Download The Plant Endomembrane System—A Complex

The Plant Endomembrane System—A Complex Network
Supporting Plant Development and Physiology
Miyo Terao Morita1,* and Tomoo Shimada2,*
1
Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa, Nagoya, 464-8601 Japan
Department of Botany, Graduate School of Science, Kyoto University, Kyoto, 606-8502 Japan
*Corresponding author: Miyo Terao Morita, E-mail, [email protected]; Fax, +81-52-789-4123; Tomoo Shimada,
E-mail, [email protected]; Fax, +81-75-753-4141.
2
In eukaryotic cells, the endomembrane system is a functionally
inter-related membrane system including the endoplasmic
reticulum (ER), the nuclear envelope, the Golgi apparatus, vacuoles/lysosomes, endosomes, the plasma membrane (PM) and
vesicles. The endomembrane system comprises a complex network of membrane trafficking, which is essential for transport
and exchange of materials such as proteins and lipids. There is
no doubt that membrane trafficking fulfills a fundamental
function, supporting cell proliferation, maintenance of cellular
homeostasis and specific demands for higher order function in
multicellular organisms.
The plant endomembrane system is mostly conserved
amongst all eukaryotes, but also displays some highly complex
and unique characteristics. Homology-based approaches, which
have been greatly supported by the Arabidopsis genome
project, have shaped our understanding of the conserved
framework underlying the plant endomembrane system
(Bassham et al. 2008). In addition, cumulative knowledge
about the genes involved as well as the development of live
cell imaging tools has led to an explosion of studies highlighting
the many diverse plant-specific cellular and developmental
processes, and whole plant-related phenomena that are
supported by the endomembrane system. This Special Focus
Issue presents a further two reviews and 12 research articles
that enhance our understanding of endomembrane function
and dynamics in plants.
Current Trends in Plant Endomembrane
Research
Membrane trafficking pathways are essential for maintaining
fundamental cellular functions as well as for responding to
various environmental stimuli. Recently, the role of membrane
trafficking in plant–microbe interactions has been highlighted.
In the first of two reviews in this issue, Inada and Ueda (2014)
comprehensively describe current understanding of the relationship between membrane trafficking and microbes for
both pathogenic and mutualistic interactions. Together with
superb illustrations, this review provides not only an update on
progress but also valuable insight into future research goals in
this field.
Cell walls perform a number of essential functions in plant
cells, such as providing shape, mechanical strength, an interface
between adjacent cells and resistance under biotic and abiotic
stress conditions. The second review by Kim and Brandizzi (2014)
neatly describes specific key discoveries related to mechanisms
and functions of the secretory pathway in cell wall biogenesis.
Novel Features of the Plant
Endomembrane System
Live cell imaging using appropriate molecular markers has revealed a wealth of information regarding the dynamic nature of
the plant endomembrane. The TGN (trans-Golgi network) functions as a sorting station that directs cargo proteins to a variety of
destinations, including post-Golgi compartments and extracellular spaces. Recent studies have demonstrated that the TGN also
functions as an early endosome (EE) in plant cells (Dettmer et al.
2006, Viotti et al. 2010). In this issue, Uemura et al. (2014) reveal
the dynamic behavior of green fluorescent protein (GFP)–SYP43
(the ortholog of Tlg2/syntaxin 16)-labeled TGN. Using superresolution confocal live imaging microscopy developed by the
authors, two independent types of TGN were identified in
Arabidopsis root cells: the GA-TGN (Golgi-associated TGN),
located on the trans-side of the Golgi apparatus, and the GITGN (Golgi-released independent TGN), located away from
the Golgi apparatus. These results revealed dynamic features of
the TGN in plant cells that differ from those of animal and yeast
cells, and will form the basis of future studies targeted at uncovering further unique functions of the TGN in plant cells.
