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Get in tune: chloroplast and nucleus harmony
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. (Åsa Strand)
2014 (English)Doctoral thesis, comprehensive summary (Other academic)Alternative title
I samklang : harmoni mellan cellens kloroplaster och kärna (Swedish)
Abstract [en]

Photosynthetic eukaryots emerged as a result of several billion years of evolution between proeukaryotic cell and ancestral cyanobacteria that formed modern chloroplasts. The symbiotic relationship led to significant rearrangements in the genomes of the plastid and the nucleus: as many as 90 % of all the plastid genes were transferred to the nucleus. The gene transfer has been accompanied by the development of sophisticated regulatory signaling networks originating in the organelle (retrograde) and in the nucleus (anterograde) that coordinate development of the plastid and ensure adequate cell responses to stress signals. In this thesis I have demonstrated that transcriptional activity of PEP in the chloroplast is essential for proper embryo and seedling development in Arabidopsis thaliana. The function of PEP is dependent on the nuclear encoded PEPassociated factor PRIN2 that is able to sense the redox status of the plastid during seedling development and different stress. In response to the plastid status PRIN2 modulates the transcription activity of the PEP enzyme complex. We further established that PRIN2, as an essential component for full PEP activity, is also required to emit the Plastid Gene Expression (PGE) retrograde signal to regulate the Photosynthesis-Associated Nuclear Genes (PhANG) in the nucleus during early seedling growth via GUN1. On the other hand, regulation of PhANG expression during the High Light (HL) conditions requires functional PRIN2 and PEP activity but is GUN1-independent. Another retrograde signal produced by the developing chloroplast is associated with the tetrapyrrole biosynthesis pathway. We have established that accumulation of the chlorophyll intermediate MgProtoIX-ME in the crd mutant triggers repression of the PhANG expression, and this negative signal is mediated by a cytoplasmic protein complex containing the PAPP5 phosphatase. The nuclear targets that receive the tetrapyrrole mediated signal are GLK1 and GLK2 transcription factors that control the PhANG expression and the expression of the enzymes involved in the biosynthesis of chlorophyll.

Abstract [sv]

Fotosyntetiserande eukaryoter uppstod från en endosymbiotisk interaktion under några miljarder år mellan en ur-eukaryot och kloroplastens förfader, den prokaryota cyanobakterien. Den symbiotiska händelsen ledde till att kloroplastens och kärnans genom blev väsentligt förändrade. Så småningom överförde kloroplasten så många som 90 % av dess gener till cellkärnan. För att koordinera genutrycket från de två genomen utvecklade växtcellen ett sofistikerat signalsystemen som inkluderar: plastid-kärn (retrograd) och kärn-plastid (anterograd) signalering som styr kloroplastens utveckling och förmåga att anpassa sig till stressförhållanden. Den här avhandlingen beskriver kloroplastens maskineri för genuttryck (PEP) som en nödvändig komponent för embryo- och växtutvecklingen hos Arabidopsis thaliana. PEP funktionen är beroende av det kärnkodade kloroplastproteinet PRIN2 som är associerat med PEP. PRIN2 mottar redox signaler från plastiden och förändrar genuttrycksaktivitet under kloroplastens utvecklingen eller under olika stressförhållanden. Jag visar dessutom att PRIN2 spelar en viktig roll i överföring av kloroplastens signal som kommunicerar genuttrycksaktivitet (PGE) via GUN1 till kärnan där den styr uttryck av de kärnkodade fotosyntetesgenerna (PhANG). Under högljus stressförhållanden styrs dock PhANG-uttrycket av signaler som uppstår från PEP-aktivitet och PRIN2 men som är oberoende av GUN1. Vidare finns det en annan retrograd signal som har sitt ursprung i biosyntesen av tetrapyrroler. Jag har visat att ackumuleringen av tetrapyrrolen MgProtoIX-ME i crd-mutanten framkallar nedreglering av PhANG-uttryck genom interaktion med ett fosfatas (PAPP5) i cytosolen. GLK1 and GLK2 är två transkriptionsfaktorer som tar emot den tetrapyrrole-medierade signalen i sin tur styr biosyntes av chlorofyll och PhANG uttryck.

