Characterization of distinct root and shoot responses to low-oxygen stress in Arabidopsis with a focus on primary C- and N-metabolism

Plant Cell and Environment

Volumn 37, Issue 10, 2014, Pages 2366-2380

  Mustroph, Angelika ^a   Barding, Gregory A ^b,c   Kaiser, Kayla A ^b,d   Larive, Cynthia K ^b   Bailey Serres, Julia ^b  

^a UNIVERSITY OF BAYREUTH   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

Arabidopsis thaliana; Flooding; GC MS; Hypoxia; Metabolite profiling; Metabolome; NMR; Submergence; Transcriptome; Translatome

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

4 AMINOBUTYRIC ACID; ARABIDOPSIS PROTEIN; CARBON; NITROGEN; OXYGEN; PROTEOME; TRANSCRIPTOME; WATER;

ADAPTATION; ANTIBODY SPECIFICITY; ARABIDOPSIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METABOLOME; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT; PLANT ROOT;

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARBON; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, PLANT; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; NITROGEN; ORGAN SPECIFICITY; OXYGEN; PLANT ROOTS; PLANT SHOOTS; PROTEOME; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME; WATER;

EID: 84908228545     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12282     Document Type: Article

References (93)

1. Allan W.L., Peiris C., Bown A.W. & Shelp B.J. (2003) Gamma-hydroxybutyrate accumulates in green tea and soybean sprouts in response to oxygen deficiency. Canadian Journal of Plant Science 83, 951-953.
2. Allan W.L., Simpson J.P., Clark S.M. & Shelp B.J. (2008) γ-Hydroxybutyrate accumulation in Arabidopsis and tobacco plants is a general response to abiotic stress: putative regulation by redox balance and glyoxylate reductase isoforms. Journal of Experimental Botany 59, 2555-2564.
3. Allan W.L., Breitkreuz K.E., Waller J.C., Simpson J.P., Hoover G.J., Rochon A., .. Shelp B.J. (2012) Detoxification of succinate semialdehyde in Arabidopsis glyoxylate reductase and NAD kinase mutants subjected to submergence stress. Botany 90, 51-61.
4. Arazi T., Baum G., Snedden W.A., Shelp B.J. & Fromm H. (1995) Molecular and biochemical analysis of calmodulin interactions with the calmodulin-binding domain of plant glutamate decarboxylase. Plant Physiology 108, 551-561.
5. Armstrong W. (1979) Aeration in higher plants. In Advances in Botanical Research (ed. H.W. Woolhouse ) pp. 226-328. Academic Press, London.
6. Aurisano N., Bertani A. & Reggiani R. (1995) Anaerobic accumulation of 4-aminobutyrate in rice seedlings; causes and significance. Phytochemistry 38, 1147-1150.
7. Bai T., Li C., Li C., Liang D. & Ma F. (2013) Contrasting hypoxia tolerance and adaptation in Malus species is linked to differences in stomatal behavior and photosynthesis. Physiologia Plantarum 147, 514-523.
8. Bailey-Serres J. & Voesenek L.A.C.J. (2008) Flooding stress: acclimations and genetic diversity. Annual Review of Plant Biology 59, 313-339.
9. Bailey-Serres J., Fukao T., Gibbs D.J., Holdsworth M.J., Lee S.C., Licausi F., .. van Dongen J.T. (2012) Making sense of low oxygen sensing. Trends in Plant Science 17, 129-138.
10. Banti V., Mafessoni F., Loreti E., Alpi A. & Perata P. (2010) The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiology 152, 1471-1483.
11. 1H-NMR spectroscopy. Journal of Proteome Research 11, 320-330.
