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Biological Nitrogen Fixation: RESEARCH CHALLENGES 2 Review of Grants Research grants involving BNF were included in the Program in Science and Technology Cooperation (PSTC), U.S.-Israel Cooperative Development Research Program (CDR), and Committee on Research Grants (CRG) of the BOSTID Research Grants Program. (See Preface for program description.) Sixty-eight small grants were awarded, involving 22 developing countries. Most grants were for a total of $150,000 or less for either 3 or 4 years. A total of 10 million dollars was awarded over an 11-year period. Most of the PSTC grants involved a U.S. scientist as co-investigator; the two CDR grants involved an Israeli scientist as co-investigator, and the CRG grants, in general, involved a U.S. investigator as consultant to the project. Following is a list of the research topics covered. BNF by various legumes—for example, common bean, pigeon pea, cowpea, peanut, bambara groundnut, rice bean, lablab, mung bean, winged bean Breeding for improved BNF BNF in farming systems BNF in tree and shrub crops BNF by Azolla-Anabaena azollae Environmental factors that affect BNF Modeling BNF systems Legumes as a food source Legume pathology
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Biological Nitrogen Fixation: RESEARCH CHALLENGES Legume pests Legumes as feed Drought tolerance of legumes Legume tissue culture Legume molecular biology Salt tolerance of host and microsymbiont Rhizobial strain improvement Rhizobial competitiveness Rhizobial molecular biology Genetic engineering of rhizobia DNA identification of rhizobia DNA identification of Frankia spp. DNA identification of Azolla spp. Associative nitrogen fixation Interaction with mycorrhizal fungi Microbial antagonisms REVIEW PROCEDURES The review procedures of the panel consisted of site visits and mail inquiries. Site Visits At its first meeting, the panel was presented with reports from each of 68 grantees. On the basis of these reports and their collective knowledge, the panel decided that a team of three scientists, including at least one panel member, should make site visits to designated grantees and their institutions. The sites chosen were in Thailand, the Philippines, Central America, and Africa. Because of lack of funds the site visit to Central America was cancelled. At an international meeting on BNF held in Mexico, some panel members had the opportunity to interview grant holders from that area. A Science and Government Fellow from AAAS (American Association for the Advancement of Science) assigned to AID was co-opted for a site visit in Kenya. Mail Inquiry At its first meeting, the panel decided to construct and mail each of the grantees a series of questions concerning their AID-funded research. These same questions were sent to co-investigators. By the time of the second panel meeting, about 50 percent had responded.
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Biological Nitrogen Fixation: RESEARCH CHALLENGES GENERAL OBSERVATIONS Despite the inherent element of uncertainty in any research, it was clear that these research grants had an impact, both scientifically and in terms of professional development. Although only half the grantees responded to the questions and many of the projects were completed only recently, they listed the following publications, presentations, and training accomplishments: Publications and Presentations Training Accomplishments Refereed journals 115 Postdoctorals 17 Proceedings 91 Ph.D. candidates 40 Extension 12 M.S. candidates 103 Others 24 Undergraduates 94 National meetings 131 Farmers 82 International meetings 156 Inoculant producers 7 Technicians 89 Others 93 Specific examples of accomplishments are described below: Research in the Philippines with mycorrhizae led to the production of inoculant for forestry, marketed commercially as “MYCOGROE” and produced by Los Baños Biotechnology Corporation in collaboration with the National Institutes of Biotechnology and Applied Microbiology, University of the Philippines. MYCOGROE tablets contain fungal spores that infect and establish in newly formed roots, resulting in increased availability of moisture and nutrients, particularly phosphorus. In Thailand, the transfer of technology from the BNF Resource Center to a commercial inoculant-production facility at the Bangkok Seed Company increased the use by farmers of rhizobial inoculants for soybean and peanut. In Brazil, sugarcane varieties were identified that received 60 percent of their nitrogen, amounting to more than 200 kg N/ha/year from BNF (Lima et al., 1987; Urquiaga, et al., 1992). These results and a subsequent report of nitrogen-fixing organisms within the vascular system of sugarcane helped to encourage the Brazilian government 's recent reactivation of the Alcohol Program. Collaboration between Honduras and the University of Wisconsin helped develop breeding techniques (involving the introduction of higher nitrogen-fixation potential into well-adapted, high-yielding local lines) that increased the capability of common bean to double the amount of nitrogen fixed.
