Response of plant metabolism to too little oxygen.

Oxygen can fall to low concentrations within plant tissues, either because of environmental factors that decrease the external oxygen concentration or because the movement of oxygen through the plant tissues cannot keep pace with the rate of oxygen consumption. Recent studies document that plants can decrease their oxygen consumption in response to low oxygen concentrations to avoid internal anoxia. This adaptive response involves a restriction of respiration and a concomitant decrease in ATP consumption that results from the inhibition of a wide range of biosynthetic processes. The inhibition of respiration is rapid and occurs at oxygen concentrations well above the K(m)(oxygen) of cytochrome oxidase, indicating that an oxygen-sensing system triggers a coordinated inhibition of ATP formation and consumption. In addition to this, low oxygen concentrations lead to the induction of a plant-specific and energy-conserving pathway of sucrose degradation, which decreases oxygen consumption and improves plant performance. Low oxygen concentrations also lead to long-term morphological adaptations, which allow respiration per volume tissue to be decreased and oxygen entry to be increased. Recently, advances have been made in elucidating possible oxygen-sensing systems and regulatory components that are involved in these responses.

[1]  Wu,et al.  Differential regulation of sugar-sensitive sucrose synthases by hypoxia and anoxia indicate complementary transcriptional and posttranscriptional responses , 1998, Plant physiology.

[2]  Martin M. Sachs,et al.  Anaerobic gene expression and flooding tolerance in maize , 1996 .

[3]  Yves Gibon,et al.  Sensitive and high throughput metabolite assays for inorganic pyrophosphate, ADPGlc, nucleotide phosphates, and glycolytic intermediates based on a novel enzymic cycling system. , 2002, The Plant journal : for cell and molecular biology.

[4]  M. Stitt,et al.  Increased levels of adenine nucleotides modify the interaction between starch synthesis and respiration when adenine is supplied to discs from growing potato tubers , 2001, Planta.

[5]  R. Hill,et al.  A cereal haemoglobin gene is expressed in seed and root tissues under anaerobic conditions , 1994, Plant Molecular Biology.

[6]  H. Peng,et al.  Signaling events in the hypoxic induction of alcohol dehydrogenase gene in Arabidopsis. , 2001, Plant physiology.

[7]  A. Pradet,et al.  Germination, respiration, and adenylate energy charge of seeds at various oxygen partial pressures. , 1985, Plant physiology.

[8]  W. Peacock,et al.  A role for haemoglobin in all plant roots , 1988 .

[9]  D. Hardie,et al.  Regulation of spinach SNF1-related (SnRK1) kinases by protein kinases and phosphatases is associated with phosphorylation of the T loop and is regulated by 5'-AMP. , 1999, The Plant journal : for cell and molecular biology.

[10]  R. Visser,et al.  Developmental changes of enzymes involved in conversion of sucrose to hexose-phosphate during early tuberisation of potato , 1997, Planta.

[11]  J. López-Barneo,et al.  Cellular mechanism of oxygen sensing. , 2001, Annual review of physiology.

[12]  N. Banks Evaluation of Methods for Determining Internal Gases in Banana Fruit , 1983 .

[13]  J. Magness Composition of Gases in Intercellular Spaces of Apples and Potatoes , 1920, Botanical Gazette.

[14]  W. Peacock,et al.  Differential Interactions of Promoter Elements in Stress Responses of the Arabidopsis Adh Gene , 1994, Plant physiology.

[15]  W. Peacock,et al.  Evidence for a role for AtMYB2 in the induction of the Arabidopsis alcohol dehydrogenase gene (ADH1) by low oxygen. , 1998, Genetics.

[16]  Ricard,et al.  Evidence for the critical role of sucrose synthase for anoxic tolerance of maize roots using a double mutant , 1998, Plant physiology.

[17]  A. Pradet,et al.  Plant metabolism under hypoxia and anoxia , 1994 .

[18]  W. Peacock,et al.  Regulated expression of an alcohol dehydrogenase 1 chimeric gene introduced into maize protoplasts , 1987, Planta.

[19]  A. Pradet,et al.  Oxygen Transport and Root Respiration of Maize Seedlings: A Quantitative Approach Using the Correlation between ATP/ADP and the Respiration Rate Controlled by Oxygen Tension. , 1983, Plant physiology.

[20]  Ute Roessner,et al.  Metabolic Profiling Allows Comprehensive Phenotyping of Genetically or Environmentally Modified Plant Systems , 2001, Plant Cell.

