EPA-600/3-76-031 March 1976 Ecological Research Series EFFECTS OF OZONE ON NITROGEN FIXATION IN LADINO CLOVER Environmental Research Laboratory Office of Research and Development U.S. Environmental Protection Agency Corvallis, Oregon 97330 ------- RESEARCH REPORTING SERIES Research reports of the Office of Research and Development, U.S. Environmental Protection Agency, have been grouped into five series. These five broad categories were established to facilitate further development and application of environmental technology. Elimination of traditional grouping was consciously planned to foster technology transfer and a maximum interface in related fields. The five series are: 1. Environmental Health Effects Research 2. Environmental Protection Technology 3. Ecological Research 4. Environmental Monitoring 5. Socioeconomic Environmental Studies This report has been assigned to the ECOLOGICAL RESEARCH series. This series describes research on the effects of pollution on humans, plant and animal species, and materials. Problems are assessed for their long- and short-term influences. Investigations include formation, transport, and pathway studies to determine the fate of pollutants and their effects. This work provides the technical basis for setting standards to minimize undesirable changes in living organisms in the aquatic, terrestrial, and atmospheric environments. This document is available to the public through the National Technical Informa- tion Service, Springfield, Virginia 22161. ------- EPA-600/3-76-031 March 1976 EFFECTS OF OZONE ON NITROGEN FIXATION IN LADING CLOVER Udo Blum and Michael Letchworth North Carolina State University Raleigh, North Carolina 27607 EPA-IAG-D5-0416 Project Officer Dr. L. C. Raniere Ecological Effects Research Division Corvallis Environmental Research Laboratory Con/all is, Oregon 97330 U.S. ENVIRONMENTAL PROTECTION AGENCY OFFICE OF RESEARCH AND DEVELOPMENT CORVALLIS ENVIRONMENTAL RESEARCH LABORATORY CORVALLIS, OREGON 97330 ------- DISCLAIMER This report has been reviewed by the Corvallis Environmental Research Laboratory, U.S. Environmental Protection Agency, and approved for publication. Approval does not signify that the contents necessarily reflect the views and policies of the U.S. Environmental Protection Agency, nor does mention of trade names or commercial products constitute endorsement or recommendation for use. ------- ABSTRACT Research was performed to determine the effects of ozone on ladino clover growth, nodulation, nitrogen fixation, nitrogen content, phenol content, energy value and root exudates. Plants were exposed once or twice to carbon-filtered air, 30 or 60 pphm ozone for 2 hrs. The effects of ozone on growth, nitrogen fixation, % nitrogen, total nitrogen and nodulation varied with age of plant and ozone concentration. Caloric content of tops (plants 4 weeks old when exposed) was reduced with two exposures of 30 or 60 pphm ozone. Root caloric content was not affected. Phenol content of tops and roots (plants 6 weeks old when exposed) was reduced with two 30 pphm ozone exposures. Clover exudates were not detectably modified by ozone exposure. This report was submitted for limited distribution in partial fulfillment of an Interagency Agreement by the Agricultural Research Service (ARS) under the sponsorship of the Environmental Protection Agency (EPA). The research included in the report was cooperatively sponsored by ARS, EPA and the North Carolina Agricultural Experiment Station. Work was completed as of June 30, 1975. ------- ACKNOWLEDGMENTS Parts of this research were conducted in the North Carolina State Unit of the Southeastern Plant Environment Laboratories. The help of the staff is appreciated. The assistance of Mr. Hans Hamann in statistical design and analysis is gratefully acknowledged. IV ------- CONTENTS Page Abstract iii Acknowledgements ' iv List of Figures vi List of Tables vii I Introduction 1 II Conclusions 2 III Recommendations 3 IV Experimental Work 4 V References 21 ------- LIST OF FIGURES Number Page 1 The effect of two 2-hr, ozone exposures on the top dry weight of ladino clover plants. 