Eubacterial origin of nuclear genes for chloroplast and cytosolic glucose-6-phosphate isomerase from spinach: sampling eubacterial gene diversity in eukaryotic chromosomes through symbiosis

Nowitzki, Ulrich; Flechner, Anke; Kellermann, Josef; Hasegawa, Masami; Schnarrenberger, Claus; Martin, William

doi:10.1016/s0378-1119(98)00229-7

Cited by 33 publications

(23 citation statements)

References 32 publications

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“…None of the introns inserted within these two genes can be aligned at the same position. Our finding supports the endosymbiotic origin of the plastidial PGI genes (Nowitzki et al, 1998).…”

Section: Cloning and Sequencing Of The Arabidopsis Pgi1 Genesupporting

confidence: 87%

“…Two isozymes of PGI exist in Arabidopsis, one in the plastids and the other in the cytosol (Caspar et al, 1985). Several plant cytosolic PGIs (Thomas et al, 1992(Thomas et al, , 1993Nowitzki et al, 1998) and a plastidial PGI of spinach (Nowitzki et al, 1998) were cloned and characterized mainly to investigate the evolutionary history of eukaryotic PGI genes. Borchert et al (1989) showed that there is a plastid transporter for hexose phosphate that transports cytosolic Glc-6-P into plastids but does not transport Glc-1-P.…”

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confidence: 99%

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Mutation of Arabidopsis Plastid Phosphoglucose Isomerase Affects Leaf Starch Synthesis and Floral Initiation

et al. 2000

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We isolated pgi1-1, an Arabidopsis mutant with a decreased plastid phospho-glucose (Glc) isomerase activity. While pgi1-1 mutant has a deficiency in leaf starch synthesis, it accumulates starch in root cap cells. It has been shown that a plastid transporter for hexose phosphate transports cytosolic Glc-6-P into plastids and expresses restricted mainly to the heterotrophic tissues. The decreased starch content in leaves of the pgi1-1 mutant indicates that cytosolic Glc-6-P cannot be efficiently transported into chloroplasts to complement the mutant's deficiency in chloroplastic phospho-Glc isomerase activity for starch synthesis. We cloned the Arabidopsis PGI1 gene and showed that it encodes the plastid phospho-Glc isomerase. The pgi1-1 allele was found to have a single nucleotide substitution, causing a Ser to Phe transition. While the flowering times of the Arabidopsis starch-deficient mutants pgi1, pgm1, and adg1 were similar to that of the wild type under long-day conditions, it was significantly delayed under short-day conditions. The pleiotropic phenotype of late flowering conferred by these starch metabolic mutations suggests that carbohydrate metabolism plays an important role in floral initiation.Most plants synthesize starch in their chloroplasts during photosynthesis and degrade it during the subsequent night. The regulation of transitory starch metabolism in photosynthetic tissues is clearly different from the long-term, reserve starch metabolism in non-photosynthetic tissues (Caspar, 1994). Many mutations that affect the starch of certain cereal seeds, potato, pea, and Chlamydomonas reinhardtii have been isolated and characterized (Hannah, 1997). Although studies of these mutants have greatly added to our knowledge of starch metabolism, these mutants studied are relatively specific for the reserve and reproductive organs, and do not affect starch metabolism in the vegetative parts of plants. Mutants that affect starch metabolism in the vegetative parts of Arabidopsis would be useful to extend our understanding on starch metabolism and its role in the plant.Previously, several nuclear-encoded, recessive mutants of Arabidopsis, pgm1, adg1, and adg2, were isolated and characterized for their low starch content or lack of starch in leaves (Caspar et al

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“…None of the introns inserted within these two genes can be aligned at the same position. Our finding supports the endosymbiotic origin of the plastidial PGI genes (Nowitzki et al, 1998).…”

Section: Cloning and Sequencing Of The Arabidopsis Pgi1 Genesupporting

confidence: 87%

mentioning

confidence: 99%

Mutation of Arabidopsis Plastid Phosphoglucose Isomerase Affects Leaf Starch Synthesis and Floral Initiation

et al. 2000

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“…Indeed, Nowitski et al (18) have identified three putative classes of this enzyme based on sequence characteristics. Although complex, the reconstructions for G6PI do not support a special affinity between the ␣Ϫproteobacterial and the eukaryotic clades.…”

Section: Resultsmentioning

confidence: 99%

“…Scattered findings of other individual bacterial taxa among eukaryotic clusters of enzymes have been offered as evidence for the descent of eukaryotic glycolytic enzymes from the bacterial lineage that gave rise to the mitochondria (3,17,18,21,22). In effect, these authors have interpreted the anomalous placement of a nominal bacterial homologue within a eukaryotic cluster as evidence that the bacterium is at the root of that eukaryotic lineage.…”

Section: Discussionmentioning

confidence: 99%

The global phylogeny of glycolytic enzymes

Canbäck

Andersson

Kurland

2002

Proc. Natl. Acad. Sci. U.S.A.

