Atmospheric CO2 captured by biogenic polyamines is transferred as a possible substrate to Rubisco for the carboxylation reaction

Abstract

Biogenic polyamines are involved in a wide range of plant cellular processes, including cell division, morphogenesis and stress responses. However, the exact roles of biogenic polyamines are not well understood. We recently reported that biogenic polyamines that have multiple amino groups can react with CO2 and accelerate calcium carbonate formation in seawater. The ability of biogenic polyamines to capture atmospheric CO2 prompted us to examine their roles in photosynthesis. Here, we demonstrated that atmospheric CO2 captured by biogenic polyamines is a candidate substrate for the carboxylation reaction of ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco), which is an enzyme involved in the first major step of carbon fixation during photosynthesis, and that biogenic polyamines can accelerate the carboxylation reaction of this enzyme because of their specific affinity for CO2. Moreover, the results of our nuclear magnetic resonance (NMR) analysis showed that putrescine, which is the most common biogenic polyamine, reacts with atmospheric CO2 and promotes the formation of carbamate derivatives and bicarbonate in aqueous environments. A sufficient amount of CO2 is well known to be produced by carbonic anhydrase from bicarbonate in vivo. The present study indicates that CO2 would be also produced by the equilibrium reaction from carbonate produced by biogenic polyamines and would be used as a substrate of Rubisco, too. Our results may suggest a new photosynthetic research strategy that involves CO2-concentrating mechanisms and also possibly constitutes a potential tool for reducing atmospheric CO2 levels and, consequently, global warming.

Chitosan-Modified Polyethyleneimine Nanoparticles for Enhancing the Carboxylation Reaction and Plants’ CO2Uptake

“…We hypothesize that PEI-Chi will increase the hydrogen bicarbonate concentration and consequently the amount of CO 2 available for RuBisCO. The ability of RuBisCO to use the CO 2 delivered by PEI-Chi as substrate for the synthesis of 3-PGA in vitro was evaluated with an enzymatic assay adapting the method previously described by Yasumoto et al . We evaluated the activity of RuBisCO in five different aqueous solutions: gPEI-Chi in water (1 mg/mL) bubbled with N 2 ( gPEI-Chi-N 2 ) or CO 2 ( gPEI-Chi-CO 2 ), deionized water (DIw) bubbled with N 2 ( DIw-N 2 ), or CO 2 ( DIw-CO 2 ) as negative controls, and 2 mM NaHCO 3 as positive control.…”

“…The enzymatic assays for determining the activity of RuBisCO were realized following the method described by Yasumoto et al . 37 The chemicals were purchased from Sigma-Aldrich (St. Louis, MO, USA).…”

“…PEI’s high positive charge condensates negatively charged polynucleotides and, at the same time, protects them from degradation, thus improving transfection efficiency. Yasumoto et al demonstrated that small biogenic polyamines, such as piperazine and putrescine, can capture atmospheric CO 2 which can then be used as a substrate for the carboxylation reaction . However, they have not studied their introduction to plants or their phytotoxicity.…”

“…Yasumoto et al demonstrated that small biogenic polyamines, such as piperazine and putrescine, can capture atmospheric CO 2 which can then be used as a substrate for the carboxylation reaction. 37 However, they have not studied their introduction to plants or their phytotoxicity. Other polyamines, such as PEI, can be highly toxic to plants depending on their molecular structure and concentration used.…”

Phenolic acids inhibit the photosynthetic productivity of poplar

“…Nonstomatal factors cause photosynthesis to decrease because of a decrease in the photosynthetic activity of mesophyll cells. Rubisco acts as a rate-limiting enzyme of photosynthesis and plays a decisive role in the plant photosynthetic rate (Yasumoto et al 2018). The leaf photosynthetic rate is closely related to Rubisco activity (Bernacchi et al 2003), and the degradation rate of Rubisco in leaves is significantly accelerated when plants are stressed (Li et al 2016), which affects the normal photosynthesis process.…”