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Effects of growth temperature and nitrogen nutrition on expression of C3–C4 intermediate traits in Chenopodium album

Abstract

Proto-Kranz plants represent an initial phase in the evolution from C3 to C3–C4 intermediate to C4 plants. The ecological and adaptive aspects of C3–C4 plants would provide an important clue to understand the evolution of C3–C4 plants. We investigated whether growth temperature and nitrogen (N) nutrition influence the expression of C3–C4 traits in Chenopodium album (proto-Kranz) in comparison with Chenopodium quinoa (C3). Plants were grown during 5 weeks at 20 or 30 °C under standard or low N supply levels (referred to as 20SN, 20LN, 30SN, and 30LN). Net photosynthetic rate and leaf N content were higher in 20SN and 30SN plants than in 20LN and 30LN plants of C. album but did not differ among growth conditions in C. quinoa. The CO2 compensation point (Γ) of C. album was lowest in 30LN plants (36 µmol mol–1), highest in 20SN plants (51 µmol mol–1), and intermediate in 20LN and 30SN plants, whereas Γ of C. quinoa did not differ among the growth conditions (51–52 µmol mol–1). The anatomical structure of leaves was not considerably affected by growth conditions in either species. However, ultrastructural observations in C. album showed that the number of mitochondria per mesophyll or bundle sheath (BS) cell was lower in 20LN and 30LN plants than in 20SN and 30SN plants. Immunohistochemical observations revealed that lower accumulation level of P-protein of glycine decarboxylase (GDC-P) in mesophyll mitochondria than in BS mitochondria is the major factor causing the decrease in Γ values in C. album plants grown under low N supply and high temperature. These results suggest that high growth temperature and low N supply lead to the expression of C3–C4 traits (the reduction of Γ) in the proto-Kranz plants of C. album through the regulation of GDC-P expression.

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Acknowledgements

We thank Akane Nagai, School of Agriculture, Kyushu University, for her valuable contribution in a preliminary study; Prof. Naoto Furuya, Faculty of Agriculture, Kyushu University, for the use of an electron microscope; and the NARO Genebank, Tsukuba, for the gift of quinoa seeds. This study was supported by a Japan Society for the Promotion of Science KAKENHI grant (JP15K14638) to O.U.

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OU conceived, and OU and JO designed the study. JO, YH, and TY conducted the experiments, and all authors analyzed the data. OU and JO wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Osamu Ueno.

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Oono, J., Hatakeyama, Y., Yabiku, T. et al. Effects of growth temperature and nitrogen nutrition on expression of C3–C4 intermediate traits in Chenopodium album. J Plant Res 135, 15–27 (2022). https://doi.org/10.1007/s10265-021-01346-9

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  • DOI: https://doi.org/10.1007/s10265-021-01346-9

Keywords

  • C3–C4 intermediate photosynthesis
  • Chenopodium album
  • CO2 compensation point
  • Glycine decarboxylase
  • Growth temperature
  • Nitrogen nutrition