi.org/10.1046/j.1365-313x.2000.00786.x	journal	July 2000
Expanded dynamic range of fluorescent indicators for Ca2+ by circularly permuted yellow fluorescent proteins Nagai, T.; Yamada, S.; Tominaga, T. Proceedings of the National Academy of Sciences, Vol. 101, Issue 29 https://doi.org/10.1073/pnas.0400417101	journal	July 2004
A plant plasma membrane Ca2+ pump is required for normal pollen tube growth and fertilization Schiott, M.; Romanowsky, S. M.; Baekgaard, L. Proceedings of the National Academy of Sciences, Vol. 101, Issue 25 https://doi.org/10.1073/pnas.0401542101	journal	June 2004
Arabidopsis plasma membrane protein crucial for Ca2+ influx and touch sensing in roots Nakagawa, Y.; Katagiri, T.; Shinozaki, K. Proceedings of the National Academy of Sciences, Vol. 104, Issue 9 https://doi.org/10.1073/pnas.0607703104	journal	February 2007
Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes Kosuta, S.; Hazledine, S.; Sun, J. Proceedings of the National Academy of Sciences, Vol. 105, Issue 28 https://doi.org/10.1073/pnas.0803499105	journal	July 2008
Calcium influx-mediated signaling is required for complete mouse egg activation Miao, Y. -L.; Stein, P.; Jefferson, W. N. Proceedings of the National Academy of Sciences, Vol. 109, Issue 11 https://doi.org/10.1073/pnas.1112333109	journal	February 2012
A calcium influx is triggered and propagates in the zygote as a wavefront during in vitro fertilization of flowering plants Antoine, A. F.; Faure, J. -E.; Cordeiro, S. Proceedings of the National Academy of Sciences, Vol. 97, Issue 19 https://doi.org/10.1073/pnas.180243697	journal	September 2000
Molecular model for receptor-stimulated calcium spiking. Meyer, T.; Stryer, L. Proceedings of the National Academy of Sciences, Vol. 85, Issue 14 https://doi.org/10.1073/pnas.85.14.5051	journal	July 1988
Genetically Encoded Indicators of Cellular Calcium Dynamics Based on Troponin C and Green Fluorescent Protein Heim, Nicola; Griesbeck, Oliver Journal of Biological Chemistry, Vol. 279, Issue 14 https://doi.org/10.1074/jbc.M312751200	journal	April 2004
A free calcium wave traverses the activating egg of the medaka, Oryzias latipes. Gilkey, J. C.; Jaffe, L. F.; Ridgway, E. B. Journal of Cell Biology, Vol. 76, Issue 2 https://doi.org/10.1083/jcb.76.2.448	journal	February 1978
Taking one for the team: self-recognition and cell suicide in pollen Wilkins, K. A.; Poulter, N. S.; Franklin-Tong, V. E. Journal of Experimental Botany, Vol. 65, Issue 5 https://doi.org/10.1093/jxb/ert468	journal	January 2014
Double Fertilization in Arabidopsis thaliana Involves a Polyspermy Block on the Egg but Not the Central Cell Scott, Rod J.; Armstrong, Susan J.; Doughty, James Molecular Plant, Vol. 1, Issue 4 https://doi.org/10.1093/mp/ssn016	journal	July 2008
Male–Female Crosstalk during Pollen Germination, Tube Growth and Guidance, and Double Fertilization Dresselhaus, Thomas; Franklin-Tong, Noni Molecular Plant, Vol. 6, Issue 4 https://doi.org/10.1093/mp/sst061	journal	July 2013
Recombinational Cloning with Plant Gateway Vectors Karimi, Mansour; Depicker, Ann; Hilson, Pierre Plant Physiology, Vol. 145, Issue 4 https://doi.org/10.1104/pp.107.106989	journal	December 2007
