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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Metabolomics analysis of postphotosynthetic effects of gaseous O2 on primary metabolism in illuminated leaves

Cyril Abadie A , Sophie Blanchet A B , Adam Carroll A and Guillaume Tcherkez A C
+ Author Affiliations
- Author Affiliations

A Research School of Biology, College of Medicine, Biology and Environment, Australian National University, Canberra, ACT 2601, Australia.

B Institute of Plant Science Paris-Saclay, UMR Université Paris-Sud-CNRS-INRA-Université Paris-Diderot-UEVE 1403, 91405 Orsay, France.

C Corresponding author. Email: guillaume.tcherkez@anu.edu.au

Functional Plant Biology 44(9) 929-940 https://doi.org/10.1071/FP16355
Submitted: 13 October 2016  Accepted: 21 March 2017   Published: 6 June 2017

Abstract

The response of underground plant tissues to O2 limitation is currently an important topic in crop plants since adverse environmental conditions (e.g. waterlogging) may cause root hypoxia and thus compromise plant growth. However, little is known on the effect of low O2 conditions in leaves, probably because O2 limitation is improbable in these tissues under natural conditions, unless under complete submersion. Nevertheless, an O2-depleted atmosphere is commonly used in gas exchange experiments to suppress photorespiration and estimate gross photosynthesis. However, the nonphotosynthetic effects of gaseous O2 depletion, particularly on respiratory metabolism, are not well documented. Here, we used metabolomics obtained under contrasting O2 and CO2 conditions to examine the specific effect of a changing O2 mole fraction from ambient (21%) to 0%, 2% or 100%. In addition to the typical decrease in photorespiratory intermediates (glycolate, glycine and serine) and a build-up in photosynthates (sucrose), low O2 (0% or 2%) was found to trigger an accumulation of alanine and change succinate metabolism. In 100% O2, the synthesis of threonine and methionine from aspartate appeared to be stimulated. These responses were observed in two species, sunflower (Helianthus annuus L.) and Arabidopsis thaliana (L.) Heynh. Our results show that O2 causes a change in the oxygenation : carboxylation ratio and also alters postphotosynthetic metabolism: (i) a hypoxic response at low O2 mole fractions and (ii) a stimulation of S metabolism at high O2 mole fractions. The latter effect is an important piece of information to better understand how photorespiration may control S assimilation.

Additional keywords: methionine, mitochondrial respiration, oxygen deficiency, photosynthesis.


References

Abadie C, Boex-Fontvieille ERA, Carroll AJ, Tcherkez G (2016a) In vivo stoichiometry of photorespiratory metabolism. Nature Plants 2, 15220
In vivo stoichiometry of photorespiratory metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsVKlsLs%3D&md5=36f16735bd5f9ae5d903df519192947dCAS |

Abadie C, Mainguet S, Davanture M, Hodges M, Zivy M, Tcherkez G (2016b) Concerted changes in phosphoproteome and metabolome under different CO2/O2 gaseous conditions in Arabidopsis rosettes. Plant & Cell Physiology 57, 1544–1556.
Concerted changes in phosphoproteome and metabolome under different CO2/O2 gaseous conditions in Arabidopsis rosettes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhs1OntbrO&md5=b969f05a980f1841eeec19cc79bc35f3CAS |

Ahsan N, Lee D-G, Lee S-H, Kang KY, Bahk JD, Choi MS, Lee I-J, Renaut J, Lee B-H (2007) A comparative proteomic analysis of tomato leaves in response to waterlogging stress. Physiologia Plantarum 131, 555–570.
A comparative proteomic analysis of tomato leaves in response to waterlogging stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVers7fE&md5=24f413956349a7b06fe6ae8675086865CAS |

Akita S, Moss DN (1973) The effect of an oxygen-free atmosphere on net photosynthesis and transpiration of barley (Hordeum vulgare L.) and wheat (Triticum aestivum L.) leaves. Plant Physiology 52, 601–603.
The effect of an oxygen-free atmosphere on net photosynthesis and transpiration of barley (Hordeum vulgare L.) and wheat (Triticum aestivum L.) leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXjsFWguw%3D%3D&md5=67aa7c44a3cc7e24b9056fd428b946b8CAS |

