PAPP5 is involved in the tetrapyrrole mediated plastid signalling during chloroplast development.

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 photosy...

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Autores principales: Juan de Dios Barajas-López, Dmitry Kremnev, Jehad Shaikhali, Aurora Piñas-Fernández, Asa Strand
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Publicado: Public Library of Science (PLoS) 2013
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spelling oai:doaj.org-article:0f07fe4b7a0e463ab574dff646df739b2021-11-18T07:51:18ZPAPP5 is involved in the tetrapyrrole mediated plastid signalling during chloroplast development.1932-620310.1371/journal.pone.0060305https://doaj.org/article/0f07fe4b7a0e463ab574dff646df739b2013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23555952/?tool=EBIhttps://doaj.org/toc/1932-6203The 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.Juan de Dios Barajas-LópezDmitry KremnevJehad ShaikhaliAurora Piñas-FernándezAsa StrandPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 8, Iss 3, p e60305 (2013)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Juan de Dios Barajas-López
Dmitry Kremnev
Jehad Shaikhali
Aurora Piñas-Fernández
Asa Strand
PAPP5 is involved in the tetrapyrrole mediated plastid signalling during chloroplast development.
description 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.
format article
author Juan de Dios Barajas-López
Dmitry Kremnev
Jehad Shaikhali
Aurora Piñas-Fernández
Asa Strand
author_facet Juan de Dios Barajas-López
Dmitry Kremnev
Jehad Shaikhali
Aurora Piñas-Fernández
Asa Strand
author_sort Juan de Dios Barajas-López
title PAPP5 is involved in the tetrapyrrole mediated plastid signalling during chloroplast development.
title_short PAPP5 is involved in the tetrapyrrole mediated plastid signalling during chloroplast development.
title_full PAPP5 is involved in the tetrapyrrole mediated plastid signalling during chloroplast development.
title_fullStr PAPP5 is involved in the tetrapyrrole mediated plastid signalling during chloroplast development.
title_full_unstemmed PAPP5 is involved in the tetrapyrrole mediated plastid signalling during chloroplast development.
title_sort papp5 is involved in the tetrapyrrole mediated plastid signalling during chloroplast development.
publisher Public Library of Science (PLoS)
publishDate 2013
url https://doaj.org/article/0f07fe4b7a0e463ab574dff646df739b
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AT jehadshaikhali papp5isinvolvedinthetetrapyrrolemediatedplastidsignallingduringchloroplastdevelopment
AT aurorapinasfernandez papp5isinvolvedinthetetrapyrrolemediatedplastidsignallingduringchloroplastdevelopment
AT asastrand papp5isinvolvedinthetetrapyrrolemediatedplastidsignallingduringchloroplastdevelopment
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