Metabolite profiles reveal interspecific variation in operation of the Calvin-Benson cycle in both C4 and C3 plants.

Stéphanie Arrivault,Thiago Alexandre Moraes,Manuela Guenther,Gian Luca Borghi,Mark Stitt,Toshihiro Obata,Martha Ludwig,Alix Boulouis,David B Medeiros,John E Lunn,Alisdair R Fernie,Armin Schlereth

doi:10.1093/jxb/erz051

Stéphanie Arrivault, Thiago Alexandre Moraes + Show 10 more

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https://doi.org/10.1093/jxb/erz051

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Abstract

Low atmospheric CO2 in recent geological time led to the evolution of carbon-concentrating mechanisms (CCMs) such as C4 photosynthesis in >65 terrestrial plant lineages. We know little about the impact of low CO2 on the Calvin-Benson cycle (CBC) in C3 species that did not evolve CCMs, representing >90% of terrestrial plant species. Metabolite profiling provides a top-down strategy to investigate the operational balance in a pathway. We profiled CBC intermediates in a panel of C4 (Zea mays, Setaria viridis, Flaveria bidentis, and F. trinervia) and C3 species (Oryza sativa, Triticium aestivum, Arabidopsis thaliana, Nicotiana tabacum, and Manihot esculenta). Principal component analysis revealed differences between C4 and C3 species that were driven by many metabolites, including lower ribulose 1,5-bisphosphate in C4 species. Strikingly, there was also considerable variation between C3 species. This was partly due to different chlorophyll and protein contents, but mainly to differences in relative levels of metabolites. Correlation analysis indicated that one contributory factor was the balance between fructose-1,6-bisphosphatase, sedoheptulose-1,7-bisphosphatase, phosphoribulokinase, and Rubisco. Our results point to the CBC having experienced different evolutionary trajectories in C3 species since the ancestors of modern plant lineages diverged. They underline the need to understand CBC operation in a wide range of species.

Highlights

IntroductionThe Calvin–Benson cycle (CBC) evolved ~2 billion years 1979; Raven, 2013), and plays a dominant role in the global ago (Rasmussen et al, 2008), is the most abundant biochemi- carbon (C) and O2 cycles.The CBC can be divided into three cal pathway on Earth in terms of nitrogen investment (Ellis, partial processes; fixation of CO2 (ribulose-1,5-bisphosphate1844 | Arrivault et al.carboxylase-oxygenase) RuBisCO into a 3-C compound, 3-phosphoglycerate (3PGA), reduction of 3PGA to triose phosphate (triose-P) using ATP and NADPH from the light reactions, and a series of reactions that use triose-P to regenerate ribulose 1,5-bisphosphate (RuBP) (von Caemmerer and Farquhar, 1981; Heldt, 2005; Stitt et al, 2010; Adam, 2017)
Each species was grown with non-saturating irradiance and appropriate temperature for rapid, healthy growth, and harvested under growth irradiance at least 2 h after the beginning of the light period.Calvin–Benson cycle (CBC) intermediates and 2PG levels were determined by LC-MS/MS, using isotope-labelled internal standards to obtain reliable quantification, or enzymatically (3PGA).The signals for ribulose-5-phosphate (Ru5P) and xylulose-5-phosphate (Xu5P) overlapped, so they were combined (‘Ru5P+Xu5P’)
RuBP levels were lower in C4 compared with C3 species, probably reflecting lower abundance of RuBisCO in C4 plants

Summary

Introduction

The Calvin–Benson cycle (CBC) evolved ~2 billion years 1979; Raven, 2013), and plays a dominant role in the global ago (Rasmussen et al, 2008), is the most abundant biochemi- carbon (C) and O2 cycles.The CBC can be divided into three cal pathway on Earth in terms of nitrogen investment (Ellis, partial processes; fixation of CO2 (ribulose-1,5-bisphosphate1844 | Arrivault et al.carboxylase-oxygenase) RuBisCO into a 3-C compound, 3-phosphoglycerate (3PGA), reduction of 3PGA to triose phosphate (triose-P) using ATP and NADPH from the light reactions, and a series of reactions that use triose-P to regenerate ribulose 1,5-bisphosphate (RuBP) (von Caemmerer and Farquhar, 1981; Heldt, 2005; Stitt et al, 2010; Adam, 2017). In the current atmosphere with 0.04% CO2 and 21% O2, in C3 plants about every fourth reaction is with O2 instead of CO2, leading to a 20–30% decrease in the net rate of photosynthesis (Osmond, 1981; Sharkey, 1988; Long et al, 2006; Betti et al, 2016).This side reaction decreases nitrogen use efficiency, because higher amounts of protein must be invested in the photosynthetic apparatus This includes an especially large investment in RuBisCO, which has a relatively low catalytic rate and represents up to half of leaf protein (Ellis, 1979; Betti et al, 2016). It negatively impacts water use efficiency because a higher internal CO2 concentration is required to support a given net rate of photosynthesis, which in turn requires higher stomatal conductance and higher evaporative water loss (Ort et al, 2015; Betti et al, 2016)

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