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.


Logo for

PLANT CELL 13 (12): 2841-2856

Copyright © 2001 by the American Society of Plant Physiologists.

A Genome-Wide Analysis of Arabidopsis Rop-Interactive CRIB Motif–Containing Proteins That Act as Rop GTPase Targets

Guang Wu1, Ying Gu1, Shundai Li, and Zhenbiao Yang2

Department of Botany and Plant Sciences, University of California, Riverside, California 92521

2 To whom correspondence should be addressed. E-mail zhenbiao.yang{at}; fax 909-787-4437

Abstract: The plant-specific Rop family GTPases are versatile molecular switches in many processes during plant growth, development, and responses to the environment. To understand how Rop achieves its functional versatility in signaling, we performed a genome-wide identification of putative Rop targets using a combination of the yeast two-hybrid method, bioinformatic tools, and a robust functional assay in pollen. In this study, we have identified 11 Arabidopsis genes encoding novel proteins, termed RICs (for Rop-interactive CRIB motif–containing proteins), that contain a CRIB (for Cdc42/Rac-interactive binding) motif required for their specific interaction with GTP-bound Rop1. RICs are divergent and classified into five groups that share little sequence homology outside of the conserved Rop-interactive domain. Overexpression in tobacco pollen tubes of the nine Ric genes that are expressed in Arabidopsis pollen causes distinct phenotypes, implying distinct functions for various RICs. RIC3 (group III) and RIC4 (group V) both cause depolarized growth like Rop1 and display Rop1-enhanced localization to the tip of pollen tubes, suggesting that these RICs may be two distinct targets of Rop1. In contrast, RIC10 (group I) promotes pollen tube elongation but does not affect pollen tube growth polarity and shows Rop1-independent localization to the cytoplasm, suggesting that RIC10 may participate in a Rop1-independent pathway probably controlled by a different Rop. Expression of all other RICs causes various degrees of growth inhibition in pollen tubes. Furthermore, these inhibitory RICs also exhibit distinct patterns of localization in pollen tubes. Our results suggest that various RICs have evolved to interact with Rops differentially and to perform distinct functions in pollen tubes. Reverse transcriptase–mediated polymerase chain reaction analysis showed that six of the nine RICs are expressed in various parts of Arabidopsis plants. On the basis of these observations, we propose that RICs function as Rop GTPase targets that control various Rop-dependent signaling pathways in plants.