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Biological Nitrogen Fixation: RESEARCH CHALLENGES In several countries, new rhizobia have been isolated and superior strains identified for use on local cultivars and under stress conditions. In Thailand, mixed cropping of maize and rice bean produced yields as much as 50 percent greater than separate cropping, and it was demonstrated with 15N that the proportion of the nitrogen derived from fixation by the legume increased as a consequence of the use of soil nitrogen by the cereal. In Latin America, geminivirus is a serious pathogen of common bean. Monoclonal antibody techniques were developed for strain identification. Surveys showed that considerable variation occurred both between and within countries. As a result, area-specific management practices will be required. For example, a bean-free period was initiated in the Dominican Republic that greatly reduced losses during the January-April growing season. In the Dominican Republic and Puerto Rico, a search was made for rhizobial strains that could inhibit stem blight of common bean. None was discovered, but a Pseudomonas strain was found effective in laboratory and greenhouse trials. Cyanobacterial mutants produced by genetic modification released significant quantities of nitrogen into the growth medium. In greenhouse trials in Florida, rice plants were able to use the released nitrogen, but limitations imposed by competition and predation in the field are yet to be overcome. The use of azolla as a source of biologically fixed nitrogen for rice is limited by the need to maintain the living plants between growing seasons as a source of inoculum. Research in Thailand determined conditions for reliable production of azolla sporocarps that can be handled like seed for one desirable species, but not for others. Seven of the grantees indicated their research led to an enhanced contribution of BNF and a consequent reduction of the use of fertilizer nitrogen. A rhizobial strain that produces nitrogen-fixing nodules on the stems of Aeschynomene spp. was shown to synthesize bacteriochlorophyll a. Photosynthetic ability in rhizobia had previously been unknown. Grantees in Thailand and at Yale University using DNA procedures developed gene probes, thus providing a relatively simple method of identifying Frankia spp. In Pakistan, in a saline soil, appreciable amounts of nitrogen were fixed by associative nitrogen-fixing organisms in the rhizosphere of Kallar grass Leptochloa fusca. Kallar grass is being used to ameliorate large areas of saline soils for return to agricultural production.
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Biological Nitrogen Fixation: RESEARCH CHALLENGES IMPACT OF THE RESEARCH GRANTS PROGRAMS This section is based on information generated during the three site visits, the responses to the questions sent to each grantee, and the grantee reports made available to panel members. Each source provided important insights into the contribution and impacts of the various research programs. The site visits enabled the panel to collect detailed information and to aid their perceptions regarding a sampling of the projects. The response of grantees to questions about their programs provided information on a range of topics. The annual and final reports summarized the technical results. The panel deliberations resulted in the overall interpretation, evaluation, and synthesis of the information and in final recommendations. The panel noted specific areas where these small competitive research grants had an impact: Human Capital and Education The Environment Fuels Sustainable Agriculture Scientific Knowledge Social Benefits Development Benefits to the United States Human Capital and Education The development of human capital is an integral part of all research programs. Training is needed to upgrade the skills of research staff, to provide new advanced-degree graduates, to develop competent technical staff, and to train future scientists and educators. The PSTC, CDR, and CRG programs have produced a cadre of scientists and technicians with skills to conduct research in BNF and related areas. This development of human capital will probably be the most lasting and effective accomplishments of the BNF programs (in the United States, a number of researchers trained in BNF became leaders in commercial biotechnology companies in the 1980s). The data collected and detailed below are from only 50 percent of the program participants. Estimates for the total program should multiply these figures by a factor of 2. They indicated that the scientific and technical abilities of at least 529 persons were improved. Two hundred forty-one students, including 94 undergraduate and 147 graduate students—
