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CO-OCCURRING STRESS: DROUGHT Mel Tyree Department of Botany University of Vermont Burlington, VT 05405 ABSTRACT Drought stress always restricts the growth of trees. The immediate factor most influencing growth response to drought is turgor pressure which is the force causing plastic enlargement of cells, leaves ant} stems. Reduced shoot and leaf growth in one dry season can reduce the vigor and growth potential of trees for several subsequent years. Net assimilation of carbohydrates is also reduced by drought through its effect on stomata! closure, increased cliffusional resistance to CO2 transport in mesophyll cells, reduction of electron flow in photosystem I and II and disruption of enzyme activity, thereby reducing the dark reactions of photosynthesis (1~. Reduction in carbohydrate reserves can cause loss of frost hardiness and subsequent stem die-back (2~. Winter dehydration can also be a very important cause of stem die-back, a symptomatology normally associated with forest decline. Winter dehydration and consequent stem embolism can reduce the capacity of small stems to conduct water by more than 80% (3~. Models indicate that during a growth season a loss of water conductivity greater than 20% can cause mid-day stomata! closure or catastrophic xylem dysfunction (4~. Although mechanisms are normally in place to reverse embolism prior to bud break, anthropogenic stresses could interfere with these mechanisms, thus leading to crown die-back. Water deficits influence all types and phases of tree growth, and always in a restrictive way. Kramer (1980) estimates that water deficits probably limit tree growth more than the effects of all other causes combined. In arid areas up to 90% of the annual variation in xylem production of conifers has been attributed to water deficits (Zahner, 1968~; in humid areas drought accounts for up to 80%. However, in temperate climates a broad mix of microenvironmental factors can determine the growth pattern of individual trees (Cook, 1987~. Drought stress alone or in combination with other This paper is intended to provide a brief introduction to some of the relevant literature regarding drought stress, and is specifically designed to point out decline syndromes caused by drought that may be confused with causes derived from atmospheric pollutants. 1987~. Drought stress alone or in combination environmental stresses can contribute to forest decline. This paper is The mediating factor most often influencing the growth response of trees to drought is turgor pressure, because it is the force causing plastic enlargement of cell walls and vegetative growth (Hsiao et al., 1976; Bradford and Hsiao, 1982; Tyree and Jarvis, 1982~. High turgor pressure is needed to cause sufficient enlargement for cells to reach the critical size for division (Doley and Leyton, 1968~. It is presumed that a minimum turgor pressure is required to permit such enlargement; low turgor will also 357

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358 reduce growth of developing tissues after cell division. Drought may affect both primary and secondary growth and the effects of a brief drought period can retard growth for years to come as outlined below. During primary growth, cell division at the apical meristem and the subsequent elongation of newly formed cells results in the formation of leaf bud primordia. Water deficits may affect the formation of leaf buds and/or the subsequent elongation of preformed leaf buds in conifers. Clements (1969) showed that the number of needle fascicles on new shoots, shoot length and fascicle spacing were correlated with the size of the bud formed the previous year. The bud size in turn depended on the level of moisture stress at the time it was formed (Kramer and Kozlowski, 1960; Lotan and Zahner, 1963~. Drought reduces both shoot growth and needle production and the resulting reduction in leaf area may have significant effects on photosynthesis and growth for years to come. Needles persist for many years in most conifers, so poor growth in one year will have a lasting depressive impact on growth and vigor for the life of the needles. Secondary growth involves three stages: (a) cambial division, (b) cell enlargement and (c) maturation where walls increase in thickness. Five requirements for cambial activity and wood formation have been identified by Kramer ~ 1964) and all but the first are influenced by drought: (1 ~ a temperature appropriate to a high level of metabolic activity, (2) a supply of growth regulators, (3) a supply of carbohydrates and nitrogen containing substances, (4) a supply of mineral nutrients and (5) sufficient water to maintain high turgor in the cells. Kennedy (1961) related high production of earlywood in Douglas fir to years of high rainfall and low temperatures in spring. Earlywood production in irrigated trees will not cease until September (Zahner et al., 1964~. The