109

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Genes encoding the glycolytic enzymes of the facultative endocellular parasite Bartonella henselae have been analyzed phylogenetically within a very large cohort of homologues from bacteria and eukaryotes. We focus on this relative of Rickettsia prowazekii along with homologues from other ␣-proteobacteria to determine whether there have been systematic transfers of glycolytic genes from the presumed ␣-proteobacterial ancestor of the mitochondrion to the nucleus of the early eukaryote. The ␣-proteobacterial homologues representing the eight glycolytic enzymes studied here tend to cluster in well-supported nodes. Nevertheless, not one of these ␣-proteobacterial enzymes is related as a sister clade to the corresponding eukaryotic homologues. Nor is there a close phylogenetic relationship between glycolytic genes from Eucarya and any other bacterial phylum. In contrast, several of the reconstructions suggest that there may have been systematic transfer of sequences encoding glycolytic enzymes from cyanobacteria to some green plants. Otherwise, surprisingly little exchange between the bacterial and eukaryotic domains is observed. The descent of eukaryotic genes encoding enzymes of intermediary metabolism is reevaluated.

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“…PGI has sometimes been described as a "workhouse" enzyme of sugar metabolism (14), and the uptake of pgi genes from environmental sources might be of advantage in improving the efficiency of sugar metabolism. Recently, the PGI family has been divided into three major subfamilies: I, eukaryotic; II, cyanobacterial/chloroplasts; III, bacterial (57,58). Most PGI sequences fall into the subfamily I and the monophyly of the major eukaryotic groups is reflected in the topology of the reconstruction.…”

Section: Molecular and Thermophilic Properties-thementioning

confidence: 99%

Bifunctional Phosphoglucose/Phosphomannose Isomerases from the Archaea Aeropyrum pernix and Thermoplasma acidophilum Constitute a Novel Enzyme Family within the Phosphoglucose Isomerase Superfamily

Hansen

Wendorff

Schönheit

2004

Journal of Biological Chemistry

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The hyperthermophilic crenarchaeon Aeropyrum pernix contains phosphoglucose isomerase (PGI) activity. However, obvious homologs with significant identity to known PGIs could not be identified in the sequenced genome of this organism. The PGI activity from A. pernix was purified and characterized. Kinetic analysis revealed that, unlike all known PGIs, the enzyme catalyzed reversible isomerization not only of glucose 6-phosphate but also of epimeric mannose 6-phosphate at similar catalytic efficiency, thus defining the protein as bifunctional phosphoglucose/phosphomannose isomerase (PGI/PMI). The gene pgi/pmi encoding PGI/PMI (open reading frame APE0768) was identified by matrixassisted laser desorption ionization time-of-flight analyses; the gene was overexpressed in Escherichia coli as functional PGI/PMI. Putative PGI/PMI homologs were identified in several (hyper)thermophilic archaea and two bacteria. The homolog from Thermoplasma acidophilum (Ta1419) was overexpressed in E. coli, and the recombinant enzyme was characterized as bifunctional PGI/PMI. PGI/PMIs showed low sequence identity to the PGI superfamily and formed a distinct phylogenetic cluster. However, secondary structure predictions and the presence of several conserved amino acids potentially involved in catalysis indicate some structural and functional similarity to the PGI superfamily. Thus, we propose that bifunctional PGI/PMI constitutes a novel protein family within the PGI superfamily.Phosphoglucose isomerase (PGI 1 ; EC 5.3.1.9) catalyzes the reversible isomerization of glucose 6-phosphate to fructose 6-phosphate. PGI plays a central role in sugar metabolism of eukarya, bacteria, and Archaea both in glycolysis via the Embden-Meyerhof pathway in eukarya and bacteria and in its modified versions found in Archaea. PGI is also involved in gluconeogenesis where the enzyme operates in the reverse direction (for the literature see Refs. 1-3). PGIs from the domains of eukarya and bacteria are well studied enzymes. A variety of PGIs have been purified and biochemically characterized, and the encoding genes have been cloned and sequenced (e.g. Refs. 4 -11). Crystal structures have been determined for the eukaryotic PGIs from pig, rabbit, human, and from the bacterium Bacillus stearothermophilus, and conserved amino acids proposed to be involved in substrate binding and/or catalysis have been identified (12-15, 17, 18, 20 -25). The eukaryal and bacterial PGIs belong to the PGI superfamily defined by its two conserved signature patternsTo date this superfamily includes more than 300 PGI sequences (see www.sanger.ac.uk/cgi-bin/Pfam/getacc?PF00342) (26) from bacteria and eukarya but only three from the archaeal domain. These include the PGI from the hyperthermophilic euryarchaeon Methanococcus jannaschii (MjPGI). This PGI has recently been characterized as the first archaeal member of the PGI superfamily. 2 So far little is known about other archaeal PGIs. Recently, two other euryarchaeal PGIs have been characterized, one from the hyperthermophilic euryarch...

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Eubacterial origin of nuclear genes for chloroplast and cytosolic glucose-6-phosphate isomerase from spinach: sampling eubacterial gene diversity in eukaryotic chromosomes through symbiosis

Cited by 33 publications

References 32 publications

Mutation of Arabidopsis Plastid Phosphoglucose Isomerase Affects Leaf Starch Synthesis and Floral Initiation

Mutation of Arabidopsis Plastid Phosphoglucose Isomerase Affects Leaf Starch Synthesis and Floral Initiation

The global phylogeny of glycolytic enzymes

Bifunctional Phosphoglucose/Phosphomannose Isomerases from the Archaea Aeropyrum pernix and Thermoplasma acidophilum Constitute a Novel Enzyme Family within the Phosphoglucose Isomerase Superfamily

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