7 2 The effect of two 2-hr, ozone exposures on the root dry weight of ladino clover. 8 3 Changes in nodulation of ladino clover plants following two 2-hr, ozone exposures. 9 4 Effects of ozone exposures on nitrogenase activity/nodule of ladino clover. 10 5 Changes in nitrogenase activity/plant of ladino clover following ozone exposure. 11 6 Effect of two 2-hr, ozone exposures on % Nitrogen of ladino clover tops. 12 7 Effect of two 2-hr, ozone exposures on % Nitrogen of ladino clover roots. 13 8 The effect of two 2-hr, ozone exposures on the total N content of ladino clover tops. 14 9 The effect of two 2-hr, ozone exposures on the total N content of ladino clover roots. 15 10 The effect of two 2-hr, ozone exposures on the total plant nitrogen of ladino clover. 16 ------- LIST OF TABLES Number Page 1 Caloric Content, Top Dry Weight, Root Dry Weight and Nodule Number of Ladino Clover Exposed to Ozone or Carbon Filtered Air. 17 2a Phenol Content, Nitrogen Content, Top Dry Weight, Root Dry Weight and Nodule Number of Ladino Clover Exposed to Ozone and Carbon-Filtered Air. 18 2b Top Dry Weight, Root Dry Weight, Nodule Number, Nitrogen Content and Phenol Content of Ladino Clover treated with Root Exudates. 18 3 Top Dry Weight, Root Dry Weight, and Nodule Number of Ladino Clover exposed to ozone or carbon^filtered Air Grown Separately or in Combination (Design is such that plants interact only by way of root exudates). 19 4 Root Exudates vs Rhizobium 20 ------- SECTION I INTRODUCTION The research presented in this report is part of a continuing coop- erative project between the Agricultural Research Service, the Environ- mental Protection Agency and the North Carolina Agricultural Experiment Station. The title of the overall project is, "Effects, fates and trans- formations of selected air pollutants in plants, microorganisms and soils." The primary objectives of this cooperative program are to understand the impact of air pollutants on plants, microorganisms and soils that are of importance to agriculture, and to assist other agencies in relation to their mission of protecting the agricultural segment of the environment. The research thrust is directed at comparative studies on vegetation effects under phytotron, greenhouse and field conditions. Emphasis is on: (1) dose-response curves; (2) the interaction of various factors on the response of the whole plant to air pollutants; (3) assessing the impact of controlled pollutant additions and ambient pollution on plant biomass, yield and quality in the greenhouse and field, and on pollutant uptake and transformations in the greenhouse; (4) acute and chronic screens; and, (5) varietal responses. Research reported here contains, as its major thrust, part of the phytotron (controlled environment) portion of the foregoing cooperative program. It was determined that ladino clover should be intensively studied under controlled conditions. The results should then be verified under greenhouse and field conditions and using selected other plant species. Ladino clover was selected as one of the most important forage species of the Southeast. Its use is increasing, especially in conjunction with certain grass species. Ladino has chronic problems under field cultivation that are not understood - air pollution may be a factor. Ladino is a legume and thus one of the important nitrogen fixing crop species. These factors make it an ideal test species. The specific objectives for this research are given in Section