Light-Enhanced Dark Respiration in Mesophyll Protoplasts from Leaves of Pea

Reddy, M. M.; Vani, T.; Raghavendra, Agepati S.

doi:10.1104/pp.96.4.1368

Cited by 45 publications

(32 citation statements)

References 20 publications

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“…This phenomenon of LEDR is already demonstrated in leaves and protoplasts (24,26). The decrease in respiratory oxygen uptake after photoinhibitory treatment could, therefore, be a consequence of restriction in the photosynthetic capacity during the preceding light period.…”

Section: Discussionsupporting

confidence: 54%

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Dark Respiration Protects Photosynthesis Against Photoinhibition in Mesophyll Protoplasts of Pea (Pisum sativum)

Saradadevi

Raghavendra²

1992

Plant Physiol.

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The optimal light intensity required for photosynthesis by mesophyll protoplasts of pea (Pisum sativum) is about 1250 microeinsteins per square meter per second. On exposure to supra-optimal light intensity (2500 microeinsteins per square meter per second) for 10 min, the protoplasts lost 30 to 40% of their photosynthetic capacity. Illumination with normal light intensity (1250 microeinsteins per square meter per second) for 10 min enhanced the rate of dark respiration in protoplasts. On the other hand, when protoplasts were exposed to photoinhibitory light, their dark respiration also was markedly reduced along with photosynthesis. The extent of photoinhibition was increased when protoplasts were incubated with even low concentrations of classic respiratory inhibitors: 1 micromolar antimycin A, 1 micromolar sodium azide, and 1 microgram per milliliter oligomycin. At these concentrations, the test inhibitors had very little or no effect directly on the process of photosynthetic oxygen evolution. The promotion of photoinhibition by inhibitors of oxidative electron transport (antimycin A, sodium azide) and phosphorylation (oligomycin) was much more pronounced than that by inhibitors of glycolysis and tricarboxylic acid cycle (sodium fluoride and sodium malonate, respectively). We suggest that the oxidative electron transport and phosphorylation in mitochondria play an important role in protecting the protoplasts against photoinhibition of photosynthesis. Our results also demonstrate that protoplasts offer an additional experimental system for studies on photoinhibition.

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Section: Discussionsupporting

confidence: 54%

“…The rate of dark respiration in leaves is increased after prolonged illumination and is presumed to be one of the long-term effects of photosynthesis. This phenomenon, which was recently termed LEDR, is demonstrated in leaves (26) as well as in protoplasts (24), even during short periods.…”

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confidence: 85%

Dark Respiration Protects Photosynthesis Against Photoinhibition in Mesophyll Protoplasts of Pea (Pisum sativum)

Saradadevi

Raghavendra²

1992

Plant Physiol.

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“…In CMSII, however, although rapidly induced, NADP-MDH remained high even when the rate of net CO 2 fixation approached that of the WT, suggesting an increased reduction state of the stroma because of insufficient electron sinks outside the chloroplast. Over-reduction of the photosynthetic system is also consistent with the pronounced second phase of postillumination CO 2 evolution in CMSII, which could reflect "light-enhanced dark respiration" (Reddy et al, 1991) possibly linked to a surplus of reducing equivalents in the light.…”

Section: Redox Adjustment Of Photosynthesis During Transients Requiresupporting

confidence: 63%

Functional Mitochondrial Complex I Is Required by Tobacco Leaves for Optimal Photosynthetic Performance in Photorespiratory Conditions and during Transients

Dutilleul¹,

et al. 2003

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The importance of the mitochondrial electron transport chain in photosynthesis was studied using the tobacco (Nicotiana sylvestris) mutant CMSII, which lacks functional complex I. Rubisco activities and oxygen evolution at saturating CO 2 showed that photosynthetic capacity in the mutant was at least as high as in wild-type (WT) leaves. Despite this, steady-state photosynthesis in the mutant was reduced by 20% to 30% at atmospheric CO 2 levels. The inhibition of photosynthesis was alleviated by high CO 2 or low O 2 . The mutant showed a prolonged induction of photosynthesis, which was exacerbated in conditions favoring photorespiration and which was accompanied by increased extractable NADP-malate dehydrogenase activity. Feeding experiments with leaf discs demonstrated that CMSII had a lower capacity than the WT for glycine (Gly) oxidation in the dark. Analysis of the postillumination burst in CO 2 evolution showed that this was not because of insufficient Gly decarboxylase capacity. Despite the lower rate of Gly metabolism in CMSII leaves in the dark, the Gly to Ser ratio in the light displayed a similar dependence on photosynthesis to the WT. It is concluded that: (a) Mitochondrial complex I is required for optimal photosynthetic performance, despite the operation of alternative dehydrogenases in CMSII; and (b) complex I is necessary to avoid redox disruption of photosynthesis in conditions where leaf mitochondria must oxidize both respiratory and photorespiratory substrates simultaneously.Plant biomass production is ultimately determined by the ratio between photosynthesis and respiratory CO 2 release, and 30% to 70% of fixed carbon can be rereleased within each 24-h cycle (Lambers, 1997). Therefore, manipulation of respiration is a potential approach to improving agricultural yields (Lewis et al., 2000). One current difficulty is that, quite apart from the roles played by respiration in heterotrophic tissues, the importance of leaf respiration for the process of carbon fixation itself is not yet fully established. Leaf mitochondria may have several functions during photosynthesis (for review, see Krö mer, 1995; Hoefnagel et al., 1998; Gardeströ m et al., 2002). These include oxidation of malate generated by the photosynthetic electron transport chain (Backhausen et al., 1998), production of organic acids for chloroplastic ammonia assimilation (Foyer et al., 2001), and generation of ATP to support UDP-Glc formation for Suc synthesis (Krö mer et al., 1988(Krö mer et al., , 1993. A key function of leaf mitochondria during photosynthesis, particularly in C 3 species, is the oxidation of Gly produced in the photorespiratory pathway (Douce and Neuburger, 1989) through reactions catalyzed by Gly decarboxylase (GDC) and Ser hydroxymethyl transferase, enzymes found in abundance in the mitochondrial matrix (Oliver et al., 1990). Although the importance of these enzymes in photorespiratory carbon recycling is well established (Somerville and Ogren, 1981; Blackwell et al., 1990; Heineke et al., 2001), and although is...