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Biological Nitrogen Fixation: RESEARCH CHALLENGES consisting of 103 M.S. and 40 Ph.D. degree candidates—completed their education as a direct result of the program. Further, this sampling of the program described the training of 17 postdoctorals, 82 farmers, 89 technicians, and 93 others (including teachers, inoculant producers, and extension agents). The program resulted in changes in university curricula in many of the countries, and has had long-term and continuing influence on student training. Sixty-two percent of the responding participants indicated that their BNF research affected teaching and curricula at their institutions. As a direct result of the research grants, special university courses were developed based on BNF: “Biology of Blue-Green Algae,” “Tree Forages,” “Nitrogen Fixation and Metabolism,” and “Special Topics.” Several traditional agriculture and biology courses at the college and high school levels now include units on mycorrhizae and rhizobia. Equipment purchased and methodologies learned and developed are still being used by advanced undergraduate and graduate students in formal courses, special projects, and for dissertation research. Participation in national and international meetings and publication of journal articles and proceedings papers provided both professional development and continuing education for principal investigators and co-investigators, technicians, and students. The responding participants indicated they had presented 156 research papers at international meetings and had published 155 articles in refereed journals, 91 articles in proceedings, and 24 in other publications that provided new information on BNF to the scientific community. In addition, 12 extension publications resulted, indicating practical applications as spinoffs from the research-based program. In an outreach effort, data from food and nutritional research on nitrogen-fixing beans was used to inform nutritionists and to issue recommendations to food processors. In another such effort, an educational television series for the general public was developed on nitrogen-fixing microorganisms. Further, annual meetings of principal investigators coordinated by BOSTID provided for an exchange of information and special training workshops. The training was in topics relevant to the research, including: serological methods for identifying bacteria; isotopic nitrogen and other methods for determining BNF quantitatively; tissue culture in legume improvement; molecular biology of BNF; and preparation of scientific articles for publication in refereed journals. A hands-on laboratory training course on rhizobium molecular genetics was hosted by BOSTID and organized and given by the Universidad Nacional Aut ónoma de México for 10 participants. U.S. collaborators in many of the projects set up training courses for staff of the developing-country institutions. As a result of student and curricula development, international expo-
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Biological Nitrogen Fixation: RESEARCH CHALLENGES sure, publications, and research progress from the BNF program, 80 percent of the respondents indicated that the program enhanced their careers. A number of principal investigators and their students won national and international awards, and several attained leadership positions in national universities. For example, Professor S.O. Keya of Kenya received the African Academy of Sciences/CIBA-GEIGY prize of US $10,000 for Agricultural Bio-Sciences. Programs in Kenya, the Philippines, Thailand, and other countries trained women and men, and several women completed Ph.D. degrees and have advanced to leadership positions in universities, national governments, and the private sector. Students have continued graduate training at institutions such as the University of California-Berkeley, University of Missouri, Purdue University, and Max Planck Institute. In Thailand, a BNF Center and a regional NifTAL training center and MIRCEN unit were established in association with other similar projects. The Thailand BNF Center provides opportunities for learning and participation in BNF research programs in progress and for use of the technology through classes, publications, national and international conferences, and student and technician training. It also encourages visits by growers and scientists. A similar center in Senegal was strengthened. The Environment The environmental problems associated with the use of fertilizer nitrogen are common to both developing and developed countries: groundwater contamination, algal blooms in lakes, altered global nitrogen cycle, and increased global greenhouse gases. With the use of nitrogen fertilizer now expanding most rapidly in the developing countries, negative environmental impacts are growing rapidly in consequence. Moreover, the projected doubling in world population will occur mainly in developing countries. Therefore, increased need for fertilizer nitrogen for food production will persist in developing countries—assuming the current emphasis on national food security will continue and that fertilizer will also continue to be the dominant source of nitrogen. Increasing and extending the role of BNF would reduce the need for fertilizer nitrogen and decrease adverse environmental effects. Because some of these adverse impacts are global, it is of worldwide interest to emphasize research, development, and adoption of environmentally acceptable biological alternatives to fertilizer nitrogen. The AID-supported BNF program resulted in examples of benefit to the environment: Seven grantees reported reduced national use of fertilizer nitro-
