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Does Bienertia cycloptera with the single-cell system of C4 photosynthesis exhibit a seasonal pattern of δ13C values in nature similar to co-existing C4 Chenopodiaceae having the dual-cell (Kranz) system?

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Abstract

Family Chenopodiaceae is an intriguing lineage, having the largest number of C4 species among dicots, including a number of anatomical variants of Kranz anatomy and three single-cell C4 functioning species. In some previous studies, during the culture of Bienertia cycloptera Bunge ex Boiss., carbon isotope values (δ13C values) of leaves deviated from C4 to C3−C4 intermediate type, raising questions as to its mode of photosynthesis during growth in natural environments. This species usually co-occurs with several Kranz type C4 annuals. The development of B. cycloptera morphologically and δ13C values derived from plant samples (cotyledons, leaves, bracts, shoots) were analyzed over a complete growing season in a salt flat in north central Iran, along with eight Kranz type C4 species and one C3 species. For a number of species, plants were greenhouse-grown from seeds collected from the site, in order to examine leaf anatomy and C4 biochemical subtype. Among the nine C4 species, the cotyledons of B. cycloptera, and of the Suaeda spp. have the same respective forms of C4 anatomy occurring in leaves, while cotyledons of members of tribe Caroxyloneae lack Kranz anatomy, which is reflected in the δ13C values found in plants grown in the natural habitat. The nine C4 species had average seasonal δ13C values of −13.9‰ (with a range between species from −11.3 to −15.9‰). The measurements of δ13C values over a complete growing season show that B. cycloptera performs C4 photosynthesis during its life cycle in nature, similar to Kranz type species, with a seasonal average δ13C value of −15.2‰.

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Abbreviations

δ13C values:

Carbon isotope values

NAD-ME:

NAD-Malic enzyme

NADP-ME:

NADP-Malic enzyme

PEP-CK:

Phosphoenolpyruvate carboxykinase

PEPC:

Phosphoenolpyruvate carboxylase

PPFD:

Photosynthetic photon flux density

Rubisco:

Ribulose bisphosphate carboxylase-oxygenase

Ci/Ca ratio:

The relationship between the concentration of CO2 in the intercellular air space of the leaf and that in the atmosphere

ϕ:

Percentage leakage of CO2 following decarboxylation of C4 acids in the C4 cycle

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Acknowledgments

This material is based, in part, on work supported by the research project Geobotanical Studies in Different Parts of Iran (6104037/01), a grant from the Research Council, University of Tehran to H. Akhani for sabbatical study, and the National Science Foundation under Grant no. IBN−0641232 to G.E. A large part of the isotope analysis was kindly provided through the valuable assistance of Dr. C. Deigele and Dipl. Eng. P. Trimborn, GSF National Research Center for Environment and Health, Munich, Germany. M.V. Lara is a Researcher Career Member of the Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina. We acknowledge the Franceschi Imaging and Microscopy Center, Washington State University, for use of facilities and the advice of the staff for anatomical studies, C. Cody, for plant growth management, and Mr. M. Djamali for providing the map in Fig. 1.

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Authors and Affiliations

  1. Department of Plant Sciences, School of Biology, College of Science, University of Tehran, P.O. Box 14155-6455, Tehran, Iran

    Hossein Akhani & Maryam Ghasemkhani

  2. Centro de Estudios Fotosintéticos y Bioquímicos. Facultad de Ciencias Bioquímicas y Farmacéuticas, Suipacha 531, Rosario, 2000, Argentina

    María Valeria Lara

  3. Kommission für Ökologie der Bayerischen Akademie der Wissenschaften, Alfons-Goppel-Str. 11, 80539, Munich, Germany

    Hubert Ziegler

  4. School of Biological Sciences, Washington State University, Pullman, WA, 99164-4236, USA

    Gerald E. Edwards

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  1. Hossein Akhani
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  2. María Valeria Lara
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  3. Maryam Ghasemkhani
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  4. Hubert Ziegler
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Correspondence to Hossein Akhani or Gerald E. Edwards.

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Akhani, H., Lara, M.V., Ghasemkhani, M. et al. Does Bienertia cycloptera with the single-cell system of C4 photosynthesis exhibit a seasonal pattern of δ13C values in nature similar to co-existing C4 Chenopodiaceae having the dual-cell (Kranz) system?. Photosynth Res 99, 23–36 (2009). https://doi.org/10.1007/s11120-008-9376-0

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