IV. ------- SECTION II CONCLUSIONS Effects of ozone, on Ladino clover growth and nodulation varies with age of plant and concentration of ozone. Nitrogen content of plants exposed to 60 pphm of ozone was reduced for all exposure ages." Nitrogen content of plants exposed to 30 pphm of ozone varied with exposure age. Caloric content of tops (plants 4 weeks old when exposed) was reduced by two ozone exposures of 30 or 60 pphm. Caloric content of roots was not affected. Phenol content and nitrogen content of tops and roots (plants 6 weeks old when exposed) were reduced with two 30 pphm ozone exposures. Clover root exudates were not detectably modified by ozone exposure of clover. ------- SECTION III RECOMMENDATION(S) Present indications are that the reductions of ladino clover (a forage crop) growth, nodulation, nitrogen content, energy content, and phenol content, observed as a result of ozone exposures, are closely re- lated to plant energy fixation and plant energy allocation. The effects of ozone on energy fixation and distribution need to be explored further, The following is recommended: 1. determination of ozone effects on carbohydrate content. 2. determination of ozone effects on metabolic pathways - ie glycolysis, carbon cycle, and monophosphate shunt. 3. determination of ozone effects on translocation. ------- SECTION IV EFFECTS OF OZONE ON NITROGEN FIXATION IN LADING CLOVER Most soils continually lose nitrogen and thus require added nitrogen to maintain soil fertility. Leguminous crops are an important source of such nitrogen. The amount added by legumes depends on plant growth and vigor as well as certain edaphic factors (ie. nutrient levels, water availability, pH and temperature). Exposure of soybean, pinto bean, and ladino clover to ozone reduces growth and nodulation (1-3). How these relate to quantitative and qualitative crop production is uncertain. The present research was undertaken with Ladino clover to determine the effects of ozone on: growth, nodulation, nitrogen fixation, nitrogen content, phenol content, energy value; and root exudates. MATERIAL AND METHODS Experiment 1 Inoculated seeds of Trifolium repens L. c.v. Tillman were planted in gravel and Jiffy Mix (2:1).Complete nutrient solution was added to pots every third day. Distilled water was given at other times. Plants were grown and exposed to ozone in the Southeastern Plant Environmental Laboratories. Growth chamber environment was as follows: 12 hrs at 45000 lux, the night was interrupted for 3 hrs with 5500 lux, temperature 22C day and 19C night, and a relative humidity of 50% during the day and 60% at night. Plants were subjected to two 2 hr exposures (one week apart) of either carbon-filtered air, 30 or 60 pphm ozone. Groups of plants were exposed at two week intervals to determine age effects. The first of 4 harvests for each exposure age occurred 1 week after the second exposure. Dry weight of tops (TDW), roots (ROW), nitrogenase activity and nitrogen content were determined. Experiment 2 Plants were grown in sand and Jiffy Mix (2:1) for one month in a greenhouse. A 1/10 normal nitrogen nutrient solution was added every third day. Plants were exposed to carbon-filtered air, 30 or 60 pphm ozone for 2 hrs. Half of the plants were harvested one week later. The remaining plants were exposed again and harvested the following week. TDW, ROW, nodule number, and caloric content of tops (TPCAL) and roots (RTCAL) were determined in each case. ------- Experiment 3 Plants were grown in sand for 6 weeks and then exposed to carbon- filtered air or 30 pphiri of ozone (2 hr) twice 3 days apart in a green- house. A 1/10 normal nitrogen nutrient solution was added every third day. Deionized water was added at other times. Root exudates were collected 7 days after the last exposure. One