Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
, 6, e0110

Chloroplast Biogenesis: Control of Plastid Development, Protein Import, Division and Inheritance

Chloroplast Biogenesis: Control of Plastid Development, Protein Import, Division and Inheritance

Wataru Sakamoto et al. Arabidopsis Book.

Abstract

The chloroplast is a multi-copy cellular organelle that not only performs photosynthesis but also synthesizes amino acids, lipids and phytohormones. The plastid also responds to environmental stimuli such as gravitropism. Biogenesis of chloroplasts is initiated from proplastids in shoot meristems, and involves a series of important events. In the last decade, considerable progress has been made towards understanding various aspects of chloroplast biogenesis at the molecular level, via studies in model systems such as Arabidopsis. This review focuses on two important aspects of chloroplast biogenesis, synthesis/assembly and division/transmission. Chloroplasts originated through endosymbiosis from an ancestor of extant cyanobacteria, and thus contain their own genomes. DNA in chloroplasts is organized into complexes with proteins, and these are called nucleoids. The synthesis of chloroplast proteins is regulated at various steps. However, a majority of proteins are synthesized in the cytosol, and their proper import into chloroplast compartments is a prerequisite for chloroplast development. Fundamental aspects of plastid gene expression/regulation and chloroplast protein transport are described, together with recent proteome analyses of the organelle. Chloroplasts are not de novo synthesized, but instead are propagated from pre-existing plastids. In addition, plastids are transmitted from generation to generation with a unique mode of inheritance. Our current knowledge on the division machinery and the inheritance of plastids is described.

