Marker-trait association of Russian wheat aphid (Diuraphisnoxia) resistance in the global diversity set of wild barely

Tahmasebi, Zahra; Safari, Sara; Arminian, Ali; Fatehi, Foad

doi:10.22058/jpmb.2023.2004093.1275

Marker-trait association of Russian wheat aphid (Diuraphisnoxia) resistance in the global diversity set of wild barely

Document Type : Original research paper

Authors

Zahra Tahmasebi ¹

Sara Safari ²

Ali Arminian ¹

Foad Fatehi ³

¹ Faculty of Agriculture, Department of Agronomy and Plant Breeding, Ilam University, Ilam, Iran

² Department of Agronomy and Plant Breeding, Ilam University, Ilam, Iran

³ Department of Agriculture, Payam Noor University (PNU), Tehran, Iran

10.22058/jpmb.2023.2004093.1275

Abstract

Russian wheat aphid (RWA, Diuraphis noxia Kurdjumov), a common pest on barley around the world, can severely damage barley yield and grain quality. The present study aimed to identify simple sequence repeat markers associated with RWA resistance in wild barley (Hordeum vulgare subsp. spontaneum). A panel of 30 wild barely accessions was selected from the ICARDA gene bank and Iran to represent 10 Asia countries scattered along the natural geographic distribution of the species for RWA resistance. Five traits including leaf chlorosis, leaf rolling, chlorophyll a, b, and total chlorophyll concentration were evaluated. Fourteen SSR markers were used to study genetic diversity. The relationship of 52 polymorphic SSR markers with the associated RWA resistance traits was tested using general linear model (GLM) and mixed linear model (MLM) approaches. The population structure analysis revealed seven subpopulations in the entire collection (K=7). Eleven trait marker-trait associations (MTA) were identified on chromosomes 1H, 2H, 3H, 4H, and 7H. Markers Bmag007, Bmag6, Bmac0399, Bmag0125, and EBmac0701 which exhibited significant associations with RWA resistance traits. All five markers were associated with traits in both GLM and MLM analyzes. This study identified novel genomic regions putatively linked with RWA resistance traits, which could be further investigated for shedding light on the genetic architecture of RWA resistance in barley. The findings could be useful for using the RWA resistance accessions of H. spontaneum as parents for breeding barley cultivars.

Keywords

Association analysis

seedling resistance

SSR marker

subpopulations

Able, J.A., Langridge, P., and Milligan, A.S. (2007). Capturing diversity in the cereals: many options but little promiscuity. Trends Plant Sci 12(2): 71-79. doi: 10.1016/j.tplants.2006.12.002.

Ahman, I., and Bengtsson, T. (2019). Introgression of resistance to Rhopalosiphum padi L. from wild barley into cultivated barley facilitated by doubled haploid and molecular marker techniques. Theor Appl Genet 132: 1397-1408.

Alvarez, M.F., Mosquera, T., and Blair, M.W. (2014). The use of association genetics approaches in plant breeding. Plant Breed Rev 38: 17-68.

Arora, S., Steuernagel, B., Gaurav, K., Chandramohan, S., Long, Y., Matny, O., Johnson, R., Enk, J., Periyannan, S., Singh, N., Asyraf Md Hatta, M., Athiyannan, N., Cheema, J., Yu, G., Kangara, N., Ghosh, S., Szabo, L.J., Poland, J., Bariana, H., et al. (2019). Resistance gene cloning from a wild crop relative by sequence capture and association genetics. Nat Biotechnol 37(2): 139-143. doi: 10.1038/s41587-018-0007-9.

Bengtsson, T., Manninen, O., Jahoor, A., and Orabi, J. (2017). Genetic diversity, population structure and linkage disequilibrium in Nordic spring barley (Hordeum vulgare L. subsp. vulgare). Genet Resour Crop Evol 64: 2021-2033.

Bradbury, P.J., Zhang, Z., Kroon, D.E., Casstevens, T.M., Ramdoss, Y., and Buckler, E.S. (2007). TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23(19): 2633-2635. doi: 10.1093/bioinformatics/btm308.

Burd, J.D., and Elliott, N.C. (1996). Changes in chlorophyll a fluorescence induction kinetics in cereals infested with Russian wheat aphid (Homopetra: Aphididea). J Econ Entomol 89(5): 1332-1337.

