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INTRODUCTION
The vacuoles of plant cells are multifunctional organelles
that are central to cellular strategies of plant development. They
share some of their basicproperties with the vacuoles of algae and
yeast and the lysosomes of animal cells. They are lytic
compartments, function as reservoirs for ions andmetabolites,
including pigments, and are crucial to processes of detoxication
and general cell homeostasis. They are involved in cellular
responses toenvironmental and biotic factors that provoke stress.
In the vegetative organs of the plant, they act in combination with
the cell wall to generate turgor,the driving force for hydraulic
stiness and growth. In seeds and specialized storage tissues, they
serve as sites for storing reserve proteins and soluble
carbohydrates. In this way, vacuoles serve physical and
metabolic functions that are essential to plant life.
lant cell vacuoles were discovered with the early microscope
and, as indicated in the etymology of the word, originally dened as
a cell space empty of cytoplasmic matter. Technical progress
has variously altered the operating denition of the plant vacuole
over time. Today, denitions continue to becolored by the tools and
concepts brought to bear in any given study. Indeed, the
combination of microscopy, biochemistry, genetics, and
molecularbiology is fundamental to research into the plant
vacuole.
THE DIVERSITY OF VACUOLES
lant cell vacuoles are widely diverse in form, size, content,
and functional dynamics, and a single cell may contain more than
one kind of vacuole.
!lthough ma"or morphological dierences were recorded by the very
rst microscopists, it has been commonly assumed that all vacuoles
have the same
origin and belong to a common group. #owever, with improvements
in cell fractionation and biochemical analyses as well as in the
use of new molecular
probes, it has become possible to characterize specialized
vacuolar compartments in the cells from a variety of tissues
In some cell types, defense or signal compounds are stored in
the vacuole, particularly within specialized cells located in
strategically favorable tissues
such as the leaf epidermis. !s early as last century, it was
observed that many pigments $e.g., anthocyanins% are localized in
the vacuoles of epidermal
cells from &owers, leaves, and stems. 'ecent ndings suggest
that the membranes of such specialized vacuoles contain specic !T
binding cassette
$!()% transporters $'ea et al., *++%. The diversity of function
and form outlined in the above examples illustrates that the
cytological denition ofvacuoles is likely to cover several
biochemically and physiologically distinct entities. -acuoles, as
dynamic organelles, can thus be viewed in the right
perspective only if their dynamic nature itself is understood.
In several instances, entities that may be variously dened
according to dierent
morphological, biochemical, and physical criteria may not
necessarily correspond to distinct physiological units.
BIOGENESIS OF VEGETATIVE VACUOLES
ntil recently, our knowledge of the biosynthesis and maintenance
of vacuoles was based largely on morphological observations.
Technological
breakthroughs over the past few years have advanced our
understanding of vacuolar biogenesis to a more detailed molecular
level. 'esident vacuolar
proteins as well as proteins destined for degradation are
delivered to the vacuole via the secretory pathway, which includes
the biosynthetic, autophagic,
and endocytotic transport routes that are presented
VACUOLAR SORTING OF STORAGE PROTEINS
/pecialized cells in seeds and vegetative organs accumulate
proteins that function primarily as reserves of amino acids. The
most common storage
proteins are the globulins, which are found in embryos, and the
prolamins, which are uni0ue to cereal endosperms. 1ost storage
proteins, includingglobulins and some prolamins, have been shown to
be transported to vacuoles via the 2olgi complex
Golgi-Dependent and Golgi-Independent Routes to PSVs
ulse3labeling experiments, morphological and immunocytochemical
studies, and biochemical analyses have provided compelling evidence
for a 2olgi3
mediated route to the /- in legumes and other dicots. /torage
proteins are synthesized as precursors that are cotranslationally
transferred into the
lumen of the rough 4' and transported via the 2olgi apparatus
into specialized vacuoles where proteolytic processing is usually
needed to promote their
stable storage.
Autophagy and PSVs
5eveloping legume cotyledons comprise a model system to study
both the ontogenesis of the /- and the intracellular transport of
vacuolar reserve
proteins $)hrispeels, *++*%. In the parenchyma cells of maturing
legume cotyledons, the very few large vegetative vacuoles become
replaced by
numerous /-s.
!t later stages of cotyledon maturation, the budding process
stops, and the main original storage vacuole, which continues to
accumulate reserve
proteins, transforms into a distinct category of large storage
vacuole. ! third type of storage protein reservoir is formed in the
cells at the middle to late
stages of seed maturation, before storage protein synthesis
ceases. /torage proteins accumulate in smooth3surfaced cisternae
and channels with
terminal dilations. These swellings may detach and become
independent spherical bodies without cisternal connections.
