Mycorrhizal mediation of plant response to atmospheric change: Air quality concepts and research considerations

Environmental Pollution 73 (1991) 163-177

Mycorrhizal Mediation of Plant Response to Atmospheric Change: Air Quality Concepts and Research Considerations S. R. Shafer USDA--ARS Air Quality Program, North Carolina State University, Raleigh, North Carolina 27695, USA

& M. M. Schoeneberger* USDA--Forest Service, Southeastern Forest Experiment Station, PO Box 12254, Research Triangle Park, North Carolina 27709, USA

A BSTRA CT The term 'global climate change' encompasses many physical and chemical changes in the atmosphere that have been induced by anthropogenic pollutants. Increases in concentrations of COz and CH4 enhance the 'greenhouse effect' of the atmosphere and may contribute to changes in temperature and precipitation patterns at the earth's surface. Nitrogen oxides and S02 are phytotoxic and also react with other pollutants to produce other phytotoxins in the troposphere such as 03 and acidic substances. However, release of chlorofluorocarbons into the atmosphere may cause depletion of stratospheric 03, increasing the transmittance of ultraviolet-B ( UV-B) radiation to the earth's surface. Increased intensities of UV-B could affect plants and enhance photochemical reactions that generate some phytotoxic pollutants. The role of mycorrhizae in plant responses to such stresses has received little attention. Although plans for several research programs have acknowledged the importance of drought tolerance and soil fertility in plant responses to atmospheric stresses, mycorrhizae are rarely targeted to receive specific investigation. Most vascular land plants form mycorrhizae, so the role of mycorrhizae in mediating plant responses to atmospheric change may be an important consideration in predicting effects of atmospheric changes on plants in managed and natural ecosystems. * Present address: Rocky Mountains Forest and Range Experiment Station, Forestry Sciences Laboratory, East Campus, University of Nebraska, Lincoln, Nebraska 68583, USA. 163

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INTRODUCTION By-products of human activities since the onset of the Industrial Revolution have caused inadvertent changes to the earth. Pollution of soil, water, and air has economic, social, and ecological consequences. The magnitude of these changes, however, are beginning to be realized as we face the possibility that chemical changes we have made in the earth's atmosphere may be altering the physical aspects of climate on the global scale. Combustion of fossil fuels in power generation, industry, and transportation releases gases into the atmosphere. Processes related to agriculture and land use, such as decomposition of animal wastes in large-scale livestock operations, paddy rice culture, and deforestation also release some of these and other gases, which contribute to the 'greenhouse effect' (Table 1) to an extent that may alter the balance among the physical and biological processes that control climate. In considering the occurrence of human-induced global climate change, three factors are widely accepted in the scientific community (World Resources Institute, 1990): (1) The 'greenhouse effect' of the gases is real. The infrared absorbing properties are well characterized and are responsible for maintaining the average temperature of the globe at 13°C, which is 33°C above that which would occur otherwise. (2) The concentrations of the gases are increasing at an unprecedented rate. Carbon dioxide (CO2) probably contributes more than any other gas to the warming effect (Table 1). The current TABLE 1 C o n t r i b u t i o n s to G l o b a l W a r m i n g b y G r e e n h o u s e G a s e s a n d H u m a n A c t i v i t y a

Sector

Energy Direct Indirect Deforestation Agriculture Industry % Warming by gas

% Warming by sector

Gasb C02

CH4

03

N2O

CFC

35 -10 3 2 50

3 1 4 8 -16

--~ 6 --2 8

4 --2 -6

----20 20

49 14 13 24

100

a T a b l e 2.4 i n W o r l d R e s o u r c e s I n s t i t u t e (1990). b Carbon dioxide, methane, ozone, nitrogen dioxide, and chlorofluorocarbons, respectively. c Not available.