António C, Päpke C, Rocha M, Diab H, Limami A, Obata T, Fernie A, von Dongen J (2016) Regulation of primary metabolism in response to low oxygen availability as revealed by carbon and nitrogen isotope redistribution. Plant Physiology 170, 43–56.
Regulation of primary metabolism in response to low oxygen availability as revealed by carbon and nitrogen isotope redistribution.Crossref | GoogleScholarGoogle Scholar |

Azcón-Bieto J (1983) Inhibition of photosynthesis by carbohydrates in wheat leaves. Plant Physiology 73, 681–686.
Inhibition of photosynthesis by carbohydrates in wheat leaves.Crossref | GoogleScholarGoogle Scholar |

Azevedo RA, Lancien M, Lea PJ (2006) The aspartic acid metabolic pathway, an exciting and essential pathway in plants. Amino Acids 30, 143–162.
The aspartic acid metabolic pathway, an exciting and essential pathway in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1Oksbw%3D&md5=838a2c7ca1a5fd24ee7b0d68da4303bdCAS |

Badger MR, Sharkey TD, von Caemmerer S (1984) The relationship between steady-state gas exchange of bean leaves and the levels of carbon-reduction-cycle intermediates. Planta 160, 305–313.
The relationship between steady-state gas exchange of bean leaves and the levels of carbon-reduction-cycle intermediates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXitVKluro%3D&md5=40f3a731352b1ce8ee3aae9e0c5579bfCAS |

Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448, 938–942.
A central integrator of transcription networks in plant stress and energy signalling.Crossref | GoogleScholarGoogle Scholar |

Bailey-Serres J, Voesenek LA (2010) Life in the balance: a signaling network controlling survival of flooding. Current Opinion in Plant Biology 13, 489–494.
Life in the balance: a signaling network controlling survival of flooding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlKls7%2FM&md5=a628268841a10e1d77430817679ea058CAS |

Bailey-Serres J, Lee SC, Brinton E (2012) Waterproofing crops: effective flooding survival strategies. Plant Physiology 160, 1698–1709.
Waterproofing crops: effective flooding survival strategies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVKmt73E&md5=837dcf1844c946482fb56732ab57bcb5CAS |

Barbour MM (2007) Stable oxygen isotope composition of plant tissue: a review. Functional Plant Biology 34, 83–93.
Stable oxygen isotope composition of plant tissue: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhs1yqsbs%3D&md5=763f5a3e632a17fd2928919804941c80CAS |

Bates DM, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |

Bertani A, Brambilla I (1982) Effect of decreasing oxygen concentration on some aspects of protein and amino-acid metabolism in rice roots. Zeitschrift für Pflanzenphysiologie 107, 193–200.
Effect of decreasing oxygen concentration on some aspects of protein and amino-acid metabolism in rice roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38Xlslyrs7Y%3D&md5=c63792871113fea5616fcfb3129f5774CAS |

Bryan JK (1990) Differential regulation of maize homoserine dehydrogenase under physiological conditions. Plant Physiology 92, 785–791.
Differential regulation of maize homoserine dehydrogenase under physiological conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhslCksrs%3D&md5=08e48a76c307cdcc474fbf8412d94839CAS |

Diab H, Limami A (2016) Reconfiguration of N metabolism upon hypoxia stress and recovery: roles of alanine aminotransferase (AlaAT) and glutamate dehydrogenase (GDH). Plants 5, 25
Reconfiguration of N metabolism upon hypoxia stress and recovery: roles of alanine aminotransferase (AlaAT) and glutamate dehydrogenase (GDH).Crossref | GoogleScholarGoogle Scholar |

Douce R, Bourguignon J, Neuburger M, Rébeillé F (2001) The glycine decarboxylase system: a fascinating complex. Trends in Plant Science 6, 167–176.
The glycine decarboxylase system: a fascinating complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFKmtbo%3D&md5=7d0d67879ae6d6e25beaf14ec6a0d256CAS |

Ellis MH, Dennis ES, Peacock WJ (1999) Arabidopsis roots and shoots have different mechanisms for hypoxic stress tolerance. Plant Physiology 119, 57–64.
Arabidopsis roots and shoots have different mechanisms for hypoxic stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmt1Gmug%3D%3D&md5=f247cd87f87e37d53055a4219ba74031CAS |