development of the small, thick-walled latewood cells appears to require moisture deficits (Zahner, 1963, 1968~. False growth rings (i.e., two or more alternating bands [earlywood-latewood] occurring within one growing season) are caused by drought early in the growth season followed by adequate moisture. At times of low moisture availability, cells spend longer times in the zone of maturation and less time in the zone of enlargement than earlier in the spring, and this accounts for the characteristic form of latewood (Whitmore and Zahner, 1966~. Water availability can also directly affect the rate of carbon fixation in two ways: 1 ~ via stomata! limitation of photosynthesis and (2) biochemical limitations of photosynthesis. Stomatal closure in response to decreasing water availability has commonly been thought to be the major contributor to reductions in photosynthesis through its restriction on carbon dioxide uptake. But photosynthesis may also decline independently of stomata! closure in response to the same factors that cause stomata! closure (Farquhar and Sharkey, 1982~. Water stress may act to reduce photosynthesis by (1) causing stomata! closure and thereby increasing the diffusional resistance to carbon dioxide uptake, (2) reducing chloroplast activity and electron flow in the light reactions of photosynthesis or (3) disrupting enzyme activity and thereby reducing the dark reactions of photosynthesis. Correlations among photosynthesis, transpiration and leaf conductance have often been interpreted to mean that the effect of water stress on photosynthesis is controlled mainly by stomata! closure (Brix, 1962; Boyer, 1976; Beadle and Jarvis, 1977~. But it is now known that drought can directly reduce electron transport in photosystems I and II (Boyer, 1976; Keck and Boyer, 1974~. Kaiser (1982) has recently demonstrated that reductions in photosynthesis during water stress were correlated with changes in total protoplast volume of leaf tissue in a variety of species. A possible mechanism for this

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359 correlation is apparently tier! to the effect of volume changes on concentration changes of K+ and H+, which affect activities of key enzymes like bisphosphatase (FBP) and RUBP carboxylase (see Berkowitz et al., 1983 and related work from his lab). All of the above effects of drought, e.g., reduced stem growth, reduced leaf production and reduced photosynthesis, can lead to reduction in carbohydrate reserves and general tree vigor. These effects can be compounded to result in loss of frost hardiness in winter and a common syndrome associated with tree dieback, i.e., death of minor branches due to frost damage (Gregory et al., 1987~. Drought in some conifers (e.g., spruce and some firs) can also cause immediate needle loss (the Christmas tree syndrome). An important mechanism by which stem dieback and general decline can occur is by stem embolism during the growth season and from winter dehydration. Since these mechanisms have not been reported until very recently, the rest of this paper will be devoted to explaining the events that lead to embolism and the consequences of it. Trees are hydraulically designed to confine most of the water stress to minor branches. This is the basis of the "segmentations hypothesis (see below) first proposed by Zimmermann. He formulated this hypothesis during his classical study of the "hydraulic architecture" of trees (Zimmermann, 1978~. Generally the minor branches of all trees are 10 to 1000 times less capable of supplying water to their leaves than the boles of trees. In minor branches the water potential gradients are 10 to 1000 times greater than in the bole to overcome the larger hydraulic resistance per unit area of leaves fed by the stem (Zimmermann, 1 97S, Tyree et al., 1983; Ewers and Zimmermann, 1984a,b; Sperry, 1986~. An important consequence of this hydraulic architecture is that the hydraulic resistance to water flow from the ground level to all minor branches is approximately the same for all twigs whether the twig is located near the base of a crown and at the end of a short hydraulic path or at the top of a crown and at the end of a long hydraulic path. All shoots are approximately equally capable of competing for the water resources of the tree (Tyree et al., 1988~. The segmentation hypothesis proposes that trees are hydraulically designed to confine embolism to minor branches. Embolism is the presence of air-filled (embolized) tracheids and vessels, and it can represent a substantial impairment of xylem transport. Environmental causes of embolism include water stress and winter freezing; potential consequences include reduction of growth and dieback. Water stress leads to embolism via the process of "cavitation," the breaking of water continuity in xylem conduits subject to negative pressures arising from static effects (dry or frozen soil) and dynamic effects (transpiration). The