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Research Project: Management of Aphids Attacking Cereals

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2020 Annual Report


Objectives
The long-term objective of this project is to improve integrated pest management (IPM) practices for cereal aphids in wheat, barley, and sorghum in the United States. To achieve this objective enhancing the role of aphid host plant resistance and natural enemies for IPM programs and providing fundamental knowledge of cereal aphid biology and ecology is required. Over the next 5 years we will focus on the following objectives: Objective 1: Determine the distribution and diversity of resistance-breaking biotypes of cereal aphids in the Great Plains states, identify new sources of resistance for wheat and sorghum, and transfer into suitable genetic backgrounds, to facilitate development of new aphid resistant cereal varieties. Subobjective 1A: Characterize the biotypic structure of Russian wheat aphid (RWA) populations in wheat and non-cultivated grasses to address biotypic diversity to provide knowledge needed to develop and deploy durable RWA resistance in wheat and barley. Subobjective 1B: Identify, characterize, and introgress greenbug resistance sources/genes into wheat germplasm. Objective 2: Determine the distribution and severity of sugarcane aphid in sorghum in the Southwest United States, identify resistant germplasm in sorghum, and evaluate population dynamics to assess the potential for development of resistance-breaking biotypes in this aphid species. Subobjective 2A: Identify sorghum germplasm with resistance to sugarcane aphid and determine the mechanisms of resistance. Subobjective 2B: Determine if biotypes exist in sugarcane aphid populations that can overcome sugarcane aphid resistance in sorghum. Objective 3: Develop and refine methods for field, landscape, and area-wide scale approaches for detecting and monitoring invasive aphid infestations, and optimizing invasive aphid biological control methods in wheat and sorghum. Subobjective 3A: Develop and refine methods for aphid infestation detection and monitoring in wheat and sorghum based on spatial pattern analysis of multispectral remotely sensed imagery. Subobjective 3B: Assess resource availability and diversity for the aphid parasite Lysephlebus testaceipes across a range of landscape/agroecosystem diversity levels. Objective 4: Apply knowledge obtained from aphid genome and transcriptome sequencing to develop plant mediated or other delivery methods for RNAi silencing of critical genes for aphid survival in a broad range of aphids affecting cereals.


Approach
Field and laboratory experiments will be conducted to : (1) characterize the biotypic structure of Russian wheat aphid (RWA) populations in wheat and non-cultivated grasses to address biotypic diversity to provide knowledge needed to develop and deploy durable RWA resistance in wheat and barley; (2) identify, characterize, and introgress greenbug resistance sources/genes into wheat germplasm; (3) identify sorghum germplasm with resistance to sugarcane aphid and determine the mechanisms of resistance; (4) determine if biotypes exist in sugarcane aphid populations that can overcome sugarcane aphid resistance in sorghum; (5) develop and refine methods for aphid infestation detection and monitoring in wheat and sorghum based on spatial pattern analysis of multispectral remotely sensed imagery; (6) assess resource availability and diversity for the aphid parasite Lysephlebus testaceipes across a range of landscape/agroecosystem diversity levels; and (7) apply knowledge obtained from aphid genome and transcriptome sequencing to develop plant mediated or other delivery methods for RNAi silencing of critical genes for aphid survival in a broad range of aphids affecting cereals.


