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Biochemical and biophysical CO2 concentrating mechanisms in two species of freshwater macrophyte within the genus Ottelia (Hydrocharitaceae)

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Abstract

Two freshwater macrophytes, Ottelia alismoides and O. acuminata, were grown at low (mean 5 μmol L−1) and high (mean 400 μmol L−1) CO2 concentrations under natural conditions. The ratio of PEPC to RuBisCO activity was 1.8 in O. acuminata in both treatments. In O. alismoides, this ratio was 2.8 and 5.9 when grown at high and low CO2, respectively, as a result of a twofold increase in PEPC activity. The activity of PPDK was similar to, and changed with, PEPC (1.9-fold change). The activity of the decarboxylating NADP-malic enzyme (ME) was very low in both species, while NAD-ME activity was high and increased with PEPC activity in O. alismoides. These results suggest that O. alismoides might perform a type of C4 metabolism with NAD-ME decarboxylation, despite lacking Kranz anatomy. The C4-activity was still present at high CO2 suggesting that it could be constitutive. O. alismoides at low CO2 showed diel acidity variation of up to 34 μequiv g−1 FW indicating that it may also operate a form of crassulacean acid metabolism (CAM). pH-drift experiments showed that both species were able to use bicarbonate. In O. acuminata, the kinetics of carbon uptake were altered by CO2 growth conditions, unlike in O. alismoides. Thus, the two species appear to regulate their carbon concentrating mechanisms differently in response to changing CO2. O. alismoides is potentially using three different concentrating mechanisms. The Hydrocharitaceae have many species with evidence for C4, CAM or some other metabolism involving organic acids, and are worthy of further study.

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Abbreviations

AMP:

Adenosine monophosphate

ATP:

Adenosine triphosphate

Alk:

Alkalinity

CAM:

Crassulacean acid metabolism

CCM:

Carbon dioxide concentrating mechanism

DIC:

Dissolved inorganic carbon

DTT:

Dithiothreitol

FW:

Fresh weight

GAPDH:

Glyceraldehyde 3-phosphate dehydrogenase

LDH:

Lactate dehydrogenase

MDH:

Malate dehydrogenase

NAD(P)-ME:

NAD(P)-malic enzyme

OAA:

Oxaloacetate

PEP:

Phosphoenol pyruvate

PEPC:

PEP carboxylase

PEPCK:

PEP carboxykinase

PGK:

Phosphoglycerate kinase

PPDK:

Pyruvate phosphate dikinase

RuBisCO:

Ribulose 1,5-bisphosphate carboxylase–oxygenase

RuBP:

Ribulose 1,5-bisphosphate

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Acknowledgments

This research was partially supported by a Chinese Academy of Sciences Visiting Professorship for Senior International Scientists (2010T2S14, 2013T1S0021) and the National Scientific Foundation of China (30700083). Two anonymous referees helped us to improve the manuscript.

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Authors and Affiliations

  1. Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, 430074, China

    Yizhi Zhang, Liyan Yin & Hong-Sheng Jiang

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Yizhi Zhang & Hong-Sheng Jiang

  3. Hubei Key Laboratory of Wetland Evolution & Ecological Restoration, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, 430074, China

    Liyan Yin & Wei Li

  4. UMR 7281, BIP, CNRS, Aix Marseille Université-CNRS, 31 Chemin Joseph Aiguier, BP71, 13 402, Marseille Cedex 20, France

    Brigitte Gontero

  5. Lake Ecosystems Group, Centre for Ecology & Hydrology, Lancaster Environment Centre, Library Avenue, Lancaster, LA1 4AP, UK

    Stephen C. Maberly

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  1. Yizhi Zhang
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  2. Liyan Yin
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  3. Hong-Sheng Jiang
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Correspondence to Liyan Yin or Stephen C. Maberly.

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Zhang, Y., Yin, L., Jiang, HS. et al. Biochemical and biophysical CO2 concentrating mechanisms in two species of freshwater macrophyte within the genus Ottelia (Hydrocharitaceae). Photosynth Res 121, 285–297 (2014). https://doi.org/10.1007/s11120-013-9950-y

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