The relationship between respiration and temperature in leaves of the arctic plant <i>Saxifraga cernua</i>

McNulty, Amy K.; Cummins, W. Raymond

doi:10.1111/j.1365-3040.1987.tb01612.x

Cited by 68 publications

(59 citation statements)

References 21 publications

(27 reference statements)

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“…Presumably, as the tissue develops in the cold a greater respiratory capacity is needed. It is not likely that heat production is the reason for the higher respiration rate or the greater alternative oxidase capacity because of the small amount of heat produced (12,13). It is more likely that the increase rates are required to prevent the accumulation of metabolites that would otherwise accumulate to toxic levels.…”

Section: Discussionmentioning

confidence: 99%

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Respiration and Alternative Oxidase in Corn Seedling Tissues during Germination at Different Temperatures

Stewart¹,

Martin²,

Reding³

et al. 1990

Plant Physiol.

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Respiration rates of Zea mays L. seedling tissues grown at 30 and 140C were measured at 250C at different stages of seedling growth. Accumulation of heat units was used to define the developmental stages to compare respiration between the two temperatures. At both temperatures, respiration rates of most tissues were highest at the youngest stages, then declined with age. Respiration rates of mesocotyl tissue were the most responsive to temperature, being nearly twofold higher when grown at 14 compared to 300C. Alternative pathway respiration increased concomitantly with respiration and was higher in mesocotyls grown in the cold. When seedlings were started at 30 then transferred to 140C, the increase in altemative pathway respiration due to cold was not observed unless the seedlings were transferred before 2 days of growth. Seedlings transferred to 140C after growth at 300C for 2 days had the same altemative oxidase capacity as seedlings grown at 300C. Seedlings grown at 140C for 10 to 12 days, then transferred to 300C, lost alternative pathway respiratory capacity over a period of 2 to 3 days. Western blots of mitochondrial proteins indicated that this loss of capacity was due to a loss of the alternative oxidase protein. Some in vitro characteristics of mitochondna were determined. The temperature optimum for measurement of alternative oxidase capacity was 15 to 200C. At 41°C, very little altemative oxidase was measured, i.e., the mitochondrial oxygen uptake was almost completely sensitive to cyanide. This inactivation at 410C was reversible. After incubation at 410C, the alternative oxidase capacity measured at 250C was the similar to when it was measured at that temperature directly. Isolated mitochondria lost alternative oxidase capacity at the same rate when incubated at 410C as they did when incubated at 250C. Increasing the supply of electrons to isolated mitochondria increased the degree of engagement of the alternative pathway, whereas lower temperature decreased the degree of engagement. Lower temperatures did not increase the degree of engagement of the pathway in intact tissues. We interpret these observations to indicate that the greater capacity of alternative oxidase in cold-grown seedlings is a consequence of development at these low temperatures which results in elevated respiration rates. Low temperature itself does not cause greater capacity or engagement of the alternative oxidase in mitochondria that have developed under warm temperatures. Our hypothesis would be that the low growth temperatures require the seedlings to have a higher respiration rate for some reason, e.g., to prevent the accumulation of a toxic metabolite, and that the alternative pathway functions in that respiration.

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Section: Discussionmentioning

confidence: 99%

“…Several reports have appeared which indicate that Valt' is higher in plants grown at low temperatures (10-15C) compared to plants grown at near optimal temperatures (25-30°C) (7,12,17,19,21). Winter wheat varieties have a greater alternative respiratory capacity than do spring varieties (11).…”

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confidence: 99%

Respiration and Alternative Oxidase in Corn Seedling Tissues during Germination at Different Temperatures

Stewart¹,

Martin²,

Reding³

et al. 1990

Plant Physiol.

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“…A few papers have attempted to relate the alternative respiratory process to low temperature growth in crop plants (7, 9, 11, 16, 18), calli (8, 20), and arctic plants (12,13). Compared to capacity in tissues grown at optimal temperature, it appears that any given plant tissue will have a greater alternative respiratory capacity when grown at temperatures near the lower limit of growth.…”

Section: Introductionmentioning

confidence: 99%

Seedling Growth, Mitochondrial Characteristics, and Alternative Respiratory Capacity of Corn Genotypes Differing in Cold Tolerance

Stewart

Martin²,

Reding³

et al. 1990

Plant Physiol.