Eriksson L, Trygg J, Wold S (2008) CV-ANOVA for significance testing of PLS and OPLS models. Journal of Chemometrics 22, 594–600.
CV-ANOVA for significance testing of PLS and OPLS models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmt1emsg%3D%3D&md5=3f753414c11ce58d5e47d6890fb8266cCAS |

Few R (2003) Flooding, vulnerability and coping strategies: local responses to a global threat. Progress in Development Studies 3, 43–58.
Flooding, vulnerability and coping strategies: local responses to a global threat.Crossref | GoogleScholarGoogle Scholar |

Flanagan L, Phillips S, Ehleringer J, Lloyd J, Farquhar G (1994) Effect of changes in leaf water oxygen isotopic composition on discrimination against C18O16O during photosynthetic gas exchange. Australian Journal of Plant Physiology 21, 221–234.
Effect of changes in leaf water oxygen isotopic composition on discrimination against C18O16O during photosynthetic gas exchange.Crossref | GoogleScholarGoogle Scholar |

Galili G (1995) Regulation of lysine and threonine synthesis. The Plant Cell 7, 899–906.
Regulation of lysine and threonine synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnt1Sgtr0%3D&md5=0f6ed251d28baf035e7948472fa41c03CAS |

Geiger DR, Sovonick SA (1975) Effects of temperature, anoxia and other metabolic inhibitors on translocation. In ‘Transport in plants I. Phloem transport’. (Eds MH Zimmermann, JA Milburn) pp. 256–286. (Springer Berlin Heidelberg: Berlin)

Goldschmidt EE, Huber SC (1992) Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars. Plant Physiology 99, 1443–1448.
Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtV2jt7o%3D&md5=56b17c7a6f8bad0dfbb81211520237a9CAS |

Griffin KL, Turnbull MH (2013) Light saturated RuBP oxygenation by Rubisco is a robust predictor of light inhibition of respiration in Triticum aestivum L. Plant Biology 15, 769–775.
Light saturated RuBP oxygenation by Rubisco is a robust predictor of light inhibition of respiration in Triticum aestivum L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFOgsLjK&md5=8a0586ced8e2a55520f5fc918422bae8CAS |

Hesse H, Kreft O, Maimann S, Zeh M, Hoefgen R (2004) Current understanding of the regulation of methionine biosynthesis in plants. Journal of Experimental Botany 55, 1799–1808.
Current understanding of the regulation of methionine biosynthesis in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntFaisbk%3D&md5=7e66f167d586a58937b315f9d098823dCAS |

Hourton-Cabassa C, Ambard-Bretteville F, Moreau F, Davy de Virville J, Rémy R, Des Francs-Small C (1998) Stress induction of mitochondrial formate dehydrogenase in potato leaves. Plant Physiology 116, 627–635.
Stress induction of mitochondrial formate dehydrogenase in potato leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXht1aju7c%3D&md5=2814d465f9d019df0ec95223d0610516CAS |

Irsigler AS, Costa MD, Zhang P, Reis PA, Dewey RE, Boston RS, Fontes EP (2007) Expression profiling on soybean leaves reveals integration of ER- and osmotic-stress pathways. BMC Genomics 8, 431
Expression profiling on soybean leaves reveals integration of ER- and osmotic-stress pathways.Crossref | GoogleScholarGoogle Scholar |

Ishii R, Murata Y (1978) Further evidence of the Kok effects in C3 plants and the effects of environmental factors on it. Nihon Sakumotsu Gakkai Kiji 47, 547–550.
Further evidence of the Kok effects in C3 plants and the effects of environmental factors on it.Crossref | GoogleScholarGoogle Scholar |

Ismond KP, Dolferus R, de Pauw M, Dennis ES, Good AG (2003) Enhanced low oxygen survival in Arabidopsis through increased metabolic flux in the fermentative pathway. Plant Physiology 132, 1292–1302.
Enhanced low oxygen survival in Arabidopsis through increased metabolic flux in the fermentative pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsFGhtLk%3D&md5=b944d91718bd8fced3ca32cfce50bd70CAS |

