High-to-Low CO2 Acclimation Reveals Plasticity of the Photorespiratory Pathway and Indicates Regulatory Links to Cellular Metabolism of Arabidopsis

Abstract

BackgroundPhotorespiratory carbon metabolism was long considered as an essentially closed and nonregulated pathway with little interaction to other metabolic routes except nitrogen metabolism and respiration. Most mutants of this pathway cannot survive in ambient air and require CO2-enriched air for normal growth. Several studies indicate that this CO2 requirement is very different for individual mutants, suggesting a higher plasticity and more interaction of photorespiratory metabolism as generally thought. To understand this better, we examined a variety of high- and low-level parameters at 1% CO2 and their alteration during acclimation of wild-type plants and selected photorespiratory mutants to ambient air.Methodology and Principal FindingsThe wild type and four photorespiratory mutants of Arabidopsis thaliana (Arabidopsis) were grown to a defined stadium at 1% CO2 and then transferred to normal air (0.038% CO2). All other conditions remained unchanged. This approach allowed unbiased side-by-side monitoring of acclimation processes on several levels. For all lines, diel (24 h) leaf growth, photosynthetic gas exchange, and PSII fluorescence were monitored. Metabolite profiling was performed for the wild type and two mutants. During acclimation, considerable variation between the individual genotypes was detected in many of the examined parameters, which correlated with the position of the impaired reaction in the photorespiratory pathway.ConclusionsPhotorespiratory carbon metabolism does not operate as a fully closed pathway. Acclimation from high to low CO2 was typically steady and consistent for a number of features over several days, but we also found unexpected short-term events, such as an intermittent very massive rise of glycine levels after transition of one particular mutant to ambient air. We conclude that photorespiration is possibly exposed to redox regulation beyond known substrate-level effects. Additionally, our data support the view that 2-phosphoglycolate could be a key regulator of photosynthetic-photorespiratory metabolism as a whole.

Serine Acts as a Metabolic Signal for the Transcriptional Control of Photorespiration-Related Genes in Arabidopsis

“…Furthermore, these changes were not persistent over the whole analyzed period and appeared solely at one or two specific time points (Supplemental Table S2). Moreover, if compared with the strong alterations observed with other photorespiratory mutants Voll et al, 2006;Engel et al, 2007;Collakova et al, 2008;Timm et al, 2012b;Eisenhut et al, 2013), these metabolic changes are of a very moderate character, confirming the suitability of hpr1 as a model to study the direct feedback of a slightly and specifically reduced internal carbon flow on the regulation of photorespiration.…”

“…First, after Gly supplementation of Arabidopsis seedlings, the internal concentration of this amino acid is reduced to one-half of that found in nontreated seedlings. Second, the accumulation of Gly in hpr1 during the high-to-low CO 2 transition after 1 d is less distinct 3 d after transfer to normal air (Timm et al, 2012b). Both findings indicate that Gly could act as a transcriptional inductor for GDC proteins to adapt plants for photorespiratory conditions.…”

“…This was done for four reasons: (1) Gly is the direct precursor of Ser; (2) both amino acids are interconverted by GDC and SHM1, for which transcriptional repression was most distinct; (3) the amount of Gly showed the highest diel amplitude, particularly if the photorespiratory carbon flow was slightly constrained in hpr1; and (4) the earlier observed strong transient accumulation of Gly after shifting Arabidopsis from low to high photorespiratory conditions (Timm et al, 2012b). However, in contrast to L-Ser supplementation, we found that external application of Gly essentially does not alter the diel pattern of photorespiratory transcripts but rather causes an enhanced induction of GDC and SHM1 expression after the onset of light.…”

“…Hence, regulation at the flux level can be investigated using mutants with defects in photorespiratory enzymes. Most null mutants of photorespiratory enzymes are heavily impaired in photorespiratory conditions (Timm and Bauwe, 2013;Timm et al, 2012b) and cannot be easily used for such experiments. In contrast, the presence of a cytosolic bypass allows mutants deficient in HPR1 to grow in a wild-type-like manner in normal air (Timm et al, 2008(Timm et al, , 2011.…”

The essential role of the phosphorylated pathway of serine biosynthesis inArabidopsis

“…12,13 In addition, a role of Ser or Ser derivatives (D-Ser) in a plant signaling mechanism or in regulating transcripcional and translational networks should also be taken into account. 3,14 Finally, it could be argued that PSP1 performs additional functions, as has been demonstrated for other metabolic enzymes in plants. Along these lines, Bachelor et al (2011) 17 found that PSP1 overexpression in mammal cells abrogates squamous cell carcinoma proliferation independently of serine levels, thus postulating additional roles for the enzyme, such as additional enzymatic substrates or novel non-enzymatic interacting proteins, which may be important for carcinogenesis.…”