Background

The air pollutant ozone is toxic to plants and occurs at sufficiently high concentrations in many parts of the country to cause visible symptoms of injury and to suppress the growth of many common crops. Ozone is a secondary pollutant that forms from nitrogen oxides and hydrocarbons that originate mostly in populated and industrialized areas, but can be transported hundreds of miles before reacting to form ozone. Some of the most productive agricultural areas in the U.S. are exposed to elevated ozone, and concentrations in rural areas are projected to increase. Data on emissions of precursors and their reaction in the atmosphere to form ozone and its subsequent transport in the atmosphere, as well as measurement of ambient ozone concentrations nationally, are readily available from other agencies such as EPA and NOAA.

Tropospheric ozone, that is, ozone occurring in that part of the atmosphere that is within 7 to 10 miles of the earth=s surface, disrupts processes that can significantly suppress photosynthesis of many plant species. It can cause significant yield losses in common crops such as soybean, cotton, and wheat. Estimates indicate ozone-induced yield losses at current concentrations ranging from negligible to approximately 20% or more in some areas, depending on the crop species and environmental conditions during plant growth and exposure.

Plants grown in elevated ozone exhibit extensive biochemical and physiological differences from plants grown at lower concentrations. For example, ozone induces common wound and defense responses. In some cases, compounds are increased that may protect the plants from further ozone-induced injury. Changes in the chemical composition of ozone-stressed plants may affect plant-pest interactions and nutrient cycling from decomposing plant debris as well. Exposure of plants to ozone can alter the extent of infestation by insect pests. Thus, biochemical changes induced in plants by these gases may have impacts on crop systems beyond direct effects on growth. Estimates of the impact of greenhouse gases on agriculture will be inaccurate unless such effects on noncrop organisms and their interactions with crop plants are considered.

Plant response to ozone is controlled genetically. Species and genotypes (cultivars, clones) within a species may exhibit a range of responses. Capitalizing on this genetic variability is one possible way to minimize the negative impacts of ozone on crop production. To incorporate these traits efficiently into crops that are otherwise desirable agronomically, the biochemical and physiological attributes that confer these traits must be determined. Collections of plants exist (e.g., snap bean genotypes and white clover clones) that exhibit a wide range in response to ozone; these will be useful as model systems for such studies. This research will contribute to development of genotypes with improved performance under ozone polluted conditions.

Effects of ozone on plant growth and biochemistry are well-documented, but impacts of this gas on crop production systems in the future currently cannot be predicted with a high degree of confidence. Uncertainties are due to the complexity of interactions among plants, gas concentrations, environmental conditions, and noncrop organisms. Studies of these interactions are at an early stage, but an improved understanding of the effects of the gases in combination and in interaction with other factors in crop systems is required before the net effect on agricultural commodities in the U.S. can be defined.

This research meets a national need for developing agricultural management strategies to respond to atmospheric change. Ozone concentrations in the atmosphere will continue to increase in the foreseeable future. Cost-effective approaches to mitigate negative effects of this gas are not currently available, and economically feasible management options need to be identified. These options are most likely to be identified by developing a thorough understanding of the plant physiological mechanisms of response, establishing the genetic/biochemical basis of stress resistance, and determining the relevant interactions of the gas effects with environment and noncrop organisms. Ozone toxicity resembles oxidative stresses caused by other environmental phenomena of importance to agriculture, such as chilling, high light intensity, herbicides, pathogens, and other pollutants. Thus, the knowledge gained from this work will have a broader application than for ozone pollution alone.

This research will show the degree of impact on agricultural production to be expected from changes in air quality and thus will indicate the level of response needed to ameliorate the effects. The agricultural community, including federal and state extension personnel, the Economic Research Service (ERS), growers, cooperating scientists, and the scientific community are users of the research results. Plant production industries are recognizing increasingly that atmospheric contaminants affect their products. Results of this research will continue to benefit regulatory and action agencies and policymakers. The Federal Clean Air Act (Sections 108 and 109) requires the periodic evaluation of data on air quality effects on public welfare (Secondary Standard) for setting National Ambient Air Quality Standards. This research will respond to that mandate by providing the best available information on ozone effects on crops.

