Martin MГјller Reisinger

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Love Bite. Primal Megaways. Several proteomic studies have identiWed additional putative components of the PEP complex of Arabidopsis, tobacco, and mustard Suzuki et al.

However, which of the identiWed factors truly associate with PEP complexes and their precise functions in transcription are still under discussion.

Originally, PEP-dependent transcription was assumed to play a role in later developmental stages of plants through transcription of photosynthesis-related genes Mullet However, recent studies revealed that PEP is already active in seeds and is required for eYcient germination Demarsy et al.

Together with the redundancy of some sigma factors and the lack of NEP and diversity of sigma factors in green algae, these results raise the question whether all of these factors are truly required for regulation of gene expression Lerbs-Mache Maier et al.

Transcript maturation Transcript maturation plays a vital role in the regulation of plastid gene expression. A broad range of nuclear-encoded factors has been described as performing and assisting in processing, editing, and splicing of plastid transcripts reviewed in Stern et al.

Recently, a proteomic study of nucleoids isolated from proplastids and mature chloroplasts from maize leaves identiWed a large number of proteins with RNA-related functions 1 indicating that transcript maturation occurs co-transcriptionally and 2 providing a set of new, so far uncharacterized proteins putatively involved in transcript maturation Majeran et al.

Here, we give a short overview of regulation of plastid transcript maturation. A detailed review on transcript processing is provided elsewhere in this issue.

Transcript processing In plastids, newly synthesized transcripts undergo several maturation steps prior to translation. Most genes are arranged in polycistronic gene clusters and transcribed from a single promoter Herrmann et al.

As translation of monocistronic RNAs is often more eVective than translation of polycistronic forms Barkan et al.

All these processes are dependent on nuclear-encoded proteins. Intercistronic cleavage is performed by endoribonucleases, which usually exhibit low sequence speciWcities, thus being supposed to be regulated by sequence-speciWc factors.

RNase E Schein et al. Some termini located in intergenic regions, e. Pfalz et al. Depending on splicing mechanisms and primary and secondary structures, organellar introns are classiWed into group I and group II introns, respectively Houghland et al.

Higher plant plastids exhibit only one group I intron located in the trnL transcript, whereas there are Wve in C.

However, there is a set of about 20 group II introns conserved among higher plant organellar genomes Schmitz-Linneweber and Barkan Originally, introns were mobile genetic elements encoding a maturase, which facilitates splicing of the host intron Eickbush ; Wank et al.

This ability has been widely lost in higher plants. The only remaining intronencoded maturase, MatK, is encoded by the trnK transcript and was found to co-immunopurify with all group IIA introns except clpP intron 2 Zoschke et al.

In fact, splicing of plastid introns is rather mediated by at least 12 nuclear-encoded proteins de Longevialle et al.

In addition, some proteins harboring diVerent sequence motifs are involved in splicing. However, despite the large number of splicing factors identiWed, there is no concrete mechanistic model for their function.

It is hypothesized that one or more factors interact with introns in a sequence-speciWc manner and change their folding, thus enabling recognition by general splicing factors de Longevialle et al.

Whether this is the general mechanism of plastid intron splicing needs to be further elucidated. It is a common mechanism in all plants, except liverworts Freyer et al.

In general, cytidine C is exchanged to uridine U in chloroplasts, but in some hornworts and ferns U is converted into C Kugita et al.

There are typically about 30 editing sites in plastids of vascular plants, e. Editing often restores conserved amino acids required for protein function Zito et al.

The mechanism of editing is so far unknown. However, both, cis- and trans-acting elements have been proposed to play a role.

On the cis-acting side sequence elements immediately upstream of the respective site are necessary, putatively serving as binding sites for trans-acting elements Bock et al.

Indeed, several exclusively nuclear-encoded transacting factors have been identiWed and all except one belong to the family of PPR proteins. It is the only factor that has been demonstrated to directly bind to its target editing site Okuda et al.

However, Wve PPR proteins have been reported to target up to three editing sites, suggesting that editing factors must be able to distinguish pyrimidines from purines and sometimes even recognize speciWc bases Hammani et al.

Regulation of translation Translation of plastid transcripts is performed by bacterialtype 70S ribosomes, in line with the prokaryotic origin of chloroplasts.

Although there is a certain degree of conservation among translation factors and most ribosomal proteins, bacterial and plastid translation machineries diVer Beligni et al.

Thus, both the large and the small ribosomal subunit also include nuclear-encoded plastid-speciWc ribosomal proteins PSRP , which were characterized in spinach, Arabidopsis and Chlamydomonas plastids Subramanian ; Yamaguchi et al.

Also, several nuclear-encoded proteins from Chlamydomonas and higher plants have been identiWed as transcript-speciWc translational regulators. The function of some of these factors will be discussed later.