The structural organization of the endomembrane system is
important for proper membrane trafficking and is fundamental
for plant physiology. To explore the mechanisms regulating
membrane trafficking and endomembrane organization in
plant cells, Uehara et al. (2014) screened Arabidopsis mutants
defective in the localization of GFP–NIP5;1 (nodulin 26-like
Plant Cell Physiol. 55(4): 667–671 (2014) doi:10.1093/pcp/pcu049, available online at www.pcp.oxfordjournals.org
! The Author 2014. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists.
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Plant Cell Physiol. 55(4): 667–671 (2014) doi:10.1093/pcp/pcu049 ! The Author 2014.
667
intrinsic protein). NIP5;1 is a PM-localized boric acid channel
belonging to the major intrinsic protein (aquaporin) family
(Takano et al. 2006). Fluorescence imaging-based screening
led to the isolation of a mutant which accumulated abnormal
intracellular aggregates labeled with GFP–NIP5;1. The responsible gene encodes UDP-glucose 4-epimerase 4 (UGE4), which is
involved in D-galactose biosynthesis, and is required for the
synthesis of the cell wall polysaccharide xyloglucan and arabinogalactan proteins (Seifert et al. 2002). Alleles of UGE4 were
previously identified as root hair defective 1 (rhd1) and root
epidermal bulgar 1 (reb1) mutants, which exhibit defective
root hair development, root morphology and susceptibility to
nematode infection (Schiefelbein and Somerville 1990, Baskin
et al. 1992, Baum et al. 2000). These observations suggest that
UGE4 activity in D-galactose synthesis is required for the structure of cell wall polysaccharides and endomembrane
organization.
Autophagy is a degradation pathway that recycles cell materials upon encountering stress conditions or during specific
developmental processes (Klionsky 2007). The AuTophaGyrelated (ATG) genes that regulate the autophagic process
were initially discovered in yeast (Xie and Klionsky 2007) and
their homologs are well conserved in mammals and plants
(Reumann et al. 2010, Tanida 2011). To better understand
the physiological roles of autophagy in plants, Merkulova
et al. (2014) carefully observed the autophagic process in
planta using different monitoring methods in Arabidopsis
roots. They identified a GFP–ATG8 fusion protein as an excellent tool for monitoring autophagy in plants. In contrast,
acidotropic dyes such as monodansylcadaverine (MDC) and
LysoTracker Red (LTR), which are often used for monitoring
autophagy in mammals and yeast, did not work well in planta.
Furthermore, assessment and optimization of autophagy monitoring methods in Arabidopsis roots provided some evidence
for the direct fusion of autophagosomes with vacuoles
(Merkulova et al. 2014).
Ubiquitination is a post-translational protein modification
that is well conserved among eukaryotic cells (Kerscher et al.
2006). A cascade of E1, E2 and E3 enzymes work together to
conjugate ubiquitin to the target protein, and this modification
can be reversed by the activity of deubiquitinating enzymes.
Recent studies have shown that ubiquitination regulates
endocytosis and the subsequent vacuolar degradation of PM
proteins in plants (Abas et al. 2006, Gohre et al. 2008, Lee et al.
2009, Barberon et al. 2011, Kasai et al. 2011). In this issue,
Katsiarimpa et al. (2014) show that ASSOCIATED MOLECULE
WITH THE SH3 DOMAIN OF STAM 3 (AMSH3) is essential for
degradation of ubiquitinated membrane proteins in
Arabidopsis. AMSH3 is a deubiquitinating enzyme that interacts with the endosomal sorting complex required for transport
(ESCRT)-III machinery (Isono et al., 2010). An enzymatic inactive AMSH3 variant inhibits the AvrPtoB-dependent endocytic
degradation of CERK1 (CHITIN ELICITOR RECEPTOR KINASE
1), and interaction of AMSH3 with ESCRT-III is important for its
function in planta.
668
The Endomembrane System and Plant
Development
The levels and distribution of the plant hormone auxin are
critical in regulating multiple developmental processes in
plants (Mockaitis and Estelle 2008, Vanneste and Friml 2009).
