Responses of Ottelia alismoides, an aquatic plant with three CCMs, to variable CO2 and light.

Hui Shao,Wen Min Huang,Brigitte Gontero,Hong Sheng Jiang,Yu Cao,Stephen C Maberly,Wei Li

doi:10.1093/jxb/erx064

Abstract

Ottelia alismoides is a constitutive C4 plant and bicarbonate user, and has facultative crassulacean acid metabolism (CAM) at low CO2. Acclimation to a factorial combination of light and CO2 showed that the ratio of phosphoenolpyruvate carboxylase (PEPC) to ribulose-bisphosphate carboxylase/oxygenase (Rubisco) (>5) is in the range of that of C4 plants. This and short-term response experiments showed that the activity of PEPC and pyruvate phosphate dikinase (PPDK) was high even at the end of the night, consistent with night-time acid accumulation and daytime carbon fixation. The diel acidity change was maximal at high light and low CO2 at 17-25 µequiv g-1 FW. Decarboxylation proceeded at ~2-3 µequiv g-1 FW h-1, starting at the beginning of the photoperiod, but did not occur at high CO2; the rate was greater at high, compared with low light. There was an inverse relationship between starch formation and acidity loss. Acidity changes account for up to 21% of starch production and stimulate early morning photosynthesis, but night-time accumulation of acid traps <6% of respiratory carbon release. Ottelia alismoides is the only known species to operate CAM and C4 in the same tissue, and one of only two known aquatic species to operate CAM and bicarbonate use.

Highlights

In terrestrial environments, some photoautotrophic plants have evolved carbon dioxide-concentrating mechanisms (CCMs), such as C4 and crassulacean acid metabolism (CAM), that allow them to maximize carbon uptake when temperature is high or water restricted, or both (Keeley and Rundel, 2003; Herrera, 2009; Silvera et al, 2010; Sage et al, 2012)
Starch content was lowest at the end of the night and increased during the day, and on average was statistically highest in the high light and high CO2 (HLHC) plants and statistically lowest in the low light and low CO2 (LLLC) plants (Fig. 1B; Supplementary Table S1)
At high light and low CO2 (HLLC), phosphoenolpyruvate carboxylase (PEPC) activity declined during the day but the PEPC:ribulose-bisphosphate carboxylase/oxygenase (Rubisco) ratio was between 1.2 and 2.6, in agreement with a previous report and in a range typical of terrestrial C4 plants (Zhang et al, 2014)

Summary

Introduction

Some photoautotrophic plants have evolved carbon dioxide-concentrating mechanisms (CCMs), such as C4 and crassulacean acid metabolism (CAM), that allow them to maximize carbon uptake when temperature is high or water restricted, or both (Keeley and Rundel, 2003; Herrera, 2009; Silvera et al, 2010; Sage et al, 2012). Physiological or biochemical strategies involve CCMs because they increase the concentration of CO2 around the active site of ribulose-bisphosphate carboxylase/oxygenase (Rubisco) (Bowes and Salvucci, 1989; Maberly and Madsen, 2002; Raven et al, 2008). The two biochemical CCMs in terrestrial plants, C4 and CAM, are found in freshwater plants Both depend on carbon fixation via the enzyme phosphoenolpyruvate carboxylase (PEPC) that is active during either the day (C4) or the night (CAM) (Keeley, 1981; Bowes and Salvucci, 1989; Bowes et al, 2002; Keeley and Rundel, 2003)

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