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concentration of C O 2 in the atmosphere (350 ppm) will double by the year 2075 if the current rate of increase continues unchanged. (3) Changes in the concentrations of these gases have matched changes in global climate in the past. Based on ice cores, trends in atmospheric CO2 and temperature have been parallel over the last 160 000 years. Beyond these three considerations, scientific consensus ends. Whether the changes induced by human activities will cause significant changes in temperature and precipitation patterns, and what the magnitudes and implications of such changes might be, are subjects of intense debate. Although the primary cause of presumed climate change--increased concentrations of infrared-absorbing gases in the atmosphere--seems simple enough, major uncertainties in the magnitude of this are introduced by feedback mechanisms that could enhance or suppress the warming effect. Uncertainties include the extent to which thermal inertia of the oceans would buffer temperature increases; the role of oceans in absorbing increased CO 2 from the air; the role of oceans in mediating energy distribution around the globe; the net effect of increased photosynthetic carbon fixation (which increases for many plant species as available CO2 increases) versus increased release of CO2 by microorganisms that decompose organic matter, which could be stimulated by the hypothetical increases in temperature; and the role of clouds and water vapor in contributing to or ameliorating the 'greenhouse effect' (World Resources Institute, 1990). Such uncertainties have led to alternate conclusions that increases in atmospheric CO2 could have little effect on global climate (e.g. Idso, 1983, 1988). In the absence of real-time experiments to determine the potential for global climate change, several general circulation models (GCM) that describe atmospheric behavior have been used to estimate certain changes that might occur in the earth's climate with increased concentrations of the greenhouse gases (see Smith & Tirpak, 1989). Although doubling of atmospheric CO2 from pre-industrial levels is not expected until the year 2075 at the current rate of increase, the net influence of the increase in the collection of gases involved may produce an equivalent change by 2030 because some of the gases absorb more infrared than CO2 (see below). Thus, when the rates of increase of all these gases are considered, the net equivalent of doubling of CO2 may occur by 2030 (Adams et al., 1990). Depending on the GCM used to prepare the estimate, the effect of this would increase the average global temperature by 2.8-5.2°C and increase global precipitation by 7.1 to 15.8% (Smith & Tirpak, 1989). However, none of the estimates for temperature and precipitation changes

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provided by the GCM are currently corrected for the uncertainties stated above. Thus, these estimated magnitudes of temperature and precipitation changes that might occur are subject to debate. Moreover, changes in the geographic distribution of precipitation could result in increased precipitation in some areas and recurring droughts in others. If net increases in temperature and changes in precipitation patterns over the globe occur, effects on agricultural, forestry, and range lands could follow. Unfortunately, although the GCM show some promise for predicting temperature and precipitation changes on a global or even continental scale, the resolution is so low that predictions for sub-continental regions are questionable (Smith & Tirpak, 1989). Thus, effects of global climate change on natural and agro-ecosystems within specific regions are extremely uncertain. Whether or not yields of agricultural crops in a specific region would increase or decrease would depend upon a balance of growth stimulation by increased CO2 available for photosynthesis; the increase in demand of mineral nutrients from the soil that would accompany increased growth of plants; the impact of a temperature increase on the specific crops of that region; the type (increase or decrease) and magnitude of changes in precipitation for the region; and the net influence of the climate change on the interactions among pests, pathogens, weeds, air pollutants, and other stresses that can limit crop production. Moreover, if substantial changes occur, the types of crops that could be grown in specific regions might change, requiring new approaches to farming in the area. Climate, topography, and soil type are the main factors in determining the distribution of forest types. Changes in climate presumably would induce changes in the locations that are optimum for various forest tree species. However, forest trees are long-lived and disperse slowly. If the rate of dispersal does not match the rate with which the optimum location moves, some species may become increasingly rare or extinct. Other minimally or unmanaged plant communities could also change as the species composition shifts to those plants that are tolerant of the changes in temperature, precipitation, and pest/pathogen conditions. If climate change occurs to the extent that natural and managed plant systems are impacted, plant interactions with mycorrhizal fungi probably will be affected. The major contributors to, and byproducts of, global climate change and their relevance to mycorrhizae can be summarized as follows. Carbon dioxide (COz) Carbon dioxide is a 'greenhouse gas' of major concern. The primary anthropogenic sources are the burning of fossil fuels and deforestation (including biomass burning and loss of photosynthetic area). Major

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increases in atmospheric C O 2 concentration since industrialization probably contribute to global warming and changes in spatial and temporal distribution of precipitation more than any other pollutant (Table l). From 1860 to 1987, the estimated total release of CO2 from human activities is 241 billion tonnes, including 60 billion tonnes released from land use changes, such as deforestation (World Resources Institute, 1990). Rising CO2 concentrations are relevant to considerations in the biology of mycorrhizal associations for several reasons. Temperature and drought stress (or increases in precipitation) could lead to changes in plant species distribution and community structure. For example, a shift from coniferous forest to grasslands implies a change in the predominant types of symbiont from ectomycorrhizal fungi to arbuscular mycorrhizal fungi (Vosatka et al., 1991). Even if the plant community structure remains stable, changing moisture and temperature conditions in the soil might cause selection pressure toward different species of fungi present, and those new species could be more or less efficient in providing the nutrient benefits typical of the mycorrhizae. Furthermore, CO2 causes physiological changes in plants. These include alterations in photosynthesis, biomass accumulation, and C allocation within plants (thus altering C availability to microorganisms within and around roots) (e.g. Huber et al., 1984; Kimball et al., 1984; Rogers et al., 1984); water use efficiency (Huber et al., 1984; Kimball et al., 1985; Rogers et al., 1984); and demand for nutrients from the soil (Cure, 1985). Changes in photosynthesis and C allocation imply changes in source-sink relationships for carbon within the plant, having major implications for mycorrhizal fungi (Reid et aL, 1983; Harris & Paul, 1987; McCool, 1988; Dighton & Jansen,1991). Furthermore, increases in plant growth rates and nutrient demands suggest increased dependency of the host on nutrient supply from the endophytes. Carbon monoxide (CO)

