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Editorial
Membrane Trafficking: Intracellular Highways and
Country Roads
Membrane trafficking, or the flow of membrane
material between endomembrane compartments and
the plasmalemma, is essential for transport of proteins
and other macromolecules to various destinations inside
and outside of the cell. Membrane trafficking also underlies the fundamental need for cells to maintain cellular
homeostasis, as well as to meet specific demands
during signal perception and transduction. The pathways of membrane protein trafficking, starting from
the endoplasmic reticulum (ER), are long, branched,
and occasionally even bidirectional. The blueprint of
the endomembrane system is conserved among eukaryotes and comprises the ER, the Golgi apparatus,
endosomes, and lytic compartments. The plant endomembrane system is apparently considerably more
complex than in unicellular yeasts; the highly expanded protein repertoire devoted to the endomembrane system and vesicular processes inferred from
plant genomes as well as its divergence from other
kingdoms would argue for a system that has evolved
to serve cellular strategies that best support the plant
cell. The biosynthetic functions in the ER and Golgi
are followed by sorting at the Golgi apparatus for
antero-trafficking to the cell membrane or to lytic or
storage vacuoles and retrograde trafficking back to the
ER. Constitutive and signal-regulated endocytosis at
the plasmalemma is followed by transport to the lytic
vacuole or to the Golgi for sorting and recycling.
Voluminous studies have been devoted in past decades to structurally and biochemically characterize
the different endomembrane compartments and the
processes each undertakes in overall cellular metabolism. Arrival of the post-genomic era, together with
development of microscopic and computational tools
in the last decade, has resulted in an explosion of
studies, some reaffirming classical understanding,
others uncovering new insights on the membrane
trafficking machinery in plant cells as well as the
cellular processes and whole plant-related phenomena
that the endomembrane system supports. This Focus
Issue is organized to provide both Updates and exciting
new research articles on these recent findings and
suggest paths to chart the future.
The Updates have been written by small teams of
scientists who have impressive track records in their
specific fields and they span a broad spectrum of
topics central to membrane trafficking. The Staehelin
and Kang (2008) Update reviews state-of-the-art, highresolution capabilities in obtaining structural definitions in three dimensions for individual organelles
and, in particular, reconstruction of organelles that are
www.plantphysiol.org/cgi/doi/10.1104/pp.104.900266
undergoing dynamic changes. This is followed by the
Held et al. (2008) Update on the prowess of what
combinations of fluorescence-based microscope and
live cell imaging can achieve for spatial and functional
assignments for specific molecules within the entire
endomembrane system. The Rojo and Denecke (2008)
and Robinson et al. (2008) Updates examine the most
recently defined players in the secretory and endosomal pathways and how these may be used to
interpret, reconcile, or extend prior results. These
provide good roadmaps, especially for researchers
whose work would benefit from a membrane trafficking perspective.
The involvement of a large number of regulatory
molecules is discussed in the Updates on the small
regulatory RAB and ARF GTPases by Nielsen et al.
(2008), on SNAREs by Bassham and Blatt (2008), and
on Rho GTPases by Yalovsky et al. (2008). Studies in
these areas have advanced so much in the last few
years that these Updates have gone far beyond a
catalog of molecules and their potential functions and
include vigorous discussions on the cellular, physiological, and developmental events that these molecules regulate, how they themselves are regulated, and
how these regulatory pathways may integrate in the
control of vesicular transport.
Several Updates deal with aspects of membrane trafficking from the point of view of a particular physiological process. Kwon et al. (2008) describe recent
findings linking plant immunity to secretion pathways
depositing compounds helping plants to counteract
pathogens. Feraru and Friml (2008) focus on the acquisition of cell polarity by means of controlled deposition of membrane proteins, in particular the PIN
auxin carriers. Here, specificity in the sorting of integral
membrane proteins is evolving as a future topic of
interest. Van Damme et al. (2008) discuss the connections between the cell cycle and membrane trafficking,
while Geldner and Robatzek (2008) as well as Aker and
de Vries (2008) highlight various aspects, including
endocytosis and degradation, of plasma membrane
receptors.
A large number of research manuscripts on different
biological systems and based on a variety of approaches have been submitted to this Focus Issue.