immediate result of a cavitation is a lumen filled with water vapor and some air. Eventually the lumen becomes fully embolized when more air comes out of solution to fill the void left by the cavitation event. Winter freezing causes embolism by a variety of mechanisms including sublimation, expansion (after thaw) of air bubbles formed by freezing xylem sap, and cavitation in water-stressed trees rooted in frozen soil. We have recently obtained support for the segmentation hypothesis from modeling studies based on the water relations and hydraulic architecture of a number of woody plants from diverse taxa and environments (Tyree, 1988; Tyree and Sperry, 1988~. In these papers we discussed the relationship between dynamically changing tension gradients required to move water rapidly through the xylem conduits of plants and the proportion of conduits lost through embolism as a result of water tension. Tyree and Sperry (1988) compiled quantitative data on the water relations, hydraulic architecture

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360 and vulnerability to embolism of four widely different species: Rhizophora mangle, a salt excluding tropical mangrove, Rhizophoraceae, Cassipourea elliptica, a tropical moist-forest Rhizophoraceae, Acer saccharum, a temperate dicot, and Thuja occidentalis, a temperate gymnosperm. Using these data, we modeled the dynamics of water flow and xylem blockage for these species. The model is specifically focused on the conditions required to generate Runaway embolism, whereby the blockage of xylem conduits through embolism leads to reduced hydraulic conductance causing increased tension in the remaining vessels anti generating more tension in a vicious circle. For this reason we specified the transpiration rate rather than building stomata! regulation into the model. There were great differences among these species in hydraulic architectures, maximum transpiration rates, specific hydraulic conductances of stem tissue, and water relations. Despite these differences the model predicted for all species that: ( 1 ) embolism occurs more in minor than in major branches (thus supporting the segmentation hypothesis); (2) xylem tensions could lead to 5 to 30% loss of hydraulic conductance in minor shoots (depending on species) and still maintain a stable state; (3) if embolism causes more than 5 to 30% loss of transport capacity, then runaway embolism occurs leading to catastrophic xylem dysfunction (blockage) in a patch-work fashion throughout the crown; (4) after catastrophic failure of selected minor branches, there is an improved water balance (less negative y') of surviving minor branches due to leaf loss from dead shoots. The model predicted that all species operate near the point of catastrophic xylem failure due to dynamic water stress. The implication of these results and models is that xylem structure and vulnerability to embolism places important constraints on the water relations, morphology, and physiology of trees. Specifically the model shows that stomata! regulation and xylem physiology must function and evolve as an integrated unit in order to prevent catastrophic dysfunction. Trees must also evolve mechanisms to keep an appropriate balance for carbon allocation between leaves which increase evaporative demand and stems which supply the demand for water evaporated from leaves. It is rare to find individual trees that suffer significant leaf loss due to drought. This is presumably because stomates close and reduce evaporative flux before catastrophic xylem dysfunction and leaf loss. But progressive minor amounts of embolism presumably cannot be reversed during the growth season in trees. And as embolism increases, then minor branches will maintain lower stomata! conductances for longer periods of the day especially during times of high evaporative demands. Since embolisms are not easily reversible, the effects of drought can be more or less permanent during any one growth season. But summer embolism and embolism from winter dehydration may be reversible in spring. To our knowledge, our study of sugar maple (Sperry et al., 1988) is the only one in which the natural incidence of xylem embolism has been systematically quantified over the longterm. We studied 5-8-year-old saplings as well as forest trees from May 1986 to July 1987. During the growth season embolism in minor branches grew enough to reduce the hydraulic conductance of stems by 10 to 30%. According to our model this is enough to begin causing partial stomata! closure during periods of high evaporative demand. In winter, however, very extensive embolism occurred. In February embolism was enough to reduce hydraulic conductance by 69% in stems 1 to 3 cm diameter and by 84 to 100% in minor branches. Perfusion of 0. 1% safranin dye though main-axis segments revealed that embolism was localized on the southern sides of the trunk. Partly embolized twigs also showed one-sided embolism.