hundred ml was collected from each pot. Exudates were collected the day before nutrient appli- cation. This was done to minimize inorganic ion input into the exudate. The exudate was used to water 3 week old seedlings of clover for 14 con- secutive days. All plants were then harvested. TDW, ROW, nodule number, nitrogen content, and phenol content (4) were determined. Experiment 4 » Plants were grown in sand culture with 1/10 normal nitrogen nutrient solution as described by Kochhar (1974). Four week old plants were exposed twice 3 days apart to carbon-filtered air, 30 or 60 pphm ozone. Plants were harvested 4 weeks later. TDW, RDM and nodule number were determined. Root exudates (100 ml) from each reservoir were flash evaporated and taken up in acetone (5 ml). Acetone fraction was tested for toxicity against Rhizobium with sensitivity disks. All data was subjected to analysis of variance unless otherwise stated. Least significant differences at the 5% probability level were used to illustrate differences among treatment means. RESULTS Experiment 1 Growth and Nodulation-- Fig l-3iA double exposure of ozone reduced top growth, root growth, and nodulation. Plant responses to ozone varied with age and concentration of ozone. ' Nitrogenase activity— Fig 4-5. Some stimulation of nitrogen activity per nodule was observed for exposure age 28+35 and 42+49. However, these responses were not signifi- cantly different from the controls. Nitrogenase activity per plant was reduced for exposure age 14+21. Nitrogen content— Fig 6-10 [Also see Table 2a] Percent nitrogen for tops and roots was significantly higher for exposure age 14+21 for both the 30 and 60 pphm ozone exposures. Percent nitrogen was higher for tops with the 30 pphm exposures and higher for the roots with*the 60 pphm exposures for exposure age 28+35. Total plant nitrogen was reduced for exposure age 14+21 and 28+35 for both ozone exposures. For exposure age 42+49 and 56+63 only the 60 pphm exposures reduced total nitrogen content of clover plants. Similar trends were ob- served for nitrogen content of tops and roots. ------- Experiment 2 Energy Content-- Table 1. Caloric content was significantly reduced for the tops with 2 ozone exposures of 30 or 60 pphm. Caloric content of roots was not significantly reduced. Experiment 3 Phenol content-- Table 2a+b. Exposures of ladino clover to 30 pphm of ozone significantly reduced phenol content of tops and roots. Nitrogen content was also deter- mined here. Nitrogen of tops and roots was significantly reduced from controls. Experiments 3 and 4 Root Exudates— Tables 2b, 3, 4. Exudates from ozone exposed plants did not inhibit the growth or nodulation of ladino clover seedlings when compared to con- trol plant exudates. Exudates from ozone exposed plants were not inhibi- tory to Rhizobium when compared to controls. ------- o: o Q_ o 20 18 16 14 12 10 8 6 4 2 14+21 Figure 1. CONTROL^' . 30 PPHM 03 60.PPHM 03 iii , LSD-0.05=li27|; J 28+35 42+49 EXPOSURE AGE (DAYS) 56+63 The effect of two 2-hr, ozone exposures on the top dry weight of ladino clover plants. A.-significant difference between control and test. B.-significant difference between 30 and 60 pphm ozone. ------- 3.0 2.0 CO CD 1.0 o § 14+21 28+35 42+49 EXPOSURE AGE (DAYS) 56+63 Figure 2. The effect of two 2-hr ozone exposures on the root dry weight of ladino clover. A.-significant difference between control and test. B.-significant difference between 30 and 60 pphm ozone. 8 ------- 600 500 400 EC LU CQ i 300 Q O 200 100 0 14+21 28+35 42+49 EXPOSURE AGE (DAYS) 56+63 Figure 3. Changes in nodulation of ladino clover plants following two 2-hr, ozone exposures. A.