Multi-locus genome-wide association study of chickpea reference set identifies genetic determinants of Pratylenchus thornei resistance

Article

Channale, Sonal, Thompson, John P., Varshney, Rajeev K., Thudi, Mahendar and Zwart, Rebecca S.. 2023. "Multi-locus genome-wide association study of chickpea reference set identifies genetic determinants of Pratylenchus thornei resistance." Frontiers in Plant Science. 14. https://doi.org/10.3389/fpls.2023.1139574
Article Title

Multi-locus genome-wide association study of chickpea reference set identifies genetic determinants of Pratylenchus thornei resistance

ERA Journal ID200524
Article CategoryArticle
AuthorsChannale, Sonal, Thompson, John P., Varshney, Rajeev K., Thudi, Mahendar and Zwart, Rebecca S.
Journal TitleFrontiers in Plant Science
Journal Citation14
Article Number1139574
Number of Pages12
Year2023
PublisherFrontiers Media SA
ISSN1664-462X
Digital Object Identifier (DOI)https://doi.org/10.3389/fpls.2023.1139574
Web Address (URL)https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2023.1139574/full
AbstractPratylenchus thornei is an economically important species of root-lesion nematode adversely affecting chickpea (Cicer arietinum) yields globally. Integration of resistant