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Low assimilation efficiency of photorespiratory ammonia in conifer leaves

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Abstract

Glutamine synthetase (GS) localized in the chloroplasts, GS2, is a key enzyme in the assimilation of ammonia (NH3) produced from the photorespiration pathway in angiosperms, but it is absent from some coniferous species belonging to Pinaceae such as Pinus. We examined whether the absence of GS2 is common in conifers (Pinidae) and also addressed the question of whether assimilation efficiency of photorespiratory NH3 differs between conifers that may potentially lack GS2 and angiosperms. Search of the expressed sequence tag database of Cryptomeria japonica, a conifer in Cupressaceae, and immunoblotting analyses of leaf GS proteins of 13 species from all family members in Pinidae revealed that all tested conifers exhibited only GS1 isoforms. We compared leaf NH3 compensation point (γNH3) and the increments in leaf ammonium content per unit photorespiratory activity (NH3 leakiness), i.e. inverse measures of the assimilation efficiency, between conifers (C. japonica and Pinus densiflora) and angiosperms (Phaseolus vulgaris and two Populus species). Both γNH3 and NH3 leakiness were higher in the two conifers than in the three angiosperms tested. Thus, we concluded that the absence of GS2 is common in conifers, and assimilation efficiency of photorespiratory NH3 is intrinsically lower in conifer leaves than in angiosperm leaves. These results imply that acquisition of GS2 in land plants is an adaptive mechanism for efficient NH3 assimilation under photorespiratory environments.

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References

  • Avila C, García-Gutiérrez A, Crespillo R, Cánovas FM (1998) Effects of phosphinotricin treatment on glutamine synthetase isoforms in Scots pine seedlings. Plant Physiol Biochem 36:857–863

    Article  CAS  Google Scholar 

  • Avila C, Suárez MF, Gómez-Maldonado J, Cánovas FM (2001) Spatial and temporal expression of two cytosolic glutamine synthetase genes in Scots pine: functional implications on nitrogen metabolism during early stages of conifer development. Plant J 25:93–102

    Article  CAS  Google Scholar 

  • Avila-Sáez C, Muñoz-Chapuli R, Plomion C, Frigerio J-M, Cánovas FM (2000) Two genes encoding distinct cytosolic glutamine synthetases are closely linked in the pine genome. FEBS lett 477:237–243

    Article  Google Scholar 

  • Bauer D, Biehler K, Fock H, Carrayol E, Hirel B, Migge A, Becker TW (1997) A role for cytosolic glutamine synthetase in the remobilization of leaf nitrogen during water stress in tomato. Physiol Plant 99:241–248

    Article  CAS  Google Scholar 

  • Bernacchi CJ, Portis AR, Nakano H, von Caemmerer S, Long SP (2002) Temperature response of mesophyll conductance. Implications for the determination of rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiol 130:1992–1998

    Article  CAS  Google Scholar 

  • Berner RA (1999) Atmospheric oxygen over Phanerozoic time. Proc Natl Acad Sci USA 96:10955–10957

    Article  CAS  Google Scholar 

  • Blackwell RD, Murray AJS, Lea PJ (1987) Inhibition of photosynthesis in barley with decreased levels of chloroplastic glutamine synthetase activity. J Exp Bot 38:1799–1809

    Article  CAS  Google Scholar 

  • Cánovas FM, Cantón FR, Gallardo F, García-Gutiérrez A, de Vicente A (1991) Accumulation of glutamine synthetase during early development of maritime pine (Pinus pinaster) seedlings. Planta 185:372–378

    Article  Google Scholar 

  • Cánovas FM, Avila C, Cantón FR, Cañas RA, de la Torre F (2007) Ammonium assimilation and amino acid metabolism in conifers. J Exp Bot 58:2307–2318

    Article  Google Scholar 

  • Cantón FR, García-Gutiérrez A, Gallardo F, de Vicente A, Cánovas FM (1993) Molecular characterization of a cDNA clone encoding glutamine synthetase from a gymnosperm, Pinus sylvestris. Plant Mol Biol 22:819–828