-significant difference between control and test. ------- .0050 . LU _l O 0.0040 S i.0030 LU O ".0020 .0010 JL CONTROL 30 PPHM 0, 60 PPHM 0, LSD-0.05= 0.00181 14+21 28+35 42+49 56+63 EXPOSURE AGE (DAYS) Figure 4. Effects of ozone exposures on nitrogenase activity/nodule of ladino clover. *LSD for analysis of first 2 exposure ages only. 10 ------- 3.0 3 2.0 O. § o 1.0 14+21 • CONTROL A 30 PPHM 0 * 60 PPHM 0 LSD-0.05=0.512 28+35 42+49 56+63 EXPOSURE AGE (DAYS) Figure 5. Changes in nitrogenase activity/plant of ladino clover following ozone exposure. A. -significant difference between control and test. *LSD for analysis of first 2 exposure ages only. 11 ------- 1 5.0 4.0 3.0 2.0 1.0 14+21 4. 28+35 42+49 56+63 EXPOSURE AGE (DAYS) • CONTROL A 30 PPHM 03 • 60 PPHM 06 LSD-0.05=0.269 Figure 6. Effect of two 2-hr ozone exposures on % Nitrogen of ladino clover tops. (. A.-significant difference between control and test. • 12 ------- en 5.0 4.0 3.0 2.0 1.0 0 14+21 J_ 28+35 42+49 EXPOSURE AGE (DAYS) 56+63 P CONTROL A 30 PPHM 03 • 60 PPHM 03 LSD 0.05=0.278 Figure 7. Effect of two 2-hr ozone exposures on % Nitrogen of ladino clover roots. A.-significant difference between control and test. 13 ------- CO CD LJJ CD § 55 50 45 40 35 30 25 20 15 10 5 0 14+21 28+35 42+49 EXPOSURE AGE (DAYS) CONTROL 30 PPHM 0, 60 PPHM 0 3 LSD-0.05=3.69 56+63 Figure 8. The effect of two 2-hr ozone exposures on the total N content of ladino clover tops. A.-significant difference between control and test. B.-significant difference between 30 and 60 pphm ozone. 14 ------- CD § 14+21 Figure 9. 28+35 42+49 EXPOSURE AGE (DAYS) 56+63 The effect of two 2-hr ozone exposures on the total N content of ladino clover roots. A.-significant difference between control and test. B.-significant difference between 30 and 60 pphm ozone. 15 ------- 50 LU CD O cc Q_ 40 30 20 10 14+21 •CONTROL A30 PPHM 03 • 60 PPHM 03 LSD-0.05=4.06 28+35 42+49 EXPOSURE AGE (DAYS) 56+63 Figure 10. The effect of two 2-hr ozone exposures on the total plant nitrogen of ladino clover. A.-significant difference between control and test. B.-significant difference between 30 and 60 pphm ozone. 16 ------- Table 1 [Ex 2] Caloric Content, Top Dry Weight, Root Dry Weight and.Nodule Number of Ladino Clover Exposed to Ozone or Carbon Filtered Air. TDW (gm) ROW NODULE TPCAL RTCAL (gm) (#) (cal/gm) Harvest 1 Non-Exposed 30 pphm 03 60 pphm 03 Harvest 2 1.01 c** 0.62 d 0.59 d 0.35 b 137 be 0.21 cd 105 c 0.19 d 96 c 3980 be 3621 a 3951 c 3655 a 3919 c 3683 a Non-Exposed 30 60 pphm pphm LSD °3 °3 0.05 2. 1. 0. 0. 66 a 36 b 93 c 28 0. 0. 0. 0- 61 a 28 be 19 d 07 239 a 169 b 99 c 58 4136 a 4031 b 3844 d 70 3838 a 3734 a 3712 a 154 (NS)* * non significant **means followed by the same letter are not statistically significant at the 5% level of probability. [N-10]. 17 ------- Table 2a [Ex 3] Phenol Content, Nitrogen Content, Top Dry Weight, Root Dry Weight and Nodule Number of Ladino Clover Exposed to Ozone and Carbon-Filtered Air. TDW ROW NODULE NIT* NIT NIT PH* PH PH (gm.) (gm.) (#) TOPS ROOTS TOT TOPS ROOTS TOT. (mg) (mg) (mg) (mg) (mg) (mg) Non-Exposed Plants 0.78 a** 0.30a 30 pphm 03 0.38 b 0.14b LSD 0.05 j).16 0.05 243a 34a lla 137b 15b 5b 65.8 8.4 2 45a 168a 14a 182a 20b 85b 4b 89b 10 34 2 35 *NIT=Nitrogen *PH=Phenol **Means followed by the same letter are not statistically significant at the 5% level of probability [N=10]. Table 2b [Ex. 3] Top Dry Weight, Root Dry Weight, Nodule Number, Nitrogen Content and Phenol Content of Ladino Clover treated with Root Exudates. Non-Exposed Plant Exudate 30 pphm 0., Exposed Plant Exudate TDW ROW NODULE NITROGEN** (#) TOTAL (gm) (gm) (mg.) 0.055* 0.024 51.3 0.034 0.0608 0.029 54.6 0.033 PHENOL** TOTAL (mg.) 0.16 0.19 *no significant difference found. [N=10] **Data not analyzed. 18 ------- Table 3 [Ex 4] Top Dry Weight, Root Dry Weight, and Nodule Number of Ladino Clover exposed to ozone or carbon-filtered Air Grown Separately or in Combination (Design is such that plants interact only by way of root exudates). N Ex ** N Ex + 30 N Ex + 60 60 30 30 + N Ex 60 + N Ex LSD 0.05 0. 