Versatile Roles of Plastids in Plant Growth and Development
Interdisciplinary Research Organization, Faculty of Agriculture, University of Miyazaki, 1-1 Gakuenkibanadai-nishi, Miyazaki, 889-2192 Japan
*Corresponding author: E-mail, [email protected]; Fax, +81-985-58-7865
(Received September 12, 2010; Accepted September 27, 2010)
Plastids, found in plants and some parasites, are of
endosymbiotic origin. The best-characterized plastid is the
plant cell chloroplast. Plastids provide essential metabolic
and signaling functions, such as the photosynthetic process
in chloroplasts. However, the role of plastids is not limited to
production of metabolites. Plastids affect numerous aspects
of plant growth and development through biogenesis, varying
functional states and metabolic activities. Examples include,
but are not limited to, embryogenesis, leaf development,
gravitropism, temperature response and plant–microbe
interactions. In this review, we summarize the versatile roles
of plastids in plant growth and development.
Keywords: Plastids.
Abbreviations: AOX, alternative oxidase; GFP, green fluorescent
protein; TIC, translocon at the inner envelope membrane of the
chloroplast; TOC, translocon at the outer envelope membrane
of the chloroplast.
Introduction
Plastids are a diverse group of organelles found in plants and
some parasites, and originated from a photosynthetic bacterial
endosymbiont (Dyall et al. 2004). The archetypical plastid is
the chloroplast, found in photosynthetic cells; however, plastids in land plants have acquired the ability to differentiate
into specialized plastid types in different tissues and cell types.
For instance, chromoplasts are the predominant form of plastids in fruit tissues and amyloplasts are the major type of
plastids in storage organs (Staehelin and Newcomb 2000).
Most of these plastids are interconvertible under certain developmental or environmental conditions. In addition, proplastids
that serve as the precursors of other plastids are found in
meristematic cells. Plastids are generally surrounded by two
membranes, the outer and inner envelopes, which are believed
to be derived from the bacterial ancestor. Although plastids
found in land plants no longer have peptidoglycan, the moss,
Physcomitrella patens, still retains genes for peptidoglycan
biosynthesis (Machida et al. 2006, Homi et al. 2009, Takano and
Takechi 2010). Other organisms, such as euglenids, acquired
plastids through secondary endosymbiosis and have additional
membranes (Archibald 2009). Nonetheless, all plastids are
believed to have evolved from a common ancestor that was
incorporated into the eukaryotic cell about 1.2–1.5 billion years
ago (Dyall et al. 2004, Archibald 2009).
Because purification of plastids from plant cells is relatively
easy (e.g. Packer and Douce 1987), a number of studies have
focused on the metabolic pathways and biochemical function
of polypeptides located in these organelles. In addition, genetic
evidence in recent years has shown that plastid proteins play
key roles in plant developmental regulation. Significantly, many
of these developmental regulations are not directly related
to photosynthesis. This review summarizes the versatile roles
of plastids in plant growth and development as well as key
processes for plastid biogenesis and maintenance. Other comprehensive reviews cover broad aspects of plastid function
(Sakamoto et al. 2008, Woodson and Chory 2008, Waters and
Langdale 2009, Li and Chiu 2010), and space limitations prevent
us from providing adequate coverage of all aspects of plastid
biogenesis and plant development.
