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Ole Pedersen, Jack of all trades – C4 photosynthesis, CAM and HCO3− use in the same tissue. A commentary on: ‘Structural basis for C4 photosynthesis without Kranz anatomy in leaves of the submerged freshwater plant Ottelia alismoides’, Annals of Botany, Volume 125, Issue 6, 8 May 2020, Pages iv–vi, https://doi.org/10.1093/aob/mcaa034
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Rates of underwater photosynthesis by submerged aquatic plants are often limited by CO2 availability. In the water within dense plant stands (Fig. 1), CO2 is depleted during the day but respiratory CO2 accumulates during the night with dissolved O2 following the opposite pattern. These diurnal fluctuations are all caused by the restricted exchange of gases with the atmosphere above due to slow diffusion; in water, molecular diffusion of CO2 is 104-fold slower than in air. Moreover, the slow diffusion under water also exacerbates the effects of diffusive boundary layers forming a major component of resistance to gas exchange with the surrounding water. Consequently, submerged aquatic plants are under strong selection pressure to develop CO2-concentrating mechanisms (CCMs). In the study by Han et al. (2020) in this issue of Annals of Botany, the authors have addressed this issue and demonstrated that there is sufficient structural diversity within the leaf of the submerged freshwater plant Ottelia alismoides to support dual-cell C4 photosynthesis in the absence of Kranz anatomy, the classic C4 cell compartmentation.
Indeed, three different types of CCM operate in submerged aquatic plants: (1) C4 photosynthesis, (2) Crassulacean acid metabolism (CAM) and (3) bicarbonate-use (HCO3−-use) but the case of Ottelia alismoides is the only known example in which all three CCMs operate in the same individual plant (Zhang et al., 2014). In terrestrial plants, the two known CCMs (C4 and CAM photosynthesis) are both linked to climatic factors (i.e. high temperature and/or arid conditions). In contrast, it was recently shown that HCO3−-use in submerged freshwater plants is globally controlled by catchment properties and not by temperature (Iversen et al., 2019); HCO3−-use is more prevalent in lakes situated in landscapes with soils rich in carbonates. As the carbonate minerals in the soils slowly weather, HCO3− is formed and carried to lakes via the groundwater where it serves as an alternative source of inorganic carbon for plants possessing the trait of HCO3−-use. The ability to tap into this source of inorganic carbon becomes a competitive advantage when dissolved CO2 is depleted during periods of extensive photosynthesis. HCO3−-use is the most widespread of the three CCMs in aquatic angiosperms, with about half of all diagnosed species possessing this trait. Ottelia alismoides constitutively expresses HCO3−-use but the carbon extraction capacity is greater in mature leaves compared to juvenile leaves (Huang et al., 2018). Cultivated under conditions of low CO2 availability, the carbon extraction capacity, mainly driven by HCO3−-use, is of similar magnitude to that of other fast-growing submerged aquatic plants such as species of Myriophyllum and Elodea.
Also, CAM photosynthesis is present in some submerged aquatic freshwater plants. This trait is clearly not related to water conservation, which is the case for terrestrial CAM plants that primarily occupy arid habitats. Aquatic CAM photosynthesis instead serves to tap into the high nocturnal CO2 availability resulting from respiratory CO2 that accumulates due to the slow gas diffusion in water. In fact, CAM photosynthesis may first have evolved in aquatic Lycopodiopsida (Raven et al., 2008) and it is currently known from aquatic representatives in the families Isoetaceae, Plantaginaceae, Crassulaceae and Hydrocharitaceae. Interestingly, CAM photosynthesis and HCO3−-use rarely occur side-by-side because HCO3−-use is commonly found in plants occupying habitats of high alkalinity (hard water) whereas CAM photosynthesis is more common in acidic waters (soft water). Nocturnal fixation of CO2 results in a great competitive advantage during the daytime when CO2 is depleted in dense plant stands and in some situations CAM can account for up to two-thirds of the daily carbon fixation. The CAM activity reported in O. alismoides, although clearly present, is however at the low end with diel fluctuations in tissue acidity of 25–58 µmol H+ equivalents g−1 f. wt (Shao et al., 2017; Han et al., 2020), which is only 10–20 % of that seen in some species of Isoetes. Nevertheless, the fact that it operates side-by-side with HCO3−-use is an exciting discovery that will surely spur new interest in the topics of HCO3−-use and CAM photosynthesis in submerged aquatic plants.