Cakir, M., Vitou, J., Kollehn, D., Lawson, W., Ilbi, H., Haley, S., Peairs, F., Mornhinweg, D., Bohssini, M., and Ogbonnaya, F. (2009). "A global effort in breeding for resistance to Russian wheat aphid in wheat and barley", in: 19th International Triticeae Mapping Initiative - 3rd COST Tritigen. (Clermont-Ferrand, France).

Capo-Chichi, L.J.A., Elakhdar, A., Kubo, T., Nyachiro, J., Juskiw, P., Capettini, F., Slaski, J.J., Ramirez, G.H., and Beattie, A.D. (2022). Genetic diversity and population structure assessment of Western Canadian barley cooperative trials. Front Plant Sci 13: 1006719. doi: 10.3389/fpls.2022.1006719.

Collard, B.C., and Mackill, D.J. (2008). Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc Lond B Biol Sci 363(1491): 557-572. doi: 10.1098/rstb.2007.2170.

Dahleen, L.S., Bregitzer, P., Mornhinweg, D., and Jackson, E.W. (2012). Association mapping of Russian wheat aphid resistance in barley as a method to identify diversity in the national small grains collection. Crop Sci 52(4): 1651-1662.

Dahleen, L.S., Bregitzer, P., Mornhinweg, D., and Klos, K.E. (2015). Genetic diversity for Russian wheat aphid resistance as determined by genome‐wide association mapping and inheritance in progeny. Crop Sci 55(5): 1925-1933.

Fouche, A., Verhoeven, R., Hewitt, P., Walters, M., Friel, C., and De Jager, J. (1984). Russian aphid (Diuraphis noxia) feeding damage on wheat, related cereals and a Bromus grass species. Tech commun - Repub S Afr Dep Agric: 22–33.

Franzen, L.D., Gutsche, A.R., Heng-Moss, T.M., Higley, L.G., Sarath, G., and Burd, J.D. (2014). Physiological and biochemical responses of resistant and susceptible wheat to injury by Russian wheat aphid. J Econ Entomol 100(5): 1692-1703.

Gharaghanipor, N., Arzani, A., Rahimmalek, M., and Ravash, R. (2022). Physiological and transcriptome indicators of salt tolerance in wild and cultivated barley. Front Plant Sci 13: 819282. doi: 10.3389/fpls.2022.819282.

Girma, M., Wilde, G.E., and Harvey, T. (1993). Russian wheat aphid (Homoptera: Aphididae) affects yield and quality of wheat. J Econ Entomol 86(2): 594-601.

Gray, S.N., Robinson, P., Wilding, N., and Markham, P. (1990). Effect of oleic acid on vegetative growth of the aphid-pathogenic fungus Erynia neoaphidis. FEMS Microbiol Ecol 68(1-2): 131-136.

Gupta, P.K., Rustgi, S., and Kulwal, P.L. (2005). Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Mol Biol 57(4): 461-485. doi: 10.1007/s11103-005-0257-z.

Heng-Moss, T., Ni, X., Macedo, T., Markwell, J.P., Baxendale, F.P., Quisenberry, S., and Tolmay, V. (2003). Comparison of chlorophyll and carotenoid concentrations among Russian wheat aphid (Homoptera: Aphididae)-infested wheat isolines. J Econ Entomol 96(2): 475-481.

Joukhadar, R., El-Bouhssini, M., Jighly, A., and Ogbonnaya, F. (2013). Genome-wide association mapping for five major pest resistances in wheat. Mol Breed 32: 943-960.

Kisten, L., Tolmay, V.L., Mathew, I., Sydenham, S.L., and Venter, E. (2020). Genome-wide association analysis of Russian wheat aphid (Diuraphis noxia) resistance in Dn4 derived wheat lines evaluated in South Africa. PLoS One 15(12): e0244455. doi: 10.1371/journal.pone.0244455.

Kulwal, P.L., and Singh, R. (2021). Association mapping in plants. Methods Mol Biol 2264: 105-117. doi: 10.1007/978-1-0716-1201-9_8.

