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  • Review Article
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Traffic jams affect plant development and signal transduction

Nature Reviews Molecular Cell Biology volume 5, pages 100–109 (2004)Cite this article

A Correction to this article was published on 01 April 2004

Key Points

  • The vacuole is necessary for plant viability — the recent isolation and characterization of Arabidopsis thaliana vacuoless 1, a mutant impaired in vacuole formation and function, is embryonic lethal.

  • A functional vacuole is necessary for the shoot gravitropic response. Two A. thaliana mutations that affect vacuole formation, sgr2 and zig, have shoot gravitropic response defects.

  • Arabidopsis SNARE proteins have been implicated in the following functional pathways: autophagy, shoot gravitropism, tissue specification, cytokinesis, abscisic acid and stress responses, as well as plant pathogen responses.

  • Vesicle cycling is linked to plant hormone responses: PIN proteins, which are auxin-efflux carrier proteins and involved in the polar transport of auxin, have been shown to cycle between the plasma membrane and an uncharacterized endosomal compartment in an actin-dependent manner.

  • We also discuss emerging methods and new approaches to the functional analysis of vacuolar and endomembrane systems. Among these are new tools for visualizing vacuole morphology, new high-throughput methods, and chemical-genetic screens.

Abstract

Analysis of the Arabidopsis thaliana endomembrane system has shown that plant cell viability depends on a properly functioning vacuole and intact vesicular trafficking. The endomembrane system is also essential for various aspects of plant development and signal transduction. In this review, we discuss examples of these newly discovered roles for the endomembrane system in plants, and new experimental approaches and technologies that are based on high-throughput screens, which combine chemical genetics and automated confocal microscopy.

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Figure 1: The plant endomembrane system.
Figure 2: The role of vacuoles in shoot gravitropism.
Figure 3: The VTI family of v-SNAREs.
Figure 4: Polar auxin transport and vesicle cycling.
Figure 5: Cytokinesis pathways.

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Acknowledgements

We apologize to many authors for the omission of references to their work owing to space restrictions. We are grateful to D. Bassham, S. Bednarek, T. Friedman, G. Hicks, A. Sanderfoot, A. Vitale and the reviewers for critical reading of the manuscript. Research in the authors' laboratory is supported by grants from the National Science Foundation and from the Department of Energy, Division of Energy Biosciences.

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Authors and Affiliations

  1. Center for Plant Cell Biology, University of California, Riverside, 92521, California, USA

    Marci Surpin & Natasha Raikhel

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  1. Marci Surpin
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  2. Natasha Raikhel
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Related links

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DATABASES

TAIR

gnom

KNOLLE

keule

NPSN11

pgm

PIN1

scr

SGR2

SGR3

SGR4

shr

SYP21

SYP22

SYP31

SYP61

SYP121

vcl1

VPS33

VPS45

VSR1

VTI12

VTI13

Further information

Arabidopsis SNAREs

Glossary

TURGOR PRESSURE

Force generated by water pushing outward on the plant cell wall, resulting in plant rigidity. The loss of turgor pressure causes wilting.

PHENOLICS

A diverse group of secondary metabolites. They function in the defence responses against herbivores and pathogens; provide mechanical support; absorb harmful UV light; contribute to taste, odour and flower colour; attract pollinators and fruit dispensers; and can reduce competition by inhibiting the growth of nearby plants.

ALKALOIDS

Generally, nitrogen-containing basic plant compounds that are often used as pharmacological agents, although there are examples of alkaloids that are not basic and/or of plant origin. Alkaloids participate in plant defences and are secreted in response to tissue damage. Compounds include nicotine, caffeine, quinine, cocaine, heroin, codeine and morphine.

PRE-VACUOLAR COMPARTMENT

(PVC). An intermediate compartment between the late endosome and the vacuole, or between the trans-Golgi network and the vacuole.

SWEET POTATO SPORAMIN

The major storage protein (up to 80% of the total soluble protein) in the tuberous roots of sweet potatoes.

BARLEY ALEURAIN

A vacuolar thiol protease with high homology to mammalian lysosomal cathepsin H.

NPIR MOTIF

An amino-terminal sequence motif in precursor proteins that is required for correct targeting to the vacuole.