    Article  Google Scholar 

  • Castro-Rodríguez V, García-Gutiérrez A, Canales J, Avila C, Kirby EG, Cánovas FM (2011) The glutamine synthetase gene family in Populus. BMC Plant Biol 11:119

    Article  Google Scholar 

  • Choi YA, Kim SG, Kwon YM (1999) The plastidic glutamine synthetase activity is directly modulated by means of redox change at two unique cysteine residues. Plant Sci 149:175–182

    Article  CAS  Google Scholar 

  • Christenhusz MJM, Reveal JL, Farjon A, Gardner MF, Mill RR, Chase MW (2011) A new classification and linear sequence of extant gymnosperms. Phytotaxa 19:55–70

    Article  Google Scholar 

  • Cock JM, Brock IW, Watson AT, Swarup R, Morby AP, Cullimore JV (1991) Regulation of glutamine synthetase genes in leaves of Phaseolus vulgaris. Plant Mol Biol 17:761–771

    Article  CAS  Google Scholar 

  • de la Torre F, García-Gutiérrez A, Crespillo R, Cantón F, Ávila C, Cánovas FM (2002) Functional expression of two pine glutamine synthetase in bacteria reveals that they encode cytosolic holoenzymes with different molecular and catalytic properties. Plant Cell Physiol 43:802–809

    Article  Google Scholar 

  • Epron D, Godard D, Cornic G, Genty B (1995) Limitation of net CO2 assimilation rate by internal resistances to CO2 transfer in the leaves of two tree species (Fagus sylvatica L.nd Castanea sativa Mill.). Plant Cell Environ 18:43–51

    Article  Google Scholar 

  • Ethier GJ, Livingston NJ (2004) On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar–von Caemmerer–Berry leaf photosynthesis model. Plant Cell Environ 27:137–153

    Article  CAS  Google Scholar 

  • Farquhar GD, Firth PM, Wetselaar R, Weir B (1980a) On the gaseous exchange of ammonia between leaves and the environment: determination of the ammonia compensation point. Plant Physiol 66:710–714

    Article  CAS  Google Scholar 

  • Farquhar GD, von Caemmerer S, Berry JA (1980b) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90

    Article  CAS  Google Scholar 

  • Fu J, Sampalo R, Gallardo F, Cánovas FM, Kirby EG (2003) Assembly of a cytosolic pine glutamine synthetase holoenzyme in leaves of transgenic poplar leads to enhanced vegetative growth in young plants. Plant Cell Environ 26:411–418

    Article  CAS  Google Scholar 

  • Galmés J, Flexas J, Keys AJ, Cifre J, Mitchell RAC, Madgwick PJ, Haslam RP, Medrano H, Parry MAJ (2005) Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves. Plant Cell Environ 28:571–579

    Article  Google Scholar 

  • García-Gutiérrez A, Dubois F, Cantón FR, Gallardo F, Sangwan RS, Cánovas FM (1998) Two different modes of early development and nitrogen assimilation in gymnosperm seedlings. Plant J 13:187–199

    Article  Google Scholar 

  • Geßler A, Rienks M, Rennenberg H (2002) Stomatal uptake and cuticular adsorption contribute to dry deposition of NH3 and NO2 to needles of adult spruce (Picea abies) trees. New Phytol 156:179–194

    Article  Google Scholar 

  • Haworth M, Elliot-Kingston C, McElwain JC (2011) Stomatal control as a driver of plant evolution. J Exp Bot 62:2419–2423

    Article  CAS  Google Scholar 

  • Hayashi K, Hiradate S, Ishikawa S, Nouchi I (2008) Ammonia exchange between rice leaf blade and the atmosphere: Effect of broadcast urea and changes in xylem sap and leaf apoplastic ammonium concentrations. Soil Sci Plant Nutr 54:807–818

    Article  CAS  Google Scholar 

  • Hermida-Carrera C, Kapralov MV, Galmés J (2016) Rubisco catalytic properties and temperature response in crops. Plant Physiol 171:2549–2561

    CAS  PubMed  PubMed Central  Google Scholar 

  • Husted S, Hebbern CA, Mattsson M, Schjoerring JK (2000) A critical experimental evaluation of methods for determination of NH4 + in plant tissue, xylem sap and apoplastic fluid. Physiol Plant 109:167–179

