Lack of GLYCOLATE OXIDASE1, but Not GLYCOLATE OXIDASE2, Attenuates the Photorespiratory Phenotype of CATALASE2-Deficient Arabidopsis

Abstract

The genes coding for the core metabolic enzymes of the photorespiratory pathway that allows plants with C3-type photosynthesis to survive in an oxygen-rich atmosphere, have been largely discovered in genetic screens aimed to isolate mutants that are unviable under ambient air. As an exception, glycolate oxidase (GOX) mutants with a photorespiratory phenotype have not been described yet in C3 species. Using Arabidopsis (Arabidopsis thaliana) mutants lacking the peroxisomal CATALASE2 (cat2-2) that display stunted growth and cell death lesions under ambient air, we isolated a second-site loss-of-function mutation in GLYCOLATE OXIDASE1 (GOX1) that attenuated the photorespiratory phenotype of cat2-2. Interestingly, knocking out the nearly identical GOX2 in the cat2-2 background did not affect the photorespiratory phenotype, indicating that GOX1 and GOX2 play distinct metabolic roles. We further investigated their individual functions in single gox1-1 and gox2-1 mutants and revealed that their phenotypes can be modulated by environmental conditions that increase the metabolic flux through the photorespiratory pathway. High light negatively affected the photosynthetic performance and growth of both gox1-1 and gox2-1 mutants, but the negative consequences of severe photorespiration were more pronounced in the absence of GOX1, which was accompanied with lesser ability to process glycolate. Taken together, our results point toward divergent functions of the two photorespiratory GOX isoforms in Arabidopsis and contribute to a better understanding of the photorespiratory pathway.The increase in atmospheric CO 2 levels linked to global warming, which entails unpredictable climate conditions, poses an unprecedented pressure on modern agriculture (Lobell and Gourdji, 2012; Wheeler and von Braun, 2013). However, apart from its greenhouse properties, CO 2 and its photosynthetic assimilation into biomass are the primary foundation of life on Earth. Thus, atmospheric CO 2 content has a direct effect on agricultural production, and even a modest CO 2 increase might in theory result in higher crop yields, especially in plants with C3-type photosynthesis (Walker et al., 2016). In contrast to C4 and CAM-type plants, C3 plants do not possess carbon concentrating mechanisms, and the first stable CO 2 assimilation product is 3-phosphoglycerate that is further processed in the Calvin-Benson cycle to fuel sugar synthesis. C4 plants initially incorporate CO 2 into four-carbon acids that are subsequently decarboxylated in the vicinity of the primary CO 2 -assimilating enzyme Rubisco. The C4-type photosynthesis evolved independently over 60 times (Sage et al., 2011), reflecting the need to counteract the highly promiscuous nature of Rubisco that apart from carboxylation of ribulose-1,5-bisphosphate also catalyzes its oxygenation to 2-phosphoglycolate (PG). This oxygenation reaction initiates the photorespiratory pathway that recycles PG back to 3-phosphoglycerate with the release of CO 2 in a series of enzymatic steps distributed between chl...

Stress Marker Signatures in Lesion Mimic Single and Double Mutants Identify a Crucial Leaf Age-Dependent Salicylic Acid Related Defense Signal

“…Especially in cat2 this means that the photorespiration is lower in the youngest leaves and would not accumulate as high levels of H 2 O 2 as the mature and old leaves. Consistent with this observation, when cat2 is put into conditions of severe high light stress the youngest leaves do not develop cell death [47]. Similarly, in dnd1 , spontaneous cell death is more prominent in the mature and old leaves [27].…”

“…Overall, this suggests that the youngest leaves have not yet entered into a strong defense or cell death program, and may instead be under regulation by a developmental program. Furthermore, the youngest leaves are likely to be sink leaves that receive their photosynthates from the mature and old leaves [47]. Especially in cat2 this means that the photorespiration is lower in the youngest leaves and would not accumulate as high levels of H 2 O 2 as the mature and old leaves.…”

The fluorescent protein sensor roGFP2‐Orp1 monitors in vivo H2O2 and thiol redox integration and elucidates intracellular H2O2 dynamics during elicitor‐induced oxidative burst in Arabidopsis

“…We anticipate that these mutants may have altered steady state H 2 O 2 levels because the missing pathways normally supply electrons for H 2 O 2 detoxification by peroxidases. In addition, cat2‐1 , impaired in catalase 2 (Queval et al ., ; Kerchev et al ., ), as a high capacity sink for H 2 O 2 in the peroxisomes, sapx impaired in ascorbate peroxidase activity in the plastid stroma and the mitochondrial matrix (Giacomelli et al ., ), as well as prxII F , impaired in mitochondrial matrix peroxiredoxin‐II F (Finkemeier et al ., ) were selected (Fig. a).…”

The Arabidopsis catalase triple mutant reveals important roles of catalases and peroxisome‐derived signaling in plant development

“…However, the necrotic lesions of cat2 leaves only arise under long days, and can be recovered by high CO 2 , indicating that CAT2 is the main catalase isoform to scavenge H 2 O 2 during photorespiration (Mhamdi et al ). The lesion phenotype and redox perturbation in the cat2 mutant can also be alleviated by reducing generation of H 2 O 2 in peroxisomes (Kerchev et al ; Waszczak et al ), suggesting that catalase is involved in the regulation of plant growth and redox state by controlling H 2 O 2 levels.…”