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Review
a;
*, Peter Westho
Botanisches Institut der Christian-Albrechts-Universitat Kiel, Am Botanischen Garten 1^9, D-24118 Kiel, Germany
Institut fur Entwicklungs- und Molekularbiologie der Panzen, Heinrich-Heine-Universitat Dusseldorf, Universitatsstrasse 1,
D-40225 Dusseldorf, Germany
Received 25 July 2001; accepted 1 August 2001
Abstract
Thylakoids are photosynthetically active membranes found in Cyanobacteria and chloroplasts. It is likely that they
originated in photosynthetic bacteria, probably in close connection to the occurrence of photosystem II and oxygenic
photosynthesis. In higher plants, chloroplasts develop from undifferentiated proplastids. These contain very few internal
membranes and the whole thylakoid membrane system is built when chloroplast differentiation takes place. During cell and
organelle division a constant synthesis of new thylakoid membrane material is required. Also, rapid adaptation to changes in
light conditions and long term adaptation to a number of environmental factors are accomplished by changes in the lipid and
protein content of the thylakoids. Thus regulation of synthesis and assembly of all these elements is required to ensure
optimal function of these membranes. 2001 Elsevier Science B.V. All rights reserved.
Keywords: Chloroplast; Photosynthesis; Plastid development; Organelle evolution; Thylakoid formation
1. Introduction
Evolution of oxygenic photosynthesis with its CO2
xation and oxygen release enabled life on earth as
we experience it today. It is assumed that oxygenic
photosynthesis developed several billion years ago in
an ancestor of today's cyanobacteria most likely
from an already existing anoxygenic photosynthesis
apparatus [1]. The capacity to perform oxygenic photosynthesis was passed on to algae and higher plants
by an endosymbiotic event that turned a cyanobacterium into a cell organelle, the chloroplast. The photosynthetic machinery of both, cyanobacteria and
chloroplasts, is located on a special internal membrane system, the thylakoids. Thanks to the unique
architecture of this membrane cyanobacteria and
chloroplasts convert solar energy into chemical energy with an eciency signicantly better than any
man-made photovoltaic system. Therefore, the ability of the cell to build and alter this membrane system is essential for ecient oxygenic photosynthesis.
Resulting from the combination of structural, biochemical, and genetic analysis, we have a well
founded knowledge of the ultrastructure and composition of thylakoid membranes, but despite the importance that the thylakoid membrane system has
for photosynthesis and the energy metabolism of
plants and cyanobacteria, the molecular processes
connected to the origin, synthesis, maintenance and
adaptation of the thylakoids remain elusive. In this
review we will discuss recent ndings on thylakoid
0167-4889 / 01 / $ ^ see front matter 2001 Elsevier Science B.V. All rights reserved.
PII: S 0 1 6 7 - 4 8 8 9 ( 0 1 ) 0 0 1 5 3 - 7
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Fig. 1. Overview of the development of chloroplasts. Chloroplast develop from undierentiated proplastids. During maturation the
complex internal thylakoid membrane network is formed. Proplastids can also develop into other plastids forms, such as etioplasts,
chromoplasts and leucoplasts. Moreover, fully dierentiated plastids retain the ability to develop into each other. Gerontoplasts are a
nal stage in plastid development in which a level of senescence is reached that is irreversible. The electron microscopic pictures of
thin sections show several stages in the development of a chloroplast.
94
tion, modication and later degradation of the proteinaceous components and are also required for the
addition of the pigments and co-factors. To complicate matters, certain components, like the two photosystems, are unevenly distributed in the thylakoid
membrane network. While photosystem I is most
abundant in the non-stacked stroma lamellae, photosystem II is the dominating component of the grana
stacks [30]. Thus thylakoid biogenesis and maintenance have to assure not only the arrangement of a
functional but at the same time asymmetric architecture of both the lipid and the protein components of
this membrane.
