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Coleataenia prionitis, a C4-like species in the Poaceae

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Abstract

C4-like plants represent the penultimate stage of evolution from C3 to C4 plants. Although Coleataenia prionitis (formerly Panicum prionitis) has been described as a C4 plant, its leaf anatomy and gas exchange traits suggest that it may be a C4-like plant. Here, we reexamined the leaf structure and biochemical and physiological traits of photosynthesis in this grass. The large vascular bundles were surrounded by two layers of bundle sheath (BS): a colorless outer BS and a chloroplast-rich inner BS. Small vascular bundles, which generally had a single BS layer with various vascular structures, also occurred throughout the mesophyll together with BS cells not associated with vascular tissue. The mesophyll cells did not show a radial arrangement typical of Kranz anatomy. These features suggest that the leaf anatomy of C. prionitis is on the evolutionary pathway to a complete C4 Kranz type. Phosphoenolpyruvate carboxylase (PEPC) and pyruvate, Pi dikinase occurred in the mesophyll and outer BS. Glycine decarboxylase was confined to the inner BS. Ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) accumulated in the mesophyll and both BSs. C. prionitis had biochemical traits of NADP-malic enzyme type, whereas its gas exchange traits were close to those of C4-like intermediate plants rather than C4 plants. A gas exchange study with a PEPC inhibitor suggested that Rubisco in the mesophyll could fix atmospheric CO2. These data demonstrate that C. prionitis is not a true C4 plant but should be considered as a C4-like plant.

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Abbreviations

A :

Net CO2 assimilation rate

BS:

Bundle sheath

CE:

Carboxylation efficiency

Chl:

Chlorophyll

C i :

Intercellular CO2 concentration

DCDP:

3,3-Dichloro-2-dihydroxyphosphinoylmethyl-2-propenoate

Г :

CO2 compensation point

GDC:

Glycine decarboxylase

GDC-P:

Glycine decarboxylase P protein

IVD:

Interveinal distance

LSU:

Large subunit

M/BS tissue area ratio:

Ratio of mesophyll area to BS area

NAD-ME:

NAD-malic enzyme

NADP-ME:

NADP-malic enzyme

PEPC:

Phosphoenolpyruvate carboxylase

PCK:

Phosphoenolpyruvate carboxykinase

PPDK:

Pyruvate, Pi dikinase

PPFD:

Photosynthetic photon flux density

PWUE:

Photosynthetic water use efficiency

Rubisco:

Ribulose 1,5-bisphosphate carboxylase/oxygenase

T r :

Transpiration rate

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Acknowledgements

We are grateful to Drs. S. Agarie and K. Saitou, Kyushu University, for their cooperation and valuable comments. We also thank Dr. C. Jenkins for supplying DCDP, Drs. S. Muto, D. Oliver and T. Sugiyama for supplying antisera, and the Plant Introduction Station, ARS, USDA and the NARO genebank for their gifts of seeds. This study was supported by the Japan Society for the Promotion of Science KAKENHI (Grant No. JP16H94868) to O.U.

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Authors and Affiliations

  1. Graduate School of Bioresources and Environmental Sciences, Kyushu University, Motooka, Fukuoka, 819-0395, Japan

    Maho Tashima & Takayuki Yabiku

  2. Faculty of Agriculture, Kyushu University, Motooka, Fukuoka, 819-0395, Japan

    Osamu Ueno

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  1. Maho Tashima
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  2. Takayuki Yabiku
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  3. Osamu Ueno
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Correspondence to Osamu Ueno.

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Figure S1. Gross morphology of Coleataenia prionitis.Supplementary file1 (TIF 8075 KB)

Figure S2. A cleared leaf of Coleataenia prionitis. Supplementary file2 (TIF 14001 KB)

11120_2020_808_MOESM3_ESM.tif

Figure S3. Immunohistochemical localization of enzymes in leaves of the control C4 plant, Sorghum bicolor. Supplementary file3 (TIF 16472 KB)

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Figure S4. Quantification of immunogold labelling of enzymes in leaves of Coleataenia prionitis. Supplementary file4 (TIF 3407 KB)

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Figure S5. Effects of concentrations of DCDP on PEPC activity in leaf extracts of Coleataenia prionitis. Supplementary file5 (TIF 1569 KB)

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Figure S6. Comparison of enzyme localization in leaves of C4-like and C4 grasses having a double chlorenchymatous bundle sheath. Supplementary file6 (TIF 5969 KB)

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Tashima, M., Yabiku, T. & Ueno, O. Coleataenia prionitis, a C4-like species in the Poaceae. Photosynth Res 147, 211–227 (2021). https://doi.org/10.1007/s11120-020-00808-w

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