Phloem Metabolism and Function Have to Cope with Low Internal Oxygen

Dongen, Joost T. van; Schurr, Ulrich; Pfister, M.; Geigenberger, Peter

doi:10.1104/pp.102.017202

Cited by 195 publications

(181 citation statements)

References 55 publications

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“…Despite these possibilities, the strong staining of vascular tissues in stems and tubers (Fig. 3) is in agreement with recent studies documenting low-oxygen concentrations in the vascular bundles of stems (van Dongen et al, 2003). To investigate whether the decrease in internal oxygen levels affects energy metabolism in transgenic tubers, ATP to ADP ratios were analyzed in tissue sampled rapidly (within 2 s) from the center of an intact tuber.…”

Section: Ectopic Expression Of Invertase Leads To Enhanced Expressionsupporting

confidence: 52%

“…The low adenylate energy state in intact tubers was rapidly reversed when tuber slices were exposed to air or aerated solutions, providing evidence that it was due to the lower internal oxygen levels present within transgenic tubers. A strong correlation between oxygen levels and adenylate energy state has been demonstrated in earlier experiments with wild-type tubers (Geigenberger et al, 2000) and in the phloem (van Dongen et al, 2003).…”

Section: The Low-oxygen Tensions Within Transgenic Tubers Lead To a Dmentioning

confidence: 72%

“…Oxygen falls to low levels within metabolically active, dense, or bulky plant tissues, even when external oxygen concentrations are high. Low internal oxygen concentrations have been reported in growing tubers (Geigenberger et al, 2000), developing seeds (Quebedeaux and Hardy, 1976;Porterfield et al, 1999;Gibon et al, 2002;Rolletscheck et al, 2002), fruits (Magness, 1920;Banks, 1983;Ke et al, 1995), roots (Lushuk and Salveit, 1991;Thomson and Greenway, 1991), and in phloem tissue (van Dongen et al, 2003). Based on studies in growing wild-type potato (Solanum tuberosum) tubers, Geigenberger et al (2000) concluded that falling internal oxygen leads to: (a) a restriction of glycolysis and respiration and a decrease in adenylate levels; (b) a widespread decrease in biosynthetic activity, which decreases ATP consumption; and (c) a switch to pathways that consume less ATP.…”

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confidence: 99%

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A Bypass of Sucrose Synthase Leads to Low Internal Oxygen and Impaired Metabolic Performance in Growing Potato Tubers

et al. 2003

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Plants possess two alternative biochemical pathways for sucrose (Suc) degradation. One involves hydrolysis by invertase followed by phosphorylation via hexokinase and fructokinase, and the other route-which is unique to plants-involves a UDP-dependent cleavage of Suc that is catalyzed by Suc synthase (SuSy). In the present work, we tested directly whether a bypass of the endogenous SuSy route by ectopic overexpression of invertase or Suc phosphorylase affects internal oxygen levels in growing tubers and whether this is responsible for their decreased starch content. (a) Oxygen tensions were lower within transgenic tubers than in wild-type tubers. Oxygen tensions decreased within the first 10 mm of tuber tissue, and this gradient was steeper in transgenic tubers. (b) Invertase-overexpressing tubers had higher activities of glyceraldehyde-3-phosphate dehydrogenase, lactate dehydrogenase, and alcohol dehydrogenase, and (c) higher levels of lactate. (d) Expression of a low-oxygen-sensitive Adh1-␤-glucuronidase reporter gene construct was more strongly induced in the invertaseoverexpressing background compared with wild-type background. (e) Intact transgenic tubers had lower ATP to ADP ratios than the wild type. ATP to ADP ratio was restored to wild type, when discs of transgenic tubers were incubated at 21% (v/v) oxygen. (f) Starch decreased from the periphery to the center of the tuber. This decrease was much steeper in the transgenic lines, leading to lower starch content especially near the center of the tuber. (g) Metabolic fluxes (based on redistribution of 14 C-glucose) and ATP to ADP ratios were analyzed in more detail, comparing discs incubated at various external oxygen tensions (0%, 1%, 4%, 8%, 12%, and 21% [v/v]) with intact tubers. Discs of Suc phosphorylase-expressing lines had similar ATP to ADP ratios and made starch as fast as wild type in high oxygen but had lower ATP to ADP ratios and lower rates of starch synthesis than wild type at low-oxygen tensions typical to those found inside an intact tuber. (h) In discs of wild-type tubers, subambient oxygen concentrations led to a selective increase in the mRNA levels of specific SuSy genes, whereas the mRNA levels of genes encoding vacuolar and apoplastic invertases decreased. (i) These results imply that repression of invertase and mobilization of Suc via the energetically less costly route provided by SuSy is important in growing tubers because it conserves oxygen and allows higher internal oxygen tensions to be maintained than would otherwise be possible.Oxygen access to internal tissues can be a problem in plants. Oxygen falls to low levels within metabolically active, dense, or bulky plant tissues, even when external oxygen concentrations are high. Low internal oxygen concentrations have been reported in growing tubers (Geigenberger et al., 2000), developing seeds (Quebedeaux and Hardy, 1976; Porterfield et al., 1999; Gibon et al., 2002; Rolletscheck et al., 2002), fruits (Magness, 1920; Banks, 1983; Ke et al., 1995), roots (Lushuk and Salveit, 1...

