The role of photorespiration during drought stress: an analysis utilizing barley mutants with reduced activities of photorespiratory enzymes

Abstract

The significance of photorespiration in drought-stressed plants was studied by withholding water from wild-type barley (Hordeum vulgare L.) and from heterozygous mutants with reduced activities of chloroplastic glutamine synthetase (GS-2), glycine decarboxylase (GDC) or serine : glyoxylate aminotransferase (SGAT). Wellwatered plants of all four genotypes had identical rates of photosynthesis. Under moderate drought stress (leaf water potentials between -1 and -2 MPa), photosynthesis was lower in the mutants than in the wild type, indicating that photorespiration was increased under these conditions. Analysis of chlorophyll a fluorescence revealed that, in the GDC and SGAT mutants, the lower rates of photosynthesis coincided with a decreased quantum efficiency of photosystem II and increased non-photochemical dissipation of excitation energy. Correspondingly, the de-epoxidation state of xanthophyll-cycle carotenoids was increased several-fold in the drought-stressed GDC and SGAT mutants compared with the wild type. Accumulation of glycine in the GDC mutant was further evidence for increased photorespiration in droughtstressed barley. The effect of drought on the photorespiratory enzymes was determined by immunological detection of protein abundance. While the contents of GS-2 and Pand H-protein of the GDC complex remained unchanged as drought stress developed, the content of NADH-dependent hydroxypyruvate reductase increased. Enzymes of the Benson-Calvin cycle, on the other hand, were either not affected (ribulose-1,5-bisphosphate carboxylase-oxygenase and plastidic fructose-1,6-bisphosphatase) or declined (sedoheptulose-1,7-bisphosphatase and NADPdependent glyceraldehyde-3-phosphate dehydrogenase). These data demonstrate that photorespiration was enhanced during drought stress in barley and that the control exerted by photorespiratory enzymes on the rate of photosynthetic electron transport and CO 2 fixation was increased.Key-words: drought stress; glutamine synthetase; glycine decarboxylase; hydroxypyruvate reductase; mutants; photorespiration; photosynthesis; serine : glyoxylate aminotransferase; xanthophyll cycle.Abbreviations: C i , intercellular CO 2 concentration; F v /F m , quantum efficiency of excitation capture by open photosystem II centres; FBPase, fructose-1,6-bisphosphatase; GAPDH, glyceraldehyde-3-phosphate dehydrogenase; GDC, glycine decarboxylase; GS-2, chloroplastic glutamine synthetase; HPR, hydroxypyruvate reductase; PFD, photon flux density; ΦCO 2 , quantum efficiency of CO 2 assimilation; ΦPSII, quantum efficiency of photosystem II electron transport; ψ, water potential; q N , non-photochemical chlorophyll a fluorescence quenching; q P , photochemical chlorophyll a fluorescence quenching; RuBP, ribulose-1,5-bisphosphate; Rubisco, ribulose-1,5-bisphosphate carboxylase-oxygenase; SBPase, sedoheptulose-1,7-bisphosphatase; SGAT, serine : glyoxylate aminotransferase. INTRODUCTIONDrought stress leads to a substantial reduction in the rate of photosynthetic CO 2 assimilation. Under mild to...

Reduced glutamine synthetase activity plays a role in control of photosynthetic responses to high light in barley leaves

“…The GS2 mutants of barley has usually normal rates of photosynthesis in moderate light and ambient CO 2 (Häusler et al, 1994a;Wingler et al, 1997); this was confirmed also by our measurements. It was previously shown that the reduced GS activity led often to decrease of CO 2 assimilation and PSII electron transport rate, but mostly in photorespiratory conditions (Häusler et al, 1994a;Wingler et al, 1999;Streb et al, 1998). This was probably the case of our measurements in natural sunlight (Fig.…”

“…The supply of glutamine to a GS2 mutant of barley restored photosynthetic activity (Blackwell et al, 1987). However, the pools of RuBP was shown to be almost unaffected by mutation of GS-2 (Leegood et al, 1995;Wingler et al, 1999).…”

“…the homozygous photorespiratory mutants) are not able to survive at ambient CO 2 concentrations, the heterozygous mutants with only partially reduced enzyme activities can be grown well in air (Wingler et al, 2000). The GS2 mutant of barley was shown to have normal rates of photosynthesis in moderate light and ambient CO 2 , but lower rates when photorespiratory flux was increased in high light and low CO 2 (Häusler et al, 1994a;Wingler et al, 1999). Wingler et al (2000) suggest three ways how the reduced photorespiratory enzyme activity may affect photosynthesis in mutant plants.…”

Drought stress and carbon assimilation in a warming climate: Reversible and irreversible impacts

“…Therefore the integral performance during the whole season is relevant for a comprehensive evaluation of a species or of a genotype. Net photosynthesis does not only depend on photosynthetic electron transport and Calvin cycle activity, since carbon losses via decarboxylation processes also contribute to the overall performance (Wingler et al, 1999;Haupt-Herting et al, 2001;Noctor et al, 2002;Bai et al, 2008;Rivero et al, 2009;Vassileva et al, 2009Vassileva et al, , 2011. The impact of heat and drought on respiration is also crucial for the carbon balance and should be considered when comparing genotypes (Flexas et al, 2006;Vassileva et al, 2011).…”

Insertional Mutants of Chlamydomonas reinhardtii That Require Elevated CO2 for Survival

“…HCR mutants with defects in several of the enzymes of the photorespiratory pathway have been isolated in the C 3 plants Arabidopsis (Somerville and Ogren, 1982) and barley (Hordeum vulgare) (Joy et al, 1992;Leegood et al, 1996;Wingler et al, 1999). These photorespiratory mutants exhibited lethality (HCR phenotype) in air levels of CO 2 for various reasons, including accumulation of toxic intermediates during photorespiration and depletion of exchangeable nitrogen in photorespiratory intermediates.…”