Differential Subcellular Localization and Expression of ATP Sulfurylase and 5′-Adenylylsulfate Reductase during Ontogenesis of Arabidopsis Leaves Indicates That Cytosolic and Plastid Forms of ATP Sulfurylase May Have Specialized Functions

Rotte, Carmen; Leustek, Thomas

doi:10.1104/pp.124.2.715

Cited by 117 publications

(97 citation statements)

References 43 publications

(43 reference statements)

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“…Although the sequences where miR395 genes reside are still in the processing of being sequenced, it is clear that miR395 genes were scattered in a range of more than a hundred kb. miR395 targets ATP sulfurylases that are involved in sulfate assimilation [33]. Sulfur is one of the most essential macronutrients required by plants.…”

Section: Discussionmentioning

confidence: 99%

Molecular evolution of the rice miR395 gene family

et al. 2005

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MicroRNAs (miRNAs) are 20-22 nucleotide non-coding RNAs that play important roles in plant and animal development. They are usually processed from larger precursors that can form stem-loop structures. Among 20 miRNA families that are conserved between Arabidopsis and rice, the rice miR395 gene family was unique because it was organized into compact clusters that could be transcribed as one single transcript. We show here that in fact this family had four clusters of total 24 genes. Three of these clusters were segmental duplications. They contained miR395 genes of both 120 bp and 66 bp long. However, only the latter was repeatedly duplicated. The fourth cluster contained miR395 genes of two different sizes that could be the consequences of intergenic recombination of genes from the first three clusters. On each cluster, both 1-duplication and 2-duplication histories were observed based on the sequence similarity between miR395 genes, some of which were nearly identical suggesting a recent origin. This was supported by a miR395 locus survey among several species of the genus Oryza, where two clusters were only found in species with an AA genome, the genome of the cultivated rice. A comparative study of the genomic organization of Medicago truncatula miR395 gene family showed significant expansion of intergenic spaces indicating that the originally clustered genes were drifting away from each other. The diverse genomic organizations of a conserved microRNA gene family in different plant genomes indicated that this important negative gene regulation system has undergone dramatic tune-ups in plant genomes.

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Section: Discussionmentioning

confidence: 99%

Molecular evolution of the rice miR395 gene family

et al. 2005

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“…1). These biomolecules include oils containing very long chain fatty acids, waxes (Pollard and Stumpf, 1980;Bao et al, 1998), flavonoids and stilbenoids (Hrazdina et al, 1978;Preisig-Muller et al, 1997), malonic acid (Stumpf and Burris, 1981), isoprenoids such as essential oils, sterols, sesquiterpenes, and polyprenols (Demetzos et al, 1994;Menhard and Zenk, 1999;Eisenreich et al, 2001), some of the cellular Cys (Rotte and Leustek, 2000;Dominguez-Solis et al, 2001), a subset of the glucosinolates (Graser et al, 2000), malonyl derivatives including D-amino acids, 1-aminocyclopropane carboxylic acid (the precursor of ethylene), and xenobiotics such as pesticides (Hohl and Barz, 1995), and, in transgenic plants, bioplastics based on derivatives of polyhydroxybutyrate (Poirier, 2001).…”

Section: Discussionmentioning

confidence: 99%

Molecular Characterization of a Heteromeric ATP-Citrate Lyase That Generates Cytosolic Acetyl-Coenzyme A in Arabidopsis,

Fatland¹,

Ke²,

Anderson³

et al. 2002

Plant Physiology

196

194

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Acetyl-coenzyme A (CoA) is used in the cytosol of plant cells for the synthesis of a diverse set of phytochemicals including waxes, isoprenoids, stilbenes, and flavonoids. The source of cytosolic acetyl-CoA is unclear. We identified two Arabidopsis cDNAs that encode proteins similar to the amino and carboxy portions of human ATP-citrate lyase (ACL). Coexpression of these cDNAs in yeast (Saccharomyces cerevisiae) confers ACL activity, indicating that both the Arabidopsis genes are required for ACL activity. Arabidopsis ACL is a heteromeric enzyme composed of two distinct subunits, ACLA (45 kD) and ACLB (65 kD). The holoprotein has a molecular mass of 500 kD, which corresponds to a heterooctomer with an A 4 B 4 configuration. ACL activity and the ACLA and ACLB polypeptides are located in the cytosol, consistent with the lack of targeting peptides in the ACLA and ACLB sequences. In the Arabidopsis genome, three genes encode for the ACLA subunit (ACLA-1, At1g10670; ACLA-2, At1g60810; and ACLA-3, At1g09430), and two genes encode the ACLB subunit (ACLB-1, At3g06650 and ACLB-2, At5g49460). The ACLA and ACLB mRNAs accumulate in coordinated spatial and temporal patterns during plant development. This complex accumulation pattern is consistent with the predicted physiological needs for cytosolic acetyl-CoA, and is closely coordinated with the accumulation pattern of cytosolic acetyl-CoA carboxylase, an enzyme using cytosolic acetyl-CoA as a substrate. Taken together, these results indicate that ACL, encoded by the ACLA and ACLB genes of Arabidopsis, generates cytosolic acetyl-CoA. The heteromeric organization of this enzyme is common to green plants (including Chlorophyceae, Marchantimorpha, Bryopsida, Pinaceae, monocotyledons, and eudicots), species of fungi, Glaucophytes, Chlamydomonas, and prokaryotes. In contrast, all known animal ACL enzymes have a homomeric structure, indicating that a evolutionary fusion of the ACLA and ACLB genes probably occurred early in the evolutionary history of this kingdom.Acetyl-coenzyme A (CoA) is an intermediate metabolite that is juxtaposed between catabolic and anabolic processes. As the entry point for the tricarboxylic acid (TCA) cycle, acetyl-CoA can be considered the gateway in the oxidation of carbon derived from the catabolism of fatty acids, certain amino acids (e.g. Leu, Ile, Lys, and Trp), and carbohydrates. Furthermore, acetyl-CoA is the intermediate precursor for the biosynthesis of a wide variety of phytochemicals. Because membranes are impermeable to CoA derivatives, it can be inferred that acetyl-CoA is generated in at least four distinct metabolic pools representing the four subcellular compartments where acetyl-CoA metabolism occurs: plastids, mitochondria, peroxisomes, and the cytosol (Fig. 1). Therefore, plants should have distinct acetyl-CoA-generating systems in mitochondria (for the TCA cycle), in plastids (for de novo fatty acid biosynthesis), in peroxisomes (the product of ␤-oxidation of fatty acids), and in the cytosol (for the biosynthesis of isoprenoids, flavo...