Klecker M, Gasch P, Peisker H, Dörmann P, Schlicke H, Grimm B, Mustroph A (2014) A shoot-specific hypoxic response of Arabidopsis sheds light on the role of the phosphate-responsive transcription factor PHOSPHATE STARVATION RESPONSE1. Plant Physiology 165, 774–790.
A shoot-specific hypoxic response of Arabidopsis sheds light on the role of the phosphate-responsive transcription factor PHOSPHATE STARVATION RESPONSE1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVWnurbJ&md5=f702b325027c0d769202b4c4b0395a9bCAS |

Komatsu S, Hiraga S, Yanagawa Y (2012) Proteomics techniques for the development of flood tolerant crops. Journal of Proteome Research 11, 68–78.
Proteomics techniques for the development of flood tolerant crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlOnsr7O&md5=eaafdc76cc5f43762a4679b76e8dcf9bCAS |

Krause GH, Köster S, Wong SC (1985) Photoinhibition of photosynthesis under anaerobic conditions studied with leaves and chloroplasts of Spinacia oleracea L. Planta 165, 430–438.
Photoinhibition of photosynthesis under anaerobic conditions studied with leaves and chloroplasts of Spinacia oleracea L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXltlyrsb8%3D&md5=c2c586368f097cada7ffe6298e062affCAS |

Kreuzwieser J, Rennenberg H (2014) Molecular and physiological responses of trees to waterlogging stress. Plant, Cell & Environment 37,
Molecular and physiological responses of trees to waterlogging stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFylsrbF&md5=8c7c68842f2a5485e8eaa69f5438fa9eCAS |

Kreuzwieser J, Hauberg J, Howell KA, Carroll A, Rennenberg H, Millar AH, Whelan J (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiology 149, 461–473.
Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjt1WqtLw%3D&md5=0a702b68edc3f5dadb1e1b71426d5998CAS |

Lasanthi-Kudahettige R, Magneschi L, Loreti E, Gonzali S, Licausi F, Novi G, Beretta O, Vitulli F, Alpi A, Perata P (2007) Transcript profiling of the anoxic rice coleoptile. Plant Physiology 144, 218–231.
Transcript profiling of the anoxic rice coleoptile.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXls1KjtL8%3D&md5=e63c8543236e96e856f99b1d2f2bee21CAS |

Leegood RC, Furbank RT (1986) Stimulation of photosynthesis by 2% oxygen at low temperatures is restored by phosphate. Planta 168, 84–93.
Stimulation of photosynthesis by 2% oxygen at low temperatures is restored by phosphate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xktl2mtLY%3D&md5=36d90d38174ab4a74282bc273973df1bCAS |

Limami AM, Glévarec G, Ricoult C, Cliquet J-B, Planchet E (2008) Concerted modulation of alanine and glutamate metabolism in young Medicago truncatula seedlings under hypoxic stress. Journal of Experimental Botany 59, 2325–2335.
Concerted modulation of alanine and glutamate metabolism in young Medicago truncatula seedlings under hypoxic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnt1Sls7w%3D&md5=5a4d86e07f63842951191dbbbb00ff6aCAS |

Limami AM, Diab H, Lothier J (2014) Nitrogen metabolism in plants under low oxygen stress. Planta 239, 531–541.
Nitrogen metabolism in plants under low oxygen stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitVWjtLbF&md5=cb573804bb374f42bf4aa23179d01fbbCAS |

Liu F, Vantoai T, Moy LP, Bock G, Linford LD, Quackenbush J (2005) Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. Plant Physiology 137, 1115–1129.
Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXislOqs7s%3D&md5=d6564a1ba6fc802b60fe2b7473a416e0CAS |

McVetty PBE, Canvin DT (1981) Inhibition of photosynthesis by low oxygen concentrations. Canadian Journal of Botany 59, 721–725.
Inhibition of photosynthesis by low oxygen concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXktVelsLk%3D&md5=b3a94a582f61857696a57f447144e6d7CAS |

Messinger SM, Buckley TN, Mott KA (2006) Evidence for involvement of photosynthetic processes in the stomatal response to CO2. Plant Physiology 140, 771–778.
Evidence for involvement of photosynthetic processes in the stomatal response to CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjsV2iu7g%3D&md5=573289208bed281e7784a5174d2d400dCAS |