Leybourne, D.J., Valentine, T.A., Robertson, J.A.H., Perez-Fernandez, E., Main, A.M., Karley, A.J., and Bos, J.I.B. (2019). Defence gene expression and phloem quality contribute to mesophyll and phloem resistance to aphids in wild barley. J Exp Bot 70(15): 4011-4026. doi: 10.1093/jxb/erz163.

Macaulay, M., Ramsay, L., and Åhman, I. (2020). Quantitative trait locus for resistance to the aphid Rhopalosiphum padi L. in barley (Hordeum vulgare L.) is not linked with a genomic region for gramine concentration. Arthropod-Plant Int 14: 57-65.

Macedo, T.B. (2003). Physiological responses of plants to piercing-sucking arthropods. Doctora of Philosophy, The University of Nebraska-Lincoln.

Mittal, S., Dahleen, L.S., and Mornhinweg, D. (2008). Locations of quantitative trait loci conferring Russian wheat aphid resistance in barley germplasm STARS‐9301B. Crop Sci 48(4): 1452-1458.

Moreira, X., Abdala-Roberts, L., Gols, R., and Francisco, M. (2018). Plant domestication decreases both constitutive and induced chemical defences by direct selection against defensive traits. Sci Rep 8(1): 12678.

Nei, M. (1973). Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci U S A 70(12): 3321-3323. doi: 10.1073/pnas.70.12.3321.

Nieto Lopez, R.M., and Blake, T.K. (1994). Russian wheat aphid resistance in barley: inheritance and linked molecular markers. Crop Sci 34(3): 655-659.

Oliver, R.E., Obert, D.E., Hu, G., Bonman, J.M., O'Leary-Jepsen, E., and Jackson, E.W. (2010). Development of oat-based markers from barley and wheat microsatellites. Genome 53(6): 458-471. doi: 10.1139/g10-021.

Pritchard, J.K., Stephens, M., and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155(2): 945-959. doi: 10.1093/genetics/155.2.945.

Radchenko, E.E., Abdullaev, R.A., and Anisimova, I.N. (2022). Genetic resources of cereal crops for Aphid resistance. Plants 11(11): 1490. doi: 10.3390/plants11111490.

Raman, H., and Read, B.J. (2000). Molecular breeding for resistance against Russian wheat aphid in Australian barley. J Agric Genome 5: 1-7.

Rohlf, F.J. (1988). NTSYS-pc: numerical taxonomy and multivariate analysis system. Exeter Publishing.

Singh, B., Bhatia, D., Narang, D., Kaur, R., and Chhuneja, P. (2023). High-resolution genetic mapping of QTL governing resistance to corn leaf aphid, Rhopalosiphum maidis (Fitch) in barley. Cereal Res Commun 51(2): 379-389.

Tocho, E., Ricci, M., Tacaliti, M., Giménez, D., Acevedo, A., Lohwasser, U., Börner, A., and Castro, A. (2012). Mapping resistance genes conferring tolerance to RWA (Diuraphis noxia) in barley (Hordeum vulgare). Euphytica 188: 239-251.

Tolmay, V., Jankielsohn, A., and Sydenham, S. (2013). Resistance evaluation of wheat germplasm containing Dn4 or Dny against R ussian wheat aphid biotype RWASA 3. J Appl Entomol 137(6): 476-480.

Tolmay, V.L., Sydenham, S.L., Sikhakhane, T.N., Nhlapho, B.N., and Tsilo, T.J. (2020). Elusive diagnostic markers for Russian wheat aphid resistance in bread wheat: deliberating and reviewing the status quo. Int J Mol Sci 21(21): 8271. doi: 10.3390/ijms21218271.

Webster, J., Baker, C., and Porter, D. (1991). Detection and mechanisms of Russian wheat aphid (Homoptera: Aphididae) resistance in barley. J Econ Entomol 84(2): 669-673.

Zhang, H., Mittal, N., Leamy, L.J., Barazani, O., and Song, B.H. (2017). Back into the wild—Apply untapped genetic diversity of wild relatives for crop improvement. Evol Appl 10(1): 5-24.

Zohary, D., and Hopf, M. (2000). Domestication of plants in the Old World: The origin and spread of cultivated plants in West Asia, Europe and the Nile Valley. Oxford University Press.