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The effects of salinity on photosynthesis and growth of the single-cell C4 species Bienertia sinuspersici (Chenopodiaceae)

Abstract

Recent research on the photosynthetic mechanisms of plant species in the Chenopodiaceae family revealed that three species, including Bienertia sinuspersici, can carry out C4 photosynthesis within individual photosynthetic cells, through the development of two cytoplasmic domains having dimorphic chloroplasts. These unusual single-cell C4 species grow in semi-arid saline conditions and have semi-terete succulent leaves. The effects of salinity on growth and photosynthesis of B. sinuspersici were studied. The results show that NaCl is not required for development of the single-cell C4 system. There is a large enhancement of growth in culture with 50–200 mM NaCl, while there is severe inhibition at 400 mM NaCl. With increasing salinity, the carbon isotope values (δ13C) of leaves increased from −17.3o/oo (C4-like) without NaCl to −14.6o/oo (C4) with 200 mM NaCl, possibly due to increased capture of CO2 from the C4 cycle by Rubisco and reduced leakiness. Compared to growth without NaCl, leaves of plants grown under saline conditions were much larger (~2 fold) and more succulent, and the leaf solute levels increased up to ~2000 mmol kg solvent−1. Photosynthesis on an incident leaf area basis (CO2 saturated rates, and carboxylation efficiency under limiting CO2) and stomatal conductance declined with increasing salinity. On a leaf area basis, there was some decline in Rubisco content with increasing salinity up to 200 mM NaCl, but there was a marked increase in the levels of pyruvate, Pi dikinase, and phosphoenolpyruvate carboxylase (possibly in response to sensitivity of these enzymes and C4 cycle function to increasing salinity). The decline in photosynthesis on a leaf area basis was compensated for on a per leaf basis, up to 200 mM NaCl, by the increase in leaf size. The influence of salinity on plant development and the C4 system in Bienertia is discussed.

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Abbreviations

A :

CO2 assimilation

A max :

Maximum photosynthetic rate under saturating CO2

C a :

Atmospheric CO2

CCC:

Central cytoplasmic compartment

CE:

Maximum carboxylation efficiency

C i :

Intercellular CO2

δ13C:

Carbon isotope discrimination value

DW:

Dry weight(s)

FW:

Fresh weight(s)

Γ :

CO2 compensation point

g s :

Stomatal conductance

IWUE:

Intrinsic water use efficiency

NAD-ME:

NAD-malic enzyme

PC:

Peripheral cytoplasmic domain

PEPC:

Phosphoenolpyruvate carboxylase

PPDK:

Pyruvate, Pi dikinase

Rubisco:

Ribulose bisphosphate carboxylase-oxygenase

Rubisco LSU:

Rubisco large subunit

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Acknowledgments

This material is based upon work supported by the National Science Foundation under Grants IBN-0236959 and IBN-0641232. Seeds of Bienertia sinuspersici were kindly provided by Dr. Abdulrahman Alsirhan, Kuwait. We appreciate the advice of M.A. Evans on statistical analyses. We thank the Franceschi Microscopy and Imaging Center of Washington State University for use of facilities and for staff assistance, C. Cody for plant growth management, and E. Voznesenskaya, N. Koteyeva, and O. Kiirats for helpful discussions during the research phase.

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Correspondence to Gerald E. Edwards.

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Leisner, C.P., Cousins, A.B., Offermann, S. et al. The effects of salinity on photosynthesis and growth of the single-cell C4 species Bienertia sinuspersici (Chenopodiaceae). Photosynth Res 106, 201–214 (2010). https://doi.org/10.1007/s11120-010-9595-z

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Keywords

  • Bienertia sinuspersici
  • C4 photosynthesis
  • Chenopodiaceae
  • Salinity tolerance
  • Single-cell C4