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A pyrenoid-based carbon-concentrating mechanism is present in terrestrial bryophytes of the class Anthocerotae

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Abstract

It has been widely accepted that carbon assimilation in bryophytes is exclusively based on the conventional C3 photosynthetic pathway. The occurrence of biochemical CO2-concentrating mechanisms (C4 or Crassulacean acid metabolism), which have developed in plants in the last 20–100 million years, has been discounted for bryophytes from studies of the carbon isotope composition (δ13C) of organic material. In contrast cyanobacteria and many algae show active accumulation of dissolved inorganic carbon via biophysical CO2-concentrating mechanisms which are also found in the photobiont partners in certain lichens. The presence of a pyrenoid, a granular particle within the chloroplast, has been linked with CO2-concentrating mechanism activity in green algae and lichens and we now show that such a mechanism is categorically associated with the occurrence of a pyrenoid in bryophytes belonging to the class of Anthocerotae. These observations have significant evolutionary implications for the development of terrestrial photosynthesis during the colonisation of the land, raising the intriguing question of why the pyrenoid-based CO2-concentrating mechanism did not persist in the terrestrial environment.

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Abbreviations

CCM:

carbon-concentrating mechanism

DIG:

dissolved inorganic carbon (CO2+HCO -3 +CO -2 )

DW:

dry weight

K0.5 :

external concentration of CO2 at which half-maximal rates of CO2 assimilation are reached

Rubisco:

ribulose-l,5-bisphosphate carboxylase-oxygenase

Δ:

carbon isotope discrimination (%)

δ13C:

carbon isotope ratio (%)

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Authors and Affiliations

  1. Department of Agricultural and Environmental Science, University of Newcastle upon Tyne, NE1 7RU, Newcastle upon Tyne, UK

    Elizabeth C. Smith & Howard Griffiths

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  1. Elizabeth C. Smith
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  2. Howard Griffiths
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Correspondence to Howard Griffiths.

Additional information

This work was supported by the Natural Environment Research Council (GR3/8813) and the Leverhulme Trust. We thank Prof. A. Roy Perry (National Museum of Wales, Cardiff), Dr. B. Coppins and Mr. D. Long (Royal Botanic Garden Edinburgh) for access to herbarium specimens and Mr. M. Fletcher for providing living bryophytes.

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Smith, E.C., Griffiths, H. A pyrenoid-based carbon-concentrating mechanism is present in terrestrial bryophytes of the class Anthocerotae. Planta 200, 203–212 (1996). https://doi.org/10.1007/BF00208310

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  • DOI: https://doi.org/10.1007/BF00208310

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