Dataset Information

Structural basis for C4 photosynthesis without Kranz anatomy in leaves of the submerged freshwater plant Ottelia alismoides.

ABSTRACT:

Background and aims

Ottelia alismoides (Hydrocharitaceae) is a freshwater macrophyte that, unusually, possesses three different CO2-concentrating mechanisms. Here we describe its leaf anatomy and chloroplast ultrastructure, how these are altered by CO2 concentration and how they may underlie C4 photosynthesis.

Methods

Light and transmission electron microscopy were used to study the anatomy of mature leaves of O. alismoides grown at high and low CO2 concentrations. Diel acid change and the activity of phosphoenolpyruvate carboxylase were measured to confirm that CAM activity and C4 photosynthesis were present.

Key results

When O. alismoides was grown at low CO2, the leaves performed both C4 and CAM photosynthesis whereas at high CO2 leaves used C4 photosynthesis. The leaf comprised an upper and lower layer of epidermal cells separated by a large air space occupying about 22 % of the leaf transverse-section area, and by mesophyll cells connecting the two epidermal layers. Kranz anatomy was absent. At low CO2, chloroplasts in the mesophyll cells were filled with starch even at the start of the photoperiod, while epidermal chloroplasts contained small starch grains. The number of chloroplasts in the epidermis was greater than in the mesophyll cells. At high CO2, the structure was unchanged but the thicknesses of the two epidermal layers, the air space, mesophyll and the transverse-section area of cells and air space were greater.

Conclusions

Leaves of O. alismoides have epidermal and mesophyll cells that contain chloroplasts and large air spaces but lack Kranz anatomy. The high starch content of mesophyll cells suggests they may benefit from an internal source of CO2, for example via C4 metabolism, and are also sites of starch storage. The air spaces may help in the recycling of decarboxylated or respired CO2. The structural similarity of leaves at low and high CO2 is consistent with the constitutive nature of bicarbonate and C4 photosynthesis. There is sufficient structural diversity within the leaf of O. alismoides to support dual-cell C4 photosynthesis even though Kranz anatomy is absent.

SUBMITTER: Han S

PROVIDER: S-EPMC7218808 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Carbon and nitrogen metabolism are basic, but pivotal metabolic pathways in plants and are tightly coupled. Maintaining the balance of carbon and nitrogen metabolism is critical for plant survival. Comprehensively revealing the metabolic balance of carbon-nitrogen interactions is important and helpful for understanding the adaptation of freshwater plants to CO2 limited aqueous environment. A comprehensive metabolomics analysis combined with physiological measurement was performed in the freshwater plant Ottelia alismoides acclimated to high and low CO2, respectively, for a better understanding of how the carbon and nitrogen metabolic adjustment in freshwater plants respond to carbon limitation. The present results showed that low CO2 acclimated O. alismoides exhibited significant diurnal titratable acidity and malate fluctuations, as well as an opposite diel pattern of starch change and high enzymatic activities required for crassulacean acid metabolism (CAM) photosynthesis, which indicates that CAM was induced under low CO2. Moreover, the metabolomic analysis showed that most intermediates of glycolysis, pentose phosphate pathway (PPP) and tricarboxylic acid (TCA) cycle, were increased under low CO2, indicative of active respiration in low-CO2-treated O. alismoides. Meanwhile, the majority of amino acids involved in pathways of glutamate and arginine metabolism, aspartate metabolism, and the branched-chain amino acids (BCAAs) metabolism were significantly increased under low CO2. Notably, γ-aminobutyric acid (GABA) level was significantly higher in low CO2 conditions, indicating a typical response with GABA shunt compensated for energy deprivation at low CO2. Taken together, we conclude that in low-CO2-stressed O. alismoides, CAM photosynthesis was induced, leading to higher carbon and nitrogen as well as energy requirements. Correspondingly, the respiration was greatly fueled via numerous starch degradation to ensure CO2 fixation in dark, while accompanied by linked promoted N metabolism, presumably to produce energy and alternative carbon sources and nitrogenous substances for supporting the operation of CAM and enhancing tolerance for carbon limitation. This study not only helps to elucidate the regulating interaction between C and N metabolism to adapt to different CO2 but also provides novel insights into the effects of CO2 variation on the metabolic profiling of O. alismoides.