Imaging of the Yellow Cameleon 3.6 Indicator Reveals That Elevations in Cytosolic Ca ²⁺ Follow Oscillating Increases in Growth in Root Hairs of Arabidopsis Monshausen, Gabriele B.; Messerli, Mark A.; Gilroy, Simon Plant Physiology, Vol. 147, Issue 4 https://doi.org/10.1104/pp.108.123638	journal	June 2008
MYB98 Is Required for Pollen Tube Guidance and Synergid Cell Differentiation in Arabidopsis Kasahara, Ryushiro D.; Portereiko, Michael F.; Sandaklie-Nikolova, Linda The Plant Cell, Vol. 17, Issue 11 https://doi.org/10.1105/tpc.105.034603	journal	October 2005
Maternal Control of Male-Gamete Delivery in Arabidopsis Involves a Putative GPI-Anchored Protein Encoded by the LORELEI Gene Capron, Arnaud; Gourgues, Mathieu; Neiva, Lissiene S. The Plant Cell, Vol. 20, Issue 11 https://doi.org/10.1105/tpc.108.061713	journal	November 2008
Ca ²⁺ Regulates Reactive Oxygen Species Production and pH during Mechanosensing in Arabidopsis Roots Monshausen, Gabriele B.; Bibikova, Tatiana N.; Weisenseel, Manfred H. The Plant Cell, Vol. 21, Issue 8 https://doi.org/10.1105/tpc.109.068395	journal	August 2009
The RootChip: An Integrated Microfluidic Chip for Plant Science Grossmann, Guido; Guo, Woei-Jiun; Ehrhardt, David W. The Plant Cell, Vol. 23, Issue 12 https://doi.org/10.1105/tpc.111.092577	journal	December 2011
Pollen Tube Growth and the Intracellular Cytosolic Calcium Gradient Oscillate in Phase while Extracellular Calcium Influx Is Delayed. Holdaway-Clarke, T. L.; Feijo, J. A.; Hackett, G. R. The Plant Cell https://doi.org/10.1105/tpc.9.11.1999	journal	November 1997
Identification of genes expressed in the Arabidopsis female gametophyte: Female gametophyte-expressed genes Steffen, Joshua G.; Kang, Il-Ho; Macfarlane, Jane The Plant Journal, Vol. 51, Issue 2 https://doi.org/10.1111/j.1365-313X.2007.03137.x	journal	June 2007
FRET-based genetically encoded sensors allow high-resolution live cell imaging of Ca2+ dynamics: Improved vectors for Ca2+ imaging in plants Krebs, Melanie; Held, Katrin; Binder, Andreas The Plant Journal, Vol. 69, Issue 1 https://doi.org/10.1111/j.1365-313X.2011.04780.x	journal	October 2011
A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures Murashige, Toshio; Skoog, Folke Physiologia Plantarum, Vol. 15, Issue 3, p. 473-497 https://doi.org/10.1111/j.1399-3054.1962.tb08052.x	journal	July 1962
The grateful dead: calcium and cell death in plant innate immunity Ma, Wei; Berkowitz, Gerald A. Cellular Microbiology, Vol. 9, Issue 11 https://doi.org/10.1111/j.1462-5822.2007.01031.x	journal	November 2007
Arbuscular mycorrhizal hyphopodia and germinated spore exudates trigger Ca2+ spiking in the legume and nonlegume root epidermis Chabaud, Mireille; Genre, Andrea; Sieberer, Björn J. New Phytologist, Vol. 189, Issue 1 https://doi.org/10.1111/j.1469-8137.2010.03464.x	journal	September 2010
Comparative Detection of Calcium Fluctuations in Single Female Sex Cells of Tobacco to Distinguish Calcium Signals Triggered by in vitro Fertilization Peng, Xiong-Bo; Sun, Meng-Xiang; Yang, Hong-Yuan Journal of Integrative Plant Biology, Vol. 51, Issue 8 https://doi.org/10.1111/j.1744-7909.2009.00857.x	journal	August 2009