Progress Report
Under Objective 1B, ARS researchers at Stillwater, Oklahoma, reported the new greenbug resistance gene Gb8 that was identified earlier and made a total of four crosses to transfer Gb8 to elite breeding lines. We also initiated a project aimed at developing germplasm resistant to most economically important greenbug biotypes by combining Gb8 and Gb1. Gb1 is a recessive gene conferring unique resistance to some greenbug biotypes. The recessive nature necessitates the use of a marker-assisted selection to achieve the project goal. Therefore, we started to map Gb1 using an F2:3 population derived from the DS28A/Custer. We have evaluated the population for responses to greenbug biotype F and genotyped the population with single nucleotide polymorphism (SNP) and simple sequence repeats (SSR) markers. Our preliminary results indicated that Gb1 resides on the short arm of chromosome 1A. We expect to develop SSR and kompetitive allele specific polymerase chain reaction (KASP) markers closely linked to Gb1 at the end of the fiscal year 2020. In addition, we evaluated a large set of Triticum monococcum accessions, and six of them are resistant to greenbug biotype B. Crosses were made to transfer the underlying greenbug resistance gene(s) to elite lines. Under Objective 2A, the effects of aphid feeding injury on plant physiology varies among aphid species and the crop species infested. We reported the physiological response of sugarcane aphid feeding on susceptible and known resistant sources of sorghum. The results provide evidence that known resistant sorghums are able to maintain/increase photosynthetic capacity and compensate under feeding pressure when compared to susceptible genotypes; this expression is more pronounced for tolerant entries and, to a lesser degree, for genotypes that express antibiotic forms of resistance. Under Objective 2B, from over 40 sugarcane aphid populations collected within the U.S. we determined that there exists 2 differing multi-locus lineages (biotypes). The first, known as MLL-D, is found mostly on sugarcane, while the other known as MLL-F, is found on sorghum and Johnson grass. To date, and to the best of our knowledge MLL-F is the most devastating type found in the U.S. agricultural landscape. Under Objective 3A, data from multispectral airborne remote sensing of sugarcane aphid infested grain sorghum fields obtained in previous years of this project were processed and analyzed, and a manuscript was published on the use of remote sensing to monitor sugarcane aphid infestations in grain sorghum. Novel analytical approaches for processing remotely sensed multispectral data that monitors the existence and progression of sugarcane aphid infestations in grain sorghum fields have been developed and utilized. Under Objective 3B, data acquired in previous years of this project on resources external to agricultural fields utilized by the key biological control organism Lysiphlebus testaceipes were collated and analyzed, describing resource requirements within the ecological system. For the subordinate project, 'Areawide pest management of the invasive sugarcane aphid in grain sorghum', the following progress was made: under Objective 3 (expand and refine myFields.info), the myFields.info website is used as a common online platform for the Sugarcane Aphid Working Group to uniformly report detections of aphid presence, which is added to an aggregate map of national sugarcane aphid (SCA) presence. In 2019, aphids were first observed and reported on 4 April in Cameron County, Texas. Since the initial detection an additional 100 reports for 94 counties in 11 states were added to the national map via myFields.info. Complimentary to reporting, the pest profile page for SCA on myFields.info was updated to include new extension-related videos and included an embedded playable map of sugarcane aphid distribution. This page was visited 1,745 times by unique users in 2019. Users arrived at the SCA page from Twitter (1,446 users), news articles (265 users), and SCA auto-generated alerts from myFields (34 users). We posted to Twitter from @myFieldsMobile 5 times in 2019 about key detections as the aphid moved across state lines. These tweets were exposed to a total of 12,393 user-feeds. Under Objective 4, areawide monitoring for the SCA and its natural enemies continued at three demonstration sites in south Texas. Similar trends for natural enemies were observed with parasitoids as the most common natural enemy at all three locations. The second year of an exclusion cage study was carried out at the Corpus Christi, Texas, location; results from 2019 are consistent with 2018 data supporting the hypothesis that the combination of aphid semi-resistant hybrids and natural enemies are managing SCA populations in South Texas AWPM demonstration sites. A sentinel pot study that evaluates the potential for different vegetation types (Johnson grass, vegetation in riparian areas, and sorghum in and out of production) to harbor natural enemies of SCA. Natural enemies were most abundant in riparian and sorghum in production habitats, indicating that growers should remove grain sorghum stalks from fields following harvest to prevent SCA build-up. Under Objective 5B, we continued to develop and refine a spatially-explicit, individual-based, stochastic model that integrates the life cycle and aeroecology of SCA with meteorological data to forecast regional infestations of sorghum fields. We analyzed impact of timing of initial aphid infestations in the south on spatiotemporal patterns of infestation throughout the region and initiated model evaluation. Under Objective 5C, comprehensive application method and insecticide efficacy trials were conducted in grain sorghum at both Tifton and Griffin, Georgia. In 2019, University of Georgia trials compared no insecticide with treatments including neonicotinoid seed treatments, in-furrow Sivanto HL applications, Sivanto HL side dress applications and foliar applied labelled and numbered compounds. Foliar compounds that were evaluated included Sivanto Prime, Sivanto HL (2-rates), Transform WG, Admire Pro, Sefina (4-rates), Fulfill and Renestra. In each plot, sugarcane aphid populations were enumerated weekly from both the bottom and top of five leaves per plot. Representative portions of each plot were harvested. Under Objective 6, in addition to activities summarized in Objective 1, tests of a pilot version of the SCA sequential sampling protocol were evaluated and training for growers, extension personnel, and other practitioners has begun. During field tests this past growing season, the sequential sampling protocol agreed with the decision reached by complete enumeration in all but one case. The protocol saved an average of 15 minutes of sampling time per field. The team is currently working to develop smartphone apps to implement the SCA sequential sampling protocol. Under Objective 7, the economic team has begun development of a mathematical programming model that determines the overall economic impact of introducing various SCA control measures including insecticide spraying and planting resistant varieties. This is a regional model and most of the focus in 2019 has been to gather and organize data needed to parameterize the model.


