Progress 06/07/22 to 05/10/24
Outputs
PROGRESS REPORT Objectives (from AD-416): Objective 1. Enhance and utilize Rhizoctonia solani pangenomic database to improve pathogen identification accuracy and characterize pathogenic mechanisms. Objective 2. Determine the impact of cropping system and soil edaphic factors on populations of pathogenic and non-pathogenic soil-borne fungi. Objective 3: Develop biological control agents for soil-borne pathogens, including Rhizoctonia solani, of field and nursery crops. Approach (from AD-416): Planned research is directed at managing important diseases caused by soil-borne plant pathogens that negatively impact farmers' livelihoods in the Mid-Atlantic region of the United States and elsewhere. A major emphasis of this research is developing sustainable disease management tools for pathogens from the Rhizoctonia solani species complex. For Objective 1 the Rhizoctonia solani pangenomic database (RsolaniDB), developed during the prior project, will be enhanced using newly generated near-chromosome-level genome assemblies. This enhanced RsolaniDB will be used to develop molecular probes for the detection and differentiation of R. solani isolates in farm fields. Specific identification technologies are required to ensure the use of appropriate controls, as isolates from this species complex can be morphologically similar but vary widely in sensitivity to chemical or biocontrol measures. The enhanced RsolaniDB will also be used to develop knowledge concerning mechanisms of pathogenicity of poorly studied isolates from the R. solani species complex. For this patho-genomic analysis of select genomes in RsolaniDB will be conducted. Also, RNAseq will be used to carry out temporal, differential gene expression analysis of interactions between a R. solani isolate and known host and non-host crops. Differential expression of R. solani genes during interactions with the host and non- host crops will provide insights into genes involved in pathogenicity and host range of this pathogen. For Objective 2 we will analyze the impact of corn, wheat, and soybean cropping systems used in the mid-Atlantic region on the ecology of R. solani. Modern microbiome molecular approaches will be used on DNA extracted from soil samples from fields used for these cropping systems. Amplicon sequencing of ribosomal markers (ITS for fungi and 16S V4 for bacteria) will provide a description of fungi, including species from the R. solani species complex, and bacteria in the different cropping system fields. Discoveries will result in best management cropping practices to minimize the inoculum of R. solani and disease in farm fields. For Objective 3, environmentally friendly biocontrol options for R. solani isolates and the critical soil-borne plant pathogens Pythium ultimum and Sclerotinia sclerotiorum will be developed. Omics approaches will be used to determine mechanisms of biocontrol. Using this multipronged approach of specific identification, development of environmentally sound biocontrol options, and best management practices to minimize inoculum and disease, this project will improve control of important soil-borne diseases and improve sustainability of farming systems in the Mid-Atlantic region and elsewhere. This is the second and final report for this project. Since the initiation of this project in September of 2022, fifteen peer-reviewed papers were published; nine of these since the FY2023 Annual Report. Goal 1.1 of Objective 1 of the project concerned enhancing the Rhizoctonia solani pangenomic database (RsolaniDB) that was developed by ARS scientists in Beltsville, Maryland, in collaboration with scientists at King Abdullah University of Science and Technology (KAUST). RsolaniDB is being used to develop molecular probes for detection and differentiation of R. solani isolates as well as in studies regarding host range and mechanisms of pathogenesis of the R. solani species complex. Improvement of RsolaniDB through long-read sequencing of the R. solani species complex genomes is necessary to increase its utility for these applications. For Goal 1.1, thirteen long-read-sequence-quality genomes of R. solani isolates covering seven AGs and select subgroups were purified to long-range genome sequencing (gDNA) quality and sent to KAUST for sequencing. Goal 1.2 of Objective 1 concerns using RsolaniDB to identify and differentiate R. solani AG4 and AG2-2IIIB isolates. This is necessary since anastomosis groups of R. solani differ regarding sensitivity to fungicides, biocontrol agents, and plant immune responses. To distinguish the genomes of AG4 and AG2-2IIIB, differential primer regions were selected using the ShuString protocol (http://adenine.biz.fh- weihenstephan.de/shustring/). Unfortunately, progress towards Goal 1.2 stalled due to