<i>CLA1</i>, a novel gene required for chloroplast development, is highly conserved in evolution

Mandel, M. Alejandra; Feldmann, Kenneth A.; Herrera-Estrella, Luis; Rocha-Sosa, Mario; León, Patricia

doi:10.1046/j.1365-313x.1996.9050649.x

Cited by 281 publications

(272 citation statements)

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“…The other possibility is that DXR might not be a determinant enzyme in the MEP pathway. In this pathway, DXS has been identified to catalyze the first step, the key step of the MEP pathway, in Arabidopsis [22,47,58]. DXS was also found to share a similar expression pattern with DXR, and both DXS and DXR null mutants displayed an [7,19,22,47].…”

Section: Discussionmentioning

confidence: 99%

Disruption of the 1-deoxy-D-xylulose-5-phosphate reductoisomerase (DXR) gene results in albino, dwarf and defects in trichome initiation and stomata closure in Arabidopsis

Xing

Miao

et al. 2010

Cell Res

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1-Deoxy-d-xylulose-5-phosphate reductoisomerase (DXR) is an important enzyme involved in the 2-C-methyl-d-erythritol-4-phosphate (MEP) pathway which provides the basic five-carbon units for isoprenoid biosynthesis. To investigate the role of the MEP pathway in plant development and metabolism, we carried out detailed analyses on a dxr mutant (GK_215C01) and two DXR transgenic co-suppression lines, OX-DXR-L2 and OX-DXR-L7. We found that the dxr mutant was albino and dwarf. It never bolted, had significantly reduced number of trichomes and most of the stomata could not close normally in the leaves. The two co-suppression lines produced more yellow inflorescences and albino sepals with no trichomes. The transcription levels of genes involved in trichome initiation were found to be strongly affected, including GLABRA1, TRANSPARENT TESTA GLABROUS 1, TRIPTYCHON and SPINDLY, expression of which is regulated by gibberellic acids (GAs). Exogenous application of GA 3 could partially rescue the dwarf phenotype and the trichome initiation of dxr, whereas exogenous application of abscisic acid (ABA) could rescue the stomata closure defect, suggesting that lower levels of both GA and ABA contribute to the phenotype in the dxr mutants. We further found that genes involved in the biosynthetic pathways of GA and ABA were coordinately regulated. These results indicate that disruption of the plastidial MEP pathway leads to biosynthetic deficiency of photosynthetic pigments, GAs and ABA, and thus the developmental abnormalities, and that the flux from the cytoplasmic mevalonate pathway is not sufficient to rescue the deficiency caused by the blockage of the plastidial MEP pathway. These results reveal a critical role for the MEP biosynthetic pathway in controlling the biosynthesis of isoprenoids.

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Section: Discussionmentioning

confidence: 99%

Disruption of the 1-deoxy-D-xylulose-5-phosphate reductoisomerase (DXR) gene results in albino, dwarf and defects in trichome initiation and stomata closure in Arabidopsis

Xing

Miao

et al. 2010

Cell Res

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“…The first step in plastid carotenoid synthesis, conversion of pyruvate and glyceraldehyde-3-phosphate to D -1-deoxyxylulose-phosphate, is catalyzed by deoxyxylulose-7-phosphate synthase ( DXS ) (Lois et al, 1998;Lichtenthaler, 1999). Because Arabidopsis TK shares 23% identity with DXS at the nucleotide level (Mandel et al, 1996), we investigated DXS expression in a large set of transformants with varying losses of chlorophyll and carotenoids. The transformants contained similar or greater DXS transcript levels than did wild-type plants, irrespective of whether plants of similar size or similar age were compared ( Figure 4K).…”

Section: Calvin Cycle Enzymes Chlorophyll and Carotenoidsmentioning

confidence: 99%

“…Because Arabidopsis TK shares 23% identity with DXS at the nucleotide level (Mandel et al, 1996), we investigated DXS expression in a large set of transformants with varying losses of chlorophyll and carotenoids. The transformants contained similar or greater DXS transcript levels than did wild-type plants, irrespective of whether plants of similar size or similar age were compared ( Figure 4K).…”

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confidence: 99%

A Small Decrease of Plastid Transketolase Activity in Antisense Tobacco Transformants Has Dramatic Effects on Photosynthesis and Phenylpropanoid Metabolism