Sources of CO are similar to those of C O 2. Carbon monoxide may also contribute to global warming, so the temperature and drought effects on plant---endophyte relations hypothesized for CO2 are of the same concern. Methane

(CH4)

Methane is produced by power generation and anaerobic decomposition of organic matter. Major anthropogenic sources include culture of paddy rice, decomposition of animal wastes in large-scale livestock operations, and deforestation procedures (Table 1). Methane contributes to global warming: a molecule of methane will trap 20-30 times as much

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heat as a CO 2 molecule (World Resources Institute, 1990). Thus, the temperature and precipitation effects on plant-endophyte relations hypothesized for CO2 and CO are of the same concern. Chlorofluorocarbons (CFC) These industrial chemicals are used in refrigerants, in the production of certain types of plastics, and as blowing agents in various manufacturing processes. Chlorofluorocarbons are extremely effective infrared-absorbing molecules; a CFC molecule can trap as much as 20 000 times as much infrared as a CO2 molecule (World Resources Institute, 1990). Thus, CFC contribute to global warming (Table 1) and associated changes in precipitation patterns, and the relevance to mycorrhizae is similar in some respects to CO2. However, CFC also deplete concentrations of ozone (03) in the stratosphere, allowing increased penetration of ultraviolet-B radiation (UV-B) to ground level. Concerns with 03 and UV-B are discussed below.

Nitrogen oxides (NO,,) Nitrogen oxides are produced through combustion of fossil fuels used in transportation and from agricultural fertilizers. In addition to contributing to global warming (Table 1), some of these gases are phytotoxic, causing decreased growth (Reinert, 1984). Nitrogen oxides are involved in photochemical reactions with oxygen (02) and organic aerosols to produce tropospheric ozone (O3), a strong oxidant that is phytotoxic (see below). Furthermore, in dry aerosols or after reaction with water vapour, nitrogen oxides are an important component of acid deposition. Although little evidence supports the hypothesis that acid deposition adversely affects annual crops, acid deposition may contribute to declines in forest health and productivity described in parts of Europe and the United States (Siccama et aL, 1982; Schutt & Cowling, 1985; Sheffield et aL, 1985; Chevone & Linzon, 1988) due to chronic stress of long-lived trees and impacts on soil chemistry. Changes in species composition and/or soil chemical characteristics of a specific area could result in altered predominating mycorrhizal types or species composition of mycorrhizal fungi in the area. Direct effects of acid deposition may alter plant fungus relations, but like many aspects of our knowledge of mycorrhizae, generalizations regarding mycorrhiza--acid deposition interactions are elusive (Smith, 1987). Effects reported from controlled experiments include inhibition of sporulation (Brewer & Heagle, 1983) and enhancement of metal uptake (Killham & Firestone, 1983) with endomycorrhizal associations, and variable effects on infection by ectomycorrhizal fungi,

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depending on the level of acid deposition (Shafer et al., 1985). Sulfur dioxide (SO2)

Sulfur dioxide is produced primarily by combustion of high-sulfur coal in industrial and power generating processes. Although it makes a negligible contribution to global warming, the gas is phytotoxic, causing altered carbon allocation and growth suppression (Miller, 1987). Under laboratory conditions, SO2 reduced respiration rates of two ectomycorrhizal fungi, segments of non-mycorrhizal roots of loblolly pine (Pinus taeda L.), and segments of roots infected by either fungus. Infected root segments were more resistant than non-infected segments to deleterious effects of SO2 (Garrett et al., 1982). Moreover, like NOx, SO2 is a major component of wet and dry acid depositions, which have significance for mycorrhizae as discussed above. Tropospheric ozone (03)

Ozone is a secondary pollutant created by photochemical reactions involving 02, NOx, organic aerosols, and peroxides. Ozone contributes to global warming (Table 1) and is extremely phytotoxic. It is the pollutant of major concern to crop production in the US (Heck et al., 1986). Impacts on forest tree species are also evident (Miller et al., 1982; Shafer & Heagle, 1989). A strong oxidant that damages biological membranes, 03 inhibits photosynthesis and biomass accumulation, suppresses phloem loading and reduces C allocation to roots (Heck et al., 1986; Miller 1987; Cooley & Manning, 1987). Under experimental conditions, 03 has suppressed infection of roots by an endomycorrhizal fungus (McCool et al., 1982; McCool & Menge, 1984) and suppressed sporulation (Brewer & Heagle, 1983). Effects on ectomycorrhizal relations have been varied (Garrett et al., 1982; Mahoney et al., 1985; Reich et al., 1985; Reich et al., 1986; Keane & Manning, 1988; Meier et al., 1990). Ultraviolet-B Radiation (UV-B)

As stratospheric 03 is depleted by CFC, penetration of sunlight in the wavelength range 280-320 nm to ground level increases. Paradoxically, increased penetration of UV-B into the atmosphere may enhance the photochemical reactions that produce phytotoxic 03 in the troposphere. Ultraviolet-B radiation is absorbed by proteins and nucleic acids in plants (Levitt 1980; Caldwell, 1981), and generates singlet oxygen, a strong oxidant, in cells (Beggs et al., 1986). Experimental evidence suggests that UV-B suppresses C assimilation and growth (Teramura, 1983).

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Thus, the occurrence of hypothetical change in the physical and chemical aspects of climate on a large scale has obvious implications for plant-mycorrhizal fungus relations. Scientists who study these relations face a major challenge in selecting topics for study that reflect a balance of: relevance to the magnitude of climate change characteristics that can be reasonably expected; perspective of answering questions regarding mycorrhizae within the framework of performing necessary research on other--and often more obvious--aspects of plant production and ecology in a changed environment; and technological feasibility with respect to environmental manipulation and response detection and measurement. Each of these considerations will be discussed in turn.

Relevance to the magnitude of climate change characteristics that can be reasonably expected. In experimental systems, test organisms can be exposed to conditions that exceed expectations for environmental change. Exposure of plant-soil microcosms to pollutant gases or simulated precipitation under controlled conditions is the obvious way to address questions of environmental stress, and the dose of the stressor can be enhanced beyond likely ambient levels. Such experiments have great value in defining the limits of response, examining variability of response among plants, determining physiological or biochemical mechanisms of observed whole-plant responses, examining complex interactions among stressors, and evaluating model systems for further study. Care should be taken in planning, however, so that the plant-fungus relationship can eventually be examined in the context of environmental conditions that can be reasonably anticipated. This does not imply that treatment designs should not exceed current estimations for maximum doses of the stressors. In certain types of studies, doses of a stressor that seem to exceed current limits may enhance the statistical strength of an experiment and provide predictive information for levels of the stress that exceed current levels. Dose-response treatment designs are notable examples of this, in which regression analysis defines a range of responses that can be predicted over a range of doses; estimation of responses can then be accomplished for dose levels that may not have been specifically included in the experimental design. This approach has been used successfully in field research on effects of tropospheric 03 on crops (Heck et al., 1988) and trees (Sharer & Heagle, 1989) and in greenhouse research on effects of acid deposition on formation of ectomycorrhizae (Shafer et al., 1985). Thus, although experimental designs should not be confined to 'ambient versus control' comparisons, experiments can be designed so

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that conclusions relevant to predicted levels can be reached.

Perspective of answering questions regarding mycorrhizae within the framework of performing necessary research on other aspects of plant production and ecology in a changed environment Passioura (1979) wrote that 'Plant physiologists have two responsibilities to the public whose money supports them. One is to make profound discoveries. The other is to make useful ones.' When public funds are expended on research, a high priority is understandably placed on obtaining information that benefits the public. Research priorities must be established, but much information on apparently less important subjects may be lost, Studies of mycorrhizal relations frequently fall into the 'lost' category. An illustration of this is the National Crop Loss Assessment Network (NCLAN). The N C L A N program had three objectives: to develop quantitative 03 dose-crop yield response relationships with crops grown in the field; to develop regional estimates of 03 concentrations for the major agricultural areas of the United States; and to develop economic models to estimate the impact of 03 on American agriculture. The N C L A N program was extremely successful in accomplishing these goals, and much was learned about crop responses to this important pollutant (Heck et al., 1988). In the process, the participating scientists were also able to study many aspects of plant responses to pollutants (Environ. Pollut., (1988), which includes NCLAN-related and other work). However, the primary goal of each N C L A N field experiment was to quantify effects of different doses on yield. Thus, opportunities to examine effects of 03 on root growth dynamics and mycorrhizal relations over time were in conflict with the goal because sampling for mycorrhizae would have inflicted excessive damage on the chamber-enclosed plots. Sampling at season end after the crop had produced a marketable yield would have provided only a static evaluation of a senescent plant-fungus relationship. The effort to obtain valuable information on the role of endomycorrhizae in crop systems under environmental stress (including drought, which was one variable in some N C L A N studies) was not practical in the context of that program. The importance of mycorrhizae in the growth of trees was eventually recognized in the development of research plans for the Forest Response Program (FRP), a major research program on effects of pollutants on forest resources in the US (Schroeder & Kiester, 1989). Assessment of the economic impact of pollutants on forests is a major goal of the FRP, but the perennial characteristic of trees necessitates a research emphasis on many aspects of physiology and ecology and that was not essential in

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the NCLAN program. The necessity of using mechanistic models to integrate experimental data on tree/stand growth and pollutant stress was acknowledged from the program's inception. One conceptual model used in planning FRP research specifically included aspects of root structure and function with respect to nutrient uptake, water absorption, and carbon relations with the shoot (Ford & Kiester, 1990). However, this conceptual model largely reflected the opinion that, for modeling purposes, parameters related to mycorrhizae could be considered within the overall context of the root system and viewed as a mere extension of the roots rather than as a separate entity that would incur a major expense and effort for special consideration (Grigal, 1990). Later planning reflected increased detail, however, and mycorrhizae were recognized as specific components of the plant-environment system. Although mycorrhizae received some attention in several of the research projects conducted under the auspices of the FRP, spatial and temporal sampling considerations within chamber-enclosed plots of limited size and plant populations still hindered a comprehensive effort. The question remains whether intensive studies of mycorrhizae, within the framework of large studies on plant stress, can supply information that truly enhances the understanding of ecological and economical impacts of global climate change. Others in this issue (O'Neill et ai., 1991) will address this issue in detail.

Technological feasibility with respect to environmental manipulation and response detection and measurement Manipulation of physical or chemical climate usually necessitates an enclosure of some type. Small laboratory chambers such as continuousstirred tank reactors (Heck et al., 1978) and large open-top field chambers (Heagle et al., 1973; 1989) are commonly used for exposure of plants to pollutant gases. Manipulation of the physical climate (e.g. temperature, water availability, UV-B exposure) may require chambers ranging from growth cabinets to walk-in phytotron chambers to field enclosures. In nearly all cases, however, plots are likely to be of limited size, restricting the frequency and size of the destructive samples necessary for mycorrhiza studies. Unless the biology of roots and mycorrhizae are a central focus of a study, limitations on sampling will continue to restrain research. The difficulties in controlling and measuring many aspects of the plantfungus interaction remain technologically difficult. Physiological aspects of nutrient uptake, carbon relations, and host-endophyte recognition are all phenomena that could be altered with changes in the environment

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(Reid et al., 1983; Harris & Paul, 1987). Unfortunately, these are among the most difficult aspects of the plant-fungus relationship to study. Quantitative assessments of morphology or infection levels can provide information to empirical models, and data on changes in fungal species associated with the roots can provide more valuable information on stress responses than simple quantification of mycorrhizal tips (Meier, 1991). However, information on the function of the symbiosis is needed to contribute to the more flexible, predictive mechanistic models (see Andersen & Rygiewicz, 1991). Perhaps one of the largest challenges to researchers in the field of mycorrhizae lies in identifying our own 'Medawar Zone' (Loehle, 1990), which is that range of research activity that is not so technologically difficult as to be unreachable, yet not so mundane as to have little intellectual or practical payoff. Currently, few reliable quantitative generalizations can be made about the role of mycorrhizae on individual plants, let alone communities (Read et a/.,1985; Perry et al., 1989). However, this is required for useful information on mycorrhizae in predictions of effects of atmospheric change (see Dixon & Turner, 1991; Vosatka et al., 1991).

SUMMARY The earth's atmosphere contains gases that maintain the average global temperature approximately 33°C higher than it would be otherwise. The concentrations of these and other gases have risen rapidly since the onset of the Industrial Revolution, and many--although not all--scientists believe that global climate will be altered as a result. If this occurs, major implications for agriculture, forestry, and natural ecosystems must be faced. Without fundamental alterations in industrial, power-generating, transportation, forestry, and agricultural practices, we may be unable to ameliorate the chemical and physical changes in the atmosphere. Thus, our challenge will be to understand our new environment to the best of our abilities. The role mycorrhizae in the biology of vascular plants, from the physiological level to the ecosystem level, is widely recognized. The specific role of mycorrhizae in mediating plant responses to atmospheric change remains to be determined.

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