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Biological Nitrogen Fixation: RESEARCH CHALLENGES gen. In one example, the usual recommendation of 100 kg N fertilizer/ha for a grain legume crop was reduced more than 50 percent (with split application so as to minimize inhibition of nodular nitrogen fixation) without any reduction in yield. In Brazil, BNF is replacing the application of fertilizer nitrogen to sugarcane. As a consequence of a BNF program in the Philippines, expanded use of nitrogen-fixing trees is reducing erosion. In the Philippines, researchers developed “MYCOGROE,” which enhances the growth of trees grown in the reforestation programs. Fuels The Brazilian Alcohol Program is the only large-scale biofuel program; it supports 4 million automobiles running on 95 percent ethanol. Many other countries have programs in which a small percentage of the gasoline is replaced by ethanol, such as the gasohol program in the United States. The key to success in Brazil is the use of sugarcane as the raw material for alcohol production. Experiments using the 15N-dilution method have shown that some cultivars of sugarcane accumulated significant amounts of nitrogen, up to 200 kg N/ha/year, apparently from BNF (Urquiaga et al., 1992). If a cultivar capable of supporting high levels of BNF were used for alcohol production with just 60 kg N/ha applied instead of the usual 300-500 kg N/ha, the ratio of energy gained to energy used in production would increase from 1.0 to 2.5. Using media with high sucrose content, endophytic diazotrophic bacteria have been isolated from the roots, stems, and leaves of sugarcane. The endophyte Acetobacter diazotrophicus was found to excrete nitrogenous compounds under appropriate in vitro conditions, suggesting that nitrogen fixation may occur in the endophytic state, for instance, within xylem vessels (Döbereiner et al., 1993). This exciting possibility needs to be evaluated. Sustainable Agriculture Legumes are used for food, fodder, shade, fuel, timber, green manure, and as cover crops. The agricultural systems in which they are grown in developing countries include plantation systems—where legume cover crops, food crops, or shade trees are grown with tree crops such as cocoa, tea, coffee, rubber, and oil palm; tillage systems—where legumes are grown with tillage in rotation or intercropped with cereals; traditional tillage systems—principally represented by shifting cultivation and natural bush fallow; grazing systems—which include extensive
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Biological Nitrogen Fixation: RESEARCH CHALLENGES grazing of natural vegetation in semiarid regions, intensive pastoral type agriculture, and “cut-and carry” systems (Peoples and Herridge, 1990). A keystone technique in making agriculture more sustainable will be the expanded use of BNF in new farming systems. This will require site-and situation-specific research on crops and microorganisms, and good management practices. Present knowledge is inadequate to provide economically competitive alternatives to fertilizer nitrogen in many situations. Research under this program has contributed to increased feasibility of the use of BNF in developing economically sustainable agriculture and forestry as discussed below. Plants with Increased BNF Capacity Common bean (Phaseolus vulgaris) is generally a poor nitrogen fixer. Scientists in Honduras and at the University of Wisconsin collaborated to increase the capability of common bean to fix nitrogen. Starting with a genotype with a greater fixing capacity than local Honduran cultivars, they bred higher nitrogen-fixation capacity into well-adapted local high-yielding lines to produce well-adapted superior cultivars with a doubled level of fixed nitrogen in the plant. A number of free-living procaryotes are capable of nitrogen fixation, but they supply little fixed nitrogen to the soil because they lack adequate sources of energy to support nitrogen fixation. However, some can associate loosely on and in nonleguminous roots and derive sufficient energy from the plant to support nitrogen fixation. Kallar grass (Leptochloa fusca) introduced into an area of poorly productive high saline soils in the Indus Valley in Pakistan established successfully