12. Barding G.A. Jr., Béni S., Fukao T., Bailey-Serres J. & Larive C.K. (2013) Comparison of GC-MS and NMR for metabolite profiling of rice subjected to submergence stress. Journal of Proteome Research 12, 898-909.
13. Baum G., Chen Y., Arazi T., Takatsuji H. & Fromm H. (1993) A plant glutamate decarboxylase containing a calmodulin binding domain. Cloning, sequence, and functional analysis. The Journal of Biological Chemistry 268, 19610-19617.
14. Blasiak J., Mulcahy D.L. & Musgrave M.E. (2001) Oxytropism: a new twist in pollen tube orientation. Planta 213, 318-322.
15. Bond D.M., Wilson I.W., Dennis E.S., Pogson B.J. & Finnegan J.E. (2009) VERNALIZATION INSENSITIVE 3 (VIN3) is required for the response of Arabidopsis thaliana seedlings exposed to low oxygen conditions. The Plant Journal 59, 576-587.
16. Bouché N. & Fromm H. (2004) GABA in plants: just a metabolite? Trends in Plant Science 9, 110-115.
17. Bouché N., Fait A., Bouchez D., Moller S.G. & Fromm H. (2003) Mitochondrial succinic-semialdehyde dehydrogenase of the γ-aminobutyrate shunt is required to restrict levels of reactive oxygen intermediates in plants. Proceedings of the National Academy of Sciences of the United States of America 100, 6843-6848.
18. Bouché N., Fait A., Zik M. & Fromm H. (2004) The root-specific glutamate decarboxylase (GAD1) is essential for sustaining GABA levels in Arabidopsis. Plant Molecular Biology 55, 315-325.
19. Bradford K.J. & Yang S.F. (1980) Xylem transport of 1-aminocyclopropane-1-carboxylic acid, an ethylene precursor, in waterlogged tomato plants. Plant Physiology 65, 322-326.
20. Branco-Price C., Kaiser K.A., Jang C.J.H., Larive C.K. & Bailey-Serres J. (2008) Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. The Plant Journal 56, 743-755.
21. Breitkreuz K.E. & Shelp B.J. (1995) Subcellular compartmentation of the 4-aminobutyrate shunt in protoplasts from developing soybean cotyledons. Plant Physiology 108, 99-103.
22. Breitkreuz K.E., Allan W.L., Van Cauwenberghe O.R., Jakobs C., Talibi D., Andre B. & Shelp B.J. (2003) A novel gamma-hydroxybutyrate dehydrogenase: identification and expression of an Arabidopsis cDNA and potential role under oxygen deficiency. The Journal of Biological Chemistry 278, 41552-41556.
23. Busch K., Piehler J. & Fromm H. (2000) Plant succinic semialdehyde dehydrogenase: dissection of nucleotide binding by surface plasmon resonance and fluorescence spectroscopy. Biochemistry 39, 10110-10117.
24. Busch K.B. & Fromm H. (1999) Plant succinic semialdehyde dehydrogenase. Cloning, purification, localization in mitochondria, and regulation by adenine nucleotides. Plant Physiology 121, 589-597.
25. Castonguay Y., Nadeau P. & Simard R.R. (1993) Effects of flooding on carbohydrate and ABA levels in roots and shoots of alfalfa. Plant, Cell and Environment 16, 695-702.
26. Chang R., Jang C.J.H., Branco-Price C., Nghiem P. & Bailey-Serres J. (2012) Transient MPK6 activation in response to oxygen deprivation and reoxygenation is mediated by mitochondria and aids seedling survival in Arabidopsis. Plant Molecular Biology 78, 109-122.
27. Christianson J.A., Wilson I.W., Llewellyn D.J. & Dennis E.S. (2009) The low-oxygen-induced NAC domain transcription factor ANAC102 affects viability of Arabidopsis seeds following low-oxygen treatment. Plant Physiology 149, 1724-1738.
28. Christianson J.A., Llewellyn D.J., Dennis E.S. & Wilson I.W. (2010) Global gene expression responses to waterlogging in roots and leaves of cotton (Gossypium hirsutum L. Plant and Cell Physiology 51, 21-37.