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361 This embolism was primarily due to dehydration on sunny cold days in January and February. Beginning with the March measurement, embolism gradually declined until June 1987, when it was not significantly higher than the previous year. In some trees this recovery occurred over a very short period in response to positive stem pressures that dissolved air bubbles to make the vessels functional again. We do not believe that maple could be unusual in its susceptibility to winter dehydration. Presumably conifers will dehydrate just as much if not more and mechanisms must be in place to reverse this presumed embolism. Our models show that without embolism reversal the stems would be hydraulically incapable of supplying water to the foliage attached to it. Without reversal there would be stem and leaf dieback--a syndrome that would be difficult to distinguish from other causes of dieback. We have begun studies to look at these underlying biological processes. We have not ruled out the possibility that the mechanism of damage by anthropogenic stresses might be that it inhibits or otherwise damages mechanisms in place to reverse natural winter embolism. Measurement of water potential parameters or embolism alone could not be used as markers for air pollution effects. However, many of the symptoms of drought stress might be confused with pollution induced decline syndromes, e.g., reduced leaf size, reduced leaf area, reduced bole diameter growth, reduced shoot elongation and stem dieback. For this reason it may be advisable to measure water relations parameters before ascribing a cause-and-effect relationship between decline and air pollution levels. REFERENCES Beadle, C.L., and P.G. Jarvis. 1977. Effects of shoot water status on some photosynthetic partial processes in Sitka Spruce. Physiol. Plant 41: 7-13. Berkowitz, G.A., C. Chen, and M. Gibbs. 1983. Stromal acidification mediates in viva water stress inhibition of nonstomatal-controlled photosynthesis. Plant Physiol. 72: 1123-1126. Boyer, ].S. 1976. Water deficits and photosynthesis. Pp. 154-191 in Kozlowski, T.T. (ed.), Water deficits and plant growth. Vol. 4, Academic Press, New York. Bradford, K.J., and T.S. Hsiao. 1982. Physiological responses to moderate water stress. P. 263 in Encyclopedia of Plant Physiology NS, Vol. 12b, Springer-Verlag, Berlin, Heidelberg, New York. Brix, H. 1962. Effects of water stress on the rates of photosynthesis and respiration in tomato plants and loblolly pine seedlings. Physiol. Plant 15:10-20. Clements, J.R. 1969. Shoot responses of young red pine to watering applied over two seasons. Can. J. Bot. 48:75-86. Cook, E.R. 1987. The use and limitations of dendrochonology in studying effects of air pollution on forests. Pp. 277-240 in Hutchinson, T.C., and Meema, K.M. (eds), Effects of Atmospheric Pollutants on Forests, Wetlands and Agricultural Ecosystems. Springer-Verlag, New York.

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362 Doley, D., and L. Leyton. 1968. Effects of growth regulating substances and water potential on the development of secondary xylem in Fraxinus. New Phytologist 67: 579-594. Ewers, F.W., and M.H. Zimmermann. 1984ae The hydraulic architecture of balsam fir (Abies balsamea). Physiol. Plant. 60: 453-458. Ewers, F.W., and M.H. Zimmermann. 1984b. The hydraulic architecture of eastern hemlock (Tsuga canadensis). Can. J. Bot. 62:940-946. Farquhar, G.D., and T.D. Sharkey. 1982. Stomatal conductance and photosynthesis. Ann. Rev. Plant Physiol. 33:317-345. Gregory, R.A., M.W. Williams, J. Donnelly, and M.T. Tyree. 1987. The effects of stress factors on carbohydrate reserves, cold acclimation, and dieback in sugar maple. Pp. 186- 191 in NAPAP Terrestrial Effects Task Group V. Session C, Tree Physiology. NAPAP, Washington, DC. Hsiao, T.C., E. Acevedo, E. Fereres, and D.W. Henderson. 1976. Water stress, growth, and osmotic adjustment. Phil. Trans. R. Soc. Lond B 273: 479-500. Kaiser, W.M. 1982. Correlation between changes in photosynthetic activity and changes in total protoplast volume in leaf tissue from hygro-, meso-, and xerophytes under osmotic stress. Planta 154: 538-545. Keck, R.W., and J.S. Boyer. 