with the slow disappearance of existing weeds. Nitrogen-fixing bacteria were isolated from the rhizosphere and 15N experiments indicated significant associative nitrogen fixation. Rhizobia that Improve BNF Capability Only certain rhizobial strain/legume cultivar combinations are highly effective in fixing nitrogen. When legume crops nodulate with poorly effective rhizobia, inoculation with highly effective, stress-resistant rhizobia can improve production. As plant breeders develop improved stressresistant, high-yielding varieties, superior rhizobial strains may be required to enable them to reach their full potential. In Sri Lanka, Costa Rica, India, Thailand, Senegal, Jamaica, Dominican Republic, Cameroon, Egypt, Indonesia, Haiti, Kenya, Panama, Malaysia, and the Philippines, new isolations of rhizobia have been made and superior strains identified for use with local cultivars under local
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Biological Nitrogen Fixation: RESEARCH CHALLENGES conditions. However, inoculation is not always successful, and improved inoculants and better application techniques continue to be developed and tested. Further improvements are needed, especially to displace the inferior indigenous rhizobia with superior strains in the nodule. Cropping Systems Using BNF Intercropping legumes and nonlegumes is a common practice in developing countries. Nitrogen may be supplied directly to the nonlegume, and incorporating part or all of a legume crop into the soil can provide nitrogen to the following crop. In Thailand, intercropping maize (a cereal) with rice bean, Vigna umbellata (a legume), produced total yields as much as 50 percent greater than would be expected on the basis of sole-crop yields. Detailed analysis using 15N showed that the proportion of nitrogen of the rice bean supplied by BNF increased as a consequence of the use of soil nitrogen by the maize (Rerkasem et al., 1988). Similar results were obtained in Sri Lanka with maize and peanut (R. Senaratne, University of Ruhuna, Sri Lanka, 1994, personal communication). In a Mexico-U.S. collaborative laboratory study, transfer of nitrogen from the legume to the nonlegume occurred in small amounts. Nonlegume and legume roots were separated and connected only by mycorrhiza hyphae and transfer was measured with isotopic nitrogen. Biological Disease Control in Legumes The amount of nitrogen fixed by an effectively nodulated legume plant is influenced by the health of the plant. Geminiviruses are widespread in Latin America and significantly reduce the yield of common bean. A PSTC grant aided a multidisciplinary group from Costa Rica, England, and Illinois in the United States to develop monoclonal antibody techniques to identify strains of geminiviruses. Surveys in Latin America indicated considerable variability in geminiviruses both between and within countries. Consequently, area-specific management practices are required for geminivirus control. Although developed for the Dominican Republic, they remain to be developed in other areas. Scientists in the Dominican Republic and Puerto Rico searched for Rhizobium strains that could inhibit ashy stem blight in common bean. None was found, but a Pseudomonas strain was effective in laboratory and greenhouse trials. A Mexican team investigated the concept that halo blight of bean would be reduced by genetic modification of the plant to develop resis-
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Biological Nitrogen Fixation: RESEARCH CHALLENGES tance to phaseolotoxin, the toxin causing the disease symptoms. The genetic transformation was successful, and further tests will determine fertility of the transgenic plants and heritability of the resistant trait. Use of Algae and Azolla to Supply Nitrogen to Rice Wetland rice is grown in ponded water that provides an environment in which algae and azolla can grow. Blue-green algae (cyanobacteria) can fix nitrogen symbiotically with azolla. The amount is proportional to growth. The azolla is usually incorporated into the soil, where decomposition releases nitrogen that the rice can use. This is a form of green manuring. If these organisms would “leak” nitrogen into the water, the rice would be able to use it directly (Roger and Watanabe, 1986). In Florida, cyanobacterial mutants were produced that released significant quantities of nitrogenous compounds in laboratory tests. In greenhouse trials, rice was able to use the released nitrogen, but in the field algal survival was poor because of competition and predation. These limitations have yet to be overcome. Genetic improvement of azolla has been limited by the difficulty of identifying strains. Washington State University and the International Rice Research Institute developed a “fingerprinting” technique using enzyme and protein patterns that were useful in identifying strains, but it needs improvement for greater reliability