Among the articles in this issue are several studies
based on root hairs and pollen tubes, polar growth cell
types that are favorite model cell systems for studies
in membrane trafficking. Monshausen et al. (2008) and
Bove et al. (2008) highlight the use of imaging approaches combined with computational analysis to
examine Ca21 regulation of root hair growth and
provide spatial definition of exocytic activity in pollen
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Editorial
tubes, respectively. Yoo et al. (2008) emphasize the use
of genetics to elucidate how a regulatory aspect of
membrane trafficking affects root hair growth. Wang
et al. (2008), using largely a transient expression approach, examine the involvement of an actin-binding
protein on the regulation of actin and ion dynamics in
elongating pollen tubes. Persia et al. (2008) report on
biochemical studies that examine the localization of
pollen tube sucrose synthase, a key enzyme for cell
wall biosynthesis, and how phosphorylation may
affect its association with the secretory pathway. The
importance of cell wall biosynthesis is also highlighted
in the article by Paredez et al. (2008), which examines
the orientation and stability of the root cortical
microtubules in mutants compromised in cellulose
synthesis. The study of Kaneda et al. (2008) combines
pulse-chase labeling and high-resolution electron microscopy to dissect the delivery pathway of monolignols to the extracellular matrix, which may be
supported by specific membrane transporters rather
than via Golgi-derived vesicles. This implicates diverse strategies in the delivery of biopolymers to the
cell surface.
Several studies explore the functional connection
between structural or regulatory components of
endomembrane compartments and cellular or developmental processes. Li et al. (2008) describe an
endosome-localized Ca21-ATPase and its contribution
to root growth. Konopka and Bednarek (2008) describe
two dynamin-related proteins involved in plasma
membrane maintenance in pollen and stigma cells.
Esseling-Ozdoba et al. (2008) use synthetic fluorescent
lipophilic vesicles to highlight the role of actin in
establishing the cell plate in Tradescantia stamen hair
cells. Lam et al. (2008) study inclusion of material into
the developing cell plate that is secreted by the transGolgi network/early endosomal compartment rather
then from the prevacuolar compartment/multivesicular bodies. Guo and Ho (2008) present a case for the
involvement of the barley (Hordeum vulgare) aleurone
HVA22 protein as a negative regulator of GA-mediated
vacuolation/programmed cell death by means of inhibiting vesicular trafficking.
OUTLOOK
From the Updates as well as the research articles, it
becomes evident that membrane trafficking is a very
active and vigorous area of plant research. We hope
that readers will find this collection of use as a
teaching tool and an important resource for research
in the area. Expected next thrusts in the field are to
mine genomics and transcriptomics databases and to
use state-of-the-art proteomics approaches to identify
structural and regulatory components of the endomembrane system. Examples of this can be found in
the research report of Kamei et al. (2008) on the
combined use of bioinformatics and functional studies
on PRA1, a membrane trafficking regulatory protein,
and in the Groen et al. (2008) Update that reviews
recent advanced proteomics to achieve more precise
organellar assignment for proteins in the endomembrane system. What is emerging from a number of
studies and Updates is that one simply cannot assume
that plant counterparts of yeast or animal endomembrane proteins have the same function. Therefore,
detailed genetic manipulations, biochemical analysis,
and advanced imaging are indispensible to elucidate
the precise biological role of the endomembrane
system and its constituents.
ACKNOWLEDGMENTS
We are very grateful to the authors of the Updates, the numerous reviewers
who were mobilized, and staff members of the Plant Physiology Editorial
Office who efficiently shepherded the entire process.
