Photorespiration: origins and metabolic integration in interacting compartments

This special issue on photorespiration focuses on recent advances in this topic. The majority of the papers summarizes and extends contributions given at the 2nd workshop, ‘Photorespiration–key to better crops’, held in Warnemuende, Germany in June 2015. This was organized by the DFG (German Research Foundation)-supported research network, ‘Photorespiration: origins and metabolic integration in interacting compartments’ (FOR 1186–Promics).

biochemically verified (Bordych et al., 2013;Pick et al., 2013). Research on C 4 plants not only showed that PR is essential for these plants (Zelitch et al., 2009), but also provided increasing evidence for the important role of PR in the evolution of C 4 photosynthesis (Sage, 2004). The different location of photorespiratory enzymes in so-called C 3 -C 4 intermediate plants generated/established an ancient CO 2 pump based on the transport of glycine and serine, which is also called C 2 photosynthesis, as the precursor for the final dicarboxyacid-based C 4 cycle (e.g. Mallmann et al., 2014). Last but not least, the identification of functional photorespiratory processes in cyanobacteria resulted in the view that photorespiration is an ancient process which coevolved with oxygenic photosynthesis (Eisenhut et al., 2006(Eisenhut et al., , 2008Kern et al., 2011Kern et al., , 2013Bauwe et al., 2012;Hagemann et al., 2013).
The present special issue reports on different aspects of actual PR research. It comprises one insight paper, eight review papers, three opinion papers, and nine original research papers.
The insight paper and three reviews discuss the current view on PR and its evolution. Sage (this issue) summarized the stepwise development of C 4 photosynthesis from C 3 photosynthesis, whereby the localization of photorespiratory enzymes and metabolic fluxes between bundle sheath and mesophyll played a crucial role. Bräutigam and Gowik (this issue) highlight the important role of PR in the evolution of C 4 photosynthesis via intermediary stages, in which the capacity for PR is lost from leaf mesophyll cells and relocated to the bundle sheath cells. As shown by Döring et al. (this issue), in fully evolved C 4 plants such as sorghum, the majority of genes encoding components of PR are also expressed preferentially in bundle sheath cells. Khoshravesh et al. (this issue) highlight the importance of organelle positioning in bundle sheath cells and the relocation of photorespiratory activity to this tissue during the evolution of C 4 photosynthesis in grasses. Hagemann et al. (this issue) review the current position on the continuous coevolution of photosynthesis and PR. The evolution of all photorespiratory enzymes was elucidated and it was revealed that the present-day plant photorespiratory enzymes originated from archaeal, bacterial, and cyanobacterial sources, which served as eukaryotic host cell (Archaea), and mitochondrial (proteobacteria) or plastdial (cyanobacteria) endosymbionts, respectively. Moreover, calculating in terms of the geological era, ancient CO 2 /O 2 ratios indicated that photorespiratory metabolism existed from the invention of oxygenic photosynthesis and remained necessary in cells evolving different types of carbon-concentrating mechanisms (CCM).
Another set of contributions deals with the intertwining of the photorespiratory pathway with the central metabolism and its significance for engineering plant productivity. For example, Fromm et al. (this issue), by using mutants that lack the activity of mitochondrial NADH dehydrogenase, analysed the role of the mitochondrial electron transport chain in photosynthesis. Using transcriptomic analysis of Lotus japonicus wild type and GS2 mutant plants on a range of different nitrogen concentrations and at ambient and elevated CO 2 , Pérez-Delgado et al. (this issue) show that primary nitrogen assimilation and PR are transcriptionally co-regulated. They also identify candidate transcription factors mediating this co-ordinated response. Betti et al. ( also explore the regulatory effect of light reactions on PR in their opinion paper. They employ the framework of modularity in the cyanobacterium Fremyella diplosiphon and suggest a highly controlled interplay among light reactions, PR, and CCM. The opinion paper by Orf et al. (this issue) also centres on cyanobacteria. According to their comparative meta-analysis of cyanobacterial and plant metabolite profiles, the authors propose that cyanobacteria can serve as a much simpler surrogate to study the complex, highly compartmentalized, plant PR metabolism.
A deeper understanding of PR requires technology to determine rates of PR and photosynthesis accurately and this is reviewed by Hanson et al. (this issue). Alonso-Cantabrana and von Caemmerer (this issue) report on using carbon isotope discrimination as a tool to quantify C 4 -like photosynthesis in C 3 -C 4 intermediate species. Labelling with the stable carbon isotope 13 C also revealed a strong effect of reduced mitochondrial malate dehydrogenase activity on PR (Lindén et al., this issue). Sharwood et al. (this issue) emphasize the importance of standardized and validated protocols for quantifying carbon fixation capacity in plants with differing carbon assimilation strategies, with particular emphasis on quantifying Rubisco activity.
Four papers deal with the specific role of the central enzyme, glycolate oxidase. The biochemistry of this peroxisomal enzyme converting glycolate into glyoxylate is reviewed by Hodges et al. (this issue). Dellero et al. report on the impact of reduced photorespiratory glycolate oxidase activity on leaf metabolism in Arabidopsis (Dellero et al., a, this issue) and review recent advances in the understanding of glyoxylate metabolism in different plant organs (Dellero et al., b, this issue). Knocking out glycolate oxidase of Cyanidioschyzon merolae resulted in the first mutant with a photorespiratory phenotype among red algae (Rademacher et al., this issue). This finding revealed that the plant-type photorespiratory cycle using a peroxisomal glycolate oxidase evolved before the split of red and green algae, and it represents a further example that organisms, though carrying a CCM, also depend on functional PR.

Concluding remarks
The past decades of research on the process of PR have revealed that this pathway is an indispensable companion to oxygenic photosynthesis and includes photosynthetic organisms that feature highly efficient CCMs such as cyanobacteria, many algae, and C 4 plants. Not only is it essential to support photosynthetic carbon assimilation, it is also heavily intertwined with other metabolic pathways and is the driving force for the evolution of C 4 photosynthesis (Heckmann et al., 2013), the most efficient mode of photosynthetic carbon assimilation in the angiosperms. In extant oxygenic photosynthetic organisms, the only means to reduce the rate of PR and hence enhance photosynthetic efficiency is to increase the concentration of CO 2 at the site of Rubisco. Therefore, future research aimed at increasing the efficiency of photosynthesis in crop plants might want to focus on this aspect. In the short term, perhaps the most promising path towards increased crop efficiency might be founded on a deeper understanding of natural variation in photosynthetic capacity to unravel those genes that determine source strength.
Here, a better understanding of PR regulation and its integration into the cellular metabolism via yet unidentified transporters (e.g. exchanging glycine and serine between mitochondria and peroxisomes) would be an important future aim. However, in the long-term, it is also envisaged that synthetic pathways for carbon assimilation (i.e. pathways not existing in nature), that are not affected by oxygen, might become a reality (Bar-Even et al., 2010;Ort et al., 2015), thereby enabling hitherto unimaginable gains in productivity.