Figures

Figure 1.
Figure 1.
Continuity and differentiation of plastids in plant cells. (A) Schematic representation of plastid differentiation and of the distribution of several plastid types in different tissues. (B) Electron micrographs of a chloroplast (upper), a proplastid (lower left) and an etioplast (lower right) in Arabidopsis. gr, grana; ie, inner envelope membrane; oe, outer envelope membrane; pg, plastoglobule; pl, prolamelar body; rs, ribosome; sg, starch granule; st, stroma. Scale bars: upper and lower right panels, 1 μm; lower left panel, 200 nm; inset of upper panel, 50 nm; inset of lower right panel, 100 nm. (B, courtesy of Dr. Chieko Saito in RIKEN).
Figure 2.
Figure 2.
Morphological change of plastid nucleoids in the first true leaves of Arabidopsis. (A) Plant material used for preparing thin sections. An eight-day-old Arabidopsis seedling (left; a top view is shown) was selected and the two cotyledons were removed (as indicated by black lines). One of the first true leaves of this same plant (right; a side view is shown) was used for the detection of plastid nucleoids. (B) A thin cross-section of the selected true leaf petiole and lamina, stained by Toluidine blue. The positions indicated by the arrows (1 to 3) were further examined by SYBR-green I staining (as shown in C). (C) Examination of thin sections by SYRB green I. Signals corresponding to nuclear and plastid DNAs are shown by red and yellow arrows, respectively. Close-up views of the plastids in the respective areas (1 to 3) are shown below each panel.
Figure 3.
Figure 3.
A regulatory network of nuclear and chloroplast gene expression. This schematic view represents chloroplast gene expression and the assembly of photosynthetic proteins. The process is governed by the coordinated transcription mediated by the NEP and PEP polymerases, and by the post-transcriptional regulatory steps mediated by PPR proteins. A time-course of chloroplast development is illustrated spatially, from left to right. The flow of gene products (NEP, SIG, PPR, and photosynthetic proteins) is indicated by arrows. At an initial stage, NEP and SIG are synthesized and imported into proplastids. These molecules drive the subsequent expression of NEP-dependent genes, including PEP, and lead to the ‘switching-on’ of chloroplast transcription. Numerous PPR proteins are concomitantly imported from the cytosol, and play roles in RNA processing, editing and translation. The products of photosynthetic genes in the chloroplast genome are finally assembled into complexes with other subunits encoded by the nuclear genome, the latter components having been synthesized in the cytosol and imported. To enable coordinated regulation between the nuclear and chloroplast genomes, Mg-protoporphyrin-IX (Mg-proto) and ROS act as possible retrograde signals (indicated by the dotted line); the precise nature of these retrograde signaling pathways is not clear at the present time.
Figure 4.
Figure 4.
Overview of the protein import and routing systems of chloroplasts. Most proteins access the chloroplast interior via the TOC/TIC machinery (yellow; centre of figure). Examples of proteins that utilize this canonical pathway are shown schematically, and their final destinations are indicated parenthetically. Transit peptides (see key) mediate envelope translocation, and are cleaved by SPP (represented by scissors) on arrival in the stroma. Then, imported proteins may either adopt their final conformation, or engage one of several internal sorting pathways. Lumenal proteins cross the thylakoid membrane via the Sec pathway (blue) or the Tat pathway (red). Distinct Sec and Tat lumenal targeting peptides engage the respective translocation machineries, and are cleaved by the thylakoidal processing peptidase (TPP; represented by scissors) in the lumen. Most thylakoid membrane proteins do not possess a cleavable targeting signal. Some of these proteins are targeted by the SRP machinery (white), whereas others insert ‘spontaneously’ into the membrane. Similarly, most outer envelope membrane proteins are targeted without the aid of a cleavable targeting signal; while it has been proposed that their insertion occurs spontaneously (see dotted line), recent evidence suggests that such proteins utilize TOC component(s) during their insertion. Two different TOC/TIC-based pathways mediate targeting to the inner envelope membrane: in the ‘post-import’ pathway, complete translocation into the stroma is followed by export to the inner membrane; in the ‘stop-transfer’ pathway, transmembrane domains within the mature part of the protein cause lateral exit from the TIC machinery. Recently, non-canonical, TOC/TIC-independent pathways for chloroplast protein targeting have been identified. In the first of these (right side of figure), proteins with non-cleavable, internal targeting signals are directed to the inner membrane by one or more novel pathways. Such import is energy dependent, but the translocon component(s) have not been identified. In the second (left side of figure), proteins are synthesized with a signal peptide for ER translocation. These proteins follow a pathway through the ER and Golgi, where they may become glycosylated; exactly how such proteins traverse the envelope membranes is not known. This figure has been adapted from Jarvis (2008).
Figure 5.
Figure 5.
The TOC/TIC protein import machinery. Diagram showing the main components implicated in the import of proteins into chloroplasts. Outer envelope membrane components form the TOC complex, while inner envelope membrane components form the TIC complex. Components are identified by their predicted molecular weights (black text), and some key functional domains are indicated (white text). The TOC core-complex is formed by Toc159, Toc34 and Toc75. The former two proteins are receptors that together control preprotein recognition, while Toc75 forms the translocation channel. Different isoforms of the receptors exist in Arabidopsis (red text), and these associate preferentially to form distinct TOC complexes with substrate specificity. This may prevent the bulk flow of abundant precursors from out-competing the import of relatively scarce preproteins during the (potentially rate-limiting) early stages of import; once this potential bottleneck has been passed, the import pathways may converge at a common TIC machinery. Cytosolic 14-3-3, Hsp70 and Hsp90 proteins may form ‘guidance complexes’ that direct preproteins to the TOC apparatus. It has been suggested that Toc12, Hsp70 and Tic22 act to facilitate the passage of preproteins across the intermembrane space. The inner membrane translocation channel may be formed by Tic110 and/or Tic20. The former protein is also thought to coordinate late events in import by recruiting stromal chaperones to import sites; Tic110 has been proposed to collaborate with Tic40 and Hsp93 in a putative stromal import motor complex. Upon arrival in the interior, the transit peptide is cleaved by SPP, and other chaperones (Cpn60 or Hsp70) may assist in the folding or onward transport of the mature domain. Finally, the Tic62, Tic55 and Tic32 components may enable the regulation of import in response to redox signals; these components might only be recruited to import sites under certain conditions or for certain preproteins.
Figure 6.
Figure 6.
Plastid division and the division machinery. (A) Chloroplasts dividing in Arabidopsis hypocotyl cells. (B) Localization of GFP-tagged DRP5B dynamin protein at the cytosolic side of the division site in Arabidopsis mesophyll cell chloroplasts. (C) Schematic representation of the plastid division machinery. A ‘bacterial’ division complex based on FtsZ forms first at the division site. This is then followed by the formation of the inner and outer PD rings, and finally the recruitment of DRP5B dynamin. Constriction at the vision site then initiates. Scale bars in (A) and (B), 10 μm.
Figure 7.
Figure 7.
Plastid inheritance in Arabidopsis. (A) A schematic representation illustrating the transmission of plastids and mitochondria and their nucleoids during pollen development. Note that organelle DNAs are represented as nucleoids detected by DAPI and other fluorescent dyes. Note also that the signals disappear in mature pollen. (B) Micrographs of a microspore (left) and a mature pollen grain (right) stained by DAPI (ecotype Columbia). Arrowheads indicate the prominent DAPI-stained signals, representing plastid nucleoids. (C) An example of maternal inheritance revealed by nuclear and plastid DNA polymorphisms. F1 plants were generated by reciprocal crosses between the ecotypes Columbia (Col) and Cape Verde Islands (Cvi). Total DNAs from the parents and the F1 plants were subjected to CAPS (Cleaved Amplified Polymorphic Sequence) analyses, to detect both nuclear and plastid DNA polymorphisms (top and bottom panels, respectively). DNA fragments representing Col and Cvi genotypes are indicated by magenta and cyan arrowheads, respectively. The CAPS markers used were G4711 for nuclear DNA, and ndhG for plastid DNA.

Similar articles

See all similar articles

Cited by 49 articles

See all "Cited by" articles

LinkOut - more resources

Feedback