Place, publisher, year, edition, pages
Umeå: Umeå University , 2014. , 87 p.
Keyword [en]
Arabidopsis thaliana, chloroplast, development, gene expression
National Category
Biochemistry and Molecular Biology Developmental Biology Other Biological Topics
Identifiers
URN: urn:nbn:se:umu:diva-96171ISBN: 978-91-7601-172-0 (print)OAI: oai:DiVA.org:umu-96171DiVA: diva2:762300
Public defence
2014-12-03, KBC-huset, Stora hörsalen, KB3B1, Umeå, 13:00 (English)
Opponent
Supervisors
Available from: 2014-11-12 Created: 2014-11-11 Last updated: 2015-05-06Bibliographically approved
List of papers
1. The plastid redox insensitive 2 mutant of Arabidopsis is impaired in PEP activity and high light-dependent plastid redox signalling to the nucleus
Open this publication in new window or tab >>The plastid redox insensitive 2 mutant of Arabidopsis is impaired in PEP activity and high light-dependent plastid redox signalling to the nucleus
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2012 (English)In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 70, no 2, 279-291 p.Article in journal (Refereed) Published
Abstract [en]

The photosynthetic apparatus is composed of proteins encoded by genes from both the nuclear and the chloroplastic genomes. The activities of the nuclear and chloroplast genomes must therefore be closely coordinated through intracellular signalling. The plastids produce multiple retrograde signals at different times of their development, and in response to changes in the environment. These signals regulate the expression of nuclear-encoded photosynthesis genes to match the current status of the plastids. Using forward genetics we identified PLASTID REDOX INSENSITIVE 2 (PRIN2), a chloroplast component involved in redox-mediated retrograde signalling. The allelic mutants prin2-1 and prin2-2 demonstrated a misregulation of photosynthesis-associated nuclear gene expression in response to excess light, and an inhibition of photosynthetic electron transport. As a consequence of the misregulation of LHCB1.1 and LHCB2.4, the prin2 mutants displayed a high irradiance-sensitive phenotype with significant photoinactivation of photosystem II, indicated by a reduced variable to maximal fluorescence ratio (Fv/Fm). PRIN2 is localized to the nucleoids, and plastid transcriptome analyses demonstrated that PRIN2 is required for full expression of genes transcribed by the plastid-encoded RNA polymerase (PEP). Similarly to the prin2 mutants, the ys1 mutant with impaired PEP activity also demonstrated a misregulation of LHCB1.1 and LHCB2.4 expression in response to excess light, suggesting a direct role for PEP activity in redox-mediated retrograde signalling. Taken together, our results indicate that PRIN2 is part of the PEP machinery, and that the PEP complex responds to photosynthetic electron transport and generates a retrograde signal, enabling the plant to synchronize the expression of photosynthetic genes from both the nuclear and plastidic genomes.

Keyword
chloroplast, redox, signalling, PEP, photosynthesis, LHCB
National Category
Biological Sciences
Identifiers
urn:nbn:se:umu:diva-55360 (URN)10.1111/j.1365-313X.2011.04865.x (DOI)000302300100008 ()
Note

In accordance with a correction published in The Plant Journal vol. 70, issue 2, page 366 (available at http://dx.doi.org/10.1111/j.1365-313X.2012.04978.x) Tatjana Kleine has been added to the list of authors for this paper.