and ease of use. The use of azolla requires massive amounts of inoculum (about 1 ton/ha) and the maintenance of material between cropping seasons. In Thailand, improved management systems for azolla maintenance between cropping seasons were developed but they require considerable management skill. Also in Thailand, the massive amounts of vegetative inoculum needed to carry over between seasons were reduced by 90 percent. Azolla forms sporocarps, but only periodically, and previous efforts to control the process were unsuccessful. However, conditions were found for reliable sporocarp induction in one azolla species. Additional research is required to modify this system for application to other species. Forestry There have been large decreases in forested areas worldwide in recent years. The losses have destroyed ecosystems, increased soil erosion, and decreased the removal of carbon dioxide from the atmosphere. AID-supported researchers studied ways for effective reforestation using fast-growing, nitrogen-fixing trees, Certain nonleguminous trees that fix nitrogen in association with
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Biological Nitrogen Fixation: RESEARCH CHALLENGES Frankia spp., an actinomycete, also have high potential for reforestation. Alder and casuarina, which fall into this group, commonly are the first trees to reestablish in ash after a volcanic eruption, or on degraded slopes after deforestation. Frankia is slow-growing, and it is difficult to determine whether nodules contain the strain supplied as inoculum. An AID-supported researcher reports success in labeling Frankia strains so that they can be recovered and identified from nodules or soil. Tree establishment is dependent not only on nitrogen but also on phosphorus as a major nutrient. Phosphorus often exists in insoluble forms in the soil, but can be mobilized by mycorrhizae. However, the production of mycorrhizal inoculum is cumbersome. Filipino investigators have developed a mycorrhizal inoculant in tablet form that is produced commercially for use in reforestation. It not only increases growth rate but enhances uptake of water and nutrients from the soil, improves survival rate of seedlings, decreases pathogenic root infection, and improves soil structure. The examples cited above summarize the impact to date, but it is anticipated that the science and technology base will foster continued improvement in sustainable agriculture and agroforestry. Scientific Knowledge As indicated, studies on BNF can have impacts of global importance. Nitrogen is so central to the growth of animals and plants, and so frequently the limiting factor in crop productivity, that enhancement of BNF has implications for food, forage, and forestry. Thousands of legume species and hundreds of nonlegume species have the capacity for symbiotic nitrogen fixation. Therefore, BNF is important in natural ecosystems as well as in agriculture. While fundamental BNF research has occurred mainly in developed countries, this program included studies of unusual, diverse, and specialized BNF systems of particular relevance to developing countries. The AID-supported BNF research resulted in many discoveries. The investigators at Cuernavaca, Mexico, have observed gene rearrangement in Rhizobium spp., suggesting that the genome is a dynamic structure (Brom et al., 1992). This example of genome rearrangement may impact studies of bacterial evolution, formation, and function. A continuing effort to obtain superior nitrogen-fixing organisms for specific applications is required. Researchers with AID support have isolated rhizobia that tolerate high temperatures, and others that tolerate wide variations in pH. An unusual organism produces nitrogen-fixing nodules on the stems of Aeschynomene spp. and has photosynthetic capacity, which confers BNF
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Biological Nitrogen Fixation: RESEARCH CHALLENGES self-sufficiency (Hungria et al., 1992), a most important finding for both developing and developed countries. Nodules on the stem allow nitrogen fixation when the roots are submerged and essentially anaerobic. Cultivars with highly active fixation have been found with potential as green manure. Common bean is a major source of dietary protein in many developing countries. Studies of the amino acid composition of its seed have contributed information of nutritional importance. It also has been subjected to genetic modification to confer disease resistance. The root nodules of nonleguminous nitrogen-fixing woody plants contain the actinomycete Frankia. Molecular methods were developed for identification of Frankia strains. This is particularly useful to study success of inoculation under field conditions. Differences observed in the molecular genetics indicated possible strain/host specificity, which may facilitate genetic improvement. Social Benefits The social benefits