Mini Review
Takehito Inaba* and Yasuko Ito-Inaba
Biogenesis and maintenance of
chloroplast/plastids
The archetypical plastid, the chloroplast, is predicted to contain ∼3000 different proteins. However, most of the genes
encoded by the bacterial ancestor have been transferred to
the host nuclear genome. At present, the plastid genome of
land plants encodes only ∼100 genes. Therefore, the posttranslational import of nuclear-encoded plastid proteins into
plastids is indispensable for plastid biogenesis (Kessler and
Schnell 2009). In general, the majority of these proteins are
produced as precursor proteins which usually contain a
‘transit peptide’ that is both necessary and sufficient for
delivery of the protein to plastids. The transit peptide is
located at the N-terminus of the precursor and is eventually
cleaved within the plastid. The import of transit peptidedependent proteins is mediated by the TOC–TIC machinery
(Fig. 1), which consists of receptive components, channels,
molecular chaperones and other accessory proteins (Soll and
Schleiff 2004, Inaba and Schnell 2008, Jarvis 2008, Li and Chiu
2010). Components of the TOC–TIC machinery are of both
eukaryotic and prokaryotic origins. In vivo analysis of Arabidopsis
toc and tic mutants supports the hypothesis that the TOC–TIC
Plant Cell Physiol. 51(11): 1847–1853 (2010) doi:10.1093/pcp/pcq147, available online at www.pcp.oxfordjournals.org
© The Author 2010. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists.
All rights reserved. For permissions, please email: [email protected]
Plant Cell Physiol. 51(11): 1847–1853 (2010) doi:10.1093/pcp/pcq147 © The Author 2010.
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T. Inaba and Y. Ito-Inaba
Fig. 1 Biogenesis and maintenance of chloroplast/plastids within the
plant cell. Most plastid proteins are encoded by the nucleus so
that import of these proteins is a prerequisite for plastid biogenesis.
The TOC–TIC machinery and other pathways are responsible for
protein targeting to plastids. In photosynthetic tissue, chloroplast
protein import and the expression of nuclear-encoded chloroplast
proteins are coordinated by GUN1 and GLK1. Several other proteins
involved in retrograde signaling from plastids to the nucleus have also
been identified. The plastid division machinery is also important to
maintain plastids within plant cells. Although this model has emerged
from studies on chloroplasts, other plastids might also utilize similar
mechanisms. PhANGs, photosynthesis-associated nuclear genes.
machinery is key to plastid protein import (Jarvis et al. 1998,
Bauer et al. 2000, Chou et al. 2003, Baldwin et al. 2005, Inaba
et al. 2005). Recent studies have indicated the presence of several additional plastid protein import pathways. For instance,
Tic32 (Nada and Soll 2004) and ceQORH (Miras et al. 2007),
which apparently lack cleavable transit peptides, are imported
into chloroplasts both in vivo and in vitro. Plastid-localized glycoproteins are delivered via the secretory pathway (Villarejo
et al. 2005, Nanjo et al. 2006, Kitajima et al. 2009). Thus, protein
import into plastids seems to be more diverse than previously
thought.
To accomplish appropriate plastid biogenesis in a specific
cell type, both plastid protein import and the gene expression of
nuclear-encoded plastid proteins must be coordinated (Fig. 1).
In photosynthetic tissue, this coordination is probably mediated by the retrograde signaling pathway involving GUN1,
a plastid-localized pentatricopeptide repeat protein, and GLK1
(Koussevitzky et al. 2007, Kakizaki et al. 2009, Inaba 2010). GLK
proteins are members of the GARP superfamily of transcription
factors and coordinate the expression of a set of nuclearencoded photosynthesis-related genes (Nakamura et al. 2009,
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Waters et al. 2009). Ectopic overexpression of OsGLK1 is
sufficient to induce chloroplast development in rice calli
(Nakamura et al. 2009). When chloroplasts are damaged,
GUN1 inhibits the expression of GLK1, which in turn represses
photosynthesis-related genes (Fig. 1). Since the expression of
GLK1 is induced by light (Fitter et al. 2002), GLK1 probably
regulates chloroplast differentiation in response to both external and intracellular environments. It also appears that other
components, such as ABI4 and EXECUTERs, play key roles in
regulating retrograde signaling from chloroplasts to the nucleus
that is primarily related to stress response (Kim et al. 2008,
Woodson and Chory 2008). Much less is known about the
cross-talk between other plastids and the nucleus; however,
according to a proteome analysis, cross-talk between etioplasts
and the nucleus seems to be active even in etiolated tissues
(Kanervo et al. 2008).