COVID restrictions and the collaborator from North Dakota State University (NDSU) leaving this project for an administrative position. Going forward, primers can be designed from differential genomic regions of AG4 and AG2-2IIIB isolates and PCR tested to determine selectivity. The first milestone for Goal 1.3 was at 36 months, which is after termination of the project, so there is no progress to report for this goal. In support of Objective 2, the impact of corn, wheat, and soybean cropping systems used in the mid-Atlantic region of the United States on the ecology of R. solani was to be analyzed. Modern microbiome molecular approaches were to be used on DNA extracted from soil samples from fields used for these cropping systems. Amplicon sequencing of ribosomal markers (ITS for fungi and 16S V4 for bacteria) was to provide a description of fungi, including species from the R. solani species complex and bacteria in the different cropping system fields that would ultimately inform best management cropping practices for disease control. Progress on this Objective was stalled by delayed implementation of the project plan, the Covid pandemic, and the detail of one of the project scientists to the USDA Office of the Chief Scientist. In support of Objective 3 develop biological control agents for the important soil-borne pathogens R. solani, Pythium ultimum, and Sclerotinia sclerotiorum. For Goal 3.1, two in vitro assays each for 13 myxobacterial strains were conducted to determine antagonistic potential against two isolates each from R. solani AG2-2IIIB and R. solani AG4, and one isolate each from S. sclerotiorum and P. ultimum. The experiments confirmed that seven myxobacteria strains showed in vitro antagonism against these four pathogens. However, survival assays of one myxobacterial isolate (BS 249) in greenhouse potting mix and garden soil were interrupted due to: (A) prolonged (over one year) non-functionality of the only elevator in Bldg. 001 and the lack of availability of certified biosafety cabinets in SASL laboratory space (over one year). This put all media sterilization work on hold, leading to postponement of biocontrol experiments. Genome-sequence-quality DNA was extracted from 11 of these myxobacterial isolates and genome sequencing and contig generation was completed by CD Genomics for isolates DK 836, DK 897, and BS 247. In collaboration with scientists from NDSU, three different inoculum sources (mycelium, sclerotium, pathogen-colonized barley grains) were compared to determine a suitable inoculum source for screening sugar beet germplasm for resistance against damping-off caused by R. solani AG2- 2IIIB. For Goal 3.2, a library of mutants of Serratia marcescens N4-5 was completed. This library was to be screened for mutants that no longer produced compounds necessary for suppression of damping-off caused by P. ultimum. In this way, compounds from this strain responsible for suppression of disease would be identified. For Goal 3.3, data resulting from two years of field trials testing biocontrol isolate combinations for control was partially organized for analysis. In other work, in collaboration with NDSU, we published (1) four First Reports of new pathogens in sugar beets from North Dakota, Minnesota, and Wyoming. (2) evaluated four adjuvant types for control of Cercospora leaf spot on sugar beet. In collaboration with scientists at the University of Nebraska, Lincoln, we analyzed the differential expression of microRNAs that may influence the susceptibility and resistance interactions of wheat to both Wheat Streak Mosaic Virus (WSMV) and Triticum Mosaic Virus (TriMV). In collaboration with scientists at the Rani Lakshmi Bai Central Agricultural University, Jhansi, India, we isolated, and morphologically and molecularly characterized Trichoderma species from 16 crops from 7 districts of Rajasthan, India. Some of the Trichoderma strains were found to effectively biocontrol Fusarium verticillioides, Sclerotium rolfsii, and R. solani on maize and tomato, either in the field or in pot experiments. Certain Trichoderma isolates provide biofertilizer, biocontrol, and other plant-beneficial activities while inhabiting the soil or internal plant issues; their use in agricultural systems could contribute to sustainable food production. However, choosing isolates from more than 500 known Trichoderma species for use in non-targeted evaluation screens for biocontrol or biofertilizer applications is time-consuming and expensive. We conducted an exploratory survey of common soil inhabitant, rhizospheric, and endophytic Trichoderma species from different continents and performed molecular phylogenetic analyses. These analyses predicted that by preferentially selecting species from T. atroviride, T. asperellum/T. asperelloides, T. hamatum, species