Research Project: Management Strategies for Invasive Aphid Pests of Cereals

Location: Peanut and Small Grains Research Unit

2022 Annual Report

Objectives
The long-term goal 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 goal, we will increase the knowledge of aphid host plant resistance and natural enemies for IPM programs and provide fundamental knowledge of cereal aphid biology and ecology. Over the next 5 years we will focus on the following objectives: OBJECTIVE 1: Determine regional distribution and significance of invasive aphid species on cereals and alternate grass hosts, discover changes or shifts in the populations, generate relevant phenotypic information, and work with breeders or geneticists to map and pyramid resistant genes. Subobjective 1A: Determine the biotype diversity of the S. Maydis known as the hedgehog aphid (HGA) in cereals and native grasses in advance of discovering and utilizing resistant sources used in breeding for resistance. Subobjective 1B: Identify wheat germplasm resistant to HGA, as well as wheat accessions resistant to all U.S. RWA biotypes. Subobjective 1C: Characterize RWA and HGA resistance genes and develop molecular markers for their introgression into locally adapted breeding lines and cultivars. OBJECTIVE 2: Determine the biological differences and interactions among available sugarcane aphid resistance genes, including comparisons of cross-resistance genes, elucidate resistance mechanisms, and work with breeders and geneticists to map, pyramid, and deploy resistant genes. Subobjective 2A: Develop forage sorghum germplasm resistant to sugarcane aphids. OBJECTIVE 3: Develop effective multi-scale aphid infestation monitoring and sampling technology, develop geographically explicit cereal aphid pest infestation risk models, and elucidate and integrate field and landscape-level components of the natural enemy populations into improved management systems for invasive cereal aphids. Subobjective 3A: Use field research methods and statistical modeling and hypothesis testing to develop a detailed understanding of spatial and temporal factors that determine colonization, population dynamics, and community development of aphid natural enemies in grain sorghum fields and their importance for sugarcane aphid biological control. Subobjective 3B: Develop and disseminate new, time-efficient, and statistically accurate and precise methods for sampling aphid natural enemies in sorghum.

Approach
The combined annual economic value of wheat, sorghum, and barley within the United States is over $16 billion. Cereal aphids are major pests of world agriculture that vector numerous plant viruses and remove photoassimilates by inserting their mouthparts into the sieve elements of the phloem tissue. The direct loss from feeding and the transmission of viral diseases during the process of feeding make cereal aphids the most significant threat to U.S. cereal crop producers. Although aphids in general are small in size, the reproductive potential is at the higher end of the spectrum when compared to all arthropods, with exponential increases and short generation times. Significant yield reductions occur from the direct effect of endemic or epidemic aphid populations. New information on the factors affecting insect populations and new integrated pest management (IPM) tools, control technologies, and aphid-resistant germplasm are needed in order to advance sustainable IPM programs for cereals. The objectives of this project that will deliver the associated products to the consumer are to: 1) determine the biotypic diversity in aphid populations which threatens deployment of aphid-resistant cereals; 2) identify new sources of resistance to aphids in wheat and sorghum and barley; 3) determine the extent and severity of new aphid pest species attacking cereal crops; and 4) develop or refine methods for detecting and monitoring aphid infestations to optimize biocontrol in cereals. The specifically designed research provided in this plan will increase our knowledge on the genomics of virulent cereal aphid biotypes within the U.S. and increase the knowledge of available genetic sources of resistance in wheat, barley, and sorghum. Once identified these resistant sources will be introgressed into available breeding lines. In addition, the benefits and ecological associations of beneficial insects in the agricultural landscape will be better understood and utilized as a result of areawide studies on these organisms.