1974. Chloroplast response to low leaf water potentials. III. Differing inhibition of electron transport and photophosphorylation. Plant Physiol. 53: 474-479. Kennedy, R.W. 1961. Variation and periodicity of summer wood in some second growth Douglas fir. TAPPI 44: 161-166. Kramer, P.J. 1964. The role of water in wood formation. Pp. 519-532 in Zimmermann, M.H. (ed.~. The formation of wood in forest trees. Academic Press, New York. Kramer, P.J. 1980. Drought, stress and the origin of adaptations. P. 7 in Turner, N.C., and Kramer, P.~. (eds.), Adaptations of plants to water and high temperature stress. Wiley & Sons, New York. Kramer, P.J., and T.T. Kozlowski. 1960. Physiology of Trees. McGraw-Hill, New York. Lotan, J.E., and R. Zahner. 1963. Shoot and needle responses of 20-year-old red pine to current soil moisture regimes. Forest Sci. 9:497-506. Sperry, J.S. 1986. Relationship of xylem pressure potential, stomata! closure and shoot morphology in the palm Rhapis excelsa. Plant Physiol. 80:110- 116. Sperry, J.S., J. Donnelly, and M.T. Tyree. 1988. Seasonal occurrence of xylem embolism in sugar maple (Acer saccharum). Amer. J. Bot. In press. Tyree, M.T. 1988. A dynamic model for water flow in a single tree. Tree Physiol. In press.

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361 This embolism was primarily due to dehydration on sunny cold days in January and February. Beginning with the March measurement, embolism gradually declined until June 1987, when it was not significantly higher than the previous year. In some trees this recovery occurred over a very short period in response to positive stem pressures that dissolved air bubbles to make the vessels functional again. We do not believe that maple could be unusual in its susceptibility to winter dehydration. Presumably conifers will dehydrate just as much if not more and mechanisms must be in place to reverse this presumed embolism. Our models show that without embolism reversal the stems would be hydraulically incapable of supplying water to the foliage attached to it. Without reversal there would be stem and leaf dieback--a syndrome that would be difficult to distinguish from other causes of dieback. We have begun studies to look at these underlying biological processes. We have not ruled out the possibility that the mechanism of damage by anthropogenic stresses might be that it inhibits or otherwise damages mechanisms in place to reverse natural winter embolism. Measurement of water potential parameters or embolism alone could not be used as markers for air pollution effects. However, many of the symptoms of drought stress might be confused with pollution induced decline syndromes, e.g., reduced leaf size, reduced leaf area, reduced bole diameter growth, reduced shoot elongation and stem dieback. For this reason it may be advisable to measure water relations parameters before ascribing a cause-and-effect relationship between decline and air pollution levels. REFERENCES Beadle, C.L., and P.G. Jarvis. 1977. Effects of shoot water status on some photosynthetic partial processes in Sitka Spruce. Physiol. Plant 41: 7-13. Berkowitz, G.A., C. Chen, and M. Gibbs. 1983. Stromal acidification mediates in viva water stress inhibition of nonstomatal-controlled photosynthesis. Plant Physiol. 72: 1123-1126. Boyer, ].S. 1976. Water deficits and photosynthesis. Pp. 154-191 in Kozlowski, T.T. (ed.), Water deficits and plant growth. Vol. 4, Academic Press, New York. Bradford, K.J., and T.S. Hsiao. 1982. Physiological responses to moderate water stress. P. 263 in Encyclopedia of Plant Physiology NS, Vol. 12b, Springer-Verlag, Berlin, Heidelberg, New York. Brix, H. 1962. Effects of water stress on the rates of photosynthesis and respiration in tomato plants and loblolly pine seedlings. Physiol. Plant 15:10-20. Clements, J.R. 1969. Shoot responses of young red pine to watering applied over two seasons. Can. J. Bot. 48:75-86. Cook, E.R. 1987. The use and limitations of dendrochonology in studying effects of air pollution on forests. Pp. 277-240 in Hutchinson, T.C., and Meema, K.M. (eds), Effects of Atmospheric Pollutants on Forests, Wetlands and Agricultural Ecosystems. Springer-Verlag, New York.