0. 0. 0. 0. 0. 0. 0. TDW (gm) 426 a* 443 a 466 a 214 b 124 c 153 be 109 c 087 0. 0. 0. } 0. 0. 0. 0. 0. ROW (gm) 144 a 133 a 135 a 077 b 032 c 047 c 033 c 028 NODULE (#) 53. 58. 49. 26. 21. 33. 23. 18. 5 8 6 1. 9 3 3 9 a a ab c c be c *means followed by the same letter are not statistically significant at the 5% level of probability {N=10]. ** N Ex - Non exposed plant grown alone. N Ex + 30 - Non exposed plant grown with plants exposed to 30 pphm of ozone. \ N Ex + 60 - same as N Ex + 30 but plants exposed to 60 pphm instead of 30 pphm. 30 N 60 - exposed plants grown alone. 30 + N Ex - exposed plants from N Ex + 30. 60 + N Ex - exposed plants from N Ex + 60. 19 ------- Table 4 [Ex 4] Root Exudates vs Rhizobium ZONES OF INHIBITION (nun) N Ex Plant Exudates ** 0.096 * N Ex + 30 Exudates 0.081 N Ex +"60 Plant Exudates 0.080 30 Plant Exudates 0.065 60 Plant Exudates 0.040 Acetone 0.15 LSD 0.05 0.10 [NS] Prob > F 0.099 c.v. = 77% * Non significant [N=16] ** N Ex - non exposed 30 - plants exposed to 30 pphm ozone 60 - plants exposed to 60 pphm ozone 20 ------- SECTION V REFERENCES 1. Reinert, R.A., D.T. Tingey, and C.E. Koons. The Early Growth of Soy- beans as Influenced by Ozone Stress. Agron. Abst. 63:148. 1971. 2. Tingey, D.T. and U. Blum. Effects of Ozone on Soybean Nodules. J. Environ. Qual 2: 341-342. 1973. 3. Kochhar, M. Phytotoxic and Competitive Effects of Tall Fescue on Ladino Clover as Modified by Ozone and/or Rhizoctomia So1am'. Dissertation. 1974. 4. Andersen, R.A. and J.R. Todd. Estimation of Total Tobacco Plant Phenols by Their Bonding to Polyvinyl Phyrrolitone. Tobacco Science 12: 107-111. 1968. 21 ------- TECHNICAL REPORT DATA (Please read Instructions on the reverse before completing) 1. REPORT NO. EPA-600/3-76-031 3. RECIPIENT'S ACCESSION>NO. 4. TITLE AND SUBTITLE EFFECTS OF OZONE ON NITROGEN FIXATIO.N IN LADING CLOVER 5. REPORT DATE March 1976 6. PERFORMING ORGANIZATION CODE 7. AUTHOR(S) Udo Blum and Michael Letchworth 8. PERFORMING ORGANIZATION REPORT NO. 9. PERFORMING ORGANIZATION NAME AND ADDRESS Botany Dept. North Carolina State University Raleigh, North Carolina 27607 10. PROGRAM ELEMENT NO. 1AA006 ROAP 21ALR Task 24 11. CONTRACT/GRANT NO. EPA-IAG-D5-0416 12. SPONSORING AGENCY NAME AND ADDRESS Corvallis Environmental Research Laboratory Ecological Effects Research Division Office of Research and Development U.S. Environmental Protection Agency Corvallis, Oregon 97330 13. TYPE OF REPORT AND PERIOD COVERED Interim Final 14. SPONSORING AGENCY CODE EPA-ORD 15. SUPPLEMENTARY NOTES 16. ABSTRACT Research was performed to determine the effects of ozone on ladino clover growth, nodulation, nitrogen fixation, nitrogen content, phenol content, energy value and root exudates. Plants were exposed once or twice to carbon-filtered air, 30 or 60 pphm ozone for 2 hrs. The effects of ozone on growth, nitrogen fixation, % nitrogen, total nitrogen and nodulation varied with age of plant and ozone concentration. Caloric content of tops (plants 4 weeks old when exposed) was reduced with two ex- posures of 30 or 60 pphm ozone. Root caloric content was not affected. Phenol content of tops and roots (plants 6 weeks old when exposed) was reduced with two 30 pphm ozone exposures. Clover exudates were not detectably modified by ozone exposure, 17. KEY WORDS AND DOCUMENT ANALYSIS DESCRIPTORS b.IDENTIFIERS/OPEN ENDED TERMS C. COSATI Field/Group ozone nitrogen fixation plant growth air pollutants microorganisms soils air pollution ozone exposure 51 B. DISTRIBUTION STATEMEN1 LIMITED 19. SECURITY CLASS (ThisReport) UNCLASSIFIED 21. NO. OF PAGES 28 20. SECURITY CLASS (Thispage) UNCLASSIFIED 22. PRICE EPA Form 2220-1 (9-73) 22 GPO 995-565 ------- |