Cis-acting elements in plastid transcripts Besides varying trans-acting factors, the organization of cis-elements displays a major diVerence between plastid and bacterial translation.

The SD sequence is located between 5 and 9 nucleotides upstream from the start codon and mediates correct positioning of the ribosome for translational initiation Laursen et al.

While translation of some transcripts is dependent on SD-like sequences rbcL, atpE, and rps14 from tobacco; psbA from Chlamydomonas , other transcripts are only partially dependent rps12 and petB from tobacco or independent of them psbA and atpB from tobacco; petD, atpB, atpE, rps4, and rps7 from Chlamydomonas; MayWeld et al.

Interestingly, the rps2 SD-like sequence from tobacco was even shown to be a negative regulatory element for translation Plader and Sugiura In tobacco this element is dispensable for translation Hirose and Sugiura , which stands in contrast to the requirement of a SD-like sequence in Chlamydomonas psbA-translation MayWeld et al.

Trans-acting translational regulators Trans-acting factors of translation are encoded in the nucleus and are generally speciWc to single transcripts.

Besides general regulation of plastid translation, many trans-factors were described as modulating translation in a light- and assembly-dependent manner Marin-Navaro et al.

The best-studied mechanism of light-regulated translation was described for the psbA transcript in Chlamydomonas.

As is the case for psbA, translation of psbD is induced by light Malnoe et al. Besides light regulation, plastid translation can also be modulated by the assembly status of proteins into their respective complexes.

Regulation of the cytochrome f subunit of the cytochrome b6f complex from Chlamydomonas is the best-studied process so far. When not assembled into the complex, cytochrome f interacts with MCA1, which usually binds and stabilizes the petA transcript and interacts with the translational factor TCA1 Raynaud et al.

Interaction with unassembled cytochrome f induces proteolysis of MCA1. This destabilizes the petA transcript and prevents its translation, which Wnally results in autoinhibition of cytochrome f synthesis Raynaud et al.

Regulation of translational initiation is clearly the most important step of plastid translation. However, elongation and termination also display targets for regulatory processes.

Recognition of stop codons and translational termination is dependent on release factors in both eukaryotes and prokaryotes. Post-translational regulation: protein maturation and complex assembly The last important steps of plastid gene expression include protein maturation, i.

In addition, thylakoid membrane proteins have to be inserted into the lipid bilayer or transported across it. All of these processes can occur post- or co-translationally and are dependent on both general and complexspeciWc auxiliary factors.

Membrane insertion Transport of complex subunits across or insertion into the thylakoid membrane is facilitated by four distinct pathways.

Both the secretory Sec and twin-arginine-translocase Tat pathways transport proteins across the thylakoid membrane into the lumen.

The maturation and assembly of the thylakoid membrane complexes are likely mediated by more speciWc factors since each complex and each subunit exhibit diVerent properties.

D1 is synthesized as a precursor pD1 with a C-terminal extension of nine amino acid residues in higher plants Marder et al.

During its integration into the thylakoid membrane, the D1 precursor is processed to its mature form by the nuclear-encoded lumenal carboxy-terminal processing protease CtpA; Anbudurai et al.

Recently, additional components facilitating the processing of the D1 precursor protein have been identiWed in Synechocystis PratA; Klinkert et al.

C-terminal processing was reported to be a prerequisite for binding of the manganese cluster to PSII Nixon et al. Another aspect of protein maturation is the binding of co-factors.

The photosynthetic complexes contain pigments for light harvesting and charge separation as well as redoxactive factors for electron transfer.

Similarly, PSI is associated with a large number of chlorophylls and xanthophylls, in line with the function of both photosystems in light harvesting.

Based on spectroscopic measurements using Synechococcus sp. Homologs of RubA are encoded by higher plant genomes but their function has not been elucidated so far.

As mentioned above, the cytochrome b6f complex is associated with four hemes. The two non-covalently bound b-type hemes are bound by the cytochrome b6 polypeptide and are believed to bind spontaneously Robertson et al.

On the contrary, the two c-type hemes bind covalently to cytochrome b6 and cytochrome f, respectively.

System III, which occurs in mitochondria of fungi, vertebrates and invertebrates, is the simplest system and consists of a heme lyase as the single component Dumont et al.

System I or Ccm system occurs in archaea, - and -proteobacteria and the mitochondria of plants and red algae, and consists of up to 10 membrane-bound proteins Allen et al.

System II operates in some gram-positive bacteria, cyanobacteria, some -, - and -proteobacteria and plastids of plants and algae Kranz et al.

Martin MГјller Reisinger - Beiträge zum Thema Martin Reisinger

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In fact, splicing of plastid introns is rather mediated by at least 12 nuclear-encoded proteins de Longevialle et al. In addition, some proteins harboring diVerent sequence motifs are involved in splicing.