[21]  S. Merchant,et al.  Oxygen Deficiency Responsive Gene Expression inChlamydomonas reinhardtii through a Copper-Sensing Signal Transduction Pathway1 , 2002, Plant Physiology.

[22]  P. Quick,et al.  Tuber physiology and properties of starch from tubers of transgenic potato plants with altered plastidic adenylate transporter activity. , 2001, Plant physiology.

[23]  K. Kwast,et al.  Acute Depression of Mitochondrial Protein Synthesis during Anoxia , 1996, The Journal of Biological Chemistry.

[24]  G. Fronza,et al.  Differences in the Anaerobic Lactate-Succinate Production and in the Changes of Cell Sap pH for Plants with High and Low Resistance to Anoxia. , 1989, Plant physiology.

[25]  M. Sachs,et al.  Elevation of cytosolic calcium precedes anoxic gene expression in maize suspension-cultured cells. , 1994, The Plant cell.

[26]  R. Boutilier,et al.  Surviving hypoxia without really dying. , 1999, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[27]  M. Stitt Pyrophosphate as an Energy Donor in the Cytosol of Plant Cells: an Enigmatic Alternative to ATP , 1998 .

[28]  M. Stitt,et al.  Combined expression of glucokinase and invertase in potato tubers leads to a dramatic reduction in starch accumulation and a stimulation of glycolysis. , 1998, The Plant journal : for cell and molecular biology.

[29]  R. Crawford,et al.  Oxygen deprivation stress in a changing environment , 1996 .

[30]  M. Ellis,et al.  Molecular strategies for improving waterlogging tolerance in plants. , 2000, Journal of experimental botany.

[31]  E. J. Klok,et al.  Molecular Basis of the Anaerobic Response in Plants , 2001, IUBMB life.

[32]  B. Glick,et al.  Flooding tolerance of transgenic tomato plants expressing the bacterial enzyme ACC deaminase controlledby the 35S, rolD or PRB-1b promoter , 2001 .

[33]  P. Perata,et al.  Effect of Anoxia on Carbohydrate Metabolism in Rice Seedlings , 1995, Plant physiology.

[34]  P. W. Hochachka,et al.  Mechanism, origin, and evolution of anoxia tolerance in animals. , 2000, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[35]  M. Vayda,et al.  Hypoxic stress inhibits multiple aspects of the potato tuber wound response. , 1990, Plant physiology.

[36]  U. Sonnewald,et al.  Sucrose synthase activity does not restrict glycolysis in roots of transgenic potato plants under hypoxic conditions , 1999, Planta.

[37]  B. Cobb,et al.  Hypoxic Induction of Anoxia Tolerance in Roots of Adh1 Null Zea mays L , 1994, Plant physiology.

[38]  S. Biemelt,et al.  Re-Aeration following Hypoxia or Anoxia Leads to Activation of the Antioxidative Defense System in Roots of Wheat Seedlings , 1998, Plant physiology.

[39]  U. Wobus,et al.  Sugar import and metabolism during seed development , 1997 .

[40]  H. Greenway,et al.  Evidence for down-regulation of ethanolic fermentation and K+ effluxes in the coleoptile of rice seedlings during prolonged anoxia. , 2001, Journal of experimental botany.

[41]  A. Hanson,et al.  Metabolic Control of Anaerobic Glycolysis (Overexpression of Lactate Dehydrogenase in Transgenic Tomato Roots Supports the Davies-Roberts Hypothesis and Points to a Critical Role for Lactate Secretion , 1994, Plant physiology.

[42]  A L Burlingame,et al.  Patterns of protein synthesis and tolerance of anoxia in root tips of maize seedlings acclimated to a low-oxygen environment, and identification of proteins by mass spectrometry. , 2000, Plant physiology.

[43]  M. Stitt,et al.  Metabolic Activity Decreases as an Adaptive Response to Low Internal Oxygen in Growing Potato Tubers , 2000, Biological chemistry.

[44]  D. Olson,et al.  Analysis of LE-ACS3, a 1-Aminocyclopropane-1-carboxylic Acid Synthase Gene Expressed during Flooding in the Roots of Tomato Plants (*) , 1995, The Journal of Biological Chemistry.

[45]  R. E. Sharp,et al.  A microsensor for direct measurement of O2 partial pressure within plant tissues3 , 1996 .