of the USAID-BOSTID BNF research are just emerging. When asked if any individual or groups had benefited from their research, 20 percent of the responding researchers identified farmers and consumers. In addition, they reported that a diverse group of more than 500 people had been trained and educated in conjunction with their research. Although graduate and undergraduate students constituted the majority, farmers (16 percent) were important recipients of training and education. Although a majority of the respondents indicated that the research had not yet had an effect on the practices and/or economic situation of farmers and producers in their country, approximately 30 percent reported a moderate–to–great impact on producers. Some examples are the increasing use of green manure, decreased use of nitrogen fertilizer by participating farmers, and sales of inoculant (Thailand's rhizobia inoculation program). Most respondents indicated that assessment of applicability is premature. Often, additional research and extension would be necessary before application by farmers becomes practical. Certainly the potential exists for significant social impact. Development The AID-BOSTID research grants programs—involving developing country scientists as equal partners—have had an impact on national development. One of the grants helped to convince the government of Thailand to
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Biological Nitrogen Fixation: RESEARCH CHALLENGES institute a policy promoting the industrial production of biofertilizers. Also in Thailand, the technology of rhizobial inoculant production was transferred to private enterprise, the Bangkok Seed Company. These developments have resulted in increased use by farmers of rhizobial inoculants for soybean and peanut, lowering the cost of inputs and improving human nutrition. As a result of work on geminivirus, the government of the Dominican Republic has initiated a cropping program that recommends a beanfree period to break the disease cycle and thus decrease crop losses. The Brazilian government, in its alcohol program, is considering the utility of the work with sugarcane involving cultivars with high rates of associated nitrogen fixation. In the Philippines, research on mycorrhizae has led to commercial production of the inoculant “MYCOGROE” for forestry. Twelve extension publications should have an effect on agricultural development at the farm level. Each project had a limited timeframe. It is anticipated that the examples above, the published research papers, and presentations made at meetings will extrapolate to benefits for development, particularly if funding can be continued and expanded. Benefit to the United States It was not the primary purpose of these funding programs to benefit the United States directly. Nevertheless, they do. Advances in methods to identify Frankia spp. in a U.S.-Thailand project are useful for the United States. The same holds true for other methodologies such as identification of Phaseolus genotypes by use of PCR on DNA extracted directly from seed (a U.S.-Colombia project), methods to predict the response to rhizobial inoculation (a U.S.-Thailand project), the use of supplemental saline water for growth of peanuts (a U.S.-Israel-Philippines project), and the construction of a saturation linkage map of the common bean (a U.S.-Colombia project). The mycorrhizal research in the Philippines leading to the commercial production of inoculant for trees may affect U.S. reforestation programs. Several of the projects provided genetic resource material, both plant and microbial, that were deposited in national and international collections. This new germplasm may have value for U.S. research. An example is the use of tropical bean germplasm to improve BNF in common bean cultivars grown in the United States. In scientific terms, it is difficult to assess the long-term impact of these projects. The involvement of American scientists has made them more sensitive to the difficulties of functioning and solving problems
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Biological Nitrogen Fixation: RESEARCH CHALLENGES relevant to the needs of the developing world. In several cases, those interactions led to further collaboration beyond the scope of the original grant. Significant impact derives from the scientific broadening and understanding of the U.S. investigators resulting not only from the research per se, but also from foreign visits. They provided opportunities for deeper insight and appreciation for needs, constraints, utilization, and application of BNF both inside and outside the United States. Scientists are people who not only exchange technology but also philosophy, ethics, and ways of conducting research. The scientific method is a useful paradigm for democratic processes. We learn from each other.
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