Available from: 2012-05-31 Created: 2012-05-14 Last updated: 2017-12-07Bibliographically approved
2. PAPP5 is involved in the tetrapyrrole mediated plastid signalling during chloroplast development
Open this publication in new window or tab >>PAPP5 is involved in the tetrapyrrole mediated plastid signalling during chloroplast development
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2013 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 8, no 3, e60305Article in journal (Refereed) Published
Abstract [en]

The initiation of chloroplast development in the light is dependent on nuclear encoded components. The nuclear genes encoding key components in the photosynthetic machinery are regulated by signals originating in the plastids. These plastid signals play an essential role in the regulation of photosynthesis associated nuclear genes (PhANGs) when proplastids develop into chloroplasts. One of the plastid signals is linked to the tetrapyrrole biosynthesis and accumulation of the intermediates the Mg-ProtoIX and its methyl ester Mg-ProtoIX-ME. Phytochrome-Associated Protein Phosphatase 5 (PAPP5) was isolated in a previous study as a putative Mg-ProtoIX interacting protein. In order to elucidate if there is a biological link between PAPP5 and the tetrapyrrole mediated signal we generated double mutants between the Arabidopsis papp5 and the crd mutants. The crd mutant over-accumulates Mg-ProtoIX and Mg-ProtoIX-ME and the tetrapyrrole accumulation triggers retrograde signalling. The crd mutant exhibits repression of PhANG expression, altered chloroplast morphology and a pale phenotype. However, in the papp5crd double mutant, the crd phenotype is restored and papp5crd accumulated wild type levels of chlorophyll, developed proper chloroplasts and showed normal induction of PhANG expression in response to light. Tetrapyrrole feeding experiments showed that PAPP5 is required to respond correctly to accumulation of tetrapyrroles in the cell and that PAPP5 is most likely a component in the plastid signalling pathway down stream of the tetrapyrrole Mg-ProtoIX/Mg-ProtoIX-ME. Inhibition of phosphatase activity phenocopied the papp5crd phenotype in the crd single mutant demonstrating that PAPP5 phosphatase activity is essential to mediate the retrograde signal and to suppress PhANG expression in the crd mutant. Thus, our results suggest that PAPP5 receives an inbalance in the tetrapyrrole biosynthesis through the accumulation of Mg-ProtoIX and acts as a negative regulator of PhANG expression during chloroplast biogenesis and development.

National Category
Plant Biotechnology
Identifiers
urn:nbn:se:umu:diva-71099 (URN)10.1371/journal.pone.0060305 (DOI)000317263900068 ()
Available from: 2013-06-12 Created: 2013-05-20 Last updated: 2017-12-06Bibliographically approved
3. The CRYPTOCHROME1-Dependent Response to Excess Light Is Mediated through the Transcriptional Activators ZINC FINGER PROTEIN EXPRESSED IN INFLORESCENCE MERISTEM LIKE1 and ZML2 in Arabidopsis
Open this publication in new window or tab >>The CRYPTOCHROME1-Dependent Response to Excess Light Is Mediated through the Transcriptional Activators ZINC FINGER PROTEIN EXPRESSED IN INFLORESCENCE MERISTEM LIKE1 and ZML2 in Arabidopsis
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2012 (English)In: The Plant Cell, ISSN 1040-4651, E-ISSN 1532-298X, Vol. 24, no 7, 3009-3025 p.Article in journal (Refereed) Published
Abstract [en]