Storage Proteins in Cereals
)ereal grains dier from legume seeds by accumulating the
alcohol3soluble prolamins as storage proteins in endosperm cells $
/hewry et al., *++6%. )ereal
prolamins, like legume globulins, are cotranslationally loaded
into the lumen of the 4'. rolamins of other cereals, including
wheat, barley, and oat, on the
other hand, accumulate in vacuoles together with globulins $
/hotwell and 7arkins, *+87evanony et al., *++9%. 2lobulins are
transported along the
anterograde pathway via the 2olgi complex to the vacuolar
compartment, whereas prolamin (s are incorporated into the vacuole
by an autophagic
process
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ENDOCYTOSIS
4ndocytosis is dened as the uptake of extracellular and plasma
membrane materials from the cell surface into the cell. 4ndocytosis
has been
characterized morphologically in plant cells in which both
&uid3phase uptake and receptor3mediated internalizations have
been visualized $reviewed in 7ow
and )handra, *++:8 1arty, *++;8 see also (attey
et al., *+++, in this issue%. Two distinct routes of
internalization by clathrin3mediated endocytosis have
been suggested to operate in plant cells< $*% from the plasma
membrane to an endosomal compartment, including the partially
coated reticulum,
multivesicular bodies, T2=, and the -)8 and $9% from the plasma
membrane to the -) and the vacuoles
VACUOLAR SORTING SIGNALS
-acuolar soluble proteins and membrane proteins alike travel
through the early stages of the secretory pathway. 1ost probably,
they are sorted away from
proteins destined for delivery to the cell surface at the exit
of the 2olgi complex. /oluble proteins therefore re0uire a sorting
signal to tag them for
vacuolar delivery after their egress from the 2olgi complex8
indeed, in the absence of such informational tags, they are
secreted to the extracellular space.
Three types of vacuolar targeting signals have been
described. /ome vacuolar proteins $e.g., sporamin and aleurain%
contain an =3terminal propeptide
$=T% as a targeting determinant8 others $e.g., barley lectin,
phaseolin, tobacco chitinase, and (razil nut 9/ albumin% contain a
)3terminal propeptide
$)T%, whereas some vacuolar proteins $e.g., phytohemagglutinin
and legumin% contain a targeting signal in an exposed region of the
mature protein.
VACUOLAR SORTING RECEPTORS
/oluble vacuolar proteins are diverted away from the exocytotic
pathway through a receptor3mediated process that leads to their
delivery to the vacuole.
a protein of > k5, called (3>, has been a?nity puried from
a lysate of ))-s from pea. It possesses all the features expected
of a vacuolar sorting
receptor. It is a type I integral membrane protein that is
localized in the 2olgi complex and in small vacuolar structures.
These vacuolar structures are
distinct from both @3TI and A3TI vacuoles but are possibly
analogous to prevacuoles. /everal homologs have been cloned, and
the se0uences appear to
be highly conserved in monocotyledonous and dicotyledonous
plants $aris et al., *++;%.
!n alternative approach led to the identication of an
!rabidopsis receptor3like protein called !t47 $for
Arabidopsis thaliana epidermal growth factorB
likeprotein%. This second approach was based on the use of known
functional motifs present in many of the receptor proteins involved
in clathrin3
dependent intracellular protein sorting in mammalian and yeast
cells.
CONCLUSIONS AND PERSPECTIVES
4volutionary perspectives place vacuoles at a central position
in the physiological strategies of plants in their environment. In
the vast ma"ority of cells
from the plant body, vacuoles provide the true milieu
intérieur. They are responsible for the high cell
surfaceBtoBprotoplasmic volume ratio re0uired for
extensive exchanges of material and information between cells
and their environment. In cooperation with the cell wall, they
create turgor, which is basic
to cell hydraulic stiness and plant growth. In specialized
cells, pigment3 and allelochemical3accumulating vacuoles serve as
mediators of plantBplant,
plantBmicroorganism, and plantBherbivore interactions. In seeds,
vacuoles store proteins to be used for anabolism during seedling
growth. The diversity of
vacuolar functions parallels a diversity in morphology,
biochemistry, and biogenesis.
Acknowledgment
The author is grateful to past and present members of his
laboratory and to colleagues e lsewhere for their contributions to
the work discussed in this
review. The authorCs laboratory is supported by grants from the
1inistDre de lC4ducation =ationale, de la 'echerche et de la
Technologie $' 4/ :E+%, the
)entre =ational de la 'echerche /cienti0ue $5Fpartement des
/ciences de la -ie%, the )onseil 'Fgional de (ourgogne, and the
5FlFgation 'Fgionale G la
'echerche et G la Technologie.
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