A cyanobacterial photorespiratory bypass model to enhance photosynthesis by rerouting photorespiratory pathway in C3 plants

Abstract

Plants employ photosynthesis to produce sugars for supporting their growth. During photosynthesis, an enzyme Ribulose 1,5 bisphosphate carboxylase/oxygenase (Rubisco) combines its substrate Ribulose 1,5 bisphosphate (RuBP) with CO2 to produce phosphoglycerate (PGA). Alongside, Rubisco also takes up O2 and produce 2-phosphoglycolate (2-PG), a toxic compound broken down into PGA through photorespiration. Photorespiration is not only a resource-demanding process but also results in CO2 loss which affects photosynthetic efficiency in C3 plants. Here, we propose to circumvent photorespiration by adopting the cyanobacterial glycolate decarboxylation pathway into C3 plants. For that, we have integrated the cyanobacterial glycolate decarboxylation pathway into a kinetic model of C3 photosynthetic pathway to evaluate its impact on photosynthesis and photorespiration. Our results show that the cyanobacterial glycolate decarboxylation bypass model exhibits a 10% increase in net photosynthetic rate (A) in comparison with C3 model. Moreover, an increased supply of intercellular CO2 (Ci) from the bypass resulted in a 54.8% increase in PGA while reducing photorespiratory intermediates including glycolate (− 49%) and serine (− 32%). The bypass model, at default conditions, also elucidated a decline in phosphate-based metabolites including RuBP (− 61.3%). The C3 model at elevated level of inorganic phosphate (Pi), exhibited a significant change in RuBP (+ 355%) and PGA (− 98%) which is attributable to the low availability of Ci. Whereas, at elevated Pi, the bypass model exhibited an increase of 73.1% and 33.9% in PGA and RuBP, respectively. Therefore, we deduce a synergistic effect of elevation in CO2 and Pi pool on photosynthesis. We also evaluated the integrative action of CO2, Pi, and Rubisco carboxylation activity (Vcmax) on A and observed that their simultaneous increase raised A by 26%, in the bypass model. Taken together, the study potentiates engineering of cyanobacterial decarboxylation pathway in C3 plants to bypass photorespiration thereby increasing the overall efficiency of photosynthesis.

Here comes the sun: How optimization of photosynthetic light reactions can boost crop yields

“…In recent years, different strategies to improve crop yields have been proposed and reviewed, such as: (i) introducing photorespiratory bypasses (Betti et al, 2016; Hagemann and Bauwe, 2016; South et al, 2018; Eisenhut et al, 2019; López‐Calcagno et al, 2019; Maurino, 2019; Shen et al, 2019; Khurshid et al, 2020; Wang et al, 2020; Abbasi et al, 2021); (ii) introducing algal/cyanobacterial carbon concentrating mechanisms (McGrath and Long, 2014; Rae et al, 2017; Long et al, 2018; Atkinson et al, 2020; Hennacy and Jonikas, 2020; Chen et al, 2021; Rottet et al, 2021); (iii) introducing the C4 photosynthesis pathway into C3 plants (Ermakova et al, 2020, 2021a); (iv) improving mesophyll conductance (Hanba et al, 2004; Xu et al, 2019; Lundgren and Fleming, 2020; Ermakova et al, 2021c); (v) modifying metabolic processes (Rossi et al, 2015; South et al, 2019); and (vi) modifying circadian rhythms and introducing chronocultures (Steed et al, 2021). During the second half of the 20th century, the Green Revolution led to improved grain yields through conventional breeding techniques and improved pest/disease control.…”

Expression of cyanobacterial genes enhanced CO2 assimilation and biomass production in transgenic Arabidopsis thaliana

“…In addition to this, there is a need to examine the nutrient requirements of transgenic plants expressing partial or complete bypasses under ambient atmospheric CO 2 (C a ) levels as modifications in N availability or allocation could lead to an enhancement of A . In a kinetic bypass model study, we evaluated the effect of the complete glycolate decarboxylation pathway on A and reported increase in A at ambient C i concentrations, but in the A -Ci curve, the bypass model attained steady state even at 380 ppm and further increases in C i up to 950 ppm had no effect on A ( Khurshid et al, 2020 ). Furthermore, we identified that the higher C i requires more inorganic phosphate (Pi) to cause any further increase in A , which was shown in both the C 3 and bypass models ( Khurshid et al, 2020 ).…”

“…In a kinetic bypass model study, we evaluated the effect of the complete glycolate decarboxylation pathway on A and reported increase in A at ambient C i concentrations, but in the A -Ci curve, the bypass model attained steady state even at 380 ppm and further increases in C i up to 950 ppm had no effect on A ( Khurshid et al, 2020 ). Furthermore, we identified that the higher C i requires more inorganic phosphate (Pi) to cause any further increase in A , which was shown in both the C 3 and bypass models ( Khurshid et al, 2020 ).…”

Biosynthetic approaches to efficient assimilation of CO2via photorespiration modification in plant chassis

“…In addition to the implemented bypasses described above, there are some promising alternative bypasses that could be experimentally tested in plants. Such as similar to the third bypass in the chloroplast, glycolate is converted to two molecules of CO 2 completely ( Eisenhut et al, 2008 ; Claassens et al, 2020 ; Khurshid et al, 2020 ). In these bypasses, glycolate is first converted to formate with one molecule of CO 2 release by three or four enzymes and then formate oxidizes to CO 2 by formate dehydrogenase (FDH) ( Eisenhut et al, 2008 ; Claassens et al, 2020 ; Khurshid et al, 2020 ) ( Figure 2 , fonts marked by orange color).…”

“… The potentially achieved biosynthetic bypasses of photorespiration in plants. Two glycolate decarboxylation bypasses are marked by orange ( Eisenhut et al, 2008 ; Claassens et al, 2020 ; Khurshid et al, 2020 ). GDH, glycolate dehydrogenase; HDH, hydroxyacid dehydrogenase; ODC, oxalate decarboxylase; FDH, formate dehydrogenase; AGODH, CoA-acylating glyoxylate dehydrogenase; OXC, oxalyl-CoA decarboxylase; FRC, formyl-CoA transferase.…”