4. Thylakoid membrane formation
One of the most elusive aspects of thylakoid formation is the exact mechanism by which the membrane itself is formed. In young, not yet dierentiated plastids a continuum can sometimes be observed
between the inner envelope and the developing internal membrane structures [7^9]. Thus the synthesis of
early thylakoid membranes might be achieved by invagination of the inner envelope. Even in fully mature chloroplasts the thylakoid membrane is a very
dynamic system. Short-term adaptation to changing
light conditions is obtained by movement of proteins,
especially the light harvesting complex, within the
thylakoid membrane. Long-term adaptation on the
other hand is achieved by a change in the protein
and lipid content of the thylakoids. Although in mature chloroplasts a continuum between the inner envelope and the thylakoids can no longer be observed,
the membrane material required for synthesis and
maintenance of the thylakoids originates from the
chloroplast's inner envelope [7,31,32] and not from
de novo synthesis on already existing thylakoids.
How these lipids are transferred from the inner
envelope to the thylakoids is controversially discussed. One possibility would be the transfer by
vesicles which is a common phenomenon in the cytosol, where vesicle trac is involved in many dierent cellular processes including the secretory pathway, endocytosis, neural transmission and vacuole
formation [33]. A similar vesicle transfer from
the inner envelope to the thylakoids has been implicated in the synthesis of thylakoid membranes
[7,31,32,34,35]. Vesicles inside plastids have been observed in early electron microscopic studies [7^9].
They are common in proplastids and have also
been observed on the inner envelope of etioplasts
in dark-grown cells of the Chlamydomonas y-1 mutant, shortly after illumination when chloroplast development sets in [36]. On the other hand vesicles are
very rarely detected in mature chloroplasts. They do
accumulate in the stromal space between the inner
envelope and the thylakoids after a low temperature
incubation of leaf tissue [34,35]. A similar phenomenon is described for vesicle transport in animal cells,
i.e. enodplasmic reticulum to Golgi and Golgi to
plasma membrane, where low temperature blocks
the fusion of vesicles with their target membrane
[37]. Further indication for vesicle transfer in chloroplasts comes from mutant analysis. In several plant
mutants that are aected in thylakoid biogenesis, an
accumulation of vesicles can be observed. Others,
like the vipp1 mutant of Arabidopsis, no longer exhibited low temperature vesicle accumulation [35].
The possibility of vesicle transfer inside the chloroplast raised the additional question whether solely
membrane lipids would be transported by these
vesicles. As in vacuole formation the vesicle transport in chloroplasts could be limited to the supply
of thylakoid lipids that are either synthesized at the
inner envelope, i.e. galactolipids, or imported from
the cytosol. It is also possible that non-lipid components of the thylakoid membrane might be transported by means of vesicle trac [38,39]. Several of
the non-lipid components required for the biogenesis
and maintenance of thylakoids are synthesized on
the envelope, i.e. carotenoids, or in the cytosol
[40,41]. Especially hydrophobic components would
require a system to travel through the aqueous stroma.
During chloroplast maturation an extensive formation of thylakoid membranes occurs in concert
with the accumulation of the photosynthetic complexes. Several of the proteinaceous components are
nuclear encoded and post-translationally imported
into the chloroplasts. It was suggested that in Chlamydomonas the nuclear encoded light harvesting
complex proteins are inserted into newly developing
membranes at the inner envelope immediately upon
their entrance in the organelle [42]. Later on, the
development of the thylakoid system continues with
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Fig. 2. Schematic display of nucleus^chloroplast interaction. Synthesis of plastid encoded proteins is regulated by nuclear encoded factors from the point of gene expression and translation until the nal incorporation into the thylakoid membrane. At the same time
the chloroplast signals the nucleus about its state of development. This signal inuences the expression of nuclear encoded genes. This
gure is based on a scheme presented by Rochaix [102].
communication between the organelle and the nucleus can ensure a coordinated supply of all the different factors required.
