Journal of Plant Research

, Volume 132, Issue 6, pp 839–855 | Cite as

Transition from C3 to proto-Kranz to C3–C4 intermediate type in the genus Chenopodium (Chenopodiaceae)

  • Yuki Yorimitsu
  • Aya Kadosono
  • Yuto Hatakeyama
  • Takayuki Yabiku
  • Osamu UenoEmail author
Regular Paper


The Chenopodiaceae is one of the families including C4 species among eudicots. In this family, the genus Chenopodium is considered to include only C3 species. However, we report here a transition from C3 photosynthesis to proto-Kranz to C3–C4 intermediate type in Chenopodium. We investigated leaf anatomical and photosynthetic traits of 15 species, of which 8 species showed non-Kranz anatomy and a CO2 compensation point (Γ) typical of C3 plants. However, 5 species showed proto-Kranz anatomy and a C3-like Γ, whereas C. strictum showed leaf anatomy and a Γ typical of C3–C4 intermediates. Chenopodium album accessions examined included both proto-Kranz and C3–C4 intermediate types, depending on locality. Glycine decarboxylase, a key photorespiratory enzyme that is involved in the decarboxylation of glycine, was located predominantly in the mesophyll (M) cells of C3 species, in both M and bundle-sheath (BS) cells in proto-Kranz species, and exclusively in BS cells in C3–C4 intermediate species. The M/BS tissue area ratio, number of chloroplasts and mitochondria per BS cell, distribution of these organelles to the centripetal region of BS cells, the degree of inner positioning (vacuolar side of chloroplasts) of mitochondria in M cells, and the size of BS mitochondria also changed with the change in glycine decarboxylase localization. All Chenopodium species examined were C3-like regarding activities and amounts of C3 and C4 photosynthetic enzymes and δ13C values, suggesting that these species perform photosynthesis without contribution of the C4 cycle. This study demonstrates that Chenopodium is not a C3 genus and is valuable for studying evolution of C3–C4 intermediates.


C3–C4 intermediate plant Chenopodium CO2 compensation point Glycine decarboxylase Leaf anatomy Proto-Kranz plant 



We thank the Plant Introduction Station, ARS, USDA and the NARO Genebank, Tsukuba for their gifts of seeds and Prof. N. Furuya, Faculty of Agriculture, Kyushu University, for the use of an electron microscope. This study was supported by Japan Society for the Promotion of Science KAKENHI (Grant No. JP15K14638) to O.U.

Supplementary material

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Supplementary material 1 (PDF 4276 kb)


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Copyright information

© The Botanical Society of Japan and Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  • Yuki Yorimitsu
    • 1
  • Aya Kadosono
    • 2
  • Yuto Hatakeyama
    • 1
  • Takayuki Yabiku
    • 1
  • Osamu Ueno
    • 1
    • 2
    • 3
    Email author
  1. 1.Graduate School of Bioresource and Bioenvironmental SciencesKyushu UniversityFukuokaJapan
  2. 2.School of AgricultureKyushu UniversityFukuokaJapan
  3. 3.Faculty of AgricultureKyushu UniversityFukuokaJapan

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