Accomplishments
1. Economic impact of sugarcane aphid resistant sorghums. The development and release of sugarcane aphid resistant grain and forage sorghum has had a significant impact on sorghum economics for the U.S. sorghum producer. Researchers in Stillwater, Oklahoma, in cooperation with plant breeders, plant geneticists from both University and Industry, have provided more than 40 parental lines used for breeding resistance. It is hard to estimate the adoption of sugarcane aphid resistant varieties within the U.S. but there were 4.6 million acres of sorghum planted in the U.S. in 2019. If one fourth of that 2019 acreage was planted in available resistant sorghum varieties, an estimated net economic gain of just over $130 million dollars were saved from the reduction in economic injury as well as not having to apply expensive insecticides. If in 2019 one half of the 4.6 million acres of sorghum was planted with resistant sugarcane aphid varieties, a realized gain of over $240 million was achieved. There are several ways to estimate the realized gain in developing and providing resistant sorghums, but in this case it can be demonstrated that several million dollars were saved, and for each year from the beginning of the sugarcane aphid presence in the United States and for each year thereafter more and more resistant varieties were available, the sugarcane aphid has been reduced to a more inconsequential pest.


Review Publications
Paudyal, S., Armstrong, J.S., Harris-Shultz, K.R., Wang, H., Giles, K.L., Rott, P.C., Payton, M.E. 2019. Evidence of host plant specialization among the U.S. sugarcane aphid (Hemiptera: Aphididae) genotypes. Trends in Entomology. 15:47-58.
De Souza, M.A., Armstrong, J.S., Hoback, W.W., Mulder, P.G., Paudyal, S., Foster, J.E., Payton, M.E., Akosa, J. 2019. Temperature dependent development of sugarcane aphids Melanaphis sacchari, (Hemiptera: Aphididae) on three different host plants with estimates of the lower and upper threshold for fecundity. Current Trends in Entomology and Zoological Studies. 2:1011.
Harris-Shultz, K.R., Armstrong, J.S., Jacobson, A. 2019. Invasive cereal aphids of North America: Biotypes, genetic variation, management, and lessons learned. Trends in Entomology. 15:99-122.
Xu, X., Li, G., Carver, B.F., Armstrong, J.S. 2020. Gb8, a new gene conferring resistance to economically important greenbug biotypes in wheat. Theoretical and Applied Genetics. 133:615-622. https://doi.org/10.1007/s00122-019-03491-1.
Mornhinweg, D.W., Puterka, G.J., Armstrong, J.S. 2020. Resistance in barley (Hordeum vulgare L.) to new invasive aphid, Hedgehog grain aphid (Sipha maydis, Passerini) (Hemiptera: Aphididae). American Journal of Plant Sciences. 11:869-879. https://doi.org/10.4236/ajps.2020.116063.
Paudyal, S., Armstrong, J.S., Giles, K., Hobabk, W., Aiken, R., Payton, M. 2020. Differential responses of sorghum genotypes to sugarcane aphid feeding. Planta. 252(14):1-9. https://doi.org/10.1007/s00425-020-03419-w.
Xu, X., Li, G., Carver, B.F., Puterka, G.J. 2020. Identification of wheat germplasm resistant to major Russian wheat aphid biotypes in the United States. Crop Science. 60(3):1428-1435. https://doi.org/10.1002/csc2.20041.
Li, G., Cowger, C., Wang, X., Carver, B.F., Xu, X. 2019. Characterization of Pm65, a new powdery mildew resistance gene on chromosome 2AL of a facultative wheat cultivar. Theoretical and Applied Genetics. 132(9):2625-2632. https://doi.org/10.1007/s00122-019-03377-2.
Koralewski, T.E., Wang, H., Grant, W.E., Brewer, M.J., Elliott, N.C., Westbrook, J.K. 2020. Integrating models of atmospheric dispersion and crop-pest dynamics: Linking detection of local aphid infestations to forecasts of region-wide invasion of cereal crops. Annals of the Entomological Society of America. 113(2):79-87. https://doi:10.1093/aesa/saz047.
Vitale, J., Vitale, P.P., Epplin, F., Giles, K., Elliott, N.C., Peairs, F., Burgener, P., Keenan, S. 2020. Farm management practices used by wheat producers in the western Great Plains: Estimating their productivity and profitability. Journal of Applied Farm Economics. 3(1).
Holt, J., Styer, A., White, J., Armstrong, J.S., Nibouche, S., Costet, L., Malacrino, A., Antwi, J., Wullf, J., Peterson, G., McLaren, N., Medina, R. 2020. Differences in microbiota between two multilocus lineages of the sugarcane aphid (Melanaphis sacchari) in the continental US. Annals of the Entomological Society of America. 113(4):257-265. https://doi.org/10.1093/aesa/saaa003.
Lindenmayer, J.C., Giles, K.L., Elliott, N.C., Knutson, A.E., Bowling, R., Gordy, J.W., McCornack, B., Brown, S.A., Brewer, M., Catchot, A.L., Royer, T.A., Seiter, N.J. 2020. Development of binomial sequential sampling plans for sugarcane aphid melanaphis sacchari zehntner (Hemiptera: Aphididae) in commercial grain sorghum. Journal of Economic Entomology. 1-9. https://doi.org/10.1093/jee/toaa064.