Overexpression of alcohol dehydrogenase or pyruvate decarboxylase improves growth of hairy roots at reduced oxygen concentrations

Shiao, Tien-Li; Ellis, Marc H.; Dolferus, Rudy; Dennis, Elizabeth S.; Doran, Pauline M.

doi:10.1002/bit.10147

Cited by 52 publications

(29 citation statements)

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“…A generally high fermentation capacity does not always result in an increased rate of fermentation and a higher submergence survival. Although PDC overexpression lines of Arabidopsis showed enhanced hypoxia tolerance (Shiao et al, 2002;Ismond et al, 2003), experiments with other plant species showed the opposite effect (Tadege et al, 1998;Rahman et al, 2001). Furthermore, rice (Oryza sativa) plants expressing the transcription factor Submergence 1A exhibited enhanced expression of fermentative genes but lower fermentation rates and higher submergence survival than other genotypes (Fukao et al, 2006).…”

Section: The Submergence Tolerance Of Prt6 Mutants Is Associated Withmentioning

confidence: 99%

TheGreening after Extended Darkness1Is an N-End Rule Pathway Mutant with High Tolerance to Submergence and Starvation

et al. 2015

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Plants respond to reductions in internal oxygen concentrations with adaptive mechanisms (for example, modifications of metabolism to cope with reduced supply of ATP). These responses are, at the transcriptional level, mediated by the group VII Ethylene Response Factor transcription factors, which have stability that is regulated by the N-end rule pathway of protein degradation. N-end rule pathway mutants are characterized by a constitutive expression of hypoxia response genes and abscisic acid hypersensitivity. Here, we identify a novel proteolysis6 (prt6) mutant allele, named greening after extended darkness1 (ged1), which was previously discovered in a screen for genomes uncoupled-like mutants and shows the ability to withstand long periods of darkness at the seedling stage. Interestingly, this ethyl methanesulfonate-derived mutant shows unusual chromosomal rearrangement instead of a point mutation. Furthermore, the sensitivity of N-end rule pathway mutants ged1 and prt6-1 to submergence was studied in more detail to understand previously contradicting experiments on this topic. Finally, it was shown that mutants for the N-end rule pathway are generally more tolerant to starvation conditions, such as prolonged darkness or submergence, which was partially associated with carbohydrate conservation.During their life cycle, plant cells encounter periods of oxygen deficiency, generally termed as hypoxia stress. This stress depends on the ratio between oxygen consumption and availability. In plants, oxygen diffusion can be constrained by anatomical and morphological features (i.e. densely packed cells [e.g. meristems] and a low surface-to-volume ratio [e.g. fruits and seeds]) or external conditions that hamper gas diffusion, such as complete submergence of plants or waterlogging of soils (root flooding). Because of the requirement of oxygen for biosynthetic processes and more importantly, mitochondrial respiration, a shortage in oxygen leads to an energy deficit in hypoxic cells. To cope with this stress, plants reprogram their metabolism involving downregulation of energy-demanding processes (e.g. protein biosynthesis) and up-regulation of genes important for glycolysis, fermentation, and protection against reactive oxygen species (Bailey- Serres and Voesenek, 2008;

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Section: The Submergence Tolerance Of Prt6 Mutants Is Associated Withmentioning

confidence: 99%

TheGreening after Extended Darkness1Is an N-End Rule Pathway Mutant with High Tolerance to Submergence and Starvation

et al. 2015

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“…A cDNA library (ZipLox; Life Technologies, Rockville, MD) was prepared using poly(A) ϩ mRNA isolated from Arabidopsis thaliana hairy root cultures (ecotype C24) induced with Agrobacterium rhizogenes (Shiao et al, 2002). The roots were treated with low oxygen for 4 h in liquid Murashige and Skoog (1962) medium and incubated in a mixture of 5% O 2 and 95% N 2 .…”

Section: Preparation Of the Microarray Slidesmentioning

confidence: 99%

Expression Profile Analysis of the Low-Oxygen Response in Arabidopsis Root Cultures[W]

et al. 2002

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We used DNA microarray technology to identify genes involved in the low-oxygen response of Arabidopsis root cultures. A microarray containing 3500 cDNA clones was screened with cDNA samples taken at various times (0.5, 2, 4, and 20 h) after transfer to low-oxygen conditions. A package of statistical tools identified 210 differentially expressed genes over the four time points. Principal component analysis showed the 0.5-h response to contain a substantially different set of genes from those regulated differentially at the other three time points. The differentially expressed genes included the known anaerobic proteins as well as transcription factors, signal transduction components, and genes that encode enzymes of pathways not known previously to be involved in low-oxygen metabolism. We found that the regulatory regions of genes with a similar expression profile contained similar sequence motifs, suggesting the coordinated transcriptional control of groups of genes by common sets of regulatory factors.