Progress Report
Under Objective 1A, we surveyed and collected samples from differing grass hosts which shows that the distribution of the hedgehog grain aphid (HGA) appears to be shrinking within the Great Plains states. A total of 12 alternate grass hosts (other than cereal crops) were supporting HGA in the U.S. genetic differentiation (biotype determinations). Identifying host plant differentials are on-going and will continue this fiscal year (FY). Under Objective 1B, we evaluated the responses of a set of wheat accessions to five predominant U.S. Russian wheat aphid (RWA) biotypes – RWA1, RWA2, RWA3, RWA6, and RWA8 -- and identified 14 accessions resistant or highly resistant to all of them. Another set of 19 accessions were resistant or highly resistant to two to four biotypes. These accessions were used to develop mapping/breeding populations, some of which are ready for gene mapping. Under Objective 1C, ARS scientists at Stillwater, Oklahoma, have evaluated the responses of a core set of winter wheat germplasm (about 2000 accessions) and a set of over 280 Ae. tauschii Synthetic hexaploid wheat (SHW) (Triticum turgidum × Aegilops tauschii) lines to HGA infestation, and identified a couple of tolerant lines. Given that highly resistant lines have not been identified, we plan to screen more wheat accessions and synthetic hexaploid wheat lines in 2023. Under Objective 2A, sugarcane aphid (SCA) resistant forage sorghums were developed using male sterile backcrossing so that genetic stability (no cross-pollinating) would occur in the field. The genetic sources used to develop the backcrosses originated from grain sorghums previously developed for SCA resistance. The resistant forage sorghums used in breeding are now made available to the public. Under Objective 3A, we evaluated sugarcane aphids and the associated natural enemy guild during the growing season in 10 grain sorghum fields in each of four geographically distinct areas in Oklahoma and Texas. Under Objective 3B, a detailed sampling protocol was developed by ARS scientists at Stillwater, Oklahoma, and in conjunction with researchers at Oklahoma State University that included efficient sampling methods for sugarcane aphid predator and parasitoid guilds at two geographic locations in Oklahoma. The sampling protocol was used for two consecutive years and included in an ecological sampling model resulting in three published manuscripts on the predators and parasites in grain sorghum.

Accomplishments
1. The clonal diversity of sugarcane aphids from the U.S. and Brazil have been identified. ARS scientists at Stillwater, Oklahoma, Tifton, Georgia and Brazil identified the clonal diversity of the sugarcane aphids from 121 collections from the U.S. and Brazil. We determined using 8-9 Melanaphis spp. microsatellite markers that the multi-locus-lineage designated F (MLL-F) that remains a threat to sorghum production in the U.S. from 2013 to the present was the same lineage that invaded Brazil 6 years later. Genotyping results showed that all samples from the U.S. in 2019 and Brazil in 2020 had alleles identical to the predominant superclone MLL-F, and these were not the same as the MLL-C lineage that effects sugarcane. Knowing the genetic lineage of the two clones has helped identify the economically devastating MLL-F and the much less economically devastating MLL-C, the difference relates to millions of dollars used in the management costs for MLL-F.

2. Synoptic model of sugarcane aphid regional population dynamics. Sugarcane aphid is a pest of sorghum that depends on windborne migration to infest and damage sorghum fields at latitudes north of roughly mid-Texas. ARS scientists at Stillwater, Oklahoma, developed a computer based mathematical model which was tested to simulate within field population growth and northward migration of the aphid. The model captured salient features of population dynamics and migration. Testing showed that the model accurately predicted within field population growth and the timing of the first occurrence of migrant aphids at all test sites north of central Texas. Sorghum producers throughout the Great Plains states can track SCA infestations which is the impetus of management that can accurately predict populations all most in real time.