S-acylation anchors remorin proteins to the plasma membrane but does not primarily determine their localization in membrane microdomains Konrad, Sebastian S. A.; Popp, Claudia; Stratil, Thomas F. New Phytologist, Vol. 203, Issue 3 https://doi.org/10.1111/nph.12867	journal	June 2014
Calcium Signalling Ishiguro, H.; Lindsay, A. R. G.; Steward, M. C. The Journal of Physiology, Vol. 479, Issue suppl, p. 9-12 https://doi.org/10.1113/jphysiol.1994.sp020315	journal	August 1994
Micropylar Pollen Tube Guidance by Egg Apparatus 1 of Maize Marton, M. L. Science, Vol. 307, Issue 5709 https://doi.org/10.1126/science.1104954	journal	January 2005
The FERONIA Receptor-like Kinase Mediates Male-Female Interactions During Pollen Tube Reception Escobar-Restrepo, J. -M.; Huck, N.; Kessler, S. Science, Vol. 317, Issue 5838 https://doi.org/10.1126/science.1143562	journal	August 2007
Reprogramming Plant Cells for Endosymbiosis Oldroyd, G. E. D.; Harrison, M. J.; Paszkowski, U. Science, Vol. 324, Issue 5928 https://doi.org/10.1126/science.1171644	journal	May 2009
Conserved Molecular Components for Pollen Tube Reception and Fungal Invasion Kessler, S. A.; Shimosato-Asano, H.; Keinath, N. F. Science, Vol. 330, Issue 6006 https://doi.org/10.1126/science.1195211	journal	November 2010
Egg Cell-Secreted EC1 Triggers Sperm Cell Activation During Double Fertilization Sprunck, S.; Rademacher, S.; Vogler, F. Science, Vol. 338, Issue 6110 https://doi.org/10.1126/science.1223944	journal	November 2012
A Peptide Hormone and Its Receptor Protein Kinase Regulate Plant Cell Expansion Haruta, M.; Sabat, G.; Stecker, K. Science, Vol. 343, Issue 6169 https://doi.org/10.1126/science.1244454	journal	January 2014
An in Vitro System for Adhesion and Fusion of Maize Gametes Faure, J. -E.; Digonnet, C.; Dumas, C. Science, Vol. 263, Issue 5153 https://doi.org/10.1126/science.263.5153.1598	journal	March 1994
The Language of Calcium Signaling Dodd, Antony N.; Kudla, Jörg; Sanders, Dale Annual Review of Plant Biology, Vol. 61, Issue 1 https://doi.org/10.1146/annurev-arplant-070109-104628	journal	June 2010
Coordinating Nodule Morphogenesis with Rhizobial Infection in Legumes Oldroyd, Giles E. D.; Downie, J. Allan Annual Review of Plant Biology, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.arplant.59.032607.092839	journal	June 2008
Cytoplasmic Ca2+ changes dynamically during the interaction of the pollen tube with synergid cells Iwano, M.; Ngo, Q. A.; Entani, T. Development, Vol. 139, Issue 22 https://doi.org/10.1242/dev.081208	journal	October 2012
The cell biology of mammalian fertilization Okabe, M. Development, Vol. 140, Issue 22 https://doi.org/10.1242/dev.090613	journal	November 2013
Pollen-specific gene expression in transgenic plants: coordinate regulation of two different tomato gene promoters during microsporogenesis Twell, David; Yamaguchi, Judy; Mccormick, Sheila Development, Vol. 109, Issue 3 https://doi.org/10.1242/dev.109.3.705	journal	July 1990
First evidence of a calcium transient in flowering plants at fertilization Digonnet, C.; Aldon, D.; Leduc, N. Development, Vol. 124, Issue 15 https://doi.org/10.1242/dev.124.15.2867	journal	August 1997