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Section: Ectopic Expression Of Invertase Leads To Enhanced Expressionsupporting

confidence: 52%

Section: The Low-oxygen Tensions Within Transgenic Tubers Lead To a Dmentioning

confidence: 72%

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confidence: 99%

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A Bypass of Sucrose Synthase Leads to Low Internal Oxygen and Impaired Metabolic Performance in Growing Potato Tubers

et al. 2003

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“…Under standard plant growth conditions, the basic level of GDH activity in the CCs, which remains confined to the mitochondria, may have a housekeeping role in a tissue that has to cope with a low oxygen concentration (van Dongen et al, 2003). Under these conditions, the lack of reducing equivalents such as NADH is in favor of the enzyme having a function in oxidizing Glu as a respiratory substrate (Freebairn and Remmert, 1957), as already demonstrated to occur in vivo (Robinson et al, 1992;Aubert et al, 2001).…”

Section: Discussionmentioning

confidence: 94%

Glutamate Dehydrogenase of Tobacco Is Mainly Induced in the Cytosol of Phloem Companion Cells When Ammonia Is Provided Either Externally or Released during Photorespiration

et al. 2004

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Glutamate (Glu) dehydrogenase (GDH) catalyses the reversible amination of 2-oxoglutarate for the synthesis of Glu using ammonium as a substrate. This enzyme preferentially occurs in the mitochondria of companion cells of a number of plant species grown on nitrate as the sole nitrogen source. For a better understanding of the controversial role of GDH either in ammonium assimilation or in the supply of 2-oxoglutarate (F. Dubois, T. Tercé-Laforgue, M.B. Gonzalez-Moro, M.B. Estavillo, R. Sangwan, A. Gallais, B. Hirel [2003] Plant Physiol Biochem 41: 565-576), we studied the localization of GDH in untransformed tobacco (Nicotiana tabacum) plants grown either on low nitrate or on ammonium and in ferredoxin-dependent Glu synthase antisense plants. Production of GDH and its activity were strongly induced when plants were grown on ammonium as the sole nitrogen source. The induction mainly occurred in highly vascularized organs such as stems and midribs and was likely to be due to accumulation of phloem-translocated ammonium in the sap. GDH induction occurred when ammonia was applied externally to untransformed control plants or resulted from photorespiratory activity in transgenic plants down-regulated for ferredoxin-dependent Glu synthase. GDH was increased in the mitochondria and appeared in the cytosol of companion cells. Taken together, our results suggest that the enzyme plays a dual role in companion cells, either in the mitochondria when mineral nitrogen availability is low or in the cytosol when ammonium concentration increases above a certain threshold.Ammonium is the ultimate form of inorganic nitrogen available to the plant. It can originate from a wide variety of metabolic processes such as nitrate reduction, photorespiration, phenylpropanoid metabolism, utilization of nitrogen transport compounds, amino acid catabolism, symbiotic nitrogen fixation (Hirel and Lea, 2001), and insect digestion in carnivorous plants (Schulze et al., 1997). It is then incorporated into an organic molecule, 2-oxoglutarate, by the combined action of the enzymes Gln synthetase (GS) and Glu synthase (Gln-2-oxoglutarate aminotransferase; GOGAT) to allow the synthesis of Gln and Glu. Both amino acids are further used as amino group donors for the synthesis of virtually all the nitrogencontaining molecules including the other amino acids needed for protein synthesis and nucleotides used as basic molecules for RNA and DNA synthesis (Hirel and Lea, 2001). The GS/GOGAT cycle is the major mechanism of ammonium assimilation in higher plants regardless of the various sources of ammonium listed above. However, it has often been argued that other enzymes have the capacity to assimilate ammonium, leading to the hypothesis that alternative pathways might operate under particular physiological conditions when the GS/GOGAT pathway may not be able to fulfill its function (Harrison et al., 2003).One of these alternative pathways is the reaction catalyzed by the mitochondrial NAD(H)-dependent Glu dehydrogenase (GDH; EC 1.4.1.2), which possesses the ...

