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Trade-offs and Synergies in the Structural and Functional Characteristics of Leaves Photosynthesizing in Aquatic Environments

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The Leaf: A Platform for Performing Photosynthesis

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 44))

Summary

Aquatic plants, comprising different divisions of embryophytes, derive from terrestrial ancestors. They have evolved to live in water, both fresh and salty, an environment that presents unique challenges and opportunities for photosynthesis and growth. These include, compared to air, a low water stress, a greater density, and attenuation of light, and a more variable supply of inorganic carbon, both in concentration and chemical species, but overall a lower carbon availability, and the opportunity to take up nutrients from the water. The leaves of many aquatic plants are linear, dissected, whorled, or cylindrical with a large volume of air spaces. They tend to have a high specific leaf area, thin cuticles, and usually lack functional stomata. Exploiting the availability of chemicals in their environment, freshwater macrophytes may incorporate silica in their cell wall, while seagrasses contain sulphated polysaccharides, similar to those of marine macroalgae; both groups have low lignin content. This altered cell wall composition produces plants that are more flexible and therefore more resistant to hydraulic forces (mechanical stress arising from water movement). Aquatic plants may have enhanced light harvesting complexes conferring shade adaptation, but also have mechanisms to cope with high light. Aquatic plants have evolved numerous strategies to overcome potential carbon-limitation in water. These include growing in micro-environments where CO2 is high, producing leaves and roots that exploit CO2 from the air or sediment and operating concentrating mechanisms that increase CO2 (CCM) around the primary carboxylating enzyme, ribulose-1,5-bisphosphate carboxylase-oxygenase. These comprise C4 metabolism, crassulacean acid metabolism, and the ability to exploit the often high concentrations of HCO3 −, and ~50% of freshwater macrophytes and ~85% of seagrasses have one or more CCM. Many of these adaptations involve trade-offs between conflicting constraints and opportunities while others represent ‘synergies’ that help to maximize the productivity of this important group of plants.

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Abbreviations

A:

air

Atm:

atmospheric

ATP:

adenosine-5′-triphosphate

CAM:

crassulacean acid metabolism

CCM:

CO2-concentrating mechanism

Chl:

chlorophyll

COP1:

E3 ubiquitin ligase constitutively photomorphogenic 1

Env:

environment

FW:

freshwater

HVME1:

Hydrilla verticillata malic enzyme isoform1

Ic :

incident light at which respiratory CO2 generation is balanced by photosynthetic CO2 fixation

Ik :

incident light at which photosynthetic CO2 fixation approaches saturation

LHCB1:

light-harvesting chlorophyll-binding complex 1 of photosystem II

ME:

malic enzyme

NAD:

nicotinamide adenine dinucleotide

NADP:

nicotinamide adenine dinucleotide phosphate

PEPC:

phosphoenolpyruvate carboxylase

PEPCK:

PEP carboxykinase

PGA:

phosphoglyceric acid

PPDK:

pyruvate phosphate dikinase

ROS:

reactive oxygen species

Rubisco:

ribulose-1,5-bisphosphate carboxylase-oxygenase

RuBP:

ribulose-1,5-bisphosphate

Sed:

sedimentary

UV:

ultraviolet radiation

UVR8:

UV-B photoreceptor UV resistance locus 8

W:

water

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Acknowledgments

We are extremely grateful to Marion Cambridge, Lukasz Kotula, Ole Pedersen, and Quing-Feng Wang for contributing photographs to Figs. 11.1 and 11.2, to Dina Ronzhina for giving permission to reproduce her drawings of leaf sections reproduced in Fig. 11.2 and to Hendrik Poorter for permission to reproduce Fig. 11.4. The Chinese Academy of Sciences is thanked for providing Visiting Professorships for Senior International Scientists and the President’s International Fellowship Initiative to the authors (2015VBA023, 2016VBA006). Stephen Maberly’s work is supported by the UK Natural Environment Research Council. Brigitte Gontero’s group is supported by Centre National de la Recherche Scientifique, Aix-Marseille Université, A*Midex project (No. ANR-11-IDEX-0001-02), Agence National de la Recherche (Signaux-BioNRJ, ANR-15-CE05-0021-03).

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Authors and Affiliations

  1. Lake Ecosystems Group, Centre for Ecology & Hydrology, Lancaster Environment Centre, Lancaster, UK

    Stephen Christopher Maberly

  2. Enzymology of Supramolecular Systems, Aix Marseille Univ, CNRS, BIP, Marseille, France

    Brigitte Gontero

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  1. Stephen Christopher Maberly
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  2. Brigitte Gontero
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Correspondence to Stephen Christopher Maberly .

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  1. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA

    William W. Adams III

  2. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Bunkyo Ku, Hongo, Tokyo, Japan

    Ichiro Terashima

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Maberly, S.C., Gontero, B. (2018). Trade-offs and Synergies in the Structural and Functional Characteristics of Leaves Photosynthesizing in Aquatic Environments. In: Adams III, W., Terashima, I. (eds) The Leaf: A Platform for Performing Photosynthesis. Advances in Photosynthesis and Respiration, vol 44. Springer, Cham. https://doi.org/10.1007/978-3-319-93594-2_11

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