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Four maize (Zea mays L.) inbreds representing genetic differences in seedling cold tolerance were used to determine the effect of growth temperatures on dry weight accumulation and mitochondrial properties, especially the altemative oxidase capacity. Seedlings were grown in darkness at 30°C (constant), 140C (constant), and 150C for 16 hours and 80C for 8 hours. lnbreds B73 and B49 were characterized as cold tolerant while G50 and G84 were cold sensitive. Shoot growth rate of coldsensitive inbreds in the lower temperatures was slower relative to the tolerant inbreds. Mesocotyl tissue was particularly sensitive to low temperatures during growth after germination. There were no significant differences in relative rates of mitochondrial respiration in the cold-tolerant compared to cold-sensitive inbreds measured at 25°C. Mitochondria from all seedlings grown at all temperatures had the ability to phosphorylate as indicated by the observation of respiratory control. This result indicated that differences in low temperature growth were probably not related to mitochondrial function at low temperatures. Altemative oxidase capacity was higher in mitochondria from seedlings of all inbreds grown at 14°C compared to 300C. Capacities in seedlings of 14°C-grown B73 and G50 were higher than in B49 and G84. Capacities in seedlings grown for 16 hours at 150C and 8 hours at 80C were similar to those from 14°C-grown except in G50 which was lower and similar to those grown at 30°C. Mesocotyl tissue was the most responsive tissue to low growth temperature. Coleoptile plus leaf tissue responded similarly but contained lower capacities. Antibody probing of westem blots of mitochondrial proteins confirmed that differences in altemative oxidase capacities were due to differences in levels of the altemative oxidase protein. Male sterile lines of B73 were also grown under the three different temperature regimes. These lines grew equally as well as the normal B73 at all temperatures and the response of alternative oxidase capacity and protein to low growth temperature was similar to normal B73.Germination and early seedling growth are major determinants of stand establishment. Thus, these developmental events are particularly important for commercial production of maize (Zea mays L.). Recent trends in agronomic practices have been to plant maize earlier in the spring to take advantage of more optimal summer rainfall and temperatures and to avoid hot, dry periods during pollination and fertilization. A second recent trend in agronomic practice has been toward various forms of conservation tillage. These practices result in slower warming of soils in the early spring compared to more extensive tillage, particularly that done in the previous fall. Thus, physiological characteristics that improve germination and early seedling growth at low temperatures are increasingly of interest to maize producers (10).The capacity and activity of the mitochondrial alternative oxidase in plants has been associated with growth at low seedling becaus...

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“…Although a role for alternative respiration in resistance to low temperature was suggested at least 20 years ago (Bakumenko, 1974;Knutson, 1974), the prevailing view is that the amount of heat produced is too small to be significant (McNulty and Cummins, 1987). Although most plants, with the notable exception of thermogenic plants, clearly do not produce enough metabolic heat to raise the temperature of bulk tissue, respiratory heat may have a pronounced local effect at the subcellular level.…”

Section: Discussionmentioning

confidence: 99%

“…Chilling-sensitive plants show a respiratory burst when returned to normal temperature after exposure to low temperature, and this often involves an increase in the cyanideinsensitive alternative respiratory pathway (Kiener and Bramlage, 1981;Elthon et al, 1986;McNulty and Cummins, 1987;Rychter et al, 1988;Stewart et al, 1990a). The alternative pathway found in vascular plants, algae, fungi, and some protists bypasses the second and third energy conservation sites of the Cyt pathway and directly dissipates energy as heat (Henry and Nyns, 1975).…”

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confidence: 99%

Chilling-Induced Heat Evolution in Plants

1995

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lncreases in respiration, particularly via the alternative pathway, are observed in response to chilling. These increases result in increased heat evolution. We have measured increases in heat evolution in response to chilling in a number of plant species using a microcalorimeter. After 8 h of exposure to 8"C, heat evolution in a variety of chilling-sensitive species increased 47 to 98%. No increase in heat evolution was seen with the extremely chillingsensitive ornamental Episcia cupreafa Hook. Heat evolution increased only 7 to 22% in the chilling-resistant species. lncreases in heat evolution were observed when plants were chilled in constant light or in the dark, but not when plants were chilled at high humidity. lncreased capacity to produce respiratory heat after exposure to chilling temperatures may contribute to the cold-acclimation process.Even within their normal habitat most plants are exposed to temperature changes, including diurna1 and seasonal changes, that can limit respiration, photosynthesis, and growth. Plants can be divided into severa1 categories on the basis of their sensitivity to low temperatures (Lyons, 1973). Chilling-resistant plants show little injury even at temperatures near 0°C. Chilling-sensitive plants are injured or killed by temperatures above freezing, typically showing signs of injury at temperatures from 5 to 15°C. Some chilling-sensitive plants can be hardened, i.e. they exhibit increased resistance to chilling stress after exposure to intermediate temperatures. A few extremely chillingsensitive plants, including ornamentals from the genus Episcia (Wilson, 1979), are severely injured by temperatures as high as 10°C and do not show hardening.Chilling-sensitive plants show a respiratory burst when returned to normal temperature after exposure to low temperature, and this often involves an increase in the cyanideinsensitive alternative respiratory pathway (Kiener and Bramlage, 1981; Elthon et al., 1986;McNulty and Cummins, 1987; Rychter et al., 1988;Stewart et al., 1990a). The alternative pathway found in vascular plants, algae, fungi, and some protists bypasses the second and third energy conservation sites of the Cyt pathway and directly dissipates energy as heat (Henry and Nyns, 1975). In a few special cases heat evolution by the alternative pathway serves a (Meeuse, 1975). However, the function of the alternative pathway in nonthermogenic plants is poorly understood. Salicylic acid, which is the trigger for the increase in alternative oxidase and heat evolution in the voodoo lily (Raskin et al., 1987), also increases alternative oxidase, alternative respiration, and heat production in tobacco suspension cultures (Kapulnik et al., 1992;Rhoads and McIntosh, 1993). These results suggest that the difference between thermogenic plants and others may be quantitative rather than qualitative.We showed previously that microcalorimetry can be used to detect chilling-induced increases in respiratory heat evolution in cucumber (Cucumis sativus L.) (Ordentlich et al., 1991). The incr...

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The relationship between respiration and temperature in leaves of the arctic plant Saxifraga cernua

Cited by 68 publications

References 21 publications

Respiration and Alternative Oxidase in Corn Seedling Tissues during Germination at Different Temperatures

Respiration and Alternative Oxidase in Corn Seedling Tissues during Germination at Different Temperatures

Seedling Growth, Mitochondrial Characteristics, and Alternative Respiratory Capacity of Corn Genotypes Differing in Cold Tolerance

Chilling-Induced Heat Evolution in Plants

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