The Phosphoenolpyruvate/Phosphate Translocator Is Required for Phenolic Metabolism, Palisade Cell Development, and Plastid-Dependent Nuclear Gene Expression

Abstract

The Arabidopsis chlorophyll a/b binding protein (CAB) gene underexpressed 1 (cue1) mutant underexpresses light-regulated nuclear genes encoding chloroplast-localized proteins. cue1 also exhibits mesophyll-specific chloroplast and cellular defects, resulting in reticulate leaves. Both the gene underexpression and the leaf cell morphology phenotypes are dependent on light intensity. In this study, we determine that CUE1 encodes the plastid inner envelope phosphoenolpyruvate/phosphate translocator (PPT) and define amino acid residues that are critical for translocator function. The biosynthesis of aromatics is compromised in cue1, and the reticulate phenotype can be rescued by feeding aromatic amino acids. Determining that CUE1 encodes PPT indicates the in vivo role of the translocator in metabolic partitioning and reveals a mesophyll cell-specific requirement for the translocator in Arabidopsis leaves. The nuclear gene expression defects in cue1 suggest that a light intensity-dependent interorganellar signal is modulated through metabolites dependent on a plastid supply of phosphoenolpyruvate.

Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis

“…The transcriptional response of selected nuclear photosynthetic genes to variation in the excitation state of the two photosystems showed that the redox state of the plastoquinone pool controls the activity of the plastocyanin promoter (Pfannschmidt et al, 2001). The Arabidopsis ''chlorophyll a/b binding protein under-expression'' mutant cue1 offered additional evidence for the involvement of the redox state of the plastoquinone pool in the regulation of nuclear photosynthetic genes (Streatfield et al, 1999): lack of the CUE1-encoded phosphoenolpyruvate/phosphate translocator (PPT1) in the inner chloroplast envelope results in a reduced flux through the shikimate pathway and in a decrease in the plastoqinone pool, associated with an altered redox state of the thylakoids. The redox state of the stromal electron acceptors of PSI, in fact, seems to be crucial for the regulation of Lhcb genes (Pursiheimo et al, 2001).…”

Decrease of Photosystem II Photochemistry in Arabidopsis ppt1 Mutant Is Dependent on Leaf Age

“…Overexpression of heterologous PPT2 or orthophosphate dikinase (PPDK) can partially complement the phenotype of ppt1. Thus, the cue1 mutant phenotype cannot simply be explained by a general restriction of the supply of plastids with PEP via the PPT (López-Juez 1998;Streatfield et al 1999;Voll et al 2003).In the present study, we characterized a T-DNA-tagged allele of the ppt1 mutant that was selected on the basis of its high chlorophyll fluorescence phenotype. We compared the photosynthetic behavior of different aged leaves of the ppt1 mutant at one developmental stage.…”

“…The Arabidopsis ppt1 (or cue1) mutant is defective in AtPPT1 (at5g33320), which has been isolated in a screen for chlorophyll a/b binding protein (CAB) underexpressors (Li et al 1995; Knappe et al 2003). The affected gene in cue1 is a phosphoenolpyruvate (PEP)/phosphate translocator (PPT) of the plastid inner envelope membrane (Streatfield et al 1999). It appears that PEP is essential for plastid development and most nongreen plastids have been reported to be incapable of producing PEP from Calvin cycle intermediates (Flügge 1995; Voll et al 2002).…”

“…Overexpression of heterologous PPT2 or orthophosphate dikinase (PPDK) can partially complement the phenotype of ppt1. Thus, the cue1 mutant phenotype cannot simply be explained by a general restriction of the supply of plastids with PEP via the PPT (López-Juez 1998; Streatfield et al 1999;Voll et al 2003).…”

“…The morphological and gene underexpression phenotypes of ppt1 are light intensity dependent (Streatfield et al 1999). The chlorophyll and carotenoid components of the light-harvesting and photoprotective machinery are also diminished in ppt1 (Knappe et al 2003).…”