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OCR for page 341
AIR POLLUTANT - LOW TEMPERATURE INTERACTIONS IN TREES
R.G. Alscher J.R. Cumming J. Fincher
Virginia Polytechnic Institute
and State University
Blacksburg, VA 24061
Boyce Thompson Institute
Ithaca, NY 14853
ABSTRACT
Boyce Thompson Institute
Ithaca, NY 14X53
Evidence is accumulating to suggest a causative role for ozone
in winter injury of red spruce. This could be due to an
impairment of the winter hardening process brought about by
ozone. Hardening in conifers involves a complex series of
physiological and ultrastructural adaptations. Ozone is known to
affect both photosynthesis and carbohydrate allocation and to
stimulate antioxidant production in actively growing crop species,
but its metabolic effects on winter hardening in conifers have not
been studied. Results from a dose-response study carried out on
red spruce seedlings at Boyce Thompson Institute suggest that
ozone exposure during the summer and fall leads to changes in
carbohydrate metabolism associated with winter hardening and to
cell damage during the late fall and early winter.
Forest
a uniform
combine to
growing at high elevations are
any additional stress, such as pollutant
decline at high elevations in both Europe and North America and the lack of
causal agent have led to the suggestion that several interacting stresses
cause loss of tree vigor (Johnson and Siccama, 1983; Blank, 1985~. Trees
often
functioning at their physiological limits such that
exposure, may lead to tree mortality. In Western
Europe, data accumulated over more than a decade in Finland indicate that conifers
growing around industrial areas are more susceptible to winter injury in comparison to
trees from relatively unpolluted environments (Huttenen et al., 1981; Huttenen and
Soikkeli, 1984~. This pattern suggests that industrial pollutants are in some way altering
cold tolerance of trees. Winter injury of declining trees has repeatedly been reported in
the case of the German forests, and ozone has explicitly been proposed to play a central
role in the decline phenomenon (Rehfuess, 1987~. In the United States, extensive
evidence has been assembled for a change in the response of red spruce to temperature
at high elevations over the past 20 years at Whiteface Mountain, NY, in the Adirondack
Mountain Range. This change was found to be correlated in time with increased
incidence of tree decline (Johnson et al., l9X6, 1987~.
Recent data directly implicate ozone as a causative agent in decreased winter
hardiness of spruce. An interaction between ozone and cold temperatures leading to
visible injury has been reported in Norway spruce (Brown et al., 1987; Barnes and
Davison, 1987~. Several clones that had experienced high ozone concentrations during
the summer exhibited uniform browning and abscission of older year class needles. This
pattern contrasts with decline symptoms in North America but is consistent with observed
damage in Europe. In addition, clonal variation in response to ozone and cold
temperature exposure suggests that there is a strong genetic component to resistance, the
physiological basis of which is unknown.
341
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342
The mechanisms) by which ozone caused this pattern of injury are not understood.
Some hypotheses may be formulated, however, through the synthesis of what is known
concerning metabolic effects of ozone, changes that underlie the winter hardening
process, and physiological responses to cold temperatures.
Ozone may impair plant metabolism through the formation of toxic free radicals in
viva. Free radicals are metabolically neutralized through the action of a variety of
antioxidants, which remove free radicals and their toxic by-products. Antioxidant
compounds such as glutathione and SOD are produced in greater quantities by plant cells
in response to oxidative stress (Lee and Bennett, 1982) and represent one possible
resistance mechanism which may vary both within and among tree species. Mehlhorn et
al. (1986) demonstrated increases in the levels of GSH and alpha-tocopherol in needles
of spruce and fir as a consequence of long-term, low-level exposures to ozone. Only
when the protective capacities of these mechanisms are overwhelmed will injury, such as
lipid peroxidation, occur (Halliwell, 1981; Heath, 1987~.
The winter hardening process in conifers involves a series of orchestrated
physiological, histological, and biochemical events that prepare cells for exposure to cold
temperatures. Among these are reductions in photosynthesis, increased hydrolysis of
starch to form soluble sugars (Aronsson et al., 1976), an accumulation of antioxidants
(Esterbauer and Grill, 1978), and vast ultrastructural changes (Soikkeli, 1978) as trees
enter dormancy. The conversion of starch to soluble sugars in leaf tissue represents one
mechanism by which plant cells increase their tolerance to freezing temperatures.
Oligosaccharides such as sucrose and raffinose are known to protect membranes against
the dehydrative effects of freezing (Quinn and Williams, 1985~. Raffinose in particular
has been implicated as a cryoprotectant in Norway spruce.
In spite of these changes in the cellular environment, damage due to cold
temperatures does occur. Under conditions of relatively high light and low temperature,
excess light is absorbed by antennae pigments. Reduced electron transport capacity of
dormant tissue impairs the transfer of reductant to acceptors such as NADP (Oquist,
1982, 1983, 1986~. Instead, molecular oxygen will serve as an electron acceptor and
consequently will be reduced to superoxide in the Mehler reaction. The photoscavenging
cycle will act to remove the superoxide and attendant molecular species, and antioxidant
compounds will be consumed in the course of this process. If- it continues beyond the
limit of antioxidant capacity, the oxidation of labile components such as photosynthetic
pigments will follow. Oxidation of this kind does in fact occur. For example,
photobleaching of up to half of the total chlorophyll content of Scots pine has been
reported to occur under natural conditions in northern Sweden in early spring (Oquist,
1986~. Shade needles show less bleaching than do needles in full sun, as would be
expected from the mechanism of injury involved.