The juxtamembrane and carboxy-terminal domains of Arabidopsis PRK2 are critical for ROP-induced growth in pollen tubes.
X.-Y. Zhao, Q. Wang, S. Li, F.-R. Ge, L.-Z. Zhou, S. McCormick, and Y. Zhang (2013)
J. Exp. Bot. 64, 5599-5610
   Abstract »    Full Text »    PDF »
Flower Development under Drought Stress: Morphological and Transcriptomic Analyses Reveal Acute Responses and Long-Term Acclimation in Arabidopsis.
Z. Su, X. Ma, H. Guo, N. L. Sukiran, B. Guo, S. M. Assmann, and H. Ma (2013)
PLANT CELL 25, 3785-3807
   Abstract »    Full Text »    PDF »
CPK3-phosphorylated RhoGDI1 is essential in the development of Arabidopsis seedlings and leaf epidermal cells.
Y. Wu, S. Zhao, H. Tian, Y. He, W. Xiong, L. Guo, and Y. Wu (2013)
J. Exp. Bot. 64, 3327-3338
   Abstract »    Full Text »    PDF »
Signaling in Pollen Tube Growth: Crosstalk, Feedback, and Missing Links.
Y. Guan, J. Guo, H. Li, and Z. Yang (2013)
Mol Plant 6, 1053-1064
   Abstract »    Full Text »    PDF »
AtPRK2 Promotes ROP1 Activation via RopGEFs in the Control of Polarized Pollen Tube Growth.
F. Chang, Y. Gu, H. Ma, and Z. Yang (2013)
Mol Plant 6, 1187-1201
   Abstract »    Full Text »    PDF »
The C-Terminal Hypervariable Domain Targets Arabidopsis ROP9 to the Invaginated Pollen Tube Plasma Membrane.
S. Li, L.-Z. Zhou, Q.-N. Feng, S. McCormick, and Y. Zhang (2013)
Mol Plant 6, 1362-1364
   Full Text »    PDF »
RNA-Seq of Arabidopsis Pollen Uncovers Novel Transcription and Alternative Splicing.
A. E. Loraine, S. McCormick, A. Estrada, K. Patel, and P. Qin (2013)
Plant Physiology 162, 1092-1109
   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 »
Barley ROP Binding Kinase1 Is Involved in Microtubule Organization and in Basal Penetration Resistance to the Barley Powdery Mildew Fungus.
C. Huesmann, T. Reiner, C. Hoefle, J. Preuss, M. E. Jurca, M. Domoki, A. Feher, and R. Huckelhoven (2012)
Plant Physiology 159, 311-320
   Abstract »    Full Text »    PDF »
A Barley ROP GTPase ACTIVATING PROTEIN Associates with Microtubules and Regulates Entry of the Barley Powdery Mildew Fungus into Leaf Epidermal Cells.
C. Hoefle, C. Huesmann, H. Schultheiss, F. Bornke, G. Hensel, J. Kumlehn, and R. Huckelhoven (2011)
PLANT CELL 23, 2422-2439
   Abstract »    Full Text »    PDF »
RAC/ROP GTPases and Auxin Signaling.
H.-m. Wu, O. Hazak, A. Y. Cheung, and S. Yalovsky (2011)
PLANT CELL 23, 1208-1218
   Abstract »    Full Text »    PDF »
Differential Effects of Prenylation and S-Acylation on Type I and II ROPS Membrane Interaction and Function.
N. Sorek, O. Gutman, E. Bar, M. Abu-Abied, X. Feng, M. P. Running, E. Lewinsohn, N. Ori, E. Sadot, Y. I. Henis, et al. (2011)
Plant Physiology 155, 706-720
   Abstract »    Full Text »    PDF »
Rop GTPase and Its Target Cdc42/Rac-Interactive-Binding Motif-Containing Protein Genes Respond to Desiccation during Pollen Maturation.
S.-W. Hsu, C.-L. Cheng, T.-C. J. Tzen, and C.-S. Wang (2010)
Plant Cell Physiol. 51, 1197-1209
   Abstract »    Full Text »    PDF »
Physcomitrella patens: a model to investigate the role of RAC/ROP GTPase signalling in tip growth.
D. M. Eklund, E. M. Svensson, and B. Kost (2010)
J. Exp. Bot.
   Abstract »    Full Text »    PDF »
Interdependence of Endomembrane Trafficking and Actin Dynamics during Polarized Growth of Arabidopsis Pollen Tubes.
Y. Zhang, J. He, D. Lee, and S. McCormick (2010)
Plant Physiology 152, 2200-2210
   Abstract »    Full Text »    PDF »
Pollen-tube tip growth requires a balance of lateral propagation and global inhibition of Rho-family GTPase activity.
J.-U. Hwang, G. Wu, A. Yan, Y.-J. Lee, C. S. Grierson, and Z. Yang (2010)
J. Cell Sci. 123, 340-350
   Abstract »    Full Text »    PDF »
Oscillatory Growth in Lily Pollen Tubes Does Not Require Aerobic Energy Metabolism.
C. M. Rounds, P. K. Hepler, S. J. Fuller, and L. J. Winship (2010)
Plant Physiology 152, 736-746
   Abstract »    Full Text »    PDF »
Calcium participates in feedback regulation of the oscillating ROP1 Rho GTPase in pollen tubes.
A. Yan, G. Xu, and Z.-B. Yang (2009)
PNAS 106, 22002-22007
   Abstract »    Full Text »    PDF »
Organelle motility in the pollen tube: a tale of 20 years.
G. Cai and M. Cresti (2009)
J. Exp. Bot. 60, 495-508
   Abstract »    Full Text »    PDF »
Evaluating the microtubule cytoskeleton and its interacting proteins in monocots by mining the rice genome.
L. Guo, C.-M. K. Ho, Z. Kong, Y.-R. J. Lee, Q. Qian, and B. Liu (2009)
Ann. Bot. 103, 387-402
   Abstract »    Full Text »    PDF »
RIP1 (ROP Interactive Partner 1)/ICR1 Marks Pollen Germination Sites and May Act in the ROP1 Pathway in the Control of Polarized Pollen Growth.
S. Li, Y. Gu, A. Yan, E. Lord, and Z.-B. Yang (2008)
Mol Plant 1, 1021-1035
   Abstract »    Full Text »    PDF »
Rho-GTPase-dependent filamentous actin dynamics coordinate vesicle targeting and exocytosis during tip growth.