Another critical process for plastid biogenesis is plastid
division (Fig. 1). Because plastids are surrounded by outer and
inner envelope membranes, the constriction of two membranes
and subsequent fusion of four lipid bilayers must be coordinated. At least four rings, the FtsZ, inner PD, outer PD and
dynamin rings, have been shown to participate in plastid
division in land plants (Glynn et al. 2007, Yang et al. 2008).
To date, the FtsZ and dynamin rings have been characterized
in detail. FtsZ is a component of the stroma division apparatus
and its bacterial counterpart is involved in bacterial division.
Down-regulation of FtsZ genes in Arabidopsis reduced the cellular chloroplast number (Osteryoung et al. 1998). A dynaminrelated protein, ARC5, is localized in the cytosol and recruited
to the chloroplast division site by PDV proteins (Miyagishima
et al. 2006, Glynn et al. 2008). Although the FtsZ and dynamin
rings have been well characterized, the components of PD
rings have not yet been studied in detail. Very recently, the glycosyltransferase protein, designated as PDR1, has been isolated
from the PD ring of Cyanidioschyzon merolae chloroplasts
(Yoshida et al. 2010). Further analysis of PDR1 in land plants
will uncover the common mechanism of chloroplast division.
Much less is known about division in other types of plastids;
however, both FtsZ and ARC5 seem to be targeted to the amyloplast, suggesting their involvement in division of that plastid
type as well (Yun and Kawagoe 2009).
Versatile roles of plastids in plant growth
and development
Plastids house many essential metabolic pathways, and alteration of plastid function affects numerous aspects of plant
growth and development. Indeed, screening of seedling lethal
mutants suggested that many of these mutants carried lesions
in nuclear-encoded plastid proteins (Budziszewski et al. 2001).
During the past decade, specific phenotypes caused by plastid
protein loss of function have been studied in detail, mainly
using Arabidopsis mutants. A comprehensive, though not
exhaustive, list of examples is shown in Table 1 and briefly
summarized below.
Plant Cell Physiol. 51(11): 1847–1853 (2010) doi:10.1093/pcp/pcq147 © The Author 2010.
Versatile roles of plastids
Table 1 Examples of plant growth and development affected by plastid proteinsa,b
Embryogenesis
Leaf development
Gravitropism
Genes identified
Reference
AARS genes
Berg et al. (2005)
CLPR2, CLPR4, CLPR5
Kim et al. (2009)
CPN60
Apuya et al. (2001)
MGD1
Kobayashi et al. (2007)
TIC110
Inaba et al. (2005), Kovacheva et al. (2005)
TOC75
Baldwin et al. (2005)
VAR1, VAR2
Chen et al. (2000), Takechi et al. (2000), Sakamoto et al. (2002), Sakamoto et al. (2009)
IM
Carol et al. (1999), Wu et al. (1999)
TOC75, TOC132
Stanga et al. (2009)
SEX1
Vitha et al. (2007)
PGM1
Kiss et al. (1989)
Fertilizationc
CRSH
Masuda et al. (2008)
Heat tolerance
FtsH11
Chen et al. (2006)
cpHsc70
Su and Li (2008)
Hsp100/ClpB
Myouga et al. (2006), Lee et al. (2007)
Cold acclimation
COR15A
Artus et al. (1996), Nakayama et al. (2007)
SFR2
Fourrier et al. (2008)
Root developmentc
GAPC
Munoz-Bertomeu et al. (2009)
ribosomal protein S6
Horiguchi et al. (2003)
CASTOR, POLLUX
Imaizumi-Anraku et al. (2005), Banba et al. (2008)
Symbiosisd
a
Due to space limitations, this is not an exhaustive list.
b Unless specified, genes were identified in Arabidopsis.
c Due to space limitation, these genes are not mentioned in the text in detail.
d These genes were identified in Lotus japonicus.
Embryogenesis
Embryogenesis is the very first step of plant development.