This research also will be a major source of information used by EPA to develop the criteria document 'Air Quality Criteria for Ozone and Related Photochemical Oxidants.' This document is required to evaluate and set the National Ambient Air Quality Standards for protection of public health and welfare from adverse effects of photochemical oxidants. Recent meetingswith EPA staff indicated a continuing need for expanded and updated data for ozone effects on crops. Furthermore, the research will contribute to the information base needed to assess national and international policies for control of anthropogenic emissions.

Vision

Quality crop production free of limitations caused by tropospheric ozone

Mission

Identify ozone-tolerant crop species and varieties, response mechanisms to select or develop tolerant varieties, and production methods that minimize ozone-induced limitations on crop production and quality; and develop science-based information required for sound policy and regulatory decisions.

Table 5. ARS Research Locations Contributing to Component IV of the Air Quality National Program--Ozone Impacts

Component Problem Areas
State	Locations	Effects of Ozone on Yield & Product Quality	Mechanisms of Ozone Response	Ozone- Tolerant Crop Plants	Effects of Ozone on Pests & Parasites
MD	Beltsville		X	X
NC	Raleigh	X	X	X	X

Problem Statement

Rationale.  Because of the wide-ranging movement of ozone precursors from urbanized areas and their subsequent combination to form ozone, the problem of ozone impacts on crops is not limited to urbanized areas or to any particular part of the country. Some of the most productive agricultural areas in the eastern and midwestern parts of the U.S. are exposed to elevated ozone, in addition to the well known ozone problems in California and elsewhere. Tropospheric ozone concentrations have increased appreciably over the past 50 years. Concentrations in many areas of the U.S. are now approximately twice as high as would exist without the influence of human activities, and ozone concentrations in rural areas are projected to increase. The adverse effect of ozone on agriculture has national and international ramifications because it directly increases production costs of food and fiber, which are passed on to the consumer. In addition, tropospheric ozone adversely affects food quality and nutrition, environmental quality, biodiversity, and the atmosphere as a natural resource.

What is known.  Visible symptoms of ozone injury to plants vary in severity among species, but may consist of decreased chlorophyll, increased pigmentation, and areas of dead plant tissue. Unfortunately, these symptoms often are not distinguishable from symptoms caused by pathogens, nutrient deficiencies, or other stresses. Often, the only visible feature of ozone stress is more rapid senescence (tissue death) toward the end of the life cycle, especially with annual plants, which is noticeable only when directly compared to nonstressed plants. Field experiments with open-top chambers have shown that ambient ozone concentrations suppress the growth and yield of major crops in productive agricultural areas of the country. Agronomic crops such as soybean, cotton, peanut, and some wheat cultivars are generally sensitive to ozone. Corn and sorghum are less sensitive although there is variability in ozone sensitivity among cultivars of the same crop. Estimates of ozone-induced yield losses nationally are variable, but limited data indicate that ozone causes substantial economic losses through reduction of crop yields. The extent of loss varies not only with the ozone sensitivity of individual crops, but also highly depends on environmental conditions during plant growth and exposure. For example, plants tend to be more sensitive to injury when grown and exposed under conditions of high humidity; whereas they are less sensitive under drought and elevated atmospheric carbon dioxide. In general, detrimental effects of ozone are on crop yield although minor changes in product quality have been reported. Visible injury and suppressed growth also diminish the economic value of some horticultural and ornamental crops.