Mills WR, Lea PJ, Miflin BJ (1980) Photosynthetic formation of the aspartate family of amino acids in isolated chloroplasts. Plant Physiology 65, 1166–1172.
Photosynthetic formation of the aspartate family of amino acids in isolated chloroplasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXks1KntLc%3D&md5=9fe87b2a9d2cd100ad7335c09e4254bfCAS |

Noctor G, Bergot G, Mauve C, Thominet D, Lelarge-Trouverie C, Prioul J-L (2007) A comparative study of amino acid measurement in leaf extracts by gas chromatography-time of flight-mass spectrometry and high performance liquid chromatography with fluorescence detection. Metabolomics 3, 161–174.
A comparative study of amino acid measurement in leaf extracts by gas chromatography-time of flight-mass spectrometry and high performance liquid chromatography with fluorescence detection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhs1Ckur0%3D&md5=44c6171cab913e7b893e567b0894b6e5CAS |

Nogués S, Tcherkez G, Cornic G, Ghashghaie J (2004) Respiratory carbon metabolism following illumination in intact French bean leaves using 13C/12C isotope labeling. Plant Physiology 136, 3245–3254.
Respiratory carbon metabolism following illumination in intact French bean leaves using 13C/12C isotope labeling.Crossref | GoogleScholarGoogle Scholar |

Powles S, Osmond C (1978) Inhibition of the capacity and efficiency of photosynthesis in bean leaflets illuminated in a CO2-free atmosphere at low oxygen: a possible role for photorespiration. Australian Journal of Plant Physiology 5, 619–629.
Inhibition of the capacity and efficiency of photosynthesis in bean leaflets illuminated in a CO2-free atmosphere at low oxygen: a possible role for photorespiration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXhvFahtA%3D%3D&md5=005f28756ebc2f13f8b03286d8512eddCAS |

Ravanel S, Gakiere B, Job D, Douce R (1998) The specific features of methionine biosynthesis and metabolism in plants. Proceedings of the National Academy of Sciences of the United States of America 95, 7805–7812.
The specific features of methionine biosynthesis and metabolism in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktFCgsb8%3D&md5=a9dc34e05a83fd44ec0735a929e1d3e7CAS |

Reggiani R, Bertani A (2003) Anaerobic amino acid metabolism. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 50, 733–736.
Anaerobic amino acid metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovFWis7w%3D&md5=77f96c1bb4778e1b9447b3c5539a421dCAS |

Ricoult C, Cliquet J-B, Limami AM (2005) Stimulation of alanine amino transferase (AlaAT) gene expression and alanine accumulation in embryo axis of the model legume Medicago truncatula contribute to anoxia stress tolerance. Physiologia Plantarum 123, 30–39.
Stimulation of alanine amino transferase (AlaAT) gene expression and alanine accumulation in embryo axis of the model legume Medicago truncatula contribute to anoxia stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFeqs7g%3D&md5=9c296e36ccc566cd10c4adc85d689809CAS |

Ricoult C, Echeverria LO, Cliquet J-B, Limami AM (2006) Characterization of alanine aminotransferase (AlaAT) multigene family and hypoxic response in young seedlings of the model legume Medicago truncatula. Journal of Experimental Botany 57, 3079–3089.
Characterization of alanine aminotransferase (AlaAT) multigene family and hypoxic response in young seedlings of the model legume Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xps1ygsbk%3D&md5=81973213e8c0b0eafc82374afacce91aCAS |

Rocha M, Licausi F, Araújo WL, Nunes-Nesi A, Sodek L, Fernie AR, van Dongen JT (2010) Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiology 152, 1501–1513.
Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmsF2lsbc%3D&md5=8419139650e7936ec6086f69c3c7c2e0CAS |

Sharkey TD (1985) Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations. Botanical Review 51, 53–105.
Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations.Crossref | GoogleScholarGoogle Scholar |

Sharkey TD, Vassey TL (1989) Low oxygen inhibition of photosynthesis is caused by inhibition of starch synthesis. Plant Physiology 90, 385–387.
Low oxygen inhibition of photosynthesis is caused by inhibition of starch synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXksFCgt7o%3D&md5=cc8c6741df24f84281ebdac8a5e4836dCAS |