[46]  Joost T. van Dongen,et al.  Phloem Metabolism and Function Have to Cope with Low Internal Oxygen1 , 2003, Plant Physiology.

[47]  F. Salamini,et al.  Enzymes of carbohydrate metabolism in the developing endosperm of maize. , 1970, Plant physiology.

[48]  D M Porterfield,et al.  Oxygen-depleted zones inside reproductive structures of Brassicaceae: implications for oxygen control of seed development. , 1999, Canadian journal of botany. Journal canadien de botanique.

[49]  Nigel G Halford,et al.  Two SNF1-related protein kinases from spinach leaf phosphorylate and inactivate 3-hydroxy-3-methylglutaryl-coenzyme A reductase, nitrate reductase, and sucrose phosphate synthase in vitro. , 1999, Plant physiology.

[50]  H. Kato‐Noguchi Abscisic acid and hypoxic induction of anoxia tolerance in roots of lettuce seedlings. , 2000, Journal of experimental botany.

[51]  C. Kuhlemeier,et al.  Ethanolic fermentation in transgenic tobacco expressing Zymomonas mobilis pyruvate decarboxylase. , 1994, The EMBO journal.

[52]  J. H. Thorne Temperature and oxygen effects on C-photosynthate unloading and accumulation in developing soybean seeds. , 1982, Plant physiology.

[53]  Michael D. McLean,et al.  The Metabolism and Functions of [gamma]-Aminobutyric Acid. , 1999, Plant physiology.

[54]  P. Hunt,et al.  Increased level of hemoglobin 1 enhances survival of hypoxic stress and promotes early growth in Arabidopsis thaliana , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[55]  S. Chapman,et al.  Expression Profile Analysis of the Low-Oxygen Response in Arabidopsis Root Cultures Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.004747. , 2002, The Plant Cell Online.

[56]  Malcolm C. Drew,et al.  OXYGEN DEFICIENCY AND ROOT METABOLISM: Injury and Acclimation Under Hypoxia and Anoxia. , 1997, Annual review of plant physiology and plant molecular biology.

[57]  S. Akita,et al.  Studies on the Mechanism of Differences in Photosynthesis among Species : III. Influence of low oxygen concentration on dry matter production and grain fertility of rice plant , 1973 .

[58]  J. Zhang,et al.  Development of flooding-tolerant Arabidopsis thaliana by autoregulated cytokinin production , 2000, Molecular Breeding.

[59]  R. Bligny,et al.  Origin of the cytoplasmic pH changes during anaerobic stress in higher plant cells. Carbon-13 and phosphorous-31 nuclear magnetic resonance studies. , 2001, Plant physiology.

[60]  R. O. Poyton,et al.  Oxygen sensing and molecular adaptation to hypoxia. , 1996, Physiological reviews.

[61]  D. Llewellyn,et al.  Two hemoglobin genes in Arabidopsis thaliana: the evolutionary origins of leghemoglobins. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[62]  D. MacAlpine,et al.  Differential Induction of mRNAs for the Glycolytic and Ethanolic Fermentative Pathways by Hypoxia and Anoxia in Maize Seedlings , 1994, Plant physiology.

[63]  Trewavas Le calcium, C'est la vie: calcium makes waves , 1999, Plant physiology.

[64]  M. Drew,et al.  Programmed cell death and aerenchyma formation in roots. , 2000, Trends in plant science.

[65]  K. Koch,et al.  Rapid repression of maize invertases by low oxygen. Invertase/sucrose synthase balance, sugar signaling potential, and seedling survival. , 1999, Plant physiology.

[66]  M. Ellis,et al.  Overexpression of alcohol dehydrogenase or pyruvate decarboxylase improves growth of hairy roots at reduced oxygen concentrations. , 2002, Biotechnology and bioengineering.

[67]  M. Gilles-Gonzalez,et al.  Structure of a biological oxygen sensor: a new mechanism for heme-driven signal transduction. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[68]  A. Pradet,et al.  Stabilization of adenine nucleotide ratios at various values by an oxygen limitation of respiration in germinating lettuce (Lactuca sativa) seeds. , 1980, The Biochemical journal.

[69]  H. Rolletschek,et al.  Legume embryos develop in a hypoxic environment. , 2002, Journal of experimental botany.

[70]  M. Ellis,et al.  Arabidopsis roots and shoots have different mechanisms for hypoxic stress tolerance. , 1999, Plant physiology.