29. Clark S.M., Di Leo R., Dhanoa P.K., Van Cauwenberghe O.R., Mullen R.T. & Shelp B.J. (2009) Biochemical characterization, mitochondrial localization, expression, and potential functions for an Arabidopsis γ-aminobutyrate transaminase that utilizes both pyruvate and glyoxylate. Journal of Experimental Botany 60, 1743-1757.
30. Colmer T.D. & Voesenek L.A.C.J. (2009) Flooding tolerance: suites of plant traits in variable environments. Functional Plant Biology 36, 665-681.
31. De Sousa C.A.F. & Sodek L. (2003) Alanine metabolism and alanine aminotransferase activity in soybean (Glycine max) during hypoxia of the root system and subsequent return to normoxia. Environmental and Experimental Botany 50, 1-8.
32. Drew M.C. (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annual Review of Plant Physiology and Plant Molecular Biology 48, 223-250.
33. Ellis M.H., Dennis E.S. & Peacock W.J. (1999) Arabidopsis roots and shoots have different mechanisms for hypoxic stress tolerance. Plant Physiology 119, 57-64.
34. Else M.A., Hall K.C., Arnold G.M., Davies W.J. & Jackson M.B. (1995) Export of abscisic acid, 1-aminocyclopropane-1-carboxylic acid, phosphate, and nitrate from roots to shoots of flooded tomato plants (accounting for effects of xylem sap flow rate on concentration and delivery). Plant Physiology 107, 377-384.
35. Emanuelsson O., Nielsen H., Brunak S. & von Heijne G. (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. Journal of Molecular Biology 300, 1005-1016.
36. Fait A., Fromm H., Walter D., Galili G. & Fernie A.R. (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends in Plant Science 13, 14-19.
37. Fan T.W.N., Higashi R.M., Frenkiel T.A. & Lane A.M. (1997) Anaerobic nitrate and ammonium metabolism in flood-tolerant rice coleoptiles. Journal of Experimental Botany 48, 1655-1666.
38. Fukao T., Xu K., Ronald P.C. & Bailey-Serres J. (2006) A variable cluster of ethylene responsive-like factors (ERFs) regulates developmental and metabolic acclimation responses to submergence. The Plant Cell 18, 2021-2034.
39. Gibon Y., Vigeolas H., Tiessen A., Geigenberger P. & Stitt M. (2002) Sensitive and high throughput metabolite assays for inorganic pyrophosphate, ADPGlc, nucleotide phosphates, and glycolytic intermediates based on a novel enzymic cycling system. The Plant Journal 30, 221-235.
40. Good A.G. & Muench D.G. (1993) Long-term anaerobic metabolism in root tissue (metabolic products of pyruvate metabolism). Plant Physiology 101, 1163-1168.
41. Hothorn T., Bretz F. & Westfall P. (2008) Simultaneous inference in general parametric models. Biometrical Journal 50, 346-363.
42. Hsu F.-C., Chou M.-Y., Peng H.-P., Chou S.-J. & Shih M.-C. (2011) Insights into hypoxic systemic responses based on analyses of transcriptional regulation in Arabidopsis. PLoS ONE 6, e28888.
43. Hsu F.-C., Chou M.-Y., Chou S.-J., Li Y.-R., Peng H.-P. & Shih M.-C. (2013) Submergence confers immunity mediated by the WRKY22 transcription factor in Arabidopsis. The Plant Cell 25, 2699-2713.
44. Kreuzwieser J., Hauberg J., Howell K.A., Carroll A., Rennenberg H., Millar A.H. & Whelan J. (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiology 149, 461-473.
45. Lasanthi-Kudahettige R., Magneschi L., Loreti E., Gonzali S., Licausi F., Novi G., .. Perata P. (2007) Transcript profiling of the anoxic rice coleoptile. Plant Physiology 144, 218-231.