Sij JW, Swanson CA (1973) Effect of petiole anoxia on phloem transport in squash. Plant Physiology 51, 368–371.
Effect of petiole anoxia on phloem transport in squash.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhtVGisQ%3D%3D&md5=3929ee7212027c9f10b174c6b66d5723CAS |

Ta TC, Joy KW (1986) Metabolism of some amino acids in relation to the photorespiratory nitrogen cycle of pea leaves. Planta 169, 117–122.
Metabolism of some amino acids in relation to the photorespiratory nitrogen cycle of pea leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xls12jsbs%3D&md5=39d4b65d1bd647fb9f6bc0f5d3df8b1eCAS |

Tan YD, Xu H (2014) A general method for accurate estimation of false discovery rates in identification of differentially expressed genes. Bioinformatics 30, 2018–2025.
A general method for accurate estimation of false discovery rates in identification of differentially expressed genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFCrtLrF&md5=c9e8ee490bc1b7962def7e6a70216240CAS |

Tcherkez G, Bligny R, Gout E, Mahé A, Hodges M, Cornic G (2008) Respiratory metabolism of illuminated leaves depends on CO2 and O2 conditions. Proceedings of the National Academy of Sciences of the United States of America 105, 797–802.
Respiratory metabolism of illuminated leaves depends on CO2 and O2 conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVSjtLw%3D&md5=f7721eb18c3f264bd039bc22edd11706CAS |

Tcherkez G, Boex-Fontvieille E, Mahé A, Hodges M (2012a) Respiratory carbon fluxes in leaves. Current Opinion in Plant Biology 15, 308–314.
Respiratory carbon fluxes in leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnsl2qsb0%3D&md5=86d394a23771c158855e830fc873737cCAS |

Tcherkez G, Mahé A, Guérad F, Boex-Fontvieille ERA, Gout E, Lamothe M, Barbour MM, Bligny R (2012b) Short-term effects of CO2 and O2 on citrate metabolism in illuminated leaves. Plant, Cell & Environment 35, 2208–2220.
Short-term effects of CO2 and O2 on citrate metabolism in illuminated leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1WltbjL&md5=970402ec65a9871af11c9e1573b485eaCAS |

Tholen D, Ethier G, Genty B, Pepin S, Zhu X-G (2012) Variable mesophyll conductance revisited: theoretical background and experimental implications. Plant, Cell & Environment 35, 2087–2103.
Variable mesophyll conductance revisited: theoretical background and experimental implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1WltbnI&md5=4bafa48f258844b130223d8d1959bbe6CAS |

Wallsgrove RM, Lea PJ, Miflin BJ (1983) Intracellular localization of aspartate kinase and the enzymes of threonine and methionine biosynthesis in green leaves. Plant Physiology 71, 780–784.
Intracellular localization of aspartate kinase and the enzymes of threonine and methionine biosynthesis in green leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXhvFGjsLs%3D&md5=ee527a3339f1a53a8af0e2ff59d8ffe3CAS |

Whitfield PH (2012) Floods in future climates: a review. Journal of Flood Risk Management 5, 336–365.
Floods in future climates: a review.Crossref | GoogleScholarGoogle Scholar |

Wong SC, Cowan IR, Farquhar GD (1985) Leaf conductance in relation to rate of CO2 assimilation: III. Influences of water stress and photoinhibition. Plant Physiology 78, 830–834.
Leaf conductance in relation to rate of CO2 assimilation: III. Influences of water stress and photoinhibition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlt1Shur0%3D&md5=45ed5a68bf77aa20fc9e4ae57ac06ae4CAS |

Zhu-Shimoni JX, Galili G (1998) Expression of an Arabidopsis aspartate kinase/homoserine dehydrogenase gene is metabolically regulated by photosynthesis-related signals but not by nitrogenous compounds. Plant Physiology 116, 1023–1028.
Expression of an Arabidopsis aspartate kinase/homoserine dehydrogenase gene is metabolically regulated by photosynthesis-related signals but not by nitrogenous compounds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitVOjsrk%3D&md5=710ad298bb388c88f42df642290ce55fCAS |