LITERATURE CITED
Aker J, de Vries SC (2008) Plasma membrane receptor complexes. Plant
Physiol 147: 1560–1564
Bassham DC, Blatt MR (2008) SNAREs: cogs and coordinators in signaling
and development. Plant Physiol 147: 1504–1515
Bove J, Vaillancourt B, Kroeger J, Hepler PK, Wiseman PW, Geitmann A
(2008) 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
Esseling-Ozdoba A, Vos JW, van Lammeren AAM, Emons AMC (2008)
Synthetic lipid (DOPG) vesicles accumulate in the cell plate region but do
not fuse. Plant Physiol 147: 1699–1709
Feraru E, Friml J (2008) PIN polar targeting. Plant Physiol 147: 1553–1559
Geldner N, Robatzek S (2008) Plant receptors go endosomal: a moving view
on signal transduction. Plant Physiol 147: 1565–1574
Groen AJ, de Vries SC, Lilley KS (2008) A proteomics approach to membrane
trafficking. Plant Physiol 147: 1584–1589
Guo W-J, Ho T-HD (2008) An abscisic acid-induced protein, HVA22, inhibits
gibberellin-mediated programmed cell death in cereal aleurone cells. Plant
Physiol 147: 1710–1722
Held MA, Boulaflous A, Brandizzi F (2008) Advances in fluorescent proteinbased imaging for the analysis of plant endomembranes. Plant Physiol 147:
1469–1481
Kamei CLA, Boruc J, Vandepoele K, Van den Daele H, Maes S, Russinova E,
Inzé D, De Veylder L (2008) The PRA1 gene family in Arabidopsis. Plant
Physiol 147: 1735–1749
Kaneda M, Rensing KH, Wong JCT, Banno B, Mansfield SD, Samuels AL
(2008) Tracking monolignols during wood development in lodgepole pine.
Plant Physiol 147: 1750–1760
Konopka CA, Bednarek SY (2008) Comparison of the dynamics and functional redundancy of the Arabidopsis dynamin-related isoforms DRP1A
and DRP1C during plant development. Plant Physiol 147: 1590–1602
Kwon C, Bednarek P, Schulze-Lefert P (2008) Secretory pathways in plant
immune responses. Plant Physiol 147: 1575–1583
Lam SK, Cai Y, Hillmer S, Robinson DG, Jiang L (2008) SCAMPs highlight
the developing cell plate during cytokinesis in tobacco BY-2 cells. Plant
Physiol 147: 1637–1645
Li X, Chanroj S, Wu Z, Romanowsky SM, Harper JF, Sze H (2008) A distinct
endosomal Ca21/Mn21 pump affects root growth through the secretory
process. Plant Physiol 147: 1675–1689
Monshausen GB, Messerli MA, Gilroy S (2008) Imaging of the Yellow
Cameleon 3.6 indicator reveals that elevations in cytosolic Ca21 follow
oscillating increases in growth in root hairs of Arabidopsis. Plant Physiol
147: 1690–1698
Nielsen E, Cheung AY, Ueda T (2008) The regulatory RAB and ARF GTPases
for vesicular trafficking. Plant Physiol 147: 1516–1526
Paredez AR, Persson S, Ehrhardt DW, Somerville CR (2008) Genetic
evidence that cellulose synthase activity influences microtubule cortical
array organization. Plant Physiol 147: 1723–1734
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Editorial
Persia D, Cai G, Del Casino C, Faleri C, Willemse MTM, Cresti M (2008)
Sucrose synthase is associated with the cell wall of tobacco pollen tubes.
Plant Physiol 147: 1603–1618
Robinson DG, Jiang L, Schumacher K (2008) The endosomal system
of plants: charting new and familiar territories. Plant Physiol 147:
1482–1492
Rojo E, Denecke J (2008) What is moving in the secretory pathway of plants?
Plant Physiol 147: 1493–1503
Staehelin LA, Kang B-H (2008) Nanoscale architecture of endoplasmic
reticulum export sites and of Golgi membranes as determined by electron
tomography. Plant Physiol 147: 1454–1468
Van Damme D, Inzé D, Russinova E (2008) Vesicle trafficking during somatic
cytokinesis. Plant Physiol 147: 1544–1552
Wang H-J, Wan A-R, Jauh G-Y (2008) An actin-binding protein, LlLIM1,
mediates calcium and hydrogen regulation of actin dynamics in pollen
tubes. Plant Physiol 147: 1619–1636
Yalovsky S, Bloch D, Sorek N, Kost B (2008) Regulation of membrane
trafficking, cytoskeleton dynamics, and cell polarity by ROP/RAC
GTPases. Plant Physiol 147: 1527–1543
Yoo C-M, Wen J, Motes CM, Sparks JA, Blancaflor EB (2008) A class I ADPribosylation factor GTPase-activating protein is critical for maintaining
directional root hair growth in Arabidopsis. Plant Physiol 147: 1659–1674
Alice Y. Cheung
Sacco C. de Vries
Monitoring Editors
Plant Physiology
Plant Physiol. Vol. 147, 2008
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Copyright © 2008 American Society of Plant Biologists. All rights reserved.