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Plastid encoded RNA polymerase activity and expression of photosynthesis genes required for embryo and seed development in Arabidopsis
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).ORCID iD: 0000-0001-6664-0471
2014 (English)In: Frontiers in Plant Science, 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.

Place, publisher, year, edition, pages
Keyword [en]
chloroplast, PEP, NEP, embryo development, photosynthesis, PRIN2, CSP41b
National Category
Biochemistry and Molecular Biology Other Biological Topics
URN: urn:nbn:se:umu:diva-96168DOI: 10.3389/fpls.2014.00385OAI: diva2:762294
Available from: 2014-11-11 Created: 2014-11-11 Last updated: 2015-09-16Bibliographically approved
In thesis
1. Get in tune: chloroplast and nucleus harmony
Open this publication in new window or tab >>Get in tune: chloroplast and nucleus harmony
2014 (English)Doctoral thesis, comprehensive summary (Other academic)
Alternative title[sv]
I samklang : harmoni mellan cellens kloroplaster och kärna
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.
Arabidopsis thaliana, chloroplast, development, gene expression
National Category
Biochemistry and Molecular Biology Developmental Biology Other Biological Topics
urn:nbn:se:umu:diva-96171 (URN)978-91-7601-172-0 (ISBN)
Public defence
2014-12-03, KBC-huset, Stora hörsalen, KB3B1, Umeå, 13:00 (English)
Available from: 2014-11-12 Created: 2014-11-11 Last updated: 2015-05-06Bibliographically approved

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Kremnev, DmitryStrand, Åsa
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