Integrated Temporal Regulation of the Photorespiratory Pathway. Circadian Regulation of Two Arabidopsis Genes Encoding Serine Hydroxymethyltransferase

Abstract

The photorespiratory pathway is comprised of enzymes localized within three distinct cellular compartments: chloroplasts, peroxisomes, and mitochondria. Photorespiratory enzymes are encoded by nuclear genes, translated in the cytosol, and targeted into these distinct subcellular compartments. One likely means by which to regulate the expression of the genes encoding photorespiratory enzymes is coordinated temporal control. We have previously shown in Arabidopsis that a circadian clock regulates the expression of the nuclear genes encoding both chloroplastic (Rubisco small subunit and Rubisco activase) and peroxisomal (catalase) components of the photorespiratory pathway. To determine whether a circadian clock also regulates the expression of genes encoding mitochondrial components of the photorespiratory pathway, we characterized a family of Arabidopsis serine hydroxymethyltransferase (SHM) genes. We examined mRNA accumulation for two of these family members, including one probable photorespiratory gene (SHM1) and a second gene expressed maximally in roots (SHM4), and show that both exhibit circadian oscillations in mRNA abundance that are in phase with those described for other photorespiratory genes. In addition, we show that SHM1 mRNA accumulates in light-grown seedlings, although this response is probably an indirect consequence of the induction of photosynthesis and photorespiration by illumination.

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

“…For example, the mRNA of Glycolate Oxidase (GOX) accumulates following the illumination of tobacco (Nicotiana tabacum) seedlings and decreases in the dark (Barak et al, 2001). Similar patterns were observed for mRNA levels of other photorespiratory enzymes, for example Glycine Decarboxylase (GDC), Serine Hydroxymethyltransferase1 (SHM1), and peroxisomal Hydroxypyruvate Reductase1 (HPR1; Kim et al, 1991;Sloan et al, 1993;Srinivasan and Oliver, 1995;McClung et al, 2000;Lutziger and Oliver, 2001). More comprehensive transcript profilings revealed that light induction is a general feature of most photorespiratory genes (Foyer et al, 2009).…”

“…Extending earlier reports on individual enzymes (Kim et al, 1991;Sloan et al, 1993;Srinivasan and Oliver, 1995;McClung et al, 2000;Barak et al, 2001;Lutziger and Oliver, 2001) and the evaluation of Genevestigator data (discussed by Foyer et al, 2009), our study provides a clear experimental picture of a light-induced increase in the capacity of the photorespiratory pathway brought about by increased transcription of the photorespiratory genes. This also translates into higher amounts (and likely activities) of photorespiratory enzymes and allows the efficient recycling of 2-phosphoglycolate (2PG) into 3-phosphoglycerate (3PGA) during the day.…”

Arabidopsis Photorespiratory Serine Hydroxymethyltransferase Activity Requires the Mitochondrial Accumulation of Ferredoxin-Dependent Glutamate Synthase

“…The Arabidopsis thaliana genome includes two genes encoding distinct Fd-GOGAT isozymes; the photorespiratory function is associated exclusively with FERREDOXIN-DEPENDENT GLUTAMATE SYNTHASE1 (GLU1) (Somerville and Ogren, 1980;Coschigano et al, 1998). Similarly, the completion of the Arabidopsis genome sequence indicates that SHMT in Arabidopsis is encoded by seven SHM genes, two of which encode mitochondrial isoforms (McClung et al, 2000;Bauwe and Kolukisaoglu, 2003). However, only SHM1 is necessary and sufficient to specify photorespiratory SHMT activity (Voll et al, 2006).…”

UBIQUITIN-SPECIFIC PROTEASE16 Modulates Salt Tolerance in Arabidopsis by Regulating Na+/H+ Antiport Activity and Serine Hydroxymethyltransferase Stability

“…It has been reported that a mutation in SERINE HYDROXYMETHYLTRANSFERASE1 (shm1-2, a weak allele) leads to overaccumulation of ROS and that the mutant is more sensitive to salt stress and pathogens than is the wild type (Moreno et al, 2005). The Arabidopsis genome encodes seven SHM genes, and few of these gene products have been shown to function in mitochondria (McClung et al, 2000;Bauwe and Kolukisaoglu, 2003;Jamai et al, 2009;Engel et al, 2011). SHM1 is the major SERINE HYDROXYMETHYLTRANSFERASE (SHMT) isozyme in Arabidopsis leaves (Somerville and Ogren, 1981;McClung et al, 2000); the shm1-1 mutant was the first photorespiratory mutant identified in Arabidopsis.…”