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“…This suggests a key regulatory role for the first enzyme of ethanolic fermentation, PDC. Overexpression of Arabidopsis genes for the enzymes ADH and PDC improved the tolerance of Arabidopsis roots to low oxygen conditions (Dennis et al, 2000;Shiao et al, 2002). Loss-of-function mutations in PDC would provide a valuable tool to understand the importance of ethanolic fermentation in flooding tolerance, but such mutants have not yet been reported in plants.…”

mentioning

confidence: 99%

The Pyruvate decarboxylase1 Gene of Arabidopsis Is Required during Anoxia But Not Other Environmental Stresses

Kürsteiner¹,

Dupuis²,

Kuhlemeier³

2003

Plant Physiology

181

142

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Ethanolic fermentation is classically associated with flooding tolerance when plant cells switch from respiration to anaerobic fermentation. However, recent studies have suggested that fermentation also has important functions in the presence of oxygen, mainly in germinating pollen and during abiotic stress. Pyruvate decarboxylase (PDC), which catalyzes the first step in this pathway, is thought to be the main regulatory enzyme. Here, we characterize the PDC gene family in Arabidopsis. PDC is encoded by four closely related genes. By using real-time quantitative polymerase chain reaction, we determined the expression levels of each individual gene in different tissues, under normal growth conditions, and when the plants were subjected to anoxia or other environmental stress conditions. We show that PDC1 is the only gene induced under oxygen limitation among the PDC1 gene family and that a pdc1 null mutant is comprised in anoxia tolerance but not other environmental stresses. We also characterize the expression of the aldehyde dehydrogenase (ALDH) gene family. None of the three genes is induced by anoxia but ALDH2B7 reacts strongly to ABA application and dehydration, suggesting that ALDH may play a role in aerobic detoxification of acetaldehyde. We discuss the possible role of ethanolic fermentation as a robust back-up energy production pathway under adverse conditions when mitochondrial function is disturbed.The ethanolic fermentation pathway branches off the main glycolytic pathway at pyruvate. In the first step, pyruvate is the substrate of pyruvate decarboxylase (PDC), yielding CO 2 and acetaldehyde. Subsequently, acetaldehyde is reduced to ethanol with the concomitant oxidation of NADH to NAD ϩ by alcohol dehydrogenase (ADH). In the present day aerobic atmosphere, ethanolic fermentation is used only by specialized organisms or under particular conditions. In plants, it has been studied because of its relevance in flooding tolerance where plant cells switch from aerobic respiration to anaerobic fermentation (for review, see Drew, 1997).ADH has been the subject of numerous genetic studies, and adh mutants have been reported for a number of species, including maize (Zea mays; for review, see Freeling and Bennett, 1985), tobacco (Nicotiana tabacum; Rousselin et al., 1990), and Arabidopsis (Jacobs et al., 1988). Maize adh null mutants are sensitive to strict anoxia but no obvious phenotype is apparent in acclimated plants (Johnson et al., 1994). Experiments with isogenic maize lines differing in ADH activity over a approximately 200-fold range indicated that ADH activity does not limit the capacity for energy production by ethanolic fermentation unless there is a reduction in activity to less than 1% of wild-type levels (Roberts et al., 1989).These results suggest that ADH is present in large excess and are inconsistent with the idea of ADH as the regulatory enzyme of this pathway.Overexpression of a bacterial PDC in transgenic tobacco resulted in constitutive high and active protein levels under both normoxic an...

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Overexpression of alcohol dehydrogenase or pyruvate decarboxylase improves growth of hairy roots at reduced oxygen concentrations

Cited by 52 publications

References 30 publications

TheGreening after Extended Darkness1Is an N-End Rule Pathway Mutant with High Tolerance to Submergence and Starvation

TheGreening after Extended Darkness1Is an N-End Rule Pathway Mutant with High Tolerance to Submergence and Starvation

Expression Profile Analysis of the Low-Oxygen Response in Arabidopsis Root Cultures[W]

The Pyruvate decarboxylase1 Gene of Arabidopsis Is Required during Anoxia But Not Other Environmental Stresses

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