Low assimilation efficiency of photorespiratory ammonia in conifer leaves

  • Shin-Ichi Miyazawa
  • Mitsuru Nishiguchi
  • Norihiro Futamura
  • Tomohisa Yukawa
  • Mitsue Miyao
  • Tsuyoshi Emilio Maruyama
  • Takayuki Kawahara
Regular Paper
  • 47 Downloads

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.

Keywords

Ammonia Angiosperm Chloroplastic glutamine synthetase (GS2) Conifer NH3 compensation point Photorespiration 

Notes

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.

Supplementary material

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Copyright information

© The Botanical Society of Japan and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Shin-Ichi Miyazawa
    • 1
  • Mitsuru Nishiguchi
    • 1
  • Norihiro Futamura
    • 1
  • Tomohisa Yukawa
    • 2
  • Mitsue Miyao
    • 3
  • Tsuyoshi Emilio Maruyama
    • 1
  • Takayuki Kawahara
    • 4
  1. 1.Department of Forest Molecular Genetics and BiotechnologyForestry and Forest Products Research Institute (FFPRI)TsukubaJapan
  2. 2.Tsukuba Botanical Garden, National Museum of Nature and ScienceTsukubaJapan
  3. 3.Graduate School of Agricultural ScienceTohoku UniversitySendaiJapan
  4. 4.Hokkaido Research Center, FFPRISapporoJapan

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