from the T. harzianum Complex Clade, T. virens, and possibly nearest relatives, may speed the identification of candidates for commercialization due to the demonstrated ability of these species to successfully inhabit the soil, rhizosphere, and endorhizosphere. ACCOMPLISHMENTS 01 Crop rhizospheric Trichoderma species are a potent source of biocontrol agents. There are very few studies on Trichoderma diversity in agricultural fields that sufficiently identify and evaluate the distribution and role of the fungus in biocontrol and plant growth promotion. In collaboration with the Rani Lakshmi Bai Central Agricultural University, Jhansi, India, ARS scientists in Beltsville, Maryland, isolated Trichoderma species from 16 crops from 7 districts within Rajasthan, India. Based on DNA sequence of translation elongation factor 1a (tef-1a), and morphological characteristics, 60 Trichoderma isolates were identified to 11 species. The T. brevicompactum was found to be the most commonly occurring strain followed by T. afroharzianum. One of the isolates, T. afroharzianum BThr29, was found to effectively control the pathogens Fusarium verticillioides, Sclerotium rolfsii, and R. solani on maize and tomato in the field and in pot experiments. The information on crop selectivity, antagonistic properties, and geographic distribution of Trichoderma species will be beneficial for developing efficient Trichoderma-based biocontrol strategies. 02 Rhizoctonia-colonized barley grains are a potent source of inoculum for resistance screening of sugar beet germplasm. Sugar beet (Beta vulgaris L.) is a major sugar source worldwide. Rhizoctonia solani causes the economically important damping-off and crown and root rot disease of sugar beet, with AG 2�2 IIIB being the most damaging anastomosis group. Screening germplasm for resistance to R. solani is an effective and sustainable disease management approach. ARS scientists in Beltsville, Maryland, in collaboration with scientists at North Dakota State University, Fargo, evaluated three different inoculum types; barley grains colonized by fungal mycelium (CBG), agar plugs containing fungal mycelia, and sclerotia for their ease of production and efficacy in inducing disease in sugar beet. Overall, CBG was found to be the best inoculum due to its ease of inoculum production, low cost, and ability to consistently cause severe disease symptoms in sugar beet plants.
Impacts
(N/A)
Publications
- Jambhulkar, P., Singh, B., Raja, ., Ismaiel, A.A., Lakshman, D.K., Tomar, M., Sharma, P. 2024. Genetic diversity and antagonistic properties of Trichoderma strains from the crop rhizospheres in southern Rajasthan, India. Scientific Reports. https://doi.org/10.1038/s41598-024-58302-5.
- Khan, M., Bhuiyan, Z., Lakshman, D.K., Luis, D., Zhong, S., Liu, Z., Azizi, A., Ameen, G. 2024. Fusarium clavum (F. incarnatum-equiseti species complex 5) causes sugar beet seedling root rot in Wyoming, USA. Canadian Journal of Plant Pathology. https://doi.org/10.1080/07060661.2024.2303650.
- Bhuiyan, Z., Luis, D., Lakshman, D.K., Q, A., Khan, M. 2023. Evaluation of adjuvants added to fungicides for controlling Cercospora leaf spot on sugar beet . Crop Protection. https://doi.org/10.1016/j.cropro.2023.106471.
- Khan, M., Bhuiyan, Z., Del Rio Mendoza, L., Lakshman, D.K., Ismaiel, A.A., Baldwin, T., Azizi, A., Ameen, G. 2023. First report of Fusarium solani (Mart.) Sacc. causing sugar beet seedling rot in Minnesota, USA. Plant Disease. https://doi.org/10.1007/s42161-023-01518-7.
- Bhuiyan, Z., Solanki, S., Luis, D., Borowicz, P., Lakshman, D.K., Qi, A., Ameen, G., Khan, M. 2023. Histopathological investigation of varietal responses to Cercospora beticola infection process on sugar beet leaves. Plant Disease. https://doi.org/10.1094/PDIS-03-23-0562-RE.
- Khan, M., Bhuiyan, Z., Lakshman, D.K., Luis, D., Azizi, A. 2024. First report of Pythium deliense Meurs causing sugar beet (Beta vulgaris L.) root rot in North Dakota, USA. Plant Health Progress. https://doi.org/10. 1094/PHP-06-23-0058-RS.
- Bhuiyan, Z., Luis, D., Lakshman, D.K., Qi, A., Khan, M. 2023. Efficacies of different inoculum forms of Rhizoctonia solani AG 2-2IIIB for resistance screening of sugar beet cultivars. Journal of Plant Pathology. https://doi.org/10.1007/s42161-023-01485-z.
- Soylu, I., Tatineni, S., Lakshman, D.K., Galvez, L., Mitra, A. 2024. Differential regulation of miRNAs involved in the susceptible and resistance responses of wheat cultivars to wheat streak mosaic virus and Triticum mosaic virus. BMC Genomics. 25. Article 221. https://doi.org/10. 1186/s12864-024-10128-1.
- Ismaiel, A.A., Jambhulkar, O.P., Lakshman, D.K., Roberts, D.P. 2024. Trichoderma: species with high potentials for biocontrol and growth promotion. The Journal of Fungi. https://doi.org/10.3390/ applmicrobiol4020060.