    Article  CAS  Google Scholar 

  • Kamachi K, Yamaya T, Hayakawa T, Mae T, Ojima K (1992) Vascular bundle-specific localization of cytosolic glutamine synthetase in rice leaves. Plant Physiol 99:1481–1486

    Article  CAS  Google Scholar 

  • Kozaki A, Takeba G (1996) Photorespiration protects C3 plants from photooxidation. Nature 384:557–560

    Article  CAS  Google Scholar 

  • Kumagai E, Araki T, Hamaoka N, Ueno O (2011) Ammonia emission from rice leaves in relation to photorespiration and genotypic differences in glutamine synthetase activity. Ann Bot 108:1381–1386

    Article  CAS  Google Scholar 

  • Lara M, Porta H, Padilla J, Folch J, Sánchez F (1984) Heterogeneity of glutamine synthetase polypeptides in Phaseolus vulgaris L. Plant Physiol 76:1019–1023

    Article  CAS  Google Scholar 

  • Lea PJ (1997) Primary nitrogen metabolism. In: Dey PM, Harborne JB (eds) Plant biochemistry. Academic Press, London, pp 273–313

    Chapter  Google Scholar 

  • Lea PJ, Blackwell RD, Chen F-L, Hecht U (1990) Enzymes of ammonia assimilation. In: Lea PJ (ed) Methods in plant biochemistry, vol 3. Academic Press, London, pp 257–276

    Google Scholar 

  • Lightfoot DA, Green NK, Cullimore JV (1988) The chloroplast-located glutamine synthetase of Phaseolus vulgaris L.: nucleotide sequence, expression in different organs and uptake into isolated chloroplasts. Plant Mol Biol 11:191–202

    Article  CAS  Google Scholar 

  • Mattsson M, Schjoerring JK (2002) Dynamic and steady-state responses of inorganic nitrogen pools and NH3 exchange in leaves of Lolium perenne and Bromus erectus to changes in root nitrogen supply. Plant Physiol 128:742–750

    Article  CAS  Google Scholar 

  • Mills WR, Joy KW (1980) A rapid method for isolation of purified, physiologically active chloroplasts, used to study the intracellular distribution of amino acids in pea leaves. Planta 148:75–83

    Article  CAS  Google Scholar 

  • Miyazawa S-I, Yoshimura S, Shinzaki Y, Maeshima M, Miyake C (2008) Deactivation of aquaporins decreases internal conductance to CO2 diffusion in tobacco leaves grown under long-term drought. Funct Plant Biol 35:553–564

    Article  CAS  Google Scholar 

  • Miyazawa S-I, Hayashi K, Nakamura H, Hasegawa T, Miyao M (2014) Elevated CO2 decreases the photorespiratory NH3 production but does not decrease the NH3 compensation point in rice leaves. Plant Cell Physiol 55:1582–1591

    Article  CAS  Google Scholar 

  • Pons TL, Flexas J, von Caemmerer S, Evans JR, Genty B, Ribas-Carbo M, Brugnoli E (2009) Estimating mesophyll conductance to CO2: methodology, potential errors, and recommendations. J Exp Bot 60:2217–2234

    Article  CAS  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and chlorophyll b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Razal RA, Ellis S, Singh S, Lewis NG, Towers GHN (1996) Nitrogen recycling in pheylpropanoid metabolism. Phytochem 41:31–35

    Article  CAS  Google Scholar 

  • Sage RF (2013) Photorespiratory compensation: a driver for biological diversity. Plant Biol 15:624–638

    Article  CAS  Google Scholar 

  • Sakurai N, Hayakawa T, Nakamura T, Yamaya T (1996) Changes in the cellular localization of cytosolic glutamine synthetase protein in vascular bundles of rice leaves at various stages of development. Planta 200:306–311

    Article  CAS  Google Scholar 

  • Somerville CR, Ogren WL (1980) Inhibition of photosynthesis in Arabidopsis mutants lacking leaf glutamate synthase activity. Nature 286:257–259

    Article  CAS  Google Scholar 

  • Suárez MF, Avila C, Gallardo F, Cantón FR, García-Gutiérrez A, Claros MG, Cánovas FM (2002) Molecular and enzymatic analysis of ammonium assimilation in woody plants. J Exp Bot 53:891–904