Increased photo-oxidation of chlorophyll, as well as other free radical injury that
occurs at low temperatures and high light in conifers, may be observed under conditions
where free radicals are being, or have been, generated by an air pollutant such as ozone.
This damage may be due to the exhaustion of antioxidant mechanisms of plant cells
brought about by the joint stress of ozone during the growing and/or hardening season
and by low temperatures, which occur during the winter months. During the winter,
when de novo production of antioxidants may be low, plants that have been previously
depleted of antioxidant reserves by ozone may incur damage when protective and repair
mechanisms are insufficient to protect tissue further from cold injury.
We have biochemical and histological evidence that ozone exposure both altered
winter hardening processes and increased cellular damage during early winter frosts of
OCR for page 343
343
red spruce seedlings. Four-year-old seedlings were exposed to charcoal filtered air or to
doses of ozone ranging from ambient to 4X ambient in Ithaca, NY during the summer and
fall of 1987. In December there were no visible symptoms on any of the current year
foliage. However, histological examination of these needles showed that there was
damage to mesophyll cells in needles exposed to ozone. This damage included
vesiculation, and at its most extreme involved total disruption of cells with breakage of
cell walls and leakage of contents into intercellular spaces. In needles with patches of
damage, nearby cells appeared to be undergoing the normal transition, characterized by
alterations of chloroplasts, lack of starch, and increased tannin in vacuoles. Disruption
of this nature was not seen earlier in the season prior to freezing temperatures.
An examination of the patterns of seasonal changes in carbohydrate levels in the
seedlings revealed that exposure to ozone also resulted in a shift in the time course for
starch mobilization in the late summer and fall. Early frost susceptibility and winter
dieback of ozone-treated spruce foliage was observed by Amundson and Cumming
(unpublished). Interacting influences on cold tolerance in conifers of growth regulating
substances, oxidative stress, and seasonal cycling in response to environmental cues
remain to be understood. The combined influences on winter hardening in conifers of
growth regulating substances and oxidative stress remain to be elucidated.
SUMMARY AND DISCUSSION: METABOLIC ~THRESHOLDS" FOR STRESS
We have accumulated biochemical, physiological, and histological data suggesting that
exposure to ozone increases the susceptibility of red spruce foliage to cold temperatures.
The patterns can be fit into a scenario where prior exposure to ozone overloads the
cell's antioxidant resistance mechanisms past some critical level or "threshold," beyond
which the cells can no longer tolerate the processes associated with exposure to low
temperatures, e.g., free radical production. Were this threshold to be established
experimentally, it might be possible to use it as an indicator or "marker" of air pollution
stress on coniferous forest tress. It is important to keep in mind that a concept such as
this is useful only when implemented with discretion. A tree that is severely stressed
with respect to nutrition or water will most probably have a lower threshold for the
additional stress of oxidizing air pollutants than one which is not. As a consequence,
the need for further research to establish the impact of interacting stresses on the
physiology and metabolism of forest trees should be apparent.
Oxidative pollutant and cold temperature stresses may further interact if changes in
the timing of physiological events associated with the hardening process occur because of
pollutant exposure and such alterations increase the susceptibility of foliage directly.
Alternatively, these changes could influence the period of time during which the foliage
is vulnerable to cold temperatures. Again, further experimentation is required before any
evaluation of these various possibilities can be made.
REFERENCES
Aronsson, A., T. Ingestad, and L. Lars-Gorau.
. .. . . . . ~ .
1976. Carbohydrate metabolism and frost
naralness In pine and spruce seeollogs at different photoperiods and thermoperiods.
Physiol. Plant. 36:127-132.
Barnes, J.D., and A.W. Davison. 1987. The influence of ozone on the winter hardiness of
Norway spruce (Picea abies L.~. New Phytol. 108: 159-166.
OCR for page 344
344
Blank, L.W. 1985. A new type of forest decline in Germany. Nature. 314: 311-314.
Brown, K.A., T.M. Roberts, and L.W. Blank. 1987. Interaction between ozone and cold
sensitivity in Norway spruce: a factor contributing to the forest decline in Central
Europe? New Phytol. 105: 149-155.
Esterbauer, H., and D. Grill. 1978. Seasonal variation of glutathione and glutathione
reductase in needles of Picea abies. Plant Physiol. 61: 1 19-121.
Heath, R.L. 1987. Biochemistry of ozone attack on the plasma membrane of plant cells.
Rec. Adv. in Phytochem. 21: 29-54.
Huttunen, S., L. Karenlampi, and K. Kolari. 1981. Changes in osmotic potential and
some related physiological variables in needles of polluted Norway spruce (Picea
abies). Ann. Bot. Fennici. 18: 63-71.