Gaps.  Although limited data are available from field studies concerning ozone effects on yield and/or quality of major crops (e.g., soybean, corn, cotton, peanut, rice, wheat, sorghum), not all economically important crops have been tested. For those crops that have been studied, too few cultivars or varieties were evaluated to estimate risks to production with confidence. Furthermore, there are insufficient data on those cultivars currently used in production agriculture, and too little is known about their genetic variability in ozone sensitivity. There is a serious shortage of data on horticultural crops (food and ornamentals), which often are ozone sensitive and are very important economically. In addition, experiments to date have not been conducted under a sufficient range of climates to understand the effects of variable environmental factors on the quantification of ozone impacts. Effects of environmental variables such as temperature, relative humidity, rainfall, solar radiation, and soil properties are particularly important with the rise in atmospheric carbon dioxide concentrations and the associated changes in global climate that may occur. Ozone exposure patterns vary to some extent both geographically and year-to-year. The degree to which these variations affect plant response are not well understood. The capability to extrapolate data across years and climates is currently limited, and data are needed to develop plant growth process models and statistical models for extrapolation and prediction. Techniques and tools for experimentation and assessment need further development.

Goals

• Determine impacts of ozone on yield and quality of major crops, including variation among cultivars within species;
• Determine environmental influences on crop response to ozone; and
• Improve ability to predict ozone effects on crop production under future climate/management scenarios

Approach

This research should emphasize experiments in field plots with plants grown from germination through maturity while exposed to appropriate ozone concentrations and exposure regimes. Experiments in greenhouses and growth chambers should be conducted with supplemental light that approximates the quality and intensity of full sunlight. Typically, open-top field chambers or similar facilities will be used to control and manipulate ozone concentrations around test plants. This approach permits the experimental pollutant-exposure treatments to be defined, allowing dose-response analysis within and across years. Use of existing ambient ozone gradients, open-air treatments (similar to those used in free-air carbon dioxide enrichment studies) or chemical ozone protectants should be considered when there are distinct experimental advantages.

Plant response to ozone varies across locations and years, and therefore gas exposure concentrations should encompass a wide range. Ozone exposure regimes should be similar to those found in ambient air (i.e., simulate daily peaks and episodic nature of ambient ozone concentrations). Plant cultivars, soil variables, or other factors can be included as additional variables, as appropriate. Environmental data such as temperature, rainfall, humidity, and irradiation should be routinely recorded throughout the experiments. Prominent cultivars of economically important agronomic and horticultural species should be used unless the specific research needs dictate otherwise. Emphasis for each crop species should be on cultivars or genotypes that represent current and, as much as known, future farming practices.

Statistical dose-response models will be developed to estimate effects of ranges of ozone concentrations on yield. The experimental data, however, will represent only a small fraction of the air pollutant/climate scenarios that may be encountered. Therefore when possible, associated physiological and growth data should be used to develop mechanistic simulation models of crop growth and yield that incorporate response to ozone stress.

Outcomes

• Data will be available to determine the economic costs of ozone pollution to crop production.
• The future effects of ozone on crop production in a changing climate will be predictable.
• A scientific basis will be provided to choose among management options to limit ozone impacts on crop production.

Impact

Informed decisions by agricultural producers and regulatory and policymakers to minimize ozone impacts on agricultural production, agribusiness, and the public.

Linkages to Other ARS National Programs

• Global Change
• Integrated Agricultural Systems
• Plant Diseases

Problem Statement

Rationale. In many crops, current tropospheric ozone levels inhibit photosynthesis, alter plant structure and development, and suppress biomass and yield. Such effects are mediated by numerous metabolic pathways through which plants produce energy and carry on other activities. However, these pathways remain either unknown or only partially described. This is partly due to the current state of plant science research, which is just beginning to integrate plant biology from the molecular to the organismal level. Extension of these research efforts toward defining the mechanisms of ozone toxicity are required to understand the adverse effects of ozone on plants. Biological impairment by ozone needs further clarification if we are to provide the information needed to counteract its adverse effects.

What is known.  The mechanisms of ozone action involve both toxicity and responses that counteract, perpetuate, or even exacerbate effects of ozone exposure. In addition, some plant responses to ozone might have no role at all in counteracting ozone stress.