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Progress 10/01/22 to 09/30/23
Outputs
PROGRESS REPORT Objectives (from AD-416): Objective 1. Enhance and utilize Rhizoctonia solani pangenomic database to improve pathogen identification accuracy and characterize pathogenic mechanisms. Objective 2. Determine the impact of cropping system and soil edaphic factors on populations of pathogenic and non-pathogenic soil-borne fungi. Objective 3: Develop biological control agents for soil-borne pathogens, including Rhizoctonia solani, of field and nursery crops. Approach (from AD-416): Planned research is directed at managing important diseases caused by soil-borne plant pathogens that negatively impact farmers' livelihoods in the Mid-Atlantic region of the United States and elsewhere. A major emphasis of this research is developing sustainable disease management tools for pathogens from the Rhizoctonia solani species complex. For Objective 1 the Rhizoctonia solani pangenomic database (RsolaniDB), developed during the prior project, will be enhanced using newly generated near-chromosome-level genome assemblies. This enhanced RsolaniDB will be used to develop molecular probes for the detection and differentiation of R. solani isolates in farm fields. Specific identification technologies are required to ensure the use of appropriate controls, as isolates from this species complex can be morphologically similar but vary widely in sensitivity to chemical or biocontrol measures. The enhanced RsolaniDB will also be used to develop knowledge concerning mechanisms of pathogenicity of poorly studied isolates from the R. solani species complex. For this patho-genomic analysis of select genomes in RsolaniDB will be conducted. Also, RNAseq will be used to carry out temporal, differential gene expression analysis of interactions between a R. solani isolate and known host and non-host crops. Differential expression of R. solani genes during interactions with the host and non- host crops will provide insights into genes involved in pathogenicity and host range of this pathogen. For Objective 2 we will analyze the impact of corn, wheat, and soybean cropping systems used in the mid-Atlantic region on the ecology of R. solani. Modern microbiome molecular approaches will be used on DNA extracted from soil samples from fields used for these cropping systems. Amplicon sequencing of ribosomal markers (ITS for fungi and 16S V4 for bacteria) will provide a description of fungi, including species from the R. solani species complex, and bacteria in the different cropping system fields. Discoveries will result in best management cropping practices to minimize the inoculum of R. solani and disease in farm fields. For Objective 3, environmentally friendly biocontrol options for R. solani isolates and the critical soil-borne plant pathogens Pythium ultimum and Sclerotinia sclerotiorum will be developed. Omics approaches will be used to determine mechanisms of biocontrol. Using this multipronged approach of specific identification, development of environmentally sound biocontrol options, and best management practices to minimize inoculum and disease, this project will improve control of important soil-borne diseases and improve sustainability of farming systems in the Mid-Atlantic region and elsewhere. This project is in its first year, being approved in September of 2022, three months after the start of the project cycle. All but one of the twelve-month milestones were met or substantially met 9 months after initiation of the project. There were thirteen manuscripts submitted for publication during this period, five of which have been published or accepted for publication. An additional two manuscripts submitted during the FY2022 Annual Report cycle were published. These manuscripts dealt with use of molecular techniques in identification of fungal plant pathogens, the first report of diseases, effectiveness of fungicides for control of sugar beet pathogens, analysis of the resistance response of sugar beet to R. solani AG 2-2IIIB, the impact of cropping system on the corn metabolome, and scalable knowledge management for speeding development and transfer of agricultural technology to the agricultural community. Goal 1.1 of Objective 1 of the project concerns enhancing the Rhizoctonia solani pangenomic database (RsolaniDB) that was developed by ARS scientists in Beltsville, Maryland, in collaboration with scientists at King Abdullah University of Science and Technology (KAUST). Improvement of RsolaniDB through long-read sequencing of the R. solani species complex genomes is necessary to increase the utility of RsolaniDB regarding developing technologies for detection and identification of morphologically similar R. solani pathogens and for characterization of R. solani pathogenic genes and mechanisms. For Goal 1.1, thirteen long-read- sequence-quality