Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Subscribe

Logo for

Development 136 (19): 3279-3288

Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge

Aurélien Boisson-Dernier1,2,*, Sucharita Roy1, Konstantinos Kritsas1, Monica A. Grobei1, Miloslawa Jaciubek1, Julian I. Schroeder2, and Ueli Grossniklaus1,*

1 Institute of Plant Biology and Zürich-Basel Plant Science Center, University of Zürich, Zollikerstrasse 107, 8008 Zürich, Switzerland.
2 Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Molecular Genetics, University of California San Diego, La Jolla, CA 92093, USA.

* Authors for correspondence (aboisson{at}access.uzh.ch; grossnik{at}botinst.uzh.ch)

Accepted for publication 31 July 2009.

Abstract: 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.

Key Words: Gametophyte • Pollen tube • Receptor-like kinase • CrRLK1L • Arabidopsis • Fertilization • Pollination • FERONIA • ANXUR • Discharge

THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
The Arabidopsis general transcription factor TFIIB1 (AtTFIIB1) is required for pollen tube growth and endosperm development.
J.-J. Zhou, Y. Liang, Q.-K. Niu, L.-Q. Chen, X.-Q. Zhang, and D. Ye (2013)
J. Exp. Bot. 64, 2205-2218
   Abstract »    Full Text »    PDF »
Receptor-like kinases as surface regulators for RAC/ROP-mediated pollen tube growth and interaction with the pistil.
Y. Zou, M. Aggarwal, W.-G. Zheng, H.-M. Wu, and A. Y. Cheung (2013)
AoB Plants 2011, plr017
   Abstract »    Full Text »    PDF »
Green love talks; cell-cell communication during double fertilization in flowering plants.
T. Kawashima and F. Berger (2013)
AoB Plants 2011, plr015
   Abstract »    Full Text »    PDF »
Cytoplasmic Ca2+ changes dynamically during the interaction of the pollen tube with synergid cells.
M. Iwano, Q. A. Ngo, T. Entani, H. Shiba, T. Nagai, A. Miyawaki, A. Isogai, U. Grossniklaus, and S. Takayama (2012)
Development 139, 4202-4209
   Abstract »    Full Text »    PDF »
Using maize as a model to study pollen tube growth and guidance, cross-incompatibility and sperm delivery in grasses.
T. Dresselhaus, A. Lausser, and M. L. Marton (2011)
Ann. Bot. 108, 727-737
   Abstract »    Full Text »    PDF »
Female gametophytic cell specification and seed development require the function of the putative Arabidopsis INCENP ortholog WYRD.
O. Kirioukhova, A. J. Johnston, D. Kleen, C. Kagi, R. Baskar, J. M. Moore, H. Baumlein, R. Gross-Hardt, and U. Grossniklaus (2011)
Development 138, 3409-3420
   Abstract »    Full Text »    PDF »
Identification of genes expressed in the angiosperm female gametophyte.
G. N. Drews, D. Wang, J. G. Steffen, K. S. Schumaker, and R. Yadegari (2011)
J. Exp. Bot. 62, 1593-1599
   Abstract »    Full Text »    PDF »
Cysteine-Rich Peptides (CRPs) mediate diverse aspects of cell-cell communication in plant reproduction and development.
E. Marshall, L. M. Costa, and J. Gutierrez-Marcos (2011)
J. Exp. Bot. 62, 1677-1686
   Abstract »    Full Text »    PDF »
The walls have ears: the role of plant CrRLK1Ls in sensing and transducing extracellular signals.
A. Boisson-Dernier, S. A. Kessler, and U. Grossniklaus (2011)
J. Exp. Bot. 62, 1581-1591
   Abstract »    Full Text »    PDF »
ANK6, a mitochondrial ankyrin repeat protein, is required for male-female gamete recognition in Arabidopsis thaliana.
F. Yu, J. Shi, J. Zhou, J. Gu, Q. Chen, J. Li, W. Cheng, D. Mao, L. Tian, B. B. Buchanan, et al. (2010)
PNAS 107, 22332-22337
   Abstract »    Full Text »    PDF »
FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development.
Q. Duan, D. Kita, C. Li, A. Y. Cheung, and H.-M. Wu (2010)
PNAS 107, 17821-17826
   Abstract »    Full Text »    PDF »
FERONIA as an upstream receptor kinase for polar cell growth in plants.
M. M. Kanaoka and K. U. Torii (2010)
PNAS 107, 17461-17462
   Full Text »    PDF »
Monitoring the Outside: Cell Wall-Sensing Mechanisms.
C. Ringli (2010)
Plant Physiology 153, 1445-1452
   Full Text »    PDF »
VERDANDI Is a Direct Target of the MADS Domain Ovule Identity Complex and Affects Embryo Sac Differentiation in Arabidopsis.
L. Matias-Hernandez, R. Battaglia, F. Galbiati, M. Rubes, C. Eichenberger, U. Grossniklaus, M. M. Kater, and L. Colombo (2010)
PLANT CELL 22, 1702-1715
   Abstract »    Full Text »    PDF »
Irritable Walls: The Plant Extracellular Matrix and Signaling.
G. J. Seifert and C. Blaukopf (2010)
Plant Physiology 153, 467-478
   Full Text »    PDF »
Spatial and temporal integration of signalling networks regulating pollen tube growth.
L. Zonia (2010)
J. Exp. Bot.
   Abstract »    Full Text »    PDF »
The pollen tube journey in the pistil and imaging the in vivo process by two-photon microscopy.
A. Y. Cheung, L. C. Boavida, M. Aggarwal, H. M. Wu, and J. A. Feijo (2010)
J. Exp. Bot.
   Abstract »    Full Text »    PDF »
Pollen-pistil interactions regulating successful fertilization in the Brassicaceae.
L. A. Chapman and D. R. Goring (2010)
J. Exp. Bot. 61, 1987-1999
   Abstract »    Full Text »    PDF »
Recent Progress in Plant Reproduction Research: The Story of the Male Gametophyte through to Successful Fertilization.
G. Suzuki (2009)
Plant Cell Physiol. 50, 1857-1864
   Abstract »    Full Text »    PDF »

To Advertise     Find Products

Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882