However, despite the large number of splicing factors identiWed, there is no concrete mechanistic model for their function.

It is hypothesized that one or more factors interact with introns in a sequence-speciWc manner and change their folding, thus enabling recognition by general splicing factors de Longevialle et al.

Whether this is the general mechanism of plastid intron splicing needs to be further elucidated. It is a common mechanism in all plants, except liverworts Freyer et al.

In general, cytidine C is exchanged to uridine U in chloroplasts, but in some hornworts and ferns U is converted into C Kugita et al. There are typically about 30 editing sites in plastids of vascular plants, e.

Editing often restores conserved amino acids required for protein function Zito et al. The mechanism of editing is so far unknown. However, both, cis- and trans-acting elements have been proposed to play a role.

On the cis-acting side sequence elements immediately upstream of the respective site are necessary, putatively serving as binding sites for trans-acting elements Bock et al.

Indeed, several exclusively nuclear-encoded transacting factors have been identiWed and all except one belong to the family of PPR proteins. It is the only factor that has been demonstrated to directly bind to its target editing site Okuda et al.

However, Wve PPR proteins have been reported to target up to three editing sites, suggesting that editing factors must be able to distinguish pyrimidines from purines and sometimes even recognize speciWc bases Hammani et al.

Regulation of translation Translation of plastid transcripts is performed by bacterialtype 70S ribosomes, in line with the prokaryotic origin of chloroplasts.

Although there is a certain degree of conservation among translation factors and most ribosomal proteins, bacterial and plastid translation machineries diVer Beligni et al.

Thus, both the large and the small ribosomal subunit also include nuclear-encoded plastid-speciWc ribosomal proteins PSRP , which were characterized in spinach, Arabidopsis and Chlamydomonas plastids Subramanian ; Yamaguchi et al.

Also, several nuclear-encoded proteins from Chlamydomonas and higher plants have been identiWed as transcript-speciWc translational regulators.

The function of some of these factors will be discussed later. Cis-acting elements in plastid transcripts Besides varying trans-acting factors, the organization of cis-elements displays a major diVerence between plastid and bacterial translation.

The SD sequence is located between 5 and 9 nucleotides upstream from the start codon and mediates correct positioning of the ribosome for translational initiation Laursen et al.

While translation of some transcripts is dependent on SD-like sequences rbcL, atpE, and rps14 from tobacco; psbA from Chlamydomonas , other transcripts are only partially dependent rps12 and petB from tobacco or independent of them psbA and atpB from tobacco; petD, atpB, atpE, rps4, and rps7 from Chlamydomonas; MayWeld et al.

Interestingly, the rps2 SD-like sequence from tobacco was even shown to be a negative regulatory element for translation Plader and Sugiura In tobacco this element is dispensable for translation Hirose and Sugiura , which stands in contrast to the requirement of a SD-like sequence in Chlamydomonas psbA-translation MayWeld et al.

Trans-acting translational regulators Trans-acting factors of translation are encoded in the nucleus and are generally speciWc to single transcripts.

Besides general regulation of plastid translation, many trans-factors were described as modulating translation in a light- and assembly-dependent manner Marin-Navaro et al.

The best-studied mechanism of light-regulated translation was described for the psbA transcript in Chlamydomonas.

As is the case for psbA, translation of psbD is induced by light Malnoe et al. Besides light regulation, plastid translation can also be modulated by the assembly status of proteins into their respective complexes.

Regulation of the cytochrome f subunit of the cytochrome b6f complex from Chlamydomonas is the best-studied process so far.

When not assembled into the complex, cytochrome f interacts with MCA1, which usually binds and stabilizes the petA transcript and interacts with the translational factor TCA1 Raynaud et al.

Interaction with unassembled cytochrome f induces proteolysis of MCA1. This destabilizes the petA transcript and prevents its translation, which Wnally results in autoinhibition of cytochrome f synthesis Raynaud et al.

Regulation of translational initiation is clearly the most important step of plastid translation. However, elongation and termination also display targets for regulatory processes.

Recognition of stop codons and translational termination is dependent on release factors in both eukaryotes and prokaryotes.

Post-translational regulation: protein maturation and complex assembly The last important steps of plastid gene expression include protein maturation, i.

In addition, thylakoid membrane proteins have to be inserted into the lipid bilayer or transported across it.

All of these processes can occur post- or co-translationally and are dependent on both general and complexspeciWc auxiliary factors.

Membrane insertion Transport of complex subunits across or insertion into the thylakoid membrane is facilitated by four distinct pathways.

Both the secretory Sec and twin-arginine-translocase Tat pathways transport proteins across the thylakoid membrane into the lumen.

The maturation and assembly of the thylakoid membrane complexes are likely mediated by more speciWc factors since each complex and each subunit exhibit diVerent properties.

