Polarized tip growth is a fundamental cellular process in many eukaryotic organisms, mediating growth of neuronal axons and dendrites1 or fungal hyphae2. In plants, pollen and root hairs are cellular model systems for analysing tip growth3,4,5. Cell growth depends on membrane traffic. The regulation of this membrane traffic is largely unknown for tip-growing cells, in contrast to cells exhibiting intercalary growth. Here we show that in Arabidopsis, GBF1-related exchange factors for the ARF GTPases (ARF GEFs) GNOM and GNL2 play essential roles in polar tip growth of root hairs and pollen, respectively. When expressed from the same promoter, GNL2 (in contrast to the early-secretory ARF GEF GNL1) is able to replace GNOM in polar recycling of the auxin efflux regulator PIN1 from endosomes to the basal plasma membrane in non-tip growing cells. Thus, polar recycling facilitates polar tip growth, and GNL2 seems to have evolved to meet the specific requirement of fast-growing pollen in higher plants.
Subscribe to Journal
Get full journal access for 1 year
only $17.42 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Tang, B. L. Emerging aspects of membrane traffic in neuronal dendrite growth. Biochim. Biophys. Acta 1783, 169–176 (2008).
Steinberg, G. Hyphal growth: a tale of motors, lipids, and the Spitzenkorper. Eukaryot. Cell 6, 351–360 (2007).
Hepler, P. K., Vidali, L. & Cheung, A. Y. Polarized cell growth in higher plants. Annu. Rev. Cell Dev. Biol. 17, 159–187 (2001).
Campanoni, P. & Blatt, M. R. Membrane trafficking and polar growth in root hairs and pollen tubes. J. Exp. Bot. 58, 65–74 (2007).
Ovecka, M. et al. Endocytosis and vesicle trafficking during tip growth of root hairs. Protoplasma 226, 39–54 (2005).
Carol, R. J. & Dolan, L. Building a hair: tip growth in Arabidopsis thaliana root hairs. Phil. Trans. R. Soc. Lond. B 357, 815–821 (2002).
Zhang, Y. & McCormick, S. The regulation of vesicle trafficking by small GTPases and phospholipids during pollen tube growth. Sex. Plant Reprod. 23, 87–93 (2010).
Geldner, N. et al. The Arabidopsis GNOM ARF-GEF mediates endosomalrecycling, auxin transport, and auxin-dependent plant growth. Cell 112, 219–230 (2003).
Renault, L., Guibert, B. & Cherfils, J. Structural snapshots of the mechanismand inhibition of a guanine nucleotide exchange factor. Nature 426, 525–530 (2003).
Richter, S. et al. Functional diversification of closely related ARF-GEFs in protein secretion and recycling. Nature 448, 488–492 (2007).
Teh, O. K. & Moore, I. An ARF-GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature 448, 493–496 (2007).
Fischer, U. et al. Vectorial information for Arabidopsis planar polarity ismediated by combined AUX1, EIN2, and GNOM activity. Curr. Biol. 16, 2143–2149 (2006).
Bove, J. et al. Magnitude and direction of vesicle dynamics in growing pollen tubes using spatiotemporal image correlation spectroscopy and fluorescence recovery after photobleaching. Plant Physiol. 147, 1646–1658 (2008).
Derksen, J. et al. Quantitative analysis of the distribution of organelles in tobacco pollen tubes: implications for exocytosis and endocytosis. Protoplasma 188, 267–276 (1995).
Zonia, L. & Munnik, T. Vesicle trafficking dynamics and visualization of zones of exocytosis and endocytosis in tobacco pollen tubes. J. Exp. Bot. 59, 861–873 (2008).
Moscatelli, A. & Idilli, A. I. Pollen tube growth: a delicate equilibrium between secretory and endocytic pathways. J. Integr. Plant Biol. 51, 727–739 (2009).
Wang, Q. et al. Effects of brefeldin A on pollen germination and tube growth. Antagonistic effects on endocytosis and secretion. Plant Physiol. 139, 1692–1703 (2005).
Honys, D. & Twell, D. Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol. 5, R85.1–R85.13 (2004).
Parton, R. M., Fischer-Parton, S., Watahiki, M. K. & Trewavas, A. J. Dynamics of the apical vesicle accumulation and the rate of growth are related in individual pollen tubes. J. Cell Sci. 114, 2685–2695 (2001).
Mayer, U., Büttner, G. & Jürgens, G. Apical-basal pattern formation in the Arabidopsis embryo: studies on the role of the gnom gene. Development 117, 149–162 (1993).
Jia, D. J. et al. GNOM-LIKE 2, encoding an adenosine diphosphate-ribosylation factor-guanine nucleotide exchange factor protein homologous to GNOM and GNL1, is essential for pollen germination in Arabidopsis. J. Integr. Plant Biol. 51, 762–773 (2009).