46. Lee D.Y. & Fiehn O. (2008) High quality metabolomic data for Chlamydomonas reinhardtii. Plant Methods 4, 7.
47. Lee S.C., Mustroph A., Sasidharan R., Vashisht D., Pedersen O., Oosumi T., .. Bailey-Serres J. (2011) Molecular characterization of the submergence response of the Arabidopsis thaliana ecotype Columbia. The New Phytologist 190, 457-471.
48. Licausi F., van Dongen J.T., Giuntoli B., Novi G., Santaniello A., Geigenberger P. & Perata P. (2010) HRE1 and HRE2, two hypoxia-inducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana. The Plant Journal 62, 302-315.
49. Liepman A.H. & Olsen L.J. (2003) Alanine aminotransferase homologs catalyze the glutamate:glyoxylate aminotransferase reaction in peroxisomes of Arabidopsis. Plant Physiology 131, 215-227.
50. Linskens H.F. & Schrauwen J. (1966) Measurement of oxygen tension changes in the style during pollen tube growth. Planta 71, 98-106.
51. Loreti E., Poggi A., Novi G., Alpi A. & Perata P. (2005) A genome-wide analysis of the effects of sucrose on gene expression in Arabidopsis seedlings under anoxia. Plant Physiology 137, 1130-1138.
52. Ludewig F., Hüser A., Fromm H., Beauclair L. & Bouché N. (2008) Mutants of GABA transaminase (POP2) suppress the severe phenotype of succinic semialdehyde dehydrogenase (ssadh) mutants in Arabidopsis. PLoS ONE 3, e3383.
53. Menegus F., Cattaruzza L., Chersi A. & Fronza G. (1989) Differences in the anaerobic lactate-succinate production and in the changes of cell sap pH for plants with high and low resistance to anoxia. Plant Physiology 90, 29-32.
54. Michaeli S., Fait A., Lagor K., Nunes-Nesi A., Grillich N., Yellin A., .. Fromm H. (2011) A mitochondrial GABA permease connects the GABA shunt and the TCA cycle, and is essential for normal carbon metabolism. The Plant Journal 67, 485-498.
55. Miyashita Y. & Good A.G. (2008) Contribution of the GABA shunt to hypoxia-induced alanine accumulation in roots of Arabidopsis thaliana. Plant and Cell Physiology 49, 92-102.
56. Miyashita Y., Dolferus R., Ismond K.P. & Good A.G. (2007) Alanine aminotransferase catalyses the breakdown of alanine after hypoxia in Arabidopsis thaliana: AlaAT in Arabidopsis. The Plant Journal 49, 1108-1121.
57. Muench D.G. & Good A.G. (1994) Hypoxically inducible barley alanine aminotransferase: cDNA cloning and expression analysis. Plant Molecular Biology 24, 417-427.
58. Mustroph A. & Bailey-Serres J. (2010) The Arabidopsis translatome cell-specific mRNA atlas: mining suberin and cutin lipid monomer biosynthesis genes as an example for data application. Plant Signaling & Behavior 5, 320-324.
59. Mustroph A., Boamfa E.I., Laarhoven L.J.J., Harren F.J.M., Albrecht G. & Grimm B. (2006a) Organ-specific analysis of the anaerobic primary metabolism in rice and wheat seedlings. I: dark ethanol production is dominated by the shoots. Planta 225, 103-114.
60. Mustroph A., Boamfa E.I., Laarhoven L.J.J., Harren F.J.M., Pörs Y. & Grimm B. (2006b) Organ specific analysis of the anaerobic primary metabolism in rice and wheat seedlings II: light exposure reduces needs for fermentation and extends survival during anaerobiosis. Planta 225, 139-152.
61. Mustroph A., Zanetti M.E., Jang C.J.H., Holtan H.E., Repetti P.P., Galbraith D.W., .. Bailey-Serres J. (2009) Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 106, 18843-18848.