D1 is synthesized as a precursor pD1 with a C-terminal extension of nine amino acid residues in higher plants Marder et al. During its integration into the thylakoid membrane, the D1 precursor is processed to its mature form by the nuclear-encoded lumenal carboxy-terminal processing protease CtpA; Anbudurai et al.

Recently, additional components facilitating the processing of the D1 precursor protein have been identiWed in Synechocystis PratA; Klinkert et al.

C-terminal processing was reported to be a prerequisite for binding of the manganese cluster to PSII Nixon et al.

Another aspect of protein maturation is the binding of co-factors. The photosynthetic complexes contain pigments for light harvesting and charge separation as well as redoxactive factors for electron transfer.

Similarly, PSI is associated with a large number of chlorophylls and xanthophylls, in line with the function of both photosystems in light harvesting.

Based on spectroscopic measurements using Synechococcus sp. Homologs of RubA are encoded by higher plant genomes but their function has not been elucidated so far.

As mentioned above, the cytochrome b6f complex is associated with four hemes. The two non-covalently bound b-type hemes are bound by the cytochrome b6 polypeptide and are believed to bind spontaneously Robertson et al.

On the contrary, the two c-type hemes bind covalently to cytochrome b6 and cytochrome f, respectively. System III, which occurs in mitochondria of fungi, vertebrates and invertebrates, is the simplest system and consists of a heme lyase as the single component Dumont et al.

System I or Ccm system occurs in archaea, - and -proteobacteria and the mitochondria of plants and red algae, and consists of up to 10 membrane-bound proteins Allen et al.

System II operates in some gram-positive bacteria, cyanobacteria, some -, - and -proteobacteria and plastids of plants and algae Kranz et al.

In plastids, it is required for the biogenesis of cytochromes f and c6 Rurek Cytochrome f possesses a classical CXXCH heme-binding motif whose two cysteines form thioether linkages with the vinyl groups of the heme.

The apoprotein is synthesized in the plastid stroma but targeted to the electropositive thylakoid lumen in a Sec-dependent way Rohl and van Wijk , where the conversion of apo- to holo-cytochrome f occurs.

Ligation of heme to cytochrome f requires several steps. The heme is synthesized in the stroma, and needs to be transported to the lumen.

There it must be transferred to or kept in its reduced state to assure that the vinyl groups are chemically active.

Similarly, the cysteine residues of the heme-binding motif in the cytochrome must be reduced to form thioether bonds to the heme vinyl groups Kranz et al.

CCS1, on the other hand, is supposed to chaperone reduced apocytochromes Rurek HCF, a thioredoxin-like protein from Arabidopsis was also found to be required for cytochrome f maturation Lennartz et al.

Also, the thiol disulWde transporter homolog CCDA is required for cytochrome f maturation in Arabidopsis but it has not yet been characterized in Chlamydomonas Page et al.

In contrast to cytochrome f, cytochrome b6 binds its c-type heme heme ci on the electronegative, i. Apparently, insertion of heme ci to cytochrome b6 occurs after binding of the non-covalent b-type hemes and requires several steps in which diVerent CCB-CCB and CCB-cytochrome b6 complexes are formed Saint-Marcoux et al.

Since heme synthesis and incorporation into apocytochrome b6 take place on the same side of the thylakoid membrane, no thioredox or translocation machinery is required and the CCB proteins are more likely to operate as a heme-chaperoning and -delivery system de Vitry How the CCB proteins mediate heme attachment to apocytochrome b6 and whether there are more, so far undiscovered factors participating in these processes still needs to be elucidated in future studies.

Assembly of complexes Assembly of thylakoid membrane complexes is accomplished in a step-by-step manner. Usually, one protein serves as an anchor or scaVold for subsequent assembly steps.

For PSII, a complex consisting of the D2 protein and the and subunits of cytochrome b seems to be the initiation point of assembly Komenda et al.

The addition of the inner antenna protein CP47 leads to the formation of the RC47 complex and facilitates binding of several small subunits like the phosphoprotein PsbH Komenda et al.

After incorporation of CP43 the monomeric core complex is complete and assembly of the manganese cluster and oxygen-evolving complex can occur, as well as dimerization and supercomplex formation Rokka et al.

A multitude of assembly-assisting proteins has been identiWed for PSII, although their mode of action is largely unknown. PSII is not only synthesized de novo, but it is constantly renewed due to photooxidative damage Aro et al.

Damaged PSII complexes are phosphorylated and migrate from the grana to the stoma lamellae, where D1 is degraded and replaced by a newly synthesized protein Mulo et al.

Degradation is predominantly mediated by FtsH and Deg proteases that act in a cooperative manner Kato and Sakamoto ; Kato et al. Chlorophyll released during repair may be bound by ELIP proteins in higher plants, which belong to the LIL light-harvestinglike protein family Hutin et al.

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