genomes of R. solani isolates covering seven Anastomosis Groups (AGs) and selected subgroups were purified in preparation for shipment to CD Genomics for long-read sequencing. An agreement is in place with CD genomics to perform the long-read sequencing. Goal 1.2 of Objective 1 concerns using RsolaniDB to identify and differentiate R. solani AG4 and AG2-2IIIB isolates. This is necessary since AGs of R. solani differ regarding sensitivity to fungicides, biocontrol agents, and plant immune responses. To distinguish the genomes of AG4 and AG2-2IIB, differential primer regions were selected using the ShuString protocol (http://adenine.biz.fh-weihenstephan.de/shustring/). Unfortunately, progress towards Goal 1.2 stalled due to Covid restrictions and the student collaborator from North Dakota State University (NDSU), entrusted with this work, leaving the graduate program. Going forward primers will be designed from the differential genomic regions and PCR tested on genomes of AG4 and AG2-2IIIB isolates infecting sugar beet, for selectivity. There are no milestones for Goal 1.3 of Objective 1 until thirty-six months after project initiation. Objective 2 is designed to determine the impact of cropping system and resulting differences in soil edaphic factors on populations of pathogenic and non-pathogenic soil-borne fungi, including isolates from the R. solani species complex. For this, the Farming Systems Project (FSP) located at the ARS facility in Beltsville, Maryland, is to be used. FSP has been in place since 1997 and compares five corn-wheat-soybean cropping systems (two conventional, three organic) regarding various agronomic and economic factors. FSP is an excellent platform to compare impacts of cropping system on populations of pathogenic, beneficial, and other soil-borne microbes. Sampling of the FSP field site was delayed one year due to the late start of the project. All milestones for the project should still be able to be met as two years at the end of the project were budgeted for data analysis and manuscript preparation. Data analysis and manuscript preparation will now be compressed into the final year of the project. Objective 3 is designed to develop biological control agents for the soil-borne pathogens R. solani, Pythium ultimum, and Sclerotinia sclerotiorum. For Objective 3, Goal 3.1, in vitro antagonistic potential of 13 myxobacterial strains was evaluated against four soil-borne plant pathogens, two isolates each from R. solani AG2-2IIIB and R. solani AG4, and one isolate each from S. sclerotiorum and P. ultimum. Of the 13 myxobacterial strains tested in vitro, eight strains (ATCC 25194, ATCC 29617, ATCC 51243, ATCC 29616, ATCC 53080, DK 801, BS 247, BS 249) showed in vitro antagonism against all four pathogens and relative levels of antagonism were noted. Survival of one myxobacterial isolate (BS 249) in greenhouse potting mix and garden soil is being investigated to find a suitable planting medium for biocontrol assays against R. solani, P. ultimum, and S. sclerotiorum isolates. Genome-sequence-quality DNA was extracted from 11 selected myxobacterial isolates and genome sequencing and contig generation for three isolates (DK 836, DK 897, BS 247) completed by CD Genomics. In collaboration with scientists from NDSU two inoculation methods (i.e., crown vs. root inoculations) were compared to determine a suitable inoculation technique to screen sugar beet germplasm for resistance against damping-off caused by R. solani AG2-2IIIB. For Objective 3, Goal 3.2, a library of mutants of Serratia marcescens N4-5 was completed. This library will be screened for mutants that no longer produce compounds necessary for suppression of damping-off caused by P. ultimum. In this way compounds from this strain responsible for suppression of disease will be identified. In the future, manipulation of genes responsible for synthesis of these compounds will be used to improve disease control. For Objective 3, Goal 3.3 data resulting from two years of field trials testing biocontrol isolate combinations for control was partially organized for analysis. Analysis of this data will be able to be completed within 24 months to meet the 24-month milestone. First reports of diseases were contributed for Fusarium solani seedling damping-off of hemp (Cannabis sativa) in North Dakota and Stemphylium vesicarium leaf spot on sugar beet (Beta vulgaris) in Minnesota. In collaboration with scientists from NDSU, the identification and characterization of several more pathogens on sugar beet in the Red River Valley region of North Dakota, Minnesota, and Wyoming are in progress. In collaboration with scientists from NDSU, we determined that virulence of Cercospora baticola isolates on sugar beet is not altered due to resistance development against QoI and DMI fungicides in the north central region of the United States. In collaboration