Exposure of plants to light intensities that exceed the electron utilization capacity of the chloroplast has a dramatic impact on nuclear gene expression. The photoreceptor Cryptochrome 1 (cry1) is essential to the induction of genes encoding photoprotective components in Arabidopsis thaliana. Bioinformatic analysis of the cry1 regulon revealed the putative ciselement CryR1 (GnTCKAG), and here we demonstrate an interaction between CryR1 and the zinc finger GATA-type transcription factors ZINC FINGER PROTEIN EXPRESSED IN INFLORESCENCE MERISTEM LIKE1 (ZML1) and ZML2. The ZML proteins specifically bind to the CryR1 cis-element as demonstrated in vitro and in vivo, and TCTAG was shown to constitute the core sequence required for ZML2 binding. In addition, ZML2 activated transcription of the yellow fluorescent protein reporter gene driven by the CryR1 cis-element in Arabidopsis leaf protoplasts. T-DNA insertion lines for ZML2 and its homolog ZML1 demonstrated misregulation of several cry1-dependent genes in response to excess light. Furthermore, the zml1 and zml2 T-DNA insertion lines displayed a high irradiance-sensitive phenotype with significant photoinactivation of photosystem II (PSII), indicated by reduced maximum quantum efficiency of PSII, and severe photobleaching. Thus, we identified the ZML2 and ZML1 GATA transcription factors as two essential components of the cry1-mediated photoprotective response.

National Category
Biological Sciences
Identifiers
urn:nbn:se:umu:diva-61232 (URN)10.1105/tpc.112.100099 (DOI)000308352800024 ()
Available from: 2012-11-07 Created: 2012-11-07 Last updated: 2017-12-07Bibliographically approved
4. Plastid encoded RNA polymerase activity and expression of photosynthesis genes required for embryo and seed development in Arabidopsis
Open this publication in new window or tab >>Plastid encoded RNA polymerase activity and expression of photosynthesis genes required for embryo and seed development in Arabidopsis
2014 (English)In: Frontiers in Plant Science, ISSN 1664-462X, E-ISSN 1664-462XArticle in journal (Refereed) Published
Abstract [en]

Chloroplast biogenesis and function is essential for proper plant embryo and seed development but the molecular mechanisms underlying the role of plastids during embryogenesis are poorly understood. Expression of plastid encoded genes is dependent on two different transcription machineries; a plastid-encoded bacterial-type RNA polymerase (PEP) and a nuclear-encoded phage-type RNA polymerase (NEP), which recognize distinct types of promoters. However, the division of labor between PEP and NEP during plastid development and in mature chloroplasts is unclear. We show here that PLASTID REDOX INSENSITIVE 2 (PRIN2) and CHLOROPLAST STEM-LOOP BINDING PROTEIN 41 kDa (CSP41b), two proteins identified in plastid nucleoid preparations, are essential for proper plant embryo development. Using Co-IP assays and native PAGE we have shown a direct physical interaction between PRIN2 and CSP41b. Moreover, PRIN2 and CSP41b form a distinct protein complex in vitro that binds DNA. The prin2.2 and csp41b-2 single mutants displayed pale phenotypes, abnormal chloroplasts with reduced transcript levels of photosynthesis genes and defects in embryo development. The respective csp41b-2prin2.2 homo/heterozygote double mutants produced abnormal white colored ovules and shrunken seeds. Thus, the csp41b-2prin2.2 double mutant is embryo lethal. In silico analysis of available array data showed that a large number of genes traditionally classified as PEP dependent genes are transcribed during early embryo development from the pre-globular stage to the mature-green-stage. Taken together, our results suggest that PEP activity and consequently the switch from NEP to PEP activity, is essential during embryo development and that the PRIN2-CSP41b DNA binding protein complex possibly is important for full PEP activity during this process.

Keyword
chloroplast, PEP, NEP, embryo development, photosynthesis, PRIN2, CSP41b
National Category
Biochemistry and Molecular Biology Other Biological Topics
Identifiers
urn:nbn:se:umu:diva-96168 (URN)10.3389/fpls.2014.00385 (DOI)
Available from: 2014-11-11 Created: 2014-11-11 Last updated: 2017-12-05Bibliographically approved
5. Redox regulation of PEP activity during seedling development in Arabidopsis
Open this publication in new window or tab >>Redox regulation of PEP activity during seedling development in Arabidopsis
(English)Manuscript (preprint) (Other academic)
National Category
Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:umu:diva-96176 (URN)
Available from: 2014-11-11 Created: 2014-11-11 Last updated: 2015-05-06Bibliographically approved

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