Review Publications
Muleta, K.T., Felderhoff, T., Winans, N., Walstead, R., Charles, J.R., Armstrong, J.S., Mamidi, S., Plott, C., Vogel, J.P., Lemaux, P.G., Mockler, T., Grimwood, J., Schmutz, J., Pressoir, G., Morris, G.P. 2022. The recent evolutionary rescue of a staple crop depended on over half a century of global germplasm exchange. Science Advances. 8. Article eabj4633.
Carey, C., Armstrong, J.S., Hayes, C., Hoback, W.W., Zarrabi, A. 2022. Evaluation of A3 cytoplasmic male sterile forage sorghum lines for resistance to sugarcane aphid. Planta. 255. Article 38. https://doi.org/10.1007/s00425-022-03820-7.
Armstrong, J.S., Hoback, W.W., Springer, T.L. 2021. Host suitability for the sugarcane aphid Melanaphis sacchari (Hemiptera: Aphididae) on sorghum, sorghum-sudangrass, millets and other forage grass species. Trends in Entomology. 17:1-11.
Faris, A.M., Elliott, N.C., Brewer, M.J. 2022. Suppression of the sugarcane aphid, Melanaphis sacchari Zehntner (Hemiptera: Aphididae), by resident natural enemies on susceptible and resistant sorghum hybrids. Environmental Entomology. 51(2):332-339. https://doi.org/10.1093/ee/nvab147.
Koralewski, T.E., Wang, H., Grant, W.E., Brewer, M.J., Elliott, N.C. 2022. Evaluation of areawide forecasts of wind-borne crop pests: Sugarcane aphid (Hemiptera: Aphididae) infestations of sorghum in the Great Plains of North America. Journal of Economic Entomology. https://doi.org/10.1093/jee/toac035.
Punnuri, S., Ayele, A., Harris-Shultz, K.R., Knoll, J.E., Coffin, A.W., Tadesse, H.K., Armstrong, J.S., Wiggins, T., Li, H., Sattler, S.E., Wallace, J. 2022. Genome-wide association mapping of resistance to the sorghum aphid in sorghum bicolor. Genomics. 114(4). Article 110408. https://doi.org/10.1016/j.ygeno.2022.110408.
Xu, X., Mornhinweg, D., Bernardo, A., Li, G., Bian, R., Steffensen, B.J., Bai, G. 2022. Characterization of Rsg2.a3: A new greenbug resistance allele at the Rsg2 locus from wild barley (Hordeum vulgare ssp. spontaneum). The Crop Journal. https://doi.org/10.1016/j.cj.2022.01.010.
Xu, X., Kolmer, J., Li, G., Tan, C., Carver, B.F., Bian, R., Bernardo, A., Bai, G. 2022. Identification and characterization of the novel leaf rust resistance gene Lr81 in wheat. Journal of Theoretical and Applied Genetics. Article 04145-5. https://doi.org/10.1007/s00122-022-04145-5.
Wang, H., Grant, W.E., Koralewski, T.E., Brewer, M.J., Elliott, N.C. 2021. Simulating migration of wind-borne pests: “Deconstructing” representation of the emigration process. Ecological Modelling. https://doi.org/10.1016/j.ecolmodel.2021.109742.
Koralewski, T.E., Wang, H., Grant, W.E., Brewer, M.J., Elliott, N.C., Westbrook, J.K. 2021. Modeling the dispersal of wind-borne pests: Sensitivity of infestation forecasts to uncertainty in parameterization of long-distance airborne dispersal. Agricultural and Forest Meteorology. 301-302. Article 108357. https://doi.org/10.1016/j.agrformet.2021.108357.
Harris-Shultz, K.R., Armstrong, J.S., Carvalho, G., Pereira Segundo, J., Ni, X. 2022. Melanaphis sorghi (Hemiptera: Aphididae) clonal diversity in the United States and Brazil. Insects. 13(5):416. https://doi.org/10.3390/insects13050416.
Brewer, M.J., Elliott, N.C., Esquivel, I.L., Jacobson, A.L., Faris, A.M., Szcepaniec, A., Elkins, B.H., Gordy, J.W., Pekarcik, A.J., Wang, H-H., Koralewski, T.E., Giles, K.L., Jessie, C.N., Grant, W.E. 2022. Natural enemies, mediated by landscape and weather conditions, shape response of the sorghum agroecosystem of North America to the invasive aphid Melanaphis sorghi. Frontiers in Insect Science. 2. Article 830997. https://doi.org/10.3389/finsc.2022.830997.
Elliott, N.C., Giles, K.L., Baum, K.A., Elzay, S.D. 2021. Quantitative assessment of aphid parasitoids and predators in central Oklahoma wheat fields during five growing seasons. Southwestern Entomologist. 46(4):833-842. https://doi.org/10.3958/059.046.0404.