with scientists from Rani Lakshmi Bai Central Agricultural University, Jhansi, India, we assessed the virulence, morphologically characterized, and molecularly identified soil-borne Fusarium species causing post-flowering stalk rot of maize. In another investigation with collaborators from the Indian Agricultural Research Institute, New Delhi, India, we determined the best time for whitefly (Bemisia tabaci) vector interception with crop cover to minimize losses due to chili leaf curl virus (ChiLCV) on chilli (Capsicum annuum). ACCOMPLISHMENTS 01 Root inoculation with Rhizoctonia solani is optimal for screening sugar beet resistance. Sugar beet crown rot and root rot caused by R. solani are serious threats to sugar beet production and processing. Prior to the adoption of Roundup Ready� sugar beet (RRSB) cultivars, crown rot was a serious problem resulting from mechanical tillage operations required for weed control. Following the introduction and large-scale cultivation of RRSB, however, crown rot was reduced but root rot became severe. This necessitated reassessment of screening methods for the development of Rhizoctonia-resistant cultivars. In a collaborative study between USDA-ARS scientists from Beltsville, Maryland, and scientists from North Dakota State University, crown inoculation and root inoculation methods were evaluated for the development of Rhizoctonia root rot and assessed regarding efficacy of differentiating the disease reaction of sugar beet cultivars. Results demonstrated that the root inoculation method is optimal for consistent disease rating of sugar beet germplasm in the greenhouse. It was concluded that use of the root inoculation method is convenient and of acceptable accuracy for screening RRSB cultivars in a resistance breeding program. 02 Resistance to QoI and DMI fungicides does not alter virulence of Cercospora beticola. Cercospora leaf spot (CLS) is a destructive disease limiting sugar beet production and is managed using resistant cultivars, crop rotation, and timely applications of effective fungicides. Since 2016, its causal agent, C. beticola, (Cb) has been reported to be resistant to Quinone outside inhibitors (QoIs) and to have reduced sensitivity to Demethylation inhibitors (DMIs) in sugar beet growing areas in North Dakota and Minnesota. USDA scientists from Beltsville, Maryland, in collaboration with scientists from North Dakota State University and other USDA scientists (Fargo, North Dakota), showed that resistant Cb isolates had significantly less mycelial growth and spore production than sensitive isolates, while no significant difference in spore germination was detected. Also, resistant isolates had significantly smaller �Area Under Disease Progress Curve� (AUDPC), but still caused high disease severity as the sensitive ones. This information needs to be factored into CLS management practices.
Impacts
(N/A)
Publications
- Khan, M.F., Bhuiyan, Z.M., Lakshman, D.K., Mosher, P., Knoke, S. 2022. First report of damping off and seedling rot of hemp (Cannabis sativa L.) caused by Fusarium solani (Mart.) Sacc. in North Dakota, USA. Plant Disease. https://doi.org/10.1094/PDIS-12-21-2681-PDN.
- Bhuiyan, Z.M., Lakshman, D.K., Del Rio Mendoza, L.E., Qi, A., Khan, M.F. 2022. Comparison of crown and root inoculation methods for evaluating resistance response of sugar beet cultivars to R. solani AG 2-2IIIB. Crop Protection. https://doi.org/10.1016/j.cropro.2022.106120.
- Harish, J., Jambhulkar, P., Bajpai, R., Meenakshi, A., Babele, P., Chaturvedi, S., Kumar, A., Lakshman, D.K. 2023. Morphological characterization, pathogenicity screening, and molecular identification of Fusarium spp. isolates causing post flowering stalk rot in maize. Frontiers in Microbiology. https://doi.org/10.3389/fmicb.2023.1121781.
- Roy, B., Venu, E., Sathlyaseelan, K., Dubey, S., Lakshman, D.K., Mandal, B. , Sinha, P. 2023. Leaf curl epidemic risk in chilli as a consequence of vector migration rate and contact rate dynamics: A critical guide to management. Viruses. https://doi.org/10.3390/v15040854.
- Short, N.M.,Woodward-Greene, M.J., Buser, M.D., Roberts, D.P. 2023. Scalable knowledge management to meet global 21st century challenges in agriculture. Land. 12:588.
- Mattoo, A.K., Cavigelli, M.A., Misic, D., Gasic, U., Maksimovic, V., Kramer, M., Kaur, B., Matekalo, D., Nestorovic Zivkovic, J., Roberts, D.P. 2023. Maize metabolomics in relation to cropping system and growing year impacts. Frontiers in Sustainable Food Systems. https://doi.org/10.3389/ fsufs.2023.113008910.3389/fsufs.2023.1130089.
- Khan, M., Bhuiyan, K., Lakshman, D.K., Luis, D., Azizi, A., Ameen, G., Sarwar, A. 2023. First report of leaf spot of sugar beet caused by Stemphylium vesicarium (Wallr.) E.G. Simmons in Minnesota, USA. Plant Disease. https://doi.org/10.1094/PDIS-02-23-0256-PDN.
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