As a true jack of all trades, O. alismoides also possesses C4 photosynthesis (Zhang et al., 2014). C4 photosynthesis is usually linked to Kranz anatomy leading to spatial separation of the photosynthetic light and dark processes. High CO2 and low O2 around Rubisco greatly reduce photorespiration and consequently C4 photosynthesis is particularly beneficial at high temperatures. However, in the absence of Kranz anatomy, C4 photosynthesis can also occur in a single cell, a feature that was first discovered in the aquatic plant Hydrilla verticillata. There are some other species that also show this phenomenon, such as the terrestrial halophyte Suaeda aralocaspica (Voznesenskaya et al., 2001). Suaeda aralocaspica has dimorphic chloroplasts with most of its Rubisco and decarboxylating enzymes located in proximal chloroplasts whereas pyruvate and Pi dikinase are located in the more distally positioned chloroplasts. In this way, the photosynthetic light and dark processes are also spatially separated although at the cell level and at a smaller spatial scale than in the case of actual Kranz anatomy. Biochemically, CAM and C4 photosynthesis share most of the essential enzymes, so it is perhaps not surprising that O. alismoides possesses both CCMs.
In the study by Han et al. (2020), the authors present compelling evidence of dual-cell C4 photosynthesis, but in the absence of Kranz anatomy. C4 photosynthesis is constitutively expressed in O. alismoides but it seems to operate at higher activities when external CO2 availability is low. In such conditions, chloroplasts in the epidermal cells are spindle-shaped and only accumulate low amounts of starch, whereas mesophyll chloroplasts are spherical and accumulate substantial amounts of starch. Based on these observations, Han et al. (2020) conclude that CO2 fixation into C4 compounds takes place primarily in the epidermal cells whereas decarboxylation and fixation into sugars occur mainly in the mesophyll cells. Such dual-cell C4 photosynthesis is an exciting intermediate of the widespread C4 photosynthesis based on Kranz anatomy and the single-cell C4 photosynthesis observed in some aquatic plants and in the terrestrial halophyte S. aralocaspica.
The recent development of a novel CO2 microsensor revealed new insight into tissue CO2 dynamics of the aquatic CAM plant Littorella uniflora with high temporal resolution (Pedersen et al., 2018). Similar measurements in O. alismoides could be used to benchmark the CAM activity under various environmental conditions. More importantly, direct tissue measurements of CO2 concentrations could help to test the hypothesis presented by Han et al. (2020) that CO2 fixation into C4 compounds takes place in primarily the epidermal cells; this should lead to low tissue CO2 concentrations. Moreover, the authors suggest that decarboxylation takes place primarily in the mesophyll cells, which should result in a high tissue concentration of CO2. Such direct CO2 measurements in combination with immunolabelling of key enzymes in the chloroplast of epidermal and mesophyll cells could provide convincing evidence of spatial separation of the photosynthetic light and dark processes and thus dual-cell C4 photosynthesis in the absence of Kranz anatomy.
The fact that O. alismoides sometimes possesses all three known CCMs makes it an exciting model plant. C4 photosynthesis and HCO3−-use are constitutively expressed whereas CAM is induced during periods of low external CO2 availability. All three CCMs involve additional use of energy and production of particular enzymes compared to the typical C3 photosynthesis. Thus, O. alismoides as a model plant presents a unique opportunity to substantially progress our understanding of the pros and cons involved in the three CCMs and to describe environmental conditions under which these CCMs are fine-tuned to enable optimal resource allocation in a natural situation where CO2, O2, light and temperature all fluctuate diurnally. Unfortunately, the genome of O. alismoides is not yet known, which greatly restricts the type of molecular work that can be done on this species. However, the fact that dual-cell C4 photosynthesis, in addition to Kranz-based and single-cell C4 photosynthesis, is now described will possibly spark new hope and research efforts into further developing a C4 rice (von Caemmerer et al., 2012), with great implications for food production.
ACKNOWLEDGEMENTS
The constructive suggestions by Gustavo Striker are greatly appreciated. O.P. was supported by the Independent Research Fund Denmark grant No. 8021-00120B.