Huttunen, S., and S. Soikkeli. 1984. Pp. 117-128 in Gaseous Air Pollutants and Plant
Metabolism (Koziol, M.J., Whatley, F.R., eds.) Botany School, University of Oxford,
Oxford, UK.
Johnson, A.H., and T.G. Siccama. 1983. Acid deposition and forest decline. Environ. Sci.
Technology 17: 294a-305a.
Johnson, A.H., A.~. Friedland, and J. Dushoff. 1986. Recent and historic red spruce
mortality: Evidence of climatic influence. Water Air Soil Pollut. 30: 319-330.
Johnson, A.H., E.R. Cook, and T.G. Siccama. 1988. Relationships between climate and
red spruce growth and decline. Proc. Nat. Acad. Sci. (in press).
Lee, E.H., and J.H. Bennett. 1982. Superoxide dismutase. A possible protective enzyme
against ozone injury in snap beans (Phaseolus vulgaris L.~. Plant Physiol. 69: 1444-
1449.
Mehlhorn, H., G. Seufert, A. Schmidt, and K.J. Kunert. 1986. Effect of SO2 and O3 on
production of antioxidants in conifers. Plant Physiol. 82: 336-338.
Oquist, G. 1982. Seasonally induced changes in Acyl lipids and fatty acids of
chloroplast thylakoids of Pinus silvestris. Plant Physiol. 69: 869-875.
Oquist, G. 1983. Effects of low temperature on photosynthesis. Plant, Cell and Environ.
6: 281-300.
Oquist, G. 1986. Effects of winter stress on chlorophyll organization and function in
Scots pine. J. Plant Physiol. 122: 169-179.
Quinn, P.J., and W.P. Williams. 1985. Pp. 1-48 in Photosynthetic Mechanisms and the
Environment (Barber, J. and Baker, N.R. eds.) Vol. 6. Amsterdam, New York and
Oxford.
Rehfuess, K.E. 1987. Perceptions on forest diseases in Central Europe.
Forestry. 60~1~: 1-11.
OCR for page 345
345
Soikkeli, S. 1978. Seasonal changes in mesophyll ultrastructure of needles of Norway
spruce (Picea abies). Can. J. Bot. 56: 1932-1940.
OCR for page 346
344
Blank, L.W. 1985. A new type of forest decline in Germany. Nature. 314: 311-314.
Brown, K.A., T.M. Roberts, and L.W. Blank. 1987. Interaction between ozone and cold
sensitivity in Norway spruce: a factor contributing to the forest decline in Central
Europe? New Phytol. 105: 149-155.
Esterbauer, H., and D. Grill. 1978. Seasonal variation of glutathione and glutathione
reductase in needles of Picea abies. Plant Physiol. 61: 1 19-121.
Heath, R.L. 1987. Biochemistry of ozone attack on the plasma membrane of plant cells.
Rec. Adv. in Phytochem. 21: 29-54.
Huttunen, S., L. Karenlampi, and K. Kolari. 1981. Changes in osmotic potential and
some related physiological variables in needles of polluted Norway spruce (Picea
abies). Ann. Bot. Fennici. 18: 63-71.
Huttunen, S., and S. Soikkeli. 1984. Pp. 117-128 in Gaseous Air Pollutants and Plant
Metabolism (Koziol, M.J., Whatley, F.R., eds.) Botany School, University of Oxford,
Oxford, UK.
Johnson, A.H., and T.G. Siccama. 1983. Acid deposition and forest decline. Environ. Sci.
Technology 17: 294a-305a.
Johnson, A.H., A.~. Friedland, and J. Dushoff. 1986. Recent and historic red spruce
mortality: Evidence of climatic influence. Water Air Soil Pollut. 30: 319-330.
Johnson, A.H., E.R. Cook, and T.G. Siccama. 1988. Relationships between climate and
red spruce growth and decline. Proc. Nat. Acad. Sci. (in press).
Lee, E.H., and J.H. Bennett. 1982. Superoxide dismutase. A possible protective enzyme
against ozone injury in snap beans (Phaseolus vulgaris L.~. Plant Physiol. 69: 1444-
1449.
Mehlhorn, H., G. Seufert, A. Schmidt, and K.J. Kunert. 1986. Effect of SO2 and O3 on
production of antioxidants in conifers. Plant Physiol. 82: 336-338.
Oquist, G. 1982. Seasonally induced changes in Acyl lipids and fatty acids of
chloroplast thylakoids of Pinus silvestris. Plant Physiol. 69: 869-875.
Oquist, G. 1983. Effects of low temperature on photosynthesis. Plant, Cell and Environ.
6: 281-300.
Oquist, G. 1986. Effects of winter stress on chlorophyll organization and function in
Scots pine. J. Plant Physiol. 122: 169-179.
Quinn, P.J., and W.P. Williams. 1985. Pp. 1-48 in Photosynthetic Mechanisms and the
Environment (Barber, J. and Baker, N.R. eds.) Vol. 6. Amsterdam, New York and
Oxford.
Rehfuess, K.E. 1987. Perceptions on forest diseases in Central Europe.
Forestry. 60~1~: 1-11.
Representative terms from entire chapter:
winter hardening