Although the early embryo does not contain chloroplasts,
it does contain plastids. Thus, disruption of essential plastid
function often impairs embryogenesis (Table 1). For example,
it is easy to assume that plastid protein import is important
even in the embryonic stage. Loss of function of key players
in the TOC–TIC machinery, such as TOC75 and TIC110, results
in embryo lethality (Jarvis 2008). Likewise, mutation in the
gene encoding the key enzyme of galactolipid biosynthesis,
MGD1, compromises proper embryogenesis (Kobayashi et al.
2007). Mutation in other essential proteins, such as chaperones,
proteases and aminoacyl-tRNA synthase, in plastids also compromise embryogenesis (Table 1). According to a recent estimate, >30% of genes required for proper embryo formation
encode plastid-targeted proteins (Hsu et al. 2010), highlighting
the essential role of plastids in embryogenesis.
Leaf development
Plastid biogenesis, particularly chloroplast biogenesis, affects
leaf development as the chloroplast serves as the photosynthetic apparatus in leaf tissues. Mutants defective in chloroplast
protein often exhibit albino or pale yellow phenotypes (Myouga
et al. 2010). Because there are so many mutants exhibiting
albino or pale yellow phenotypes, we cannot describe them in
detail here. Instead, we focus on a unique leaf phenotype, variegation (Table 1). In variegated mutants, green sectors contain
normal chloroplasts while white sectors contain dysfunctional
chloroplasts (Sakamoto 2003). The immutans (im) and yellow
variegated (var) mutants exhibit this phenotype. The IM gene
encodes a plastid terminal oxidase that is similar to mitochondrial alternative oxidase (AOX; Carol et al. 1999, Wu et al. 1999),
although the precise function of IM protein remains unclear.
The var mutants were shown to lack plastid-localized FtsH protease (Chen et al. 2000, Takechi et al. 2000, Sakamoto et al.
2002), known to be involved in degradation of photodamaged
proteins; lack of FtsH causes chloroplast photobleaching.
Intriguingly, lack of plastids in certain cells did not produce the
variegated phenotype. The crl mutant, for example, is not variegated, although it contains cells without detectable plastids
(Chen et al. 2009).
Gravitropism
The starch-accumulating amyloplast is thought to be involved
in gravitropism (Morita and Tasaka 2004, Morita 2010).
Plant Cell Physiol. 51(11): 1847–1853 (2010) doi:10.1093/pcp/pcq147 © The Author 2010.
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Therefore, mutation of plastid proteins affecting amyloplast
starch content results in alteration of the gravitropic response
(Table 1). A mutant of phosphoglucomutase (pgm1) fails to
accumulate starch and is unable to mediate a normal gravitropic response (Kiss et al. 1989). In contrast, the starch excess
mutant, sex1, has a lesion in α-glucan/water dikinase and
displays increased sensitivity to gravistimulation (Vitha et al.
2007). Both PGM1 and SEX1 proteins are localized in plastids,
highlighting the role of plastid proteins in gravitropism. Intriguingly, genetic screening of mutants that enhance the altered
response to gravity 1 (agr1) mutant phenotype identified TOC
proteins in the protein translocation machinery as a possible
signal transduction component (Stanga et al. 2009). A number
of mutants defective in the vesicle trafficking pathway have
been identified as shoot gravitropic mutants (Morita and
Tasaka 2004, Morita 2010). Thus, endomembranes are also
likely to play key roles in gravitropism by affecting amyloplast
movement within the cell.
Temperature response
Adaptation to external environmental factors, such as temperature, is indispensable for plant survival (Table 1), and some
plastid proteins appear to be involved in the temperature
response. For instance, plastid-localized heat shock proteins
are known to affect thermotolerance in Arabidopsis (Myouga
et al. 2006, Lee et al. 2007, Su and Li 2008). A plastid-localized
metalloprotease, FtsH11, also affects thermotolerance (Chen
et al. 2006). From these examples, protein quality control by
plastid-localized proteases and chaperones seems to be important for thermotolerance. Likewise, COR15A and SFR2 genes,
both of which encode plastid proteins, affect acclimation to
low temperature (Artus et al. 1996, Nakayama et al. 2007,
Fourrier et al. 2008). The role of COR15A and SFR2 in cold
acclimation was confirmed by transgenic and genetic studies.