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“…Keywords: Dark Respiration, Deciduous Broadleaved Tree, Evergreen Conifer Tree, Gross Primary Production, Light Inhibition, Temperate Forest gical factors, including photosynthetic rate, specific leaf area, leaf age and relative growth rate (Reddy et al 1991, Villar et al 1995, Atkin et al 1997, Reich et al 1998, as well as environmental factors, namely, CO2 concentration, temperature, and drought (Bunce & Ziska 1996, Nakaji et al 2001, Peisker & Apel 2001, Vose & Ryan 2002, Warren & Adams 2002, Tingey et al 2007, Crous et al 2011, Zou et al 2011. However, our understanding of the inhibition of plant day respiration is still limited compared with that of night respiration, and the degree of light inhibition and the many variables that may influence it are not clear.…”

Section: Introductionmentioning

confidence: 99%

Day and night respiration of three tree species in a temperate forest of northeastern China

Sun¹,

Guan²,

Wu³

et al. 2015

iForest

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© iForest -Biogeosciences and Forestry IntroductionDark respiration (non-photorespiratory respiration), which occurs both in light and in darkness, has a critical function in modulating the carbon balance of plants and terrestrial ecosystems. Ryan (1991) showed that the proportion of carbon consumption by respiration is nearly 70% of the total photosynthetic carbon fixation, and leaf respiration accounts for approximately 50% of total plant respiration (Poorter et al. 1991). At the ecosystem level, CO2 emission from plant respiration accounts for 30-70% of the total ecosystem CO2 exchange (Amthor 2000). Plant respiration releases 60 Gt C yr -1 into the atmosphere (Schimel 1995). Therefore, understanding the carbon cycle of terrestrial ecosystems requires a more thorough understanding of the characteristics of leaf respiration.Due to difficulty in directly measuring leaf day respiration (RL), it is often assumed to be equal to night respiration (Poorter et al. 1990, Collier et al. 1992. However, Kok (1948) found that net CO2 assimilation rate (An) rapidly decreased near the light compensation point, leading to the conclusion that leaf respiration may vary with light intensity. Indeed, McCashin et al. (1988) found that 14 CO2 production during tricarboxylic acid cycle is approximately 20% lower in light than in darkness, which indicates that day respiration is inhibited in light. Subsequent studies confirmed that day respiration rates are lower than night respiration rates. Using stable 12 C/ 13 C isotope techniques, Tcherkez et al. (2005) found that two main processes (glycolysis and the Krebs cycle) of day respiration are strongly inhibited in illuminated leaves of French bean. Thus, plant respiration in light is overestimated if RL is assessed using data obtained during nighttime (Graham 1980, Sharp et al. 1984, Kirschbaum & Farquhar 1987, Kromer 1995, Atkin et al. 1997, Hoefnagel et al. 1998, Ayub et al. 2011.Plant respiration is a critical component of the gross primary production (GPP). Therefore, it is important to take into account the inhibitory effect of light on leaf respiration in order to obtain sound estimates of GPP. Wohlfahrt et al. (2005) estimated a reduction of 11-17% in GPP due to light inhibition in a mountain meadow, as compared to GPP model based on night respiration. Janssens et al. (2001) proposed that assessing day respiration by extrapolating night respiration results in an overestimation of ~15% of the total ecosystem respiration. Bruhn et al. (2011) recently reported that GPP estimation after taking into account light inhibition on leaf respiration for the average day is 76% of the GPP estimation taken without consideration of reduction in leaf respiration due to illumination. Thus, accurate estimates of the GPP requires the inhibition of leaf dark respiration by light to be considered.The Kok and Laisk methods are the two main methods used to estimate leaf day respiration. Kok (1948) analyzed the response of net photosynthesis rate to low light intensities and showed that the slope ...

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Light-Enhanced Dark Respiration in Mesophyll Protoplasts from Leaves of Pea

Cited by 45 publications

References 20 publications

Dark Respiration Protects Photosynthesis Against Photoinhibition in Mesophyll Protoplasts of Pea (Pisum sativum)

Dark Respiration Protects Photosynthesis Against Photoinhibition in Mesophyll Protoplasts of Pea (Pisum sativum)

Functional Mitochondrial Complex I Is Required by Tobacco Leaves for Optimal Photosynthetic Performance in Photorespiratory Conditions and during Transients

Day and night respiration of three tree species in a temperate forest of northeastern China

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