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“…APR expression has been reported to be transcriptionally regulated in response to sulfur and nitrogen nutrition, heavy metal stress, addition of reduced sulfur compounds and reactive oxygen species, and the day/night cycle, strongly suggesting a regulatory function (for review, see Leustek, 2002;Kopriva, 2006). In comparison, SiR activities in crude leaf extracts from Arabidopsis were 2 to 3.5 nmol mg 21 protein min 21 (Figure 2; Hä nsch et al, 2007;Heeg et al, 2008), while ATP sulfurylase activity ranged one order of magnitude higher (Rotte and Leustek, 2000). Flux control studies with Arabidopsis root cultures showed that sulfate uptake at the plasmalemma is most important for primary sulfur metabolism but confirmed that, once sulfate was inside the cell, the highly regulated reaction catalyzed by APR exerted the strongest control over the pathway (Vauclare et al, 2002).…”

Section: Decreased Sir Activity Causes Reduced Flux In Assimilatory Smentioning

confidence: 99%

“…With respect to control of the pathway, considerations of V max activities of the enzymatic steps from sulfate to sulfide in leaves of Arabidopsis remain inconclusive. Reported maximal APR activities in Col-0 plants range from 1 to 10 nmol mg 21 protein min 21 and depend on age, light, and media conditions (Kopriva et al, 1999(Kopriva et al, , 2000Rotte and Leustek, 2000;Tsakraklides et al, 2002;Loudet et al, 2007). APR expression has been reported to be transcriptionally regulated in response to sulfur and nitrogen nutrition, heavy metal stress, addition of reduced sulfur compounds and reactive oxygen species, and the day/night cycle, strongly suggesting a regulatory function (for review, see Leustek, 2002;Kopriva, 2006).…”

Section: Decreased Sir Activity Causes Reduced Flux In Assimilatory Smentioning

confidence: 99%

Sulfite Reductase Defines a Newly Discovered Bottleneck for Assimilatory Sulfate Reduction and Is Essential for Growth and Development in Arabidopsis thaliana

et al. 2010

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The role of sulfite reductase (SiR) in assimilatory reduction of inorganic sulfate to sulfide has long been regarded as insignificant for control of flux in this pathway. Two independent Arabidopsis thaliana T-DNA insertion lines (sir1-1 and sir1-2), each with an insertion in the promoter region of SiR, were isolated. sir1-2 seedlings had 14% SiR transcript levels compared with the wild type and were early seedling lethal. sir1-1 seedlings had 44% SiR transcript levels and were viable but strongly retarded in growth. In mature leaves of sir1-1 plants, the levels of SiR transcript, protein, and enzymatic activity ranged between 17 and 28% compared with the wild type. The 28-fold decrease of incorporation of 35 S label into Cys, glutathione, and protein in sir1-1 showed that the decreased activity of SiR generated a severe bottleneck in the assimilatory sulfate reduction pathway. Root sulfate uptake was strongly enhanced, and steady state levels of most of the sulfur-related metabolites, as well as the expression of many primary metabolism genes, were changed in leaves of sir1-1. Hexose and starch contents were decreased, while free amino acids increased. Inorganic carbon, nitrogen, and sulfur composition was also severely altered, demonstrating strong perturbations in metabolism that differed markedly from known sulfate deficiency responses. The results support that SiR is the only gene with this function in the Arabidopsis genome, that optimal activity of SiR is essential for normal growth, and that its downregulation causes severe adaptive reactions of primary and secondary metabolism.

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Differential Subcellular Localization and Expression of ATP Sulfurylase and 5′-Adenylylsulfate Reductase during Ontogenesis of Arabidopsis Leaves Indicates That Cytosolic and Plastid Forms of ATP Sulfurylase May Have Specialized Functions

Cited by 117 publications

References 43 publications

Molecular evolution of the rice miR395 gene family

Molecular evolution of the rice miR395 gene family

Molecular Characterization of a Heteromeric ATP-Citrate Lyase That Generates Cytosolic Acetyl-Coenzyme A in Arabidopsis,

Sulfite Reductase Defines a Newly Discovered Bottleneck for Assimilatory Sulfate Reduction and Is Essential for Growth and Development in Arabidopsis thaliana

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