Henkes¹,

Sonnewald²,

Badur³

et al. 2001

The Plant Cell

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Transketolase (TK) catalyzes reactions in the Calvin cycle and the oxidative pentose phosphate pathway (OPPP) and produces erythrose-4-phosphate, which is a precursor for the shikimate pathway leading to phenylpropanoid metabolism. To investigate the consequences of decreased TK expression for primary and secondary metabolism, we transformed tobacco with a construct containing an antisense TK sequence. The results were as follows: (1) a 20 to 40% reduction of TK activity inhibited ribulose-1,5-bisphosphate regeneration and photosynthesis. The inhibition of photosynthesis became greater as irradiance increased across the range experienced in growth conditions (170 to 700 mol m Ϫ 2 sec Ϫ 1 ). TK almost completely limited the maximum rate of photosynthesis in saturating light and saturating CO 2 . (2) Decreased expression of TK led to a preferential decrease of sugars, whereas starch remained high until photosynthesis was strongly inhibited. One of the substrates of TK (fructose-6-phosphate) is the starting point for starch synthesis, and one of the products (erythrose-4-phosphate) inhibits phosphoglucose isomerase, which catalyzes the first reaction leading to starch. (3) A 20 to 50% decrease of TK activity led to decreased levels of aromatic amino acids and decreased levels of the intermediates (caffeic acid and hydroxycinnamic acids) and products (chlorogenic acid, tocopherol, and lignin) of phenylpropanoid metabolism. (4) There was local loss of chlorophyll and carotene on the midrib when TK activity was inhibited by Ͼ 50%, spreading onto minor veins and lamina in severely affected transformants. (5) OPPP activity was not strongly inhibited by decreased TK activity. These results identify TK activity as an important determinant of photosynthetic and phenylpropanoid metabolism and show that the provision of precursors by primary metabolism colimits flux into the shikimate pathway and phenylpropanoid metabolism. INTRODUCTIONThe interaction between primary and secondary pathways is an important but poorly understood aspect of plant metabolism. Phenylpropanoids represent an important class of secondary metabolites, with roles in plant structure, defense, and signaling (Dixon and Paiva, 1995). They are derived from aromatic amino acids, which are synthesized via the shikimate pathway in the plastid. Up to 20% of the total carbon in a plant passes through this pathway (Jensen, 1985). Even though there have been numerous studies of transformants with altered expression of genes that encode enzymes in the Calvin cycle, glycolysis, the tricarboxylic acid cycle, and the oxidative pentose phosphate pathway (OPPP) (Stitt and Sonnewald, 1995;Stitt, 1999), the consequences for phenylpropanoid metabolism or other secondary pathways have not been explored. The presence of redundant enzymes and pathways for carbohydrate breakdown and glycolysis (Dennis, 1987; Dennis et al., 1997;Stitt, 1998) and the absence of marked phenotypic changes after alterations in the expression of key enzymes, including phosphofructokinase (Burrell et...

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“…Thus the analysis of the regulation of the enzymes in the MEP pathway is important in understanding the biosynthesis and possible manipulation of such terpenoids in plants. The isolation of albino plant mutants in Arabidopsis resulted in the identification of a gene required for the synthesis of both chlorophyll and carotenoids, named CLA1 (Mandel et al, 1996). In the cla1-1 mutant plastid development is impaired at an early stage resulting in almost no thylakoid membrane proliferation; the plastids resemble an early proplastid stage.…”

mentioning

confidence: 99%

“…In the cla1-1 mutant plastid development is impaired at an early stage resulting in almost no thylakoid membrane proliferation; the plastids resemble an early proplastid stage. CLA1 is a single gene in the Arabidopsis genome and its disruption affects the expression of both nuclear-and chloroplastencoded photosynthetic genes (Mandel et al, 1996). The CLA1 protein sequence has extensive identity with other reported DXP synthases.…”

mentioning

confidence: 99%

Analysis of the Expression of CLA1, a Gene That Encodes the 1-Deoxyxylulose 5-Phosphate Synthase of the 2-C-Methyl-d-Erythritol-4-Phosphate Pathway in Arabidopsis

et al. 2000

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The discovery of the 2-C-methyl-d-erythritol-4-phosphate pathway for the biosynthesis of isoprenoids raises the important question of the nature and regulation of the enzymes involved in this pathway. CLA1, a gene previously isolated from Arabidopsis, encodes the first enzyme of the 2-C-methyl-d-erythritol-4-phosphate pathway, 1-deoxy-d-xylulose-5-phosphate synthase. We demonstrate this enzyme activity by complementation of the cla1-1 mutant phenotype and by direct enzymatic assays. Based on mRNA and protein expression patterns this enzyme is expressed mainly in developing photosynthetic and non-photosynthetic tissues. The ␤-glucuronidase expression pattern driven from the CLA1 gene regulatory region supports the northern and protein data while also showing that this gene has some level of expression in most tissues of the plant. A mutation in the CLA1 gene interferes with the normal development of chloroplasts and etioplasts, but does not seem to affect amyloplast structure. Microscopic analysis also shows a pleiotropic effect of the CLA1 gene mutation in mesophyll tissue formation.In higher plants isoprenoids are derived from isopentenyl diphosphate (IPP) and synthesized in at least two different compartments, the cytoplasm and the chloroplast. For a long time it was assumed that IPP was synthesized exclusively by the mevalonate pathway in all organisms (Spurgeon and Porter, 1981; Goldstein and Brown, 1990). However, independent studies have demonstrated that in eubacteria, green algae, and plants, IPP is also synthesized by a non-mevalonate pathway designated as the 2-Cmethyl-d-erythritol-4-P (MEP) pathway (for review, see Rohmer, 1998Rohmer, , 1999Lichtenthaler, 1999). Thus in plants cytosolic IPP is synthesized by the mevalonate pathway and plastidic IPP is synthesized by the MEP pathway (Lichtenthaler, 1999). In the MEP pathway IPP is synthesized from pyruvate and glyceraldehyde-3-P via novel intermediates (Rohmer et al

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CLA1, a novel gene required for chloroplast development, is highly conserved in evolution

Cited by 281 publications

References 29 publications

Disruption of the 1-deoxy-D-xylulose-5-phosphate reductoisomerase (DXR) gene results in albino, dwarf and defects in trichome initiation and stomata closure in Arabidopsis

Disruption of the 1-deoxy-D-xylulose-5-phosphate reductoisomerase (DXR) gene results in albino, dwarf and defects in trichome initiation and stomata closure in Arabidopsis

A Small Decrease of Plastid Transketolase Activity in Antisense Tobacco Transformants Has Dramatic Effects on Photosynthesis and Phenylpropanoid Metabolism

Analysis of the Expression of CLA1, a Gene That Encodes the 1-Deoxyxylulose 5-Phosphate Synthase of the 2-C-Methyl-d-Erythritol-4-Phosphate Pathway in Arabidopsis

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