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.2005 Feb;4(2):253-61.
doi: 10.1128/EC.4.2.253-261.2005.

Multiple metabolic roles for the nonphotosynthetic plastid of the green alga Prototheca wickerhamii

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Multiple metabolic roles for the nonphotosynthetic plastid of the green alga Prototheca wickerhamii

Tudor Borza et al. Eukaryot Cell.2005 Feb.

Abstract

The presence of plastids in diverse eukaryotic lineages that have lost the capacity for photosynthesis is well documented. The metabolic functions of such organelles, however, are poorly understood except in the case of the apicoplast in the Apicomplexa, a group of intracellular parasites including Plasmodium falciparum, and the plastid of the green alga Helicosporidium sp., a parasite for which the only host-free stage identified in nature so far is represented by cysts. As a first step in the reconstruction of plastid functions in a nonphotosynthetic, predominantly free-living organism, we searched for expressed sequence tags (ESTs) that correspond to nucleus-encoded plastid-targeted polypeptides in the green alga Prototheca wickerhamii. From 3,856 ESTs, we found that 71 unique sequences (235 ESTs) correspond to different nucleus-encoded putatively plastid-targeted polypeptides. The identified proteins predict that carbohydrate, amino acid, lipid, tetrapyrrole, and isoprenoid metabolism as well as de novo purine biosynthesis and oxidoreductive processes take place in the plastid of P. wickerhamii. Mg-protoporphyrin accumulation and, therefore, plastid-to-nucleus signaling might also occur in this nonphotosynthetic organism, as we identified a transcript which encodes subunit I of Mg-chelatase, the enzyme which catalyzes the first committed step in chlorophyll synthesis. Our data indicate a far more complex metabolism in P. wickerhamii's plastid compared with the metabolic pathways predicted to be located in the apicoplast of P. falciparum and the plastid of Helicosporidium sp.

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Figures

FIG. 1.
FIG. 1.
Flow diagram of the procedures used to identify and analyze putatively plastid-targeted polypeptides inP. wickerhamii.
FIG. 2.
FIG. 2.
Overview of the metabolism and pathways predicted to be located in the plastids ofP. wickerhamii,Helicosporidium sp., andP. falciparum based on available data. The conversion of imported trioses to acetyl-coenzyme A seems to be present in all three organisms, while that of glucose-6-phosphate to starch is present only inP. wickerhamii. Enzymes are represented by solid circles, and substrates are underlined. Other pathways (indicated in boxes) predicted to be present in the plastids ofP. wickerhamii,Helicosporidium sp., andP. falciparum are shown on a white background, inP. wickerhamii andHelicosporidium sp. but not inP. falciparum are on a striped background, and only inP. wickerhamii are on a grey background. ACCase, acetyl-coenzyme A carboxylase; G1P, glucose-1-phosphate; G1PAT, glucose-1-phosphate adenylyltransferase; G6P, glucose-6-phosphate; PDH, pyruvate dehydrogenase complex; PGDH, phosphoglycerate dehydrogenase; PK, pyruvate kinase; PRPP, phosphoribosyl pyrophosphate; TIC, translocon at the inner envelope membrane of chloroplasts; TOC, translocon at the outer envelope membrane of chloroplasts. The number of identified unique sequences that are predicted to encode plastid-targeted enzymes inP. wickerhamii and are associated with the various metabolic processes are indicated in parentheses; the pentose phosphate pathway and triose phosphate transporters are probably present inP. wickerhamii, although no transcripts associated with these functions were detected.
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