Auxin transporters of the PIN-FORMED (PIN) family localize
asymmetrically at the PM and mediate directional intercellular
auxin transport (Tanaka et al. 2006, Vanneste and Friml 2009).
The subcellular localization of PIN proteins, which is mainly
regulated by vesicle trafficking, is a key determinant of polar
auxin transport. Using a fluorescence imaging-based forward
genetic approach, Tanaka et al. (2014) show that BFAVISUALIZED EXOCYTIC TRAFFICKING DEFECTIVE1 (BEX1) is
required for recycling of PIN transporters and auxin-mediated
development in Arabidopsis. BEX1 encodes a member of the
ADP-ribosylation factor (ARF) small GTPases, ARF1A1C, which
localizes to the TGN/EE and Golgi apparatus. While previous
studies have shown that the ARF guanine nucleotide exchange
factor (GEF), GNOM, plays a major role in localizing PIN1 predominantly to the basal side of the PM (Steinmann et al. 1999),
this study provides new insight into the missing link between
GNOM function and asymmetric PIN1 localization.
Polar auxin transport by PIN1 is required for normal venation patterning (Mattsson et al. 1999, Koizumi et al. 2005).
Similarly, VASCULAR NETWORK DEFECTIVE4 (VAN4) is
required for venation development and cellular growth. In
this issue, Naramoto et al (2014) further demonstrate that
VAN4 encodes a putative TRS120 subunit of the TRAPPII complex protein that functions as a Rab-GEF and/or tethering
factor (Jones et al. 2000, Sacher et al. 2008). Although the importance of VAN4 function in polar localization of PIN proteins
is still ambiguous, VAN4 localizes to the TGN/EE where it appears to be involved in the recycling of PIN proteins. Previous
reports also indicated that VAN3/SFC, ARF-GAP and VAN7/
GNOM ARF-GEF regulate venation pattern by controlling the
activity of the ARF GTPase (Koizumi et al. 2000, Koizumi et al.
2005, Sieburth et al. 2006, Naramoto et al. 2009). Collectively,
these studies provide robust evidence for the importance of
vesicle transport in leaf vascular formation.
Another link between endomembrane trafficking and plant
development was revealed by the analysis of continuous vascular ring (cov1) mutants. Previously, the cov1 mutant was reported to exhibit ectopic differentiation of vascular cells in
the Arabidopsis stem (Parker et al. 2003). In this issue,
Shirakawa et al. (2014) show that COV1 is a TGN-localized
membrane protein that is required for Golgi morphology and
vacuolar protein trafficking. In addition to the vascular patterning, COV1 is also required for the development of myrosin cells
in leaves (Shirakawa et al. 2014). These results highlight the
important relationship between endomembrane trafficking
and plant higher order function, particularly vascular patterning and myrosin cell development. Similar defects in vascular
patterning and myrosin development have been reported in
Arabidopsis syp2 mutants, which lack key components of the
Plant Cell Physiol. 55(4): 667–671 (2014) doi:10.1093/pcp/pcu049 ! The Author 2014.
vacuolar SNARE (soluble N-ethylmaleimide-sensitive factor
attachment protein receptor) (Ueda et al. 2006, Shirakawa
et al. 2010). It is thus possible that trafficking pathways (the
vacuolar trafficking pathway and/or the endocytic pathway)
common to COV1 and SYP2 family proteins affect the development of myrosin cells.