62. Mustroph A., Lee S.C., Oosumi T., Zanetti M.E., Yang H., Ma K., .. Bailey-Serres J. (2010) Cross-kingdom comparison of transcriptomic adjustments to low-oxygen stress highlights conserved and plant-specific responses. Plant Physiology 152, 1484-1500.
63. Nakamura T., Yamamoto R., Hiraga S., Nakayama N., Okazaki K., Takahashi H., .. Komatsu S. (2012) Evaluation of metabolite alteration under flooding stress in soybeans. Japan Agricultural Research Quarterly 46, 237-248.
64. Narsai R., Howell K.A., Carroll A., Ivanova A., Millar A.H. & Whelan J. (2009) Defining core metabolic and transcriptomic responses to oxygen availability in rice embryos and young seedlings. Plant Physiology 151, 306-322.
65. Narsai R., Rocha M., Geigenberger P., Whelan J. & van Dongen J.T. (2011) Comparative analysis between plant species of transcriptional and metabolic responses to hypoxia. The New Phytologist 190, 472-487.
66. Ogg R.J., Kingsley P.B. & Taylor J.S. (1994) WET, a T-1-insensitive and B-1-insensitive water-suppression method for in-vivo localized H-1-NMR spectroscopy. Journal of Magnetic Resonance. Series B 104, 1-10.
67. Palanivelu R., Brass L., Edlund A.F. & Preuss D. (2003) Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114, 47-59.
68. Reggiani R., Cantú C.A., Brambilla I. & Bertani A. (1988) Accumulation and interconversion of amino acids in rice roots under anoxia. Plant and Cell Physiology 29, 981-987.
69. Renault H., El Amrani A., Palanivelu R., Updegraff E.P., Yu A., Renou J.-P., .. Deleu C. (2011) GABA accumulation causes cell elongation defects and a decrease in expression of genes encoding secreted and cell wall-related proteins in Arabidopsis thaliana. Plant and Cell Physiology 52, 894-908.
70. Rich S.M., Pedersen O., Ludwig M. & Colmer T.D. (2013) Shoot atmospheric contact is of little importance to aeration of deeper portions of the wetland plant Meionectes brownii; submerged organs mainly acquire O2 from the water column or produce it endogenously in underwater photosynthesis. Plant, Cell & Environment 36, 213-223.
71. Roberts J.K., Callis J., Jardetzky O., Walbot V. & Freeling M. (1984a) Cytoplasmic acidosis as a determinant of flooding intolerance in plants. Proceedings of the National Academy of Sciences of the United States of America 81, 6029-6033.
72. Roberts J.K., Callis J., Wemmer D., Walbot V. & Jardetzky O. (1984b) Mechanisms of cytoplasmic pH regulation in hypoxic maize root tips and its role in survival under hypoxia. Proceedings of the National Academy of Sciences of the United States of America 81, 3379-3383.
73. Rocha M., Licausi F., Araújo W.L., Nunes-Nesi A., Sodek L., Fernie A.R. & van Dongen J.T. (2010a) Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiology 152, 1501-1513.
74. Rocha M., Sodek L., Licausi F., Hameed M.W., Dornelas M.C. & van Dongen J.T. (2010b) Analysis of alanine aminotransferase in various organs of soybean (Glycine max) and in dependence of different nitrogen fertilisers during hypoxic stress. Amino Acids 39, 1043-1053.
75. Sachs M.M., Freeling M. & Okimoto R. (1980) The anaerobic proteins of maize. Cell 20, 761-767.
76. Sachs M.M., Subbaiah C.C. & Saab I.N. (1996) Anaerobic gene expression and flooding tolerance in maize. Journal of Experimental Botany 47, 1-15.
77. Sato T., Harada T. & Ishizawa K. (2002) Stimulation of glycolysis in anaerobic elongation of pondweed (Potamogeton distinctus) turions. Journal of Experimental Botany 53, 1847-1856.
