Abstract
Photosynthesis-related pathways are regarded as a promising avenue for crop improvement. Whilst empirical studies have shown that photosynthetic efficiency is higher in microalgae than in C3 or C4 crops, the underlying reasons remain unclear. Using a tailor-made microfluidics labelling system to supply 13CO2 at steady state, we investigated in vivo labelling kinetics in intermediates of the Calvin Benson cycle and sugar, starch, organic acid and amino acid synthesis pathways, and in protein and lipids, in Chlamydomonas reinhardtii, Chlorella sorokiniana and Chlorella ohadii, which is the fastest growing green alga on record. We estimated flux patterns in these algae and compared them with published and new data from C3 and C4 plants. Our analyses identify distinct flux patterns supporting faster growth in photosynthetic cells, with some of the algae exhibiting faster ribulose 1,5-bisphosphate regeneration and increased fluxes through the lower glycolysis and anaplerotic pathways towards the tricarboxylic acid cycle, amino acid synthesis and lipid synthesis than in higher plants.
Highlights
An increase in agricultural yield of 70% or more is required by 2050 to meet the growing demand of the world population[1,2]
In addition to carboxylation[13], RuBisCO catalyses a side-reaction with O2 that leads to formation of 2-phosphoglycolic acid (2PG), which is recycled via glycine, serine and glycerate to regenerate 3-phosphoglyceric acid (3PGA), with concomitant loss of CO2 and ammonium[14]
Since many intermediates in photosynthetic metabolism have turnover times of a few seconds or less, we developed a pipeline built around a microfluidic system that allows precise short pulses and rapid quenching in ambient conditions (Fig. 1, Extended Data Fig. 1 and Supplementary text)
Summary
An increase in agricultural yield of 70% or more is required by 2050 to meet the growing demand of the world population[1,2]. Modern agriculture has witnessed an ~160% increase in global production since the 1950s. This gain was achieved without expanding cropland, by extensive use of fertilizer and plant protection agents as well as improved crop varieties. Measured efficiencies reach ~3.5% and ~4.3% for C3 and C4 plants, respectively, and 5–7% for microalgae, emphasizing the potential of microalgae as a resource for yield improvement[12]. Many factors reduce photosynthetic efficiency, including photochemical limitations and the bifunctionality of ribulose-1,5-bisphosphate carboxylase-oxygenase (RuBisCO). Several mechanisms have evolved to increase CO2 concentration around RuBisCO and decrease the rates of the side-reaction with O2. Little work has addressed photosynthesis-associated metabolism and downstream reactions (often-termed photosynthate investment) as a route to improve yield
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