Defensin-Like ZmES4 Mediates Pollen Tube Burst in Maize via Opening of the Potassium Channel KZM1 Amien, Suseno; Kliwer, Irina; Márton, Mihaela L. PLoS Biology, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pbio.1000388	journal	June 2010
A Species-Specific Cluster of Defensin-Like Genes Encodes Diffusible Pollen Tube Attractants in Arabidopsis Takeuchi, Hidenori; Higashiyama, Tetsuya PLoS Biology, Vol. 10, Issue 12 https://doi.org/10.1371/journal.pbio.1001449	journal	December 2012
ANXUR Receptor-Like Kinases Coordinate Cell Wall Integrity with Growth at the Pollen Tube Tip Via NADPH Oxidases Boisson-Dernier, Aurélien; Lituiev, Dmytro S.; Nestorova, Anna PLoS Biology, Vol. 11, Issue 11 https://doi.org/10.1371/journal.pbio.1001719	journal	November 2013
The dynamics of calcium oscillations that activate mammalian eggs Swann, Karl; Yu, Yuansong The International Journal of Developmental Biology, Vol. 52, Issue 5-6 https://doi.org/10.1387/ijdb.072530ks	journal	January 2008
Egg activation in physiological polyspermy Iwao, Yasuhiro REPRODUCTION, Vol. 144, Issue 1 https://doi.org/10.1530/REP-12-0104	journal	July 2012
Defensin-Like ZmES4 Mediates Pollen Tube Burst in Maize via Opening of the Potassium Channel KZM1 Amien, Suseno; Kliwer, Irina; Marton, Mihaela L. San Francisco : Public Library Science https://doi.org/10.15488/300	other	January 2010
Pollen Tube Growth and the Intracellular Cytosolic Calcium Gradient Oscillate in Phase while Extracellular Calcium Influx Is Delayed Holdaway-Clarke, Terena L.; Feijo, Jose A.; Hackett, Grant R. The Plant Cell, Vol. 9, Issue 11 https://doi.org/10.2307/3870560	journal	November 1997
ANXUR Receptor-Like Kinases Coordinate Cell Wall Integrity with Growth at the Pollen Tube Tip Via NADPH Oxidases Boisson-Dernier, Aurélien; Lituiev, Dmytro S.; Nestorova, Anna ETH Zurich https://doi.org/10.3929/ethz-b-000080801	text	January 2013
A calcium dialog mediated by the FERONIA Signal transduction pathway controls plant sperm delivery Ngo, Quy A.; Vogler, Hannes; Lituiev, Dmytro S. Cell Press (Elsevier) https://doi.org/10.5167/uzh-106953	text	January 2014
The FERONIA Receptor-like Kinase Mediates Male-Female Interactions During Pollen Tube Reception Escobar-Restrepo, J-M; Huck, N.; Kessler, S. American Association for the Advancement of Science https://doi.org/10.5167/uzh-173013	text	January 2007
Conserved molecular components for pollen tube reception and fungal invasion Kessler, S. A.; Shimosato-Asano, H.; Keinath, N. F. American Association for the Advancement of Science (AAAS) https://doi.org/10.5167/uzh-45448	text	January 2010
Egg cell-secreted EC1 triggers sperm cell activation during double fertilization Sprunck, Stefanie; Rademacher, Svenja; Vogler, Frank American Association for the Advancement of Science https://doi.org/10.5167/uzh-74119	text	January 2012
Cytoplasmic Ca2+ changes dynamically during the interaction of the pollen tube with synergid cells Iwano, Megumi; Ngo, Quy A.; Entani, Tetsuyuki Company of Biologists https://doi.org/10.5167/uzh-74121	text	January 2012
ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases Aurélien, Boisson-Dernier,; S., Lituiev, Dmytro; Anna, Nestorova, Public Library of Science (PLoS) https://doi.org/10.5167/uzh-89703	text	January 2013

