The underwater life of secondarily aquatic plants: Some problems and solutions

The freshwater secondarily aquatic plants, most of which are higher plants, are those returned to the water environment after spending a period of time living on land. The readaptation to living underwater has made it necessary for these plants to put in place morphological and functional strategies to cope with some major problems due to features of the aquatic environment, but also deriving from the specialized organization of their "terrestrial" bodies. The poor O-2 availability underwater accounted for the evolution of wide aerenchyma tissues throughout the plant organs to improve the photosynthetic O-2 flux from the shoot to the roots buried in anoxic sediments and to the neighboring rhizosphere. This favors sediment oxygenation, sustains the aerobic metabolism of roots, and improves the availability and uptake of mineral nutrients, whose delivery to the entire plants, without a transpirational flux, is ensured by an acropetal mass transport depending on root pressure, guttation from hydathodes and channeling by apoplast closure around the vascular tissues. A great expansion of leaf surfaces and an enhanced surface:volume ratio of chloroplast-rich photosynthetic cells help to contact the water medium and to increase the cell/environment exchanges to gain inorganic carbon. Furthermore, different physiological mechanisms operate to cope with the scarce availability of CO2 and the prevalence of HCO3- as inorganic carbon form in water. Some of them, like cell wall acidification through H extrusion by a light-dependent APFase or activation of an apoplastic carbonic anhydrase, operate outside the cells, leading to a conversion of HCO3- to CO2, which then diffuses into the cells. Others, on the contrary, act inside the cells to load the active site of Rubisco with CO2, thus favoring photosynthesis and lowering photorespiration. Aquatic macrophytes with isoetid life form, moreover, can obtain most of the fixed CO2 from sediments. In submerged species, in additin to the C-3 Cycle, the C-4 and CAM-like photosynthetic metabolisms can also operate, and are modulated by the environmental inorganic carbon availability and the plant photosynthetic demand. Interestingly, in the aquatic plants the C-4 pathway, which can be concomitant with the C-3 one, does not depend on the Kranz anatomy of leaves, but relies on the intracellular compartmentation of carboxylative and decarboxylative enzymes. The CAM-like pathway, defined AAM, which also coexists with the C-3, allows the submerged plants to fix CO2 in the dark, thus exploiting the higher CO2 availability in the water medium during the night, and extending to 24 h the period of inorganic carbon assimilation. In almost all the aquatic macrophytes the AAM is only expressed in the submersion state, whereas it is quickly inactivated in emerging leaves in a cell by cell way.