Plants take up ozone primarily through their leaves, a process largely influenced by physiological and environmental factors (carbon dioxide concentration, humidity, light, temperature, nutrient and water availability). The complex processes of metabolism following ozone uptake are thought to include decreasing the amount of carbon available for plant growth by suppressing photosynthesis and by stimulating the need for carbon in maintenance and repair processes. In addition, translocation of carbohydrates from leaves to shoot and roots is inhibited by ozone injury. In this respect, carbohydrate metabolism and allocation are important links between carbon dioxide fixation and biomass production. Analysis of carbohydrate pools and plant structure can be a valuable tool in identifying the sensitive steps in plant metabolism that reveal the mechanisms of ozone injury.

In concert with plant responses to ozone injury per se, a number of genetic responses are induced by exposure to ozone. The responses described so far involve photosynthesis, antioxidant and secondary metabolism, pathogen-defense responses, and senescence-related processes. Some of these responses correspond to defense reactions to oxidative stress. In addition, ozone induces several genetic pathways associated with senescence processes, and there are indications that ozone provokes programmed cell death.

Gaps.  A comprehensive understanding of ozone impairment of plant growth and development is lacking. This includes physiological and environmental factors controlling ozone uptake. An integrated understanding of direct and indirect effects of ozone on plant mechanisms and processes, including photosynthesis, ion regulation, carbohydrate, lipid and nitrogen metabolism, water relations, phloem loading, and biomass allocation needs to be developed from the molecular to the organismal level. The significance of ozone-induced changes in antioxidant metabolism, pathogen defense responses, and secondary metabolism needs to be assessed. How senescence processes, especially ethylene production, are induced and interact with ozone needs to be investigated. Many recent studies on photosynthesis, carbohydrate metabolism, and molecular biology have been done with woody plants and model plant systems. These findings should be addressed for applicability to herbaceous crop plants.

Goals

• Improve understanding of physiological processes and environmental factors controlling ozone uptake in crop plants;
• Determine effects of ozone on carbohydrate and nitrogen metabolic pathways;
• Expand our knowledge of genes induced by ozone and their adaptive significance;
• Characterize ozone-induced senescence processes and programmed cell death; and
• Link genetic markers to adaptive physiological traits for ozone resistance.

Approach

A multidisciplinary approach will be used to assess direct and indirect effects of ozone on the quality and quantity of seed and forage crops. Treatment facilities include indoor and outdoor controlled environment chambers, greenhouse chambers, and open-top field chambers. Experiments using model plants and crop plants will be conducted. Experts in molecular biology, plant physiology, and biochemistry will cooperate to measure and assess plant responses to ozone.

Outcomes

• Mechanisms of ozone toxicity will be defined for various crop plants and cropping systems and the information used to counteract adverse effects of ozone exposure.
• Biochemical and molecular markers will be identified that detect ozone stress when visible symptoms are absent or inconclusive.

Impact

A sustainable crop production system that minimizes adverse effects of tropospheric ozone pollution.

Linkages to Other ARS National Programs

• Global Change
• Plant Biological and Molecular Processes
• Plant Microbial and Insect Genetic Resources, Genomics, and Genetic Improvement

Problem Statement

Rationale.  Tropospheric ozone concentrations can inhibit plant growth and yield in many agricultural regions. One management strategy is to utilize ozone-tolerant varieties that perform well in high ozone environments, yet maintain yield and quality in years when ozone impact is minimal. To implement such a strategy, information is needed on the range of ozone sensitivity within cultivars of major crops. For certain crops, available cultivars may not express sufficient ozone tolerance to maintain high levels of productivity under current or future ozone levels. Therefore, new varieties are needed with enhanced ozone tolerance.

What is known.  Plants are known to exhibit a range of ozone sensitivity in terms of visible injury and yield reduction, including significant variation among genotypes or clones of the same species. Presumably, genetic variation represents differences in capacity to express one or more tolerance mechanisms. Studies to date have identified three aspects of plant physiology that determine the impact of ozone stress on plant growth. First, ozone entry into the plant is primarily via leaf stomata, so stomatal processes that limit ozone uptake could ameliorate the effect of ozone stress. However, reduced stomatal conductance also could negatively affect plant growth through reduction of carbon dioxide and water vapor gas exchange, although tolerance to drought might be improved. Second, ozone injury can be minimized or prevented by metabolic pathways that detoxify ozone and the reactive oxygen species formed from ozone. Finally, once ozone injury has been initiated, metabolic responses are induced that replace damaged cellular constituents (e.g., lipids and proteins) or alter whole plant development patterns (e.g., accelerated senescence). There also is evidence that plant responses to ozone share common features with responses to other environmental stresses (e.g., pathogen infection, chilling, drought stress), so that new knowledge about plant tolerance to other stress factors may provide insights into ozone tolerance and vice versa.