ELP/VSR1

(Arabidopsis thaliana epithelial-growth-factor-receptor-like protein). A homologue of pea BP-80 that binds NTPP sequence motifs in a pH-sensitive manner. Recently renamed as VSR1 (vacuolar sorting receptor).

BP-80

An amino-terminal propeptide (NTPP) cargo receptor protein originally purified from clathrin-coated-vesicle fractions that were isolated from pea plants. BP-80 binds NTPP sorting motifs at pH 6.0 and dissociates from them at pH 5.5.

SNARE

(soluble N-ethylmaleimide-sensitive fusion protein (NSF) attachment protein (SNAP) receptor). SNAREs are a family of membrane-tethered coiled-coil proteins that regulate fusion reactions and target specificity in the vacuolar system. They can be divided into vesicle membrane (v)-SNAREs and target membrane (t)-SNAREs on the basis of their localization.

APOPLAST

The continuous system of intercellular spaces in plant tissues.

AUTOPHAGOSOME

A double-membrane vesicle that engulfs portions of the cytosol, and is ingested by the central vacuole where it is broken down by hydrolytic enzymes.

TORPEDO STAGE

One of the stages of A. thaliana embryonic development, which also include the preglobular, globular, heart and mature embryo stages. Also known as the mid-maturation stage.

TONOPLAST

The delimiting membrane of the central vacuole.

CLASS-C VPS PROTEIN COMPLEX

A protein complex, first described in yeast, that is required for the docking stage of the homotypic fusion of vacuoles and the heterotypic fusion of vesicles with the tonoplast.

HOMOTYPIC FUSION

The fusion of identical compartments or vesicles.

SYNTAXINS

A subset of SNARE proteins originally isolated from the presynaptic plasma membrane of neuronal and secretory cells.

COILED-COIL DOMAIN

A protein structural domain that mediates subunit oligomerization. Coiled coils contain between two and five α-helices that twist around each other to form a supercoil.

PHOTOTROPIC RESPONSE

Plant growth in the direction of light.

INFLORESCENCE STEM

The post-vegetative phase of stem growth that produces floral organs.

T-DNA

DNA transferred from Agrobacterium tumefaciens and stably integrated into plant genomes. The insertion is random and might therefore disrupt genes, causing a mutation at the insertion point.

DETACHED-LEAF ASSAY

Standard assay used to evaluate the effects of plant stress induced by pathogens or mutations.

PHYLLOTAXY

The spatial arrangement of leaves around the plant stem.

FASCIATED

A defect in stem development where normally cylindrical stems become flattened.

ARF-GEF

(guanine nucleotide-exchange factor (GEF) for small G proteins of the ARF class). ARFs belong to the Ras superfamily of small GTP-binding proteins. GEFs mediate the conversion of GTP to GDP.

CYTOKINESIS

The distribution of cytoplasm to daughter cells following nuclear division.

COPI COAT PROTEIN

Coat protein of vesicles that are involved in ER and Golgi trafficking.

CLATHRIN

A protein that coats vesicles that originate on the trans-Golgi network (TGN) or plasma membrane.

SILIQUES

The fruit of A. thaliana and other cruciferous plants.

DIATOM

Unicellular alga, the cell wall of which is composed of silica.

OOMYCETES

A phylum of filamentous protists that includes downy mildews and water moulds.

AAA PROTEINS

ATPases that are associated with various cellular activities.

STOMATA

Pores in the plant cell epidermis that are composed of two guard cells. Osmotic pressure regulates the size of the guard cells, which in turn control the size of the stomatal opening. The size of the stomatal opening regulates the rate of gas exchange.

WD-40 REPEAT

Protein motif that is composed of a 40-amino-acid repeat that forms a β-propeller sheet. Proteins that contain WD-40 repeats participate in a wide array of cellular functions, including G-protein-mediated signal transduction, transcriptional regulation, RNA processing, and regulation of vesicle formation and trafficking.

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Surpin, M., Raikhel, N. Traffic jams affect plant development and signal transduction. Nat Rev Mol Cell Biol 5, 100–109 (2004). https://doi.org/10.1038/nrm1311

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