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“…For example, root tissues that show high expression of AtNIP2;1 are also the tissues that have low oxygen tension even under growth in sufficient O 2 . For example, the stele of mature root generally exhibits the metabolic symptoms of anoxia, likely due to poor radial diffusion of O 2 (43,44). Similarly, the root tip also exhibits a low O 2 tension (43) presumably due to high metabolic rates and O 2 consumption.…”

Section: Discussionmentioning

confidence: 99%

Arabidopsis NIP2;1, a Major Intrinsic Protein Transporter of Lactic Acid Induced by Anoxic Stress

Choi

Roberts

2007

Journal of Biological Chemistry

161

128

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Nodulin 26 intrinsic proteins (NIPs) are plant-specific, highly conserved water and solute transport proteins with structural and functional homology to soybean nodulin 26. Arabidopsis thaliana contains nine NIP genes. In this study, it is shown that one of these, AtNIP2;1, is exquisitely sensitive to water logging and anoxia stress. Based on quantitative PCR and promoter::GUS experiments, AtNIP2;1 is expressed at a low basal level in the root tips and the vascular bundle of differentiated roots. Transcript levels are elevated acutely and rapidly upon water logging of root or leaf tissues, increasing 70-fold in roots within the 1st h of submersion. After this large initial increase, mRNA levels decline to steady state levels that remain over 10-fold higher by 6 h post-submersion. An even greater induction of AtNIP2;1 expression was observed upon anoxia challenge of Arabidopsis seedlings, with a 300-fold increase in AtNIP2;1 transcript observed by 2 h after the initiation of oxygen deprivation. Functional analysis of AtNIP2;1 expressed in Xenopus oocytes shows that the protein differs from soybean nodulin 26, showing minimal water and glycerol transport. Instead, AtNIP2;1 displays transport of lactic acid, with a preference for the protonated acidic form of this weak acid. Overall, the data suggest that AtNIP2;1 is an anaerobic-induced gene that encodes a lactic acid transporter and may play a role in adaptation to lactic fermentation under anaerobic stress.Major intrinsic proteins (MIPs) 2 are an ancient integral membrane channel protein family of water and uncharged solute transporters that have been found in nearly all living organisms. MIPs are especially prevalent and diverse in higher plants and have been classified into four monophyletic groups as follows: the plasma membrane intrinsic proteins (PIPs), the tonoplast intrinsic proteins, the nodulin 26-like intrinsic proteins (NIPs), and the small basic intrinsic proteins (1).NIPs are named for soybean nodulin 26 (Nod26) (2), which is the major protein component of the symbiosome membrane from nitrogen-fixing soybean root nodules (3, 4). Functional analyses indicate that Nod26 is an aquaglyceroporin with a low intrinsic water permeability and the ability to transport uncharged metabolites such as glycerol (4, 5) and has also been implicated in ammonia transport (6). It has become clear that NIPs represent a large, diverse family of aquaglyceroporins, with multiple members found in every sequenced higher plant genome (1,7,8). For example, among the 35 MIP genes in Arabidopsis thaliana (1), there are nine members of the NIP subfamily. Based on molecular modeling of the pore selectivity sequences, these nine NIPs are subdivided into the following two groups: NIP subgroup I proteins are encoded by NIP1;1, NIP1;2, NIP2;1, NIP3;1, NIP4;1, and NIP4;2, and NIP subgroup II proteins are encoded by NIP5;1, NIP6;1, and NIP7;1 (9).Analysis of NIP subgroup I proteins shows that they are more similar to soybean nodulin 26 in structure and function, with several showing aqu...

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Phloem Metabolism and Function Have to Cope with Low Internal Oxygen

Cited by 195 publications

References 55 publications

A Bypass of Sucrose Synthase Leads to Low Internal Oxygen and Impaired Metabolic Performance in Growing Potato Tubers

A Bypass of Sucrose Synthase Leads to Low Internal Oxygen and Impaired Metabolic Performance in Growing Potato Tubers

Glutamate Dehydrogenase of Tobacco Is Mainly Induced in the Cytosol of Phloem Companion Cells When Ammonia Is Provided Either Externally or Released during Photorespiration

Arabidopsis NIP2;1, a Major Intrinsic Protein Transporter of Lactic Acid Induced by Anoxic Stress

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