Beneficial interaction between photosynthesis and respiration in mesophyll protoplasts of pea during short light‐dark cycles

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

doi:10.1111/j.1399-3054.1990.tb00069.x

Cited by 20 publications

(11 citation statements)

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“…We have recently reported that the processes ofphotosynthesis and respiration are mutually beneficial (20). The movement of phosphoglycerate/dihydroxyacetone phosphate and oxalacetate/malate between the chloroplasts, cytosol, and mitochondria may help to maintain a favorable balance of adenine and pyridine nucleotides in these organelles for their optimal performance (10,23).…”

Section: Discussionmentioning

confidence: 99%

“…Illumination was provided at an intensity of 50 ME m-2 s-5. The plasmolyzed leaf pieces were then digested in Petri dishes with Cellulase Onozuka R-10 and Macerozyme R-I0 (Yakult Honsha, Nishinomiya, Japan), as described in detail elsewhere (20). The preparation had about 90 to 95% intact protoplasts, as indicated by the uptake of neutral red and exclusion of Evans blue.…”

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confidence: 99%

“…Protoplasts are useful tools for studying plant metabolism because they form homogeneous suspensions; pose no problem of recycling of gas, as within ' (20) have demonstrated a strong interaction between photosynthesis and respiration in mesophyll protoplasts of pea.…”

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

Reddy¹,

Vani²,

Raghavendra³

1991

Plant Physiol.

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The respiratory oxygen uptake by mesophyll protoplasts of pea (Pisum sativum cv Arkel) was stimulated up to threefold after 15 minutes of Illumination at an intensity of 1250 microeinsteins per square meter per second in the presence of 5 millimolar bicarbonate at 300C. The extent of light-enhanced dark respiration (LEDR) increased progressively with duration of preillumination. The LEDR exhibited two phases. The initial high rate of respiration decreased in about 10 minutes to a lower steady value similar to that before Illumination. The promotion of LEDR by the presence of bicarbonate and inhibition by glyceraldehyde or 3-(3,4-dichlorophenyl)-1,1-dimethylurea suggested that LEDR was dependent on products of photosynthetic carbon assimilation/electron transport. Thus, the photosynthetic products exert a markedly quick influence on dark respiration in mesophyll protoplasts.The carbon and energy economy of a plant depend not only on photosynthesis but also on respiration. The interaction between photosynthesis and respiration, therefore, is very important. Photosynthesis over long periods of illumination leads to an accumulation of carbohydrates, which can stimulate dark respiration (3). The lowering of photosynthetic efficiency at lower light intensities, a phenomenon called the Kok effect (12), is believed to be primarily due to dark respiration (1 1, 16, 17).The magnitude ofmitochondrial (dark) respiration in leaves of higher plants during photosynthesis is not yet clearly established (7, 8). There is a large variation in the reported reduction in dark respiration on illumination, ranging from 0 to 100% (2, 4, 13). Most of the studies to date have been made with intact leaves or leaf discs, which have certain inherent problems, such as recycling of assimilated/released CO2 within the leaf (5), making it difficult to establish the interaction between photosynthesis and respiration (14).We have used isolated mesophyll protoplasts from pea (Pisum sativum cv Arkel) leaves to reevaluate the effect of light on dark respiration. Protoplasts are useful tools for studying plant metabolism because they form homogeneous suspensions; pose no problem of recycling of gas, as within ' (20) have demonstrated a strong interaction between photosynthesis and respiration in mesophyll protoplasts of pea.Our results indicate that there is a marked upsurge in respiratory 02 uptake after even short periods ofillumination. This phenomenon, termed LEDR,2 appears to be related to photosynthetic carbon metabolism/electron transport. As this article was under preparation, LEDR was described in leaves (19). This article is the first report of LEDR in protoplasts. MATERIALS AND METHODSThe first and second fully expanded leaves from 8-to 10-d-old plants of pea (Pisum sativum L. cv Arkel) grown outdoors (natural photoperiod of approximately 12 h; average daily temperatures of 30C day/20C night) were used. The leaves were picked from the plants between 9:00 and 10:00 AM, by which time the plants were exposed to sunlight for about 3 or...

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Section: Discussionmentioning

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

Reddy¹,

Vani²,

Raghavendra³

1991

Plant Physiol.

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“…Recent reports established that the oxidative metabolism in mitochondria has a beneficial and essential role in the photosynthetic process as well (12,13,28). It is possible that the marginal interference by respiratory inhibitors of photosynthetic metabolism (Table II) makes protoplasts highly susceptible to photoinhibitory light.…”

Section: Discussionmentioning

confidence: 99%

“…However, recent reports establish that there is a rapid and strong interaction between respiration and photosynthesis in plant tissue. Respiratory metabolism is beneficial for photosynthesis in the plant cell, as shown in leaves and protoplasts (12,13,28). 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.…”

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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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