PAPP5 Is Involved in the Tetrapyrrole Mediated Plastid Signalling during Chloroplast Development

Abstract

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.

HSP90, ZTL, PRR5 and HY5 integrate circadian and plastid signaling pathways to regulate CBF and COR expression.

“…S3C). This is similar to what has been reported for PHOTOSYNTHESIS-ASSOCIATED NUCLEAR GENE (PhANG) expression in earlier reports from Arabidopsis (Strand et al, 2003;Kindgren et al, 2012;Barajas-López et al, 2013b). In addition, CBF expression was repressed to less than 40% of control levels in response to norflurazon treatment in the wild type.…”

Establishment of Photosynthesis through Chloroplast Development Is Controlled by Two Distinct Regulatory Phases

“…2C). At 14 d, the thylakoid structure was complete and the size and the morphology of the cell culture chloroplasts were similar to those observed in Arabidopsis and pea (Pisum sativum) plants, where the chloroplasts typically are 5 to 10 mm long and have five to seven thylakoids per grana with intergranal thylakoids (Lopez-Juez and Pyke, 2005;Barajas-López et al, 2013b;Myouga et al, 2013).…”

Tetrapyrrole Signaling in Plants

“…As discussed above, researchers commonly elevated the endogenous levels of porphyrins with exogenous ALA because plant roots were thought to not take up porphyrins, such as Mg-Proto. More recently, Arabidopsis plants were reported to take up Mg-Proto through their roots when they were simply watered with solutions containing Mg-Proto ( Zhang et al, 2011a ; Kindgren et al, 2012 ; Barajas-López et al, 2013 ). An increase in the efficiency of Mg-Proto and hemin feeding was reported by first vacuum infiltrating seedlings prior to root feeding ( Zhang et al, 2013 ).…”

“…Exogenous Mg-Proto, Mg-ProtoME, or hemin doubled the cellular RNA content in Arabidopsis plants ( Zhang et al, 2011b ). Feeding both Mg-Proto and hemin to plants downregulated the expression of Lhcb and RbcS genes ( Zhang et al, 2011a , 2013 ; Kindgren et al, 2012 ; Barajas-López et al, 2013 ). This reduced expression of PhANGs that was induced by exogenous porphyrins was attenuated in gun1, long hypocotyl5 ( hy5 ), aba-insentive4 ( abi4 ), and phytochrome-associated protein phosphatase 5 ( papp5 ) ( Zhang et al, 2011a ; Kindgren et al, 2012 ; Barajas-López et al, 2013 ).…”

“…Feeding both Mg-Proto and hemin to plants downregulated the expression of Lhcb and RbcS genes ( Zhang et al, 2011a , 2013 ; Kindgren et al, 2012 ; Barajas-López et al, 2013 ). This reduced expression of PhANGs that was induced by exogenous porphyrins was attenuated in gun1, long hypocotyl5 ( hy5 ), aba-insentive4 ( abi4 ), and phytochrome-associated protein phosphatase 5 ( papp5 ) ( Zhang et al, 2011a ; Kindgren et al, 2012 ; Barajas-López et al, 2013 ). These findings are consistent with tetrapyrrole metabolism affecting plastid-to-nucleus signaling upstream of the chloroplastic pentatricopeptide protein GUN1 and with PAPP5 and the nuclear transcription factors HY5 and ABI4 contributing to this mechanism.…”