Brassicaceae display variation in efficiency of photorespiratory carbon-recapturing mechanisms

Abstract

Carbon concentrating mechanisms enhance the carboxylase efficiency of the central photosynthetic enzyme rubisco by providing supra-atmospheric concentrations of CO2 in its surrounding. In the C4 photosynthesis pathway, this feat is realised by combinatory changes to leaf biochemistry and anatomy. In contrast to the C4 pathway, carbon concentration can also be achieved by the photorespiratory glycine shuttle which requires fewer and less complex modifications. Plants displaying CO2 compensation points between 10 to 40 ppm are often considered to utilize such a photorespiratory shuttle and are termed ‘C3–C4 intermediates’. In the present study, we perform a physiological, biochemical and anatomical survey of a large number of Brassicaceae species to better understand the C3-C4 intermediate phenotype, including its basic components and its plasticity. Our phylogenetic analysis suggested that C3-C4 metabolism evolved up to five times independently in the Brassicaceae. The efficiency of the pathway showed considerable variation between tested plant species. Centripetal accumulation of organelles in the bundle sheath was consistently observed in all C3-C4 classified taxa indicating a crucial role of anatomical features for CO2 concentrating pathways. Leaf metabolite patterns were strongly influenced by the individual species, but accumulation of photorespiratory shuttle metabolites glycine and serine was generally observed. Analysis of PEPC activities and metabolite composition suggests that C4-like shuttles have not evolved in the investigated Brassicaceae. Convergent evolution of the photorespiratory shuttle indicates that it represents a distinct and fit photosynthesis type.

A transcription factor module mediating C2photosynthesis

“…The Brassicaceae contains at least five independent origins of C 2 photosynthesis (Schlüter et al, 2023). We hypothesized that conservation of MYC and MYB binding sites driving bundle sheath expression of GLDP1 across the Brassicaceae underpins the repeated evolution of this trait.…”

A genomic panel for studying C3‐C4 intermediate photosynthesis in the Brassiceae tribe

“…The glycine shuttle biochemistry is accompanied by enhanced centripetal organelle accumulation in the bundle sheath cells (for reviews see: Lundgren, 2020;Schlüter and Weber, 2016). Carbon concentration via the glycine shuttle is less effective than the C4 cycle, but could be advantageous under hot and dry growth conditions, when photorespiration is usually high (Bellasio & Farquhar, 2019;Oono et al, 2022;Schlüter et al, 2023;Vogan & Sage, 2012). Since the C3-C4 related features could represent transitory stages towards C4 photosynthesis, knowledge of their genetic underpinnings could also contribute to the understanding of C4 evolution.…”

“…Summary statistics of genome assemblies developed in our study along with CO 2 compensation point (CPP) and inferred photosynthesis type fromSchlüter et al (2023).…”

“…The Moricandia genus was monophyletic, while the Diplotaxis and Brassica genera species were dispersed across the phylogenetic tree (Figure4). When integrating the information of the CO 2 compensation points fromSchlüter et al (2023) in the phylogenetic tree, the result indicated that the C3-C4 intermediate photosynthesis might have developed five times independently (Figure4).…”

Rubisco is evolving for improved catalytic efficiency and CO2assimilation in plants

“…Moreover, it appears that instead of improving enzyme function, multiple lineages have evolved alternative strategies to overcome rubisco's shortcomings. For example, higher rates of CO2 assimilation are often achieved either by synthesising large quantities of rubisco (~50% of soluble protein in plants 68 and some microbes 69,70 ), or by operating CO2-concentrating mechanisms [71][72][73] . As a result, many have questioned whether the enzyme is already perfectly adapted, and whether further kinetic improvements are possible 15,63,67,[74][75][76][77][78] .…”