78. Shelp B.J., Walton C.S., Snedden W.A., Tuin L.G., Oresnik I.J. & Layzell D.B. (1995) Gaba shunt in developing soybean seeds is associated with hypoxia. Physiologia Plantarum 94, 219-228.
79. Simpson J.P., Di Leo R., Dhanoa P.K., Allan W.L., Makhmoudova A., Clark S.M., .. Shelp B.J. (2008) Identification and characterization of a plastid-localized Arabidopsis glyoxylate reductase isoform: comparison with a cytosolic isoform and implications for cellular redox homeostasis and aldehyde detoxification. Journal of Experimental Botany 59, 2545-2554.
80. Snedden W.A., Chung I., Pauls R.H. & Bown A.W. (1992) Proton/l-Glutamate symport and the regulation of intracellular pH in isolated mesophyll cells. Plant Physiology 99, 665-671.
81. Snedden W.A., Koutsia N., Baum G. & Fromm H. (1996) Activation of a recombinant petunia glutamate decarboxylase by calcium/.calmodulin or by a monoclonal antibody which recognizes the calmodulin binding domain. The Journal of Biological Chemistry 271, 4148-4153.
82. Streeter J.G. & Thompson J.F. (1972a) Anaerobic accumulation of gamma-aminobutyric acid and alanine in radish leaves (Raphanus sativus, L. Plant Physiology 49, 572-578.
83. Streeter J.G. & Thompson J.F. (1972b) In vivo and in vitro studies on gamma-aminobutyric acid metabolism with the radish plant (Raphanus sativus, L. Plant Physiology 49, 579-584.
84. Subbaiah C.C., Bush D.S. & Sachs M.M. (1994a) Elevation of cytosolic calcium precedes anoxic gene expression in maize suspension-cultured cells. The Plant Cell 6, 1747-1762.
85. Subbaiah C.C., Zhang J. & Sachs M.M. (1994b) Involvement of intracellular calcium in anaerobic gene expression and survival of maize seedlings. Plant Physiology 105, 369-376.
86. Turano F.J. & Fang T.K. (1998) Characterization of two glutamate decarboxylase cDNA clones from Arabidopsis. Plant Physiology 117, 1411-1421.
87. Van Cauwenberghe O.R. & Shelp B.J. (1999) Biochemical characterization of partially purified gaba:pyruvate transaminase from Nicotiana tabacum. Phytochemistry 52, 575-581.
88. Van Cauwenberghe O.R., Makhmoudova A., McLean M.D., Clark S.M. & Shelp B.J. (2002) Plant pyruvate-dependent gamma-aminobutyrate transaminase: identification of an Arabidopsis cDNA and its expression in Escherichia coli. Canadian Journal of Botany 80, 933-941.
89. Van Dongen J.T., Frohlich A., Ramirez-Aguilar S.J., Schauer N., Fernie A.R., Erban A., .. Geigenberger P. (2009) Transcript and metabolite profiling of the adaptive response to mild decreases in oxygen concentration in the roots of Arabidopsis plants. Annals of Botany 103, 269-280.
90. Vashisht D., Hesselink A., Pierik R., Ammerlaan J.M.H., Bailey-Serres J., Visser E.J.W., .. Sasidharan R. (2011) Natural variation of submergence tolerance among Arabidopsis thaliana accessions. The New Phytologist 190, 299-310.
91. Winkel A., Colmer T.D., Ismail A.M. & Pedersen O. (2013) Internal aeration of paddy field rice (Oryza sativa) during complete submergence - importance of light and floodwater O2. The New Phytologist 197, 1193-1203.
92. + sources in rice and wheat protoplasts. Planta 234, 271-280.
93. Zik M., Arazi T., Snedden W.A. & Fromm H. (1998) Two isoforms of glutamate decarboxylase in Arabidopsis are regulated by calcium/calmodulin and differ in organ distribution. Plant Molecular Biology 37, 967-975.