Other cold-regulated, as yet uncharacterized, genes are also
predicted to encode plastid proteins (Okawa et al. 2008).
Thus, it is reasonable to speculate that a number of other
plastid proteins may participate in the temperature response.
Plant–microbe interactions
Plastids also play key roles in plant–microbe interactions
(Table 1). Lotus japonicus mutants, castor and pollux, lack
the ability to form root nodules and arbuscular mycorrhizal
symbiosis. Identification of CASTOR and POLLUX genes and
characterization of their corresponding proteins indicated
that both CASTOR and POLLUX were targeted to plastids
(Imaizumi-Anraku et al. 2005). These proteins were also localized in the nucleus and exhibited ion channel activity when
reconstituted into proteoliposomes (Charpentier et al. 2008).
In cases of bacterial infection, targeting of bacteria-encoded
proteins into the plastid seems to be important in promoting
tumorigenesis. The Agrobacterium tumefaciens cytokinin biosynthesis enzyme, Tmr, is targeted to plastids in the absence of
a cleavable transit peptide and modifies cytokinin biosynthesis
in the host plant (Sakakibara et al. 2005). In-depth analysis of
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Tmr protein targeting may reveal the molecular mechanism of
transit peptide-independent protein targeting to plastids in
general and in plant–microbe interactions.
Future prospects
Plastid biogenesis affects numerous aspects of plant growth
and development. To analyze the role of plastids in plant
development further, precise prediction of nuclear-encoded
plastid proteins is necessary. To this end, a proteomic approach
has been utilized and a number of as yet uncharacterized
plastid proteins have been identified (Ferro et al. 2003,
Froehlich et al. 2003, Friso et al. 2004, Kleffmann et al. 2004).
As complete genome sequences accumulate, a comparative
genomics approach may be employed to predict proteins of
endosymbiotic origin (Ishikawa et al. 2009).
The role of plastids in reproductive organ development is an
exciting research area. Although few studies have focused on
the role of plastids in reproductive development, it has been
shown that interaction between mitochondria and the nucleus
plays key roles in pollen fertility (Chase 2007). For instance,
accumulation of mitochondria-encoded cytotoxic peptide
resulted in cytoplasmic male sterility in rice (Kazama et al.
2008). Although there are several other examples that exemplify the link between mitochondrial function and cytoplasmic
male sterility (Fujii and Toriyama 2008a, Fujii and Toriyama
2008b, Fujii et al. 2009), much less is known about the role of
plastids in pollen development. Recently, plastids in pollens
were visualized by green fluorescent protein (GFP)-tagged
protein, allowing real-time imaging of pollen plastids in vivo
(Tang et al. 2009). Further analysis of GFP-visualized plastids in
pollen will address the role of plastids in reproductive organ
development.
Perhaps the synergistic effects of plastids and mitochondria
on plant growth and development should be given more
attention, as these organelles exchange metabolites. A good
example is the requirement for the mitochondrial uncoupling
protein for efficient photosynthesis (Sweetlove et al. 2006).
In a var2 mutant, defective in plastid FtsH protease, the mitochondrial AOX was up-regulated (Yoshida et al. 2008). It also
appears that mitochondrial retrograde signaling pathways
utilize ABI4 to regulate AOX1a expression in the nucleus
(Giraud et al. 2009), suggesting ABI4-mediated interaction
between plastidial and mitochondrial retrograde signaling
pathways. Thus, further analysis of these endosymbiont-derived
organelles will provide novel insight into their roles in plant
growth and development.
Funding
This work was supported by the Japanese Ministry of
Education, Culture, Sports, Science and Technology [Special
Coordination Fund for Promoting Science and Technology];
the University of Miyazaki [a grant for Scientific Research on
Priority Areas].
Plant Cell Physiol. 51(11): 1847–1853 (2010) doi:10.1093/pcp/pcq147 © The Author 2010.
Versatile roles of plastids
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