Cited By (41)

Late progamic phase and fertilization affect calreticulin expression in the Hyacinthus orientalis female gametophyte Niedojadło, Katarzyna; Lenartowski, Robert; Lenartowska, Marta Plant Cell Reports, Vol. 34, Issue 12 https://doi.org/10.1007/s00299-015-1863-0	journal	September 2015
Rapid Elimination of the Persistent Synergid through a Cell Fusion Mechanism Maruyama, Daisuke; Völz, Ronny; Takeuchi, Hidenori Cell, Vol. 161, Issue 4 https://doi.org/10.1016/j.cell.2015.03.018	journal	May 2015
Dying two deaths — programmed cell death regulation in development and disease Huysmans, Marlies; Lema A., Saul; Coll, Nuria S. Current Opinion in Plant Biology, Vol. 35 https://doi.org/10.1016/j.pbi.2016.11.005	journal	February 2017
TrackMate: An open and extensible platform for single-particle tracking Tinevez, Jean-Yves; Perry, Nick; Schindelin, Johannes Methods, Vol. 115 https://doi.org/10.1016/j.ymeth.2016.09.016	journal	February 2017
Live imaging of calcium spikes during double fertilization in Arabidopsis Hamamura, Yuki; Nishimaki, Moe; Takeuchi, Hidenori Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5722	journal	August 2014
Calcium signals are necessary to establish auxin transporter polarity in a plant stem cell niche Li, Ting; Yan, An; Bhatia, Neha Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08575-6	journal	February 2019
The WASP-Arp2/3 complex signal cascade is involved in actin-dependent sperm nuclei migration during double fertilization in tobacco and maize Peng, Xiongbo; Yan, Tingting; Sun, Mengxiang Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep43161	journal	February 2017
An imbalanced parental genome ratio affects the development of rice zygotes Toda, Erika; Ohnishi, Yukinosuke; Okamoto, Takashi Journal of Experimental Botany, Vol. 69, Issue 10 https://doi.org/10.1093/jxb/ery094	journal	March 2018
An organ-on-a-chip approach for investigating root-environment interactions in heterogeneous conditions Stanley, Claire E.; Shrivastava, Jagriti; Brugman, Rik New Phytologist https://doi.org/10.1101/126987	journal	April 2017
Emerging roles for microtubules in angiosperm pollen tube growth highlight new research cues Onelli, Elisabetta; Idilli, Aurora I.; Moscatelli, Alessandra Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00051	journal	February 2015
Arabinogalactan Proteins as Interactors along the Crosstalk between the Pollen Tube and the Female Tissues Pereira, Ana M.; Lopes, Ana L.; Coimbra, Sílvia Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.01895	journal	December 2016
Identifying and Engineering Genes for Parthenogenesis in Plants Vijverberg, Kitty; Ozias-Akins, Peggy; Schranz, M. Eric Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00128	journal	February 2019
Life Is Simple—Biologic Complexity Is an Epiphenomenon Torday, John Biology, Vol. 5, Issue 2 https://doi.org/10.3390/biology5020017	journal	April 2016
Calcium: A Critical Factor in Pollen Germination and Tube Elongation Zheng, Ren; Su, Shun; Xiao, Hui International Journal of Molecular Sciences, Vol. 20, Issue 2 https://doi.org/10.3390/ijms20020420	journal	January 2019
The beginning of a seed: regulatory mechanisms of double fertilization Dresselhaus, Thomas; Bleckmann, Andrea; Alter, Svenja Universität Regensburg https://doi.org/10.5283/epub.31414	text	January 2014
Knockin' on pollen's door: live cell imaging of early polarization events in germinating Arabidopsis pollen Vogler, Frank; Konrad, Sebastian S. A.; Sprunck, Stefanie Universität Regensburg https://doi.org/10.5283/epub.31780	text	January 2015