6. Analysis of thylakoid biogenesis through mutants
Mutants are a powerful tool to study the involvement of gene products on specic processes. Many
dierent mutants that display deciencies in plastid
development and thylakoid formation exist in a wide
range of species. Many of these mutants are randomly occurring natural variations, others are manmade. In early work, new mutants were produced by
treatment of plants or algae with radiation or chemical mutagens [43,67]. Later, the necessary genetic
tools became available for random insertional mutagenesis by T-DNA of Agrobacterium tumefaciens
[68^70] or transposable elements. Only a limited set
of these mutants can be discussed within this section.
For a more detailed summary of mutants see
[43,71,72].
There are many dierent types of mutations that
aect both plastid development and thylakoid formation and the eect that a mutation has on either
is often dicult to distinguish. Often these mutants
are blocked in a step of a biosynthetic pathway located inside the chloroplasts. The resulting loss of a
functional component of the plastid then extends its
eect on the macromolecular structures. In other
mutants structural components of the thylakoid
membrane are missing or defective. Mutations can
aect plastids in all stages of thylakoid formation.
In several cases plastids are blocked very early in
development. These mutants include dcl from tomato
[73], dag from Antirrhinum [74], cla1-1 from Arabidopsis thaliana [75] and several albina mutants of
barley [65,76]. Plastids in dcl, dag and cla1-1 seem
to be arrested in the proplastid stage while plastids in
some of the barley albina mutants can reach the size
of mature chloroplasts but remain fully depleted of
internal membrane structures except for vesicles that
accumulate in some of them.
A similar phenotype can be observed in vrpoA, B
and C1 mutants that lack the bacterial-type RNA
polymerase and consequently the ability to transcribe
the photosynthetic genes which encode subunits of
thylakoid protein complexes [62,77]. Other mutants
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can be found that are blocked in later stages of plastid development, anywhere from the proplastid to
mature chloroplasts. Because of the close connection
between plastid development and thylakoid formation it is often dicult to distinguish pleiotropic effects of these mutations. In some cases mutants seem
to suer from a secondary destruction of the internal
membrane structure rather than a defect in thylakoid
synthesis [78,79].
Defects in thylakoid formation are often caused by
mutations that result in a depletion of major proteinaceous components of the thylakoid membrane, e.g.
major components of the photosystems. For instance, the hcf136 mutant of A. thaliana cannot assemble a functional photosystem II, and this defect is
associated with a drastically disturbed thylakoid
membrane system [80]. Mutations of the protein import apparatus of chloroplasts cause similar defects
in thylakoid formation [81]. Other mutations that
have a great impact on thylakoid formation are mutations that aect the import pathways by which
proteins are inserted into the thylakoid membrane
[82^84]. Examples for such mutants can be found
in maize in the form of tha1 and tha5 which inhibit
the SecA-type import pathway and hcf106 and tha4
where the vph or Tat pathway is disrupted [85,86].
Not surprisingly, mutants that aect the synthesis of
important thylakoid lipids display alterations in the
chloroplast ultrastructure. Arabidopsis dgd1 and
mdg1 mutants lack the enzymes monogalactosyl diacylglycerol synthase or digalactosyl diacylglycerol
synthase that are required for the formation of the
two major thylakoid membrane lipids. These mutants show a wide range of alterations including
changes in the chloroplast ultrastructure and protein
composition [87^89].
Also very common is the connection between deciencies in thylakoid formation and disruption of
pigment biosynthesis [43,67,90]. While pleiotropic effects of these mutations cannot be excluded in some
cases, many investigations have supported the potential inuence of chlorophyll production on chloroplast development [43,90^93]. This connection is especially interesting in light of the `plastidal factor'
that is discussed as a signal from the chloroplasts
to the nucleus (Fig. 2). As described above, the `plastidal factor' is thought to signal the developmental
stage of the plastid to the nucleus and aect the
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