Anders, N. et al. Membrane association of the Arabidopsis ARF exchange factor GNOM involves interaction of conserved domains. Plant Cell 20, 142–151 (2008).
Naramoto, S. et al. ADP-ribosylation factor machinery mediates endocytosis in plant cells. Proc. Natl Acad. Sci. USA 107, 21890–21895 (2010).
Geldner, N. et al. Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis. Development 131, 389–400 (2004).
Szumlanski, A. L. & Nielsen, E. The Rab GTPase RabA4d regulates pollen tube tip growth in Arabidopsis thaliana. Plant Cell 21, 526–544 (2009).
Hou, W., Chang, W. & Jiang, C. Qualitative distinction of carboxyl group distributions in pectins with ruthenium red. Bot. Bull. Acad. Sin. 40, 115–119 (1999).
Preuss, D., Rhee, S. Y. & Davis, R. W. Tetrad analysis possible inArabidopsis with mutation of the QUARTET (QRT) genes. Science 264, 1458–1460 (1994).
Rutherford, S. & Moore, I. The Arabidopsis Rab GTPase family: another enigma variation. Curr. Opin. Plant Biol. 5, 518–528 (2002).
Geldner, N. et al. Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J. 59, 169–178 (2009).
Zhang, Y., He, J., Lee, D. & McCormick, S. Interdependence of endomembrane trafficking and actin dynamics during polarized growth of Arabidopsis pollen tubes. Plant Physiol. 152, 2200–2210 (2010).
Kang, B. H., Nielsen, E., Preuss, M. L., Mastronarde, D. & Staehelin, L. A. Electron tomography of RabA4b- and PI-4K β1-labeled trans Golgi network compartments in Arabidopsis. Traffic 12, 313–329 (2011).
Dhonukshe, P. et al. Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 456, 962–966 (2008).
Reichardt, I. et al. Mechanisms of functional specificity among plasma-membrane syntaxins in Arabidopsis. Traffic 12, 1269–1280 (2011).
Rudall, P. J. & Bateman, R. M. Developmental bases for key innovations in the seed-plant microgametophyte. Trends Plant Sci. 12, 317–326 (2007).
Rios, G. et al. Rapid identification of Arabidopsis insertion mutants by non-radioactive detection of T-DNA tagged genes. Plant J. 32, 243–253 (2002).
Takada, S. & Jürgens, G. Transcriptional regulation of epidermal cell fate in the Arabidopsis embryo. Development 134, 1141–1150 (2007).
Lauber, M. H. et al. The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J. Cell Biol. 139, 1485–1493 (1997).
Müller, A. et al. AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 17, 6903–6911 (1998).
Boavida, L. C. & McCormick, S. Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J. 52, 570–582 (2007).
Heslop-Harrison, J. & Heslop-Harrison, Y. Evaluation of pollen viability by enzymatically induced fluorescence; intracellular hydrolysis of fluorescein diacetate. Stain Technol. 45, 115–120 (1970).
Reichardt, I. et al. Plant cytokinesis requires de novo secretory trafficking but not endocytosis. Curr. Biol. 17, 2047–2053 (2007).
Preuss, M. L., Serna, J., Falbel, T. G., Bednarek, S. Y. & Nielsen, E. The Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells. Plant Cell 16, 1589–1603 (2004).
Huson, D. H. et al. Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinform. 8, 460.1–460.6 (2007).
We thank J. Keicher, R. Gavidia and B. Maier for technical assistance, C. Knöll for formatting of data files, D. G. Robinson and S. McCormick for providing materials and members of the laboratory for critical reading of the manuscript. This work was financially supported by the Deutsche Forschungsgemeinschaft through SFB 446 (TP A9).
The authors declare no competing financial interests.
Supplementary Information (PDF 1105 kb)
Supplementary Information (MOV 1267 kb)
Supplementary Information (XLS 19 kb)
Supplementary Information (XLS 56 kb)
Supplementary Information (XLS 34 kb)
About this article
Cite this article
Richter, S., Müller, L., Stierhof, YD. et al. Polarized cell growth in Arabidopsis requires endosomal recycling mediated by GBF1-related ARF exchange factors. Nat Cell Biol 14, 80–86 (2012). https://doi.org/10.1038/ncb2389
Microscopy Research and Technique (2020)
Progress in using chemical biology as a tool to uncover novel regulators of plant endomembrane trafficking
Current Opinion in Plant Biology (2019)
Regulatory role of Golgi brefeldin A resistance factor‐1 in amyloid precursor protein trafficking, cleavage and Aβ formation
Journal of Cellular Biochemistry (2019)
Journal of Integrative Plant Biology (2019)
Seminars in Cell & Developmental Biology (2018)