New advances and future directions in plant polyspermy Tekleyohans, Dawit G.; Groß‐Hardt, Rita Molecular Reproduction and Development, Vol. 87, Issue 3 https://doi.org/10.1002/mrd.23261	journal	March 2020
Polyspermy in angiosperms: Its contribution to polyploid formation and speciation Toda, Erika; Okamoto, Takashi Molecular Reproduction and Development, Vol. 87, Issue 3 https://doi.org/10.1002/mrd.23295	journal	March 2020
Generation of a homozygous fertilization-defective gcs1 mutant by heat-inducible removal of a rescue gene Nagahara, Shiori; Takeuchi, Hidenori; Higashiyama, Tetsuya Plant Reproduction, Vol. 28, Issue 1 https://doi.org/10.1007/s00497-015-0256-4	journal	February 2015
Mechanisms of endosperm initiation Hands, Philip; Rabiger, David S.; Koltunow, Anna Plant Reproduction, Vol. 29, Issue 3 https://doi.org/10.1007/s00497-016-0290-x	journal	July 2016
Calcium controls the formation of vacuoles from mitochondria to regulate microspore development in wheat Li, Dong Xiao; Hu, Hai Yan; Li, Gan Plant Reproduction, Vol. 30, Issue 3 https://doi.org/10.1007/s00497-017-0309-y	journal	September 2017
Cytosolic calcium localization and dynamics during early endosperm development in the genus Agave (Asparagales, Asparagaceae) Barranco-Guzmán, Angel Martín; González-Gutiérrez, Alejandra G.; Rout, Nutan Prasad Protoplasma, Vol. 256, Issue 4 https://doi.org/10.1007/s00709-019-01366-2	journal	March 2019
Advances in the study of egg activation of higher plants Peng, Li; Li, Zhen Kai; Ding, Xiao Li Zygote, Vol. 26, Issue 6 https://doi.org/10.1017/s0967199418000539	journal	December 2018
MATRILINEAL, a sperm-specific phospholipase, triggers maize haploid induction Kelliher, Timothy; Starr, Dakota; Richbourg, Lee Nature, Vol. 542, Issue 7639 https://doi.org/10.1038/nature20827	journal	January 2017
Live imaging of calcium spikes during double fertilization in Arabidopsis Hamamura, Yuki; Nishimaki, Moe; Takeuchi, Hidenori Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5722	journal	August 2014
Calcium signalling mediates self-incompatibility response in the Brassicaceae Iwano, Megumi; Ito, Kanae; Fujii, Sota Nature Plants, Vol. 1, Issue 9 https://doi.org/10.1038/nplants.2015.128	journal	September 2015
Calcium signals are necessary to establish auxin transporter polarity in a plant stem cell niche Li, Ting; Yan, An; Bhatia, Neha Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08575-6	journal	February 2019
Gamete fusion is facilitated by two sperm cell-expressed DUF679 membrane proteins Cyprys, Philipp; Lindemeier, Maria; Sprunck, Stefanie Nature Plants, Vol. 5, Issue 3 https://doi.org/10.1038/s41477-019-0382-3	journal	March 2019
Insights into secrets along the pollen tube pathway in need to be discovered Lopes, Ana Lúcia; Moreira, Diana; Ferreira, Maria João Journal of Experimental Botany, Vol. 70, Issue 11 https://doi.org/10.1093/jxb/erz087	journal	March 2019
Sperm Entry into the Egg Cell Induces the Progression of Karyogamy in Rice Zygotes Ohnishi, Yukinosuke; Kokubu, Iwao; Kinoshita, Tetsu Plant and Cell Physiology, Vol. 60, Issue 8 https://doi.org/10.1093/pcp/pcz077	journal	May 2019
CrRLK1L receptor-like kinases HERCULES RECEPTOR KINASE 1 and ANJEA are female determinants of pollen tube reception Galindo-Trigo, Sergio; Blanco-Touriñán, Noel; DeFalco, Thomas A. BioRxiv https://doi.org/10.1101/428854	posted_content	January 2019