The Endomembrane System in
Plant-Specific Processes
The Arabidopsis stomatal complex is composed of a pair of
guard cells and surrounding anisocytic subsidiary cells (Serna
and Fenoll 2000). Although subsidiary cells, together with guard
cells, are thought to cause stomatal movement via bulk water
and ion flow (Raschke and Fellows 1971), the underlying
molecular mechanism remains unclear. Higaki et al. (2014)
studied the dynamic behavior and environmental responses
of PROTON-ATPase TRANSLOCATION CONTROL 1
(PATROL1) on stomatal movement. PATROL1 is a translocation factor of the PM proton pump ATPase AHA1 in guard cells
(Hashimoto-Sugimoto et al. 2013). Interestingly, subsidiary cells
showed changes in localization of GFP–PATROL1 in response
to environmental stimuli that contrasted with those in guard
cells (Higaki et al. 2014). GFP–PATROL1 and red fluorescent
protein (RFP)–AHA1 co-localized in hyperosmotic conditions,
and a mutation in PATROL1 resulted in increased GFP–AHA1
internalization in subsidiary cells. These live-cell imaging results
suggest that PATROL1-mediated membrane trafficking in subsidiary cells is important for stomatal movement.
Over 60 genes in the Arabidopsis genome encode SNARE
proteins (Uemura et al. 2004, Sanderfoot 2007), which contribute to various biological processes including growth, homeostasis, hormone and stress responses, and immunity against
pathogens (Collins et al. 2003, Lipka et al. 2007, El Kasmi et al.
2013). To characterize SNARE protein networks in cells,
Fujiwara et al. (2014) performed interactomics using immunoprecipitation and mass spectrometry as a powerful, highthroughput tool to identify the proteins that interact with 12
Arabidopsis Qa-SNAREs. Despite their redundant nature, nine
Qa-SNARE molecules have been shown to localize to the PM
(Uemura et al. 2004), implying that each PM Qa-SNARE
molecule has a specialized physiological function, yet exhibits
partially overlapping functions. Ichikawa et al. (2014) report
that two different PM-localized Qa-SNAREs, SYP123 and
SYP132, function coordinately in root hair elongation in
Arabidopsis by forming SNARE complexes with a PM
R-SNARE, VAMP721/722/724.
BiP is an ER-localized molecular chaperone of the heat shock
protein 70 (Hsp70) family and plays key roles in protein translocation, protein folding and quality control in the ER
(Nishikawa et al. 2005, Bukau et al. 2006). Flowering plants
have multiple BIP genes, in contrast to yeast and mammals.
Among three BiP paralogs in Arabidopsis, two almost identical
BiPs (BiP1 and BiP2) are ubiquitously expressed, while the less
well conserved BiP3 is expressed only under ER stress conditions
(Noh et al. 2003). Maruyama et al. (2014) demonstrate that BiP3
is expressed in pollen and pollen tubes without ER stress and
has functions that are comparable with those of BiP1 and BiP2
in male gametogenesis and pollen tube growth. The study
suggests that the multiple BiP proteins of flowering plants are
important to meet the high cellular demands for protein secretion in actively growing cells such as the pollen tube.
In mature plant cells, vacuolar membranes (VMs) display
dynamic structures, which are formed by invagination and folding of VMs into the lumenal side and can gradually move and
change shape (Saito et al. 2002, Oda et al. 2009). The dynamic
nature of VMs is important for the whole-plant-related
phenomenon, shoot gravitropism. Dynamic VM structures in
gravity-sensing cells are required for statolith (amyloplast) sedimentation in gravity susception (Morita 2010). Hashiguchi et al.
(2014) report on a novel HEAT-repeat protein, SHOOT
GRAVITROPISM6 (SGR6), which affects amyloplast sedimentation via control of dynamic VM structures within
shoot gravity-sensing cells. Live imaging analyses indicate that
VM-associated SGR6 is involved in the formation and/or maintenance of invaginated VM structures.
Final Remarks
The Nobel Prize in Physiology or Medicine 2013 was awarded
jointly to James E. Rothman, Randy W. Schekman and Thomas
C. Südhof for their discoveries of the machinery regulating
vesicle trafficking. This reaffirms the importance and expansiveness of the endomembrane research field. As introduced above,
plant endomembrane research is intimately associated with a
wide variety of research areas. We expect that this Special Focus
Issue will serve as a trigger to consider the relationship between
your research topic and the plant endomembrane system.
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