Y. J. Lee, A. Szumlanski, E. Nielsen, and Z. Yang (2008)
J. Cell Biol. 181, 1155-1168
   Abstract »    Full Text »    PDF »
Regulation of Membrane Trafficking, Cytoskeleton Dynamics, and Cell Polarity by ROP/RAC GTPases.
S. Yalovsky, D. Bloch, N. Sorek, and B. Kost (2008)
Plant Physiology 147, 1527-1543
   Full Text »    PDF »
The Arabidopsis Small G Protein ROP2 Is Activated by Light in Guard Cells and Inhibits Light-Induced Stomatal Opening.
B. W. Jeon, J.-U. Hwang, Y. Hwang, W.-Y. Song, Y. Fu, Y. Gu, F. Bao, D. Cho, J. M. Kwak, Z. Yang, et al. (2008)
PLANT CELL 20, 75-87
   Abstract »    Full Text »    PDF »
Identification of Novel Membrane-binding Domains in Multiple Yeast Cdc42 Effectors.
S. Takahashi and P. M. Pryciak (2007)
Mol. Biol. Cell 18, 4945-4956
   Abstract »    Full Text »    PDF »
NADPH oxidase-dependent reactive oxygen species formation required for root hair growth depends on ROP GTPase.
M. A. Jones, M. J. Raymond, Z. Yang, and N. Smirnoff (2007)
J. Exp. Bot. 58, 1261-1270
   Abstract »    Full Text »    PDF »
Tobacco RhoGTPase ACTIVATING PROTEIN1 Spatially Restricts Signaling of RAC/Rop to the Apex of Pollen Tubes.
U. Klahre and B. Kost (2006)
PLANT CELL 18, 3033-3046
   Abstract »    Full Text »    PDF »
Petunia Phospholipase C1 Is Involved in Pollen Tube Growth.
P. E. Dowd, S. Coursol, A. L. Skirpan, T.-h. Kao, and S. Gilroy (2006)
PLANT CELL 18, 1438-1453
   Abstract »    Full Text »    PDF »
Members of a Novel Class of Arabidopsis Rho Guanine Nucleotide Exchange Factors Control Rho GTPase-Dependent Polar Growth.
Y. Gu, S. Li, E. M. Lord, and Z. Yang (2006)
PLANT CELL 18, 366-381
   Abstract »    Full Text »    PDF »
Cinnamoyl-CoA reductase, a key enzyme in lignin biosynthesis, is an effector of small GTPase Rac in defense signaling in rice.
T. Kawasaki, H. Koita, T. Nakatsubo, K. Hasegawa, K. Wakabayashi, H. Takahashi, K. Umemura, T. Umezawa, and K. Shimamoto (2006)
PNAS 103, 230-235
   Abstract »    Full Text »    PDF »
Oscillatory ROP GTPase Activation Leads the Oscillatory Polarized Growth of Pollen Tubes.
J.-U. Hwang, Y. Gu, Y.-J. Lee, and Z. Yang (2005)
Mol. Biol. Cell 16, 5385-5399
   Abstract »    Full Text »    PDF »
RAC GTPases in Tobacco and Arabidopsis Mediate Auxin-Induced Formation of Proteolytically Active Nuclear Protein Bodies That Contain AUX/IAA Proteins.
L.-z. Tao, A. Y. Cheung, C. Nibau, and H.-m. Wu (2005)
PLANT CELL 17, 2369-2383
   Abstract »    Full Text »    PDF »
A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes.
Y. Gu, Y. Fu, P. Dowd, S. Li, V. Vernoud, S. Gilroy, and Z. Yang (2005)
J. Cell Biol. 169, 127-138
   Abstract »    Full Text »    PDF »
New Views on the Plant Cytoskeleton.
G. O. Wasteneys and Z. Yang (2004)
Plant Physiology 136, 3884-3891
   Full Text »    PDF »
Interchangeable functions of Arabidopsis PIROGI and the human WAVE complex subunit SRA1 during leaf epidermal development.
D. Basu, S. E.-D. El-Assal, J. Le, E. L. Mallery, and D. B. Szymanski (2004)
Development 131, 4345-4355
   Abstract »    Full Text »    PDF »
Pollen and Stigma Structure and Function: The Role of Diversity in Pollination.
A. F. Edlund, R. Swanson, and D. Preuss (2004)
PLANT CELL 16, S84-S97
   Full Text »    PDF »
Conserved Subgroups and Developmental Regulation in the Monocot rop Gene Family.
T. M. Christensen, Z. Vejlupkova, Y. K. Sharma, K. M. Arthur, J. W. Spatafora, C. A. Albright, R. B. Meeley, J. P. Duvick, R. S. Quatrano, and J. E. Fowler (2003)
Plant Physiology 133, 1791-1808
   Abstract »    Full Text »
Analysis of the Small GTPase Gene Superfamily of Arabidopsis.
V. Vernoud, A. C. Horton, Z. Yang, and E. Nielsen (2003)
Plant Physiology 131, 1191-1208
   Abstract »    Full Text »    PDF »
Adhesion and guidance in compatible pollination.
E. M. Lord (2003)
J. Exp. Bot. 54, 47-54
   Abstract »    Full Text »    PDF »
Regulation of pollen tube growth by Rac-like GTPases.
A. Y. Cheung, C. Y-h. Chen, L.-z. Tao, T. Andreyeva, D. Twell, and H.-m. Wu (2003)
J. Exp. Bot. 54, 73-81
   Abstract »    Full Text »    PDF »
ROP GTPase regulation of pollen tube growth through the dynamics of tip-localized F-actin.
Y. Gu, V. Vernoud, Y. Fu, and Z. Yang (2003)
J. Exp. Bot. 54, 93-101
   Abstract »    Full Text »    PDF »
Plant Reproduction: Insights into the "Abominable Mystery".
N. A. Eckardt (2002)
PLANT CELL 14, 1669-1673
   Full Text »    PDF »
RopGAP4-Dependent Rop GTPase Rheostat Control of Arabidopsis Oxygen Deprivation Tolerance.
A. Baxter-Burrell, Z. Yang, P. S. Springer, and J. Bailey-Serres (2002)
Science 296, 2026-2028
   Abstract »    Full Text »    PDF »
Small GTPases: Versatile Signaling Switches in Plants.
Z. Yang (2002)
PLANT CELL 14, S375-S388
   Full Text »    PDF »

To Advertise     Find Products

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