Pollen tube-triggered accumulation of NORTIA at the filiform apparatus facilitates fertilization in Arabidopsis thaliana Yuan, Jing; Ju, Yan; Jones, Daniel S. BioRxiv https://doi.org/10.1101/621599	posted_content	January 2020
Calcium imaging in Arabidopsis pollen cells using G-CaMP5: Calcium imaging in Arabidopsis pollen cells Diao, Min; Qu, Xiaolu; Huang, Shanjin Journal of Integrative Plant Biology, Vol. 60, Issue 9 https://doi.org/10.1111/jipb.12642	journal	April 2018
Dual-flow-RootChip reveals local adaptations of roots towards environmental asymmetry at the physiological and genetic levels Stanley, Claire E.; Shrivastava, Jagriti; Brugman, Rik New Phytologist, Vol. 217, Issue 3 https://doi.org/10.1111/nph.14887	journal	November 2017
Advances and current challenges in calcium signaling Kudla, Jörg; Becker, Dirk; Grill, Erwin New Phytologist, Vol. 218, Issue 2 https://doi.org/10.1111/nph.14966	journal	January 2018
Elucidating the roles of three β-glucuronosyltransferases (GLCATs) acting on arabinogalactan-proteins using a CRISPR-Cas9 multiplexing approach in Arabidopsis Zhang, Yuan; Held, Michael A.; Showalter, Allan M. BMC Plant Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s12870-020-02420-5	journal	May 2020
Cr RLK 1L receptor‐like kinases HERK 1 and ANJEA are female determinants of pollen tube reception Galindo‐Trigo, Sergio; Blanco‐Touriñán, Noel; DeFalco, Thomas A. EMBO reports, Vol. 21, Issue 2 https://doi.org/10.15252/embr.201948466	journal	December 2019
The beginning of a seed: regulatory mechanisms of double fertilization Bleckmann, Andrea; Alter, Svenja; Dresselhaus, Thomas Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00452	journal	September 2014
Identifying and Engineering Genes for Parthenogenesis in Plants Vijverberg, Kitty; Ozias-Akins, Peggy; Schranz, M. Eric Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00128	journal	February 2019
Calcium: A Critical Factor in Pollen Germination and Tube Elongation Zheng, Ren; Su, Shun; Xiao, Hui International Journal of Molecular Sciences, Vol. 20, Issue 2 https://doi.org/10.3390/ijms20020420	journal	January 2019
The beginning of a seed: regulatory mechanisms of double fertilization Dresselhaus, Thomas; Bleckmann, Andrea; Alter, Svenja Universität Regensburg https://doi.org/10.5283/epub.31414	text	January 2014

Similar Records

Transporters involved in pH and K⁺ homeostasis affect pollen wall formation, male fertility, and embryo development

Journal Article · Wed Feb 22 19:00:00 EST 2017 · Journal of Experimental Botany · OSTI ID:1351083

Padmanaban, Senthilkumar; Czerny, Daniel D.; Levin, Kara A.; +8 more

The SEEL motif and members of the MYB-related REVEILLE transcription factor family are important for the expression of LORELEI in the synergid cells of the Arabidopsis female gametophyte

Journal Article · Thu Oct 28 20:00:00 EDT 2021 · Plant Reproduction · OSTI ID:1845902

Noble, Jennifer A.; Seddon, Alex; Uygun, Sahra; +4 more

Polarized $\mathrm{NORTIA}$ accumulation in response to pollen tube arrival at synergids promotes fertilization

Journal Article · Tue Oct 19 20:00:00 EDT 2021 · Developmental Cell · OSTI ID:1977064

Ju, Yan; Yuan, Jing; Jones, Daniel S.; +3 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Science & Technology - Other Topics

Title: Male–female communication triggers calcium signatures during fertilization in Arabidopsis

Citation Formats

References (119)

Cited By (41)

Similar Records

Related Subjects