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  Google Scholar 

  • Tsuchida H, Tamai T, Fukayama H, Agarie S, Nomura M, Onodera H, Ono K, Nishizawa Y, Lee B-H, Hirose S, Toki S, Ku MSB, Matsuoka M, Miyao M (2001) High level expression of C4-specific NADP-malic enzyme in leaves and impairment of photoautotrophic growth of a C3 plant, rice. Plant Cell Physiol 42:138–145

    Article  CAS  Google Scholar 

  • Veromann-Jürgenson L-L, Tosens T, Laanisto L, Niinemets Ü (2017) Extremely thick cell walls and low mesophyll conductance: welcome to the world of ancient living! J Exp Bot 68:1639–1653

    Article  Google Scholar 

  • Vézina L-P, Margolis HA, Ouimet R (1988) The activity, characterization and distribution of the nitrogen assimilation enzyme, glutamine synthetase, in jack pine seedlings. Tree Physiol 4:109–118

    Article  Google Scholar 

  • von Caemmerer S, Evans JR (1991) Determination of the average partial pressure of CO2 in chloroplasts from leaves of several C3 plants. Aust J Plant Physiol 18:287–305

    Google Scholar 

  • Wallsgrove RM, Turner JC, Hall NP, Kendall AC, Bright SWJ (1987) Barley mutants lacking chloroplast glutamine synthetase—biochemical and genetic analysis. Plant Physiol 83:155–158

    Article  CAS  Google Scholar 

  • Wang L, Xu Y, Schjoerring JK (2011) Seasonal variation in ammonia compensation point and nitrogen pools in beech leaves (Fagus sylvatica). Plant Soil 343:51–66

    Article  CAS  Google Scholar 

  • Wang L, Pedas P, Eriksson D, Schjoerring JK (2013) Elevated atmospheric CO2 decreases the ammonia compensation point of barley plants. J Exp Bot 64:2713–2724

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Dr. Mitsutoshi Kitao, Dr. Hiroyuki Tobita, and Dr. Satoru Takanashi in FFPRI for providing support for gas exchange measurements. We also thank Dr. Tokuko Ihara-Udino in FFPRI for her help searching the EST database, Dr. Tomohiro Igasaki and Ms. Ai Hagiwara in FFPRI for their help growing plant materials, and Dr. Eiichi Minami and Dr. Masao Iwamoto in National Agriculture and Food Research Organization (Tsukuba, Japan) for the use of HPLC. We used SAS software provided by AFFRIT, MAFF, Japan. This work was supported by JSPS KAKENHI Grant No. 16K07791 and Research grant #201705 of FFPRI. S-IM thanks anonymous reviewers for constructive comments on early drafts of the manuscript.

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Authors and Affiliations

  1. Department of Forest Molecular Genetics and Biotechnology, Forestry and Forest Products Research Institute (FFPRI), 1 Matsunosato, Tsukuba, 305-8687, Japan

    Shin-Ichi Miyazawa, Mitsuru Nishiguchi, Norihiro Futamura & Tsuyoshi Emilio Maruyama

  2. Tsukuba Botanical Garden, National Museum of Nature and Science, 4-1-1 Amakubo, Tsukuba, 305-0005, Japan

    Tomohisa Yukawa

  3. Graduate School of Agricultural Science, Tohoku University, Aoba, Sendai, 980-0845, Japan

    Mitsue Miyao

  4. Hokkaido Research Center, FFPRI, 7 Hitsujigaoka, Toyohira, Sapporo, Hokkaido, 062-8516, Japan

    Takayuki Kawahara

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  1. Shin-Ichi Miyazawa
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  2. Mitsuru Nishiguchi
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  3. Norihiro Futamura
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  4. Tomohisa Yukawa
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Correspondence to Shin-Ichi Miyazawa.

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Miyazawa, SI., Nishiguchi, M., Futamura, N. et al. Low assimilation efficiency of photorespiratory ammonia in conifer leaves. J Plant Res 131, 789–802 (2018). https://doi.org/10.1007/s10265-018-1049-2

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