Gaps.  Although current knowledge can suggest future research efforts, no definitive ozone tolerance mechanisms have been characterized. Specific mechanisms must be identified, and an understanding is needed of how multiple mechanisms combine to produce the ozone tolerance associated with a particular genotype. The distinctions between injury prevention versus repair processes need to be clarified. Initiation of ozone injury induces a localized or general response that may permanently alter the growth and yield potential of the plant, so mechanisms that prevent injury may have greater impact than mechanisms related to cellular repair.

Evidence suggests that a range of ozone sensitivity exists within each species, but information on ozone-sensitive and tolerant cultivars is not available for each major crop. Knowledge and methodology must be developed to allow rapid selection of ozone-tolerant varieties from available germplasm.

Goals

• Identify specific aspects of physiology and metabolism that distinguish ozone-sensitive and ozone-tolerant plants;
• Formulate strategies based on genetic manipulation of key metabolic pathways that will increase yield potential under elevated ozone environments; and
• Identify ozone-sensitive and -tolerant cultivars within existing germplasm of major crop species.

Approach

Controlled environment facilities and open-top chambers will be used to conduct mechanistic studies and to screen available germplasm under a range of ozone concentrations. Ozone-sensitive and ozone-tolerant genotypes from the same species will be compared to identify biochemical and physiological characteristics that contribute to ozone tolerance. Mutants of model plants will be utilized as a tool to provide insights into tolerance mechanisms not yet recognized. Plants with known tolerance to pathogens or to stresses such as chilling and drought will be tested for cross-tolerance against ozone as an alternative approach for mechanism identification. Specific enzymes or physiological markers with the potential to affect ozone tolerance will be identified and this information used to produce plants for further testing and to develop new methods for rapidly screening germplasm.

Outcomes

• Fundamental knowledge of ozone tolerance will be developed that can be used to produce plants with enhanced performance under elevated ozone environments.
• The potential impact of ozone on crop production and quality will be demonstrated to growers, extension agents, and others.
• Ranking of modern cultivars for ozone-sensitivity will allow growers in areas of high ozone to select ozone-tolerant varieties that are compatible with current farming practices.

Impact

Crop productivity and quality maintained or improved in agricultural areas subjected to elevated tropospheric ozone.

Linkages to Other ARS National Programs

• Global Change
• Integrated Agricultural Systems
• Plant Biological and Molecular Processes

Problem Statement

Rationale.  Relationships between plants and their pests and pathogens are delicately balanced. Plants possess intricate defense mechanisms, whereas pests and pathogens possess elaborate strategies to cope with plant defenses. Any factor that upsets normal plant metabolism can affect plant defenses and threaten overall plant health. For the first time in human history, anthropogenic emissions have resulted in tropospheric ozone concentrations high enough to disrupt plant metabolism and cause the ozone-induced injuries noted earlier, which result in suppressed growth and yield. It is not surprising that this relatively sudden change in earth=s air quality also has affected interactions between plants, pests, and pathogens. Research to unravel effects of tropospheric ozone on pests and pathogens of agricultural crops has been fragmented and sporadic. Plant stress caused by ozone can increase, decrease, or have no effect on pests and pathogens, but mechanisms to explain these responses are unknown. Ozone-induced increases in pest and pathogen populations would further suppress crop yield and increase pesticide use. Increased use of pesticides would threaten environmental quality. Data are required to estimate the environmental and economic impact of such changes.

What is known.  Reports of stimulatory responses of insects feeding on plants exposed to air pollutants predominate over reports of inhibitory responses. Early investigations in Europe showed that growth rate and degree of infestation of various aphid species often were greater on plants in nonfiltered urban air than in charcoal-filtered air although two aphid species were inhibited by nonfiltered air. Specific atmospheric components responsible for effects attributed to nonfiltered air in European reports were not identified, but evidence from later experiments with specific pollutants indicates that ozone is a prime candidate. Various stimulatory responses (increased feeding, faster development, better survival) have been reported for larvae of several leaf-chewing insects when host plants were exposed to ozone. Populations of the two-spotted spider mite on white clover and peanut increased faster on plants exposed to ambient concentrations of ozone than on plants exposed to lower concentrations of ozone. Increased fecundity and shorter development time caused this increase in mite populations.

Our present knowledge of pollutant effects on plant disease stems largely from short-term experiments performed mostly in the greenhouse or laboratory, dealing with only one stage in the parasite cycle. Studies with diseases caused by fungi have predominated over diseases caused by other organisms. Foliar diseases have been studied more than diseases of other plant organs.

It is generally agreed that effects of ozone on pests and pathogens are mediated mostly through effects on host plant physiology. Effects on plant concentrations of carbohydrates, nitrogen compounds, or metabolites that may be directly involved in plant defense often have been cited as possible indirect mechanisms.

Gaps.  Effects of tropospheric ozone have been studied for only a small percentage of important pests and diseases. Most research has involved short-term exposure to one or two relatively high pollutant concentrations to measure effects on individual life stages. Studies employing long-term exposure to a wide range of pollutant concentrations allowing measures of changes in multiple life stages and population dynamics are rare. Most research has been performed in greenhouse or environmentally controlled exposure systems. Few studies have been performed in systems under near-ambient environmental conditions. Changes in host plants that may account for observed effects on pests or disease include changes in host suitability as a food source and increases or decreases in metabolites that may be involved in defense mechanisms or host attractiveness. However, pollutant-induced changes in specific host nutrients or specific metabolites have not been proven as cause for pest or disease response. Recent reports show that carbon dioxide enrichment can prevent ozone stress in many crops. Other soil-related and climatic factors also can alter plant response to ozone. Effects of carbon dioxide enrichment and other environmental factors on pest or pathogen response to ozone have not been adequately addressed.

Goals

• Determine effects of chronic ozone exposure of plants on multiple life stages and population dynamics for representative agricultural pests and pathogens;
• Identify ozone-induced changes in plant chemistry that control pest infestation; and
• Estimate effects of observed responses on crop yield and pesticide use.

Approach

Experimental ozone exposures will be performed in controlled environments, greenhouses, or open-top field chambers. Exposures will be chronic, mimic real-world exposure dynamics, and span the range of concentrations that occur in the troposphere at various locations throughout the world. Exposures will be performed before, during, and after pests or disease organisms are introduced to host plants. Temperature, rainfall, humidity, and solar radiation will be routinely recorded throughout the experiments to examine possible influence of these factors on measured responses.

Economically important pests and parasites will be selected for study, and host plants with variable degrees of tolerance to ozone will be used when possible. Measurements of individual and multiple life stages will be made to allow estimates of long-term effects on population dynamics. Measures of ozone effects on plant biochemistry will be made to identify mechanisms of pest and parasite responses. Effects of carbon dioxide enrichment and other factors such as temperature or soil nutrition on pest or pathogen response to ozone will be included as experimental variables when appropriate to increase extrapolation of results to a wider range of environments

Outcomes

• Estimates will be developed for risks to crop production from ozone-induced effects on pests and diseases.
• Ozone-induced changes in pesticide use caused by ozone impact on pests and disease will be assessed.

Impact

Minimal adverse effects on crops caused by ozone influence on plant pests and diseases and

improved regulatory and policy decisions to minimize ozone effects on agriculture

Linkages to Other ARS National Programs

• Global Change
• Integrated Agricultural Systems
• Plant Biological and Molecular Processes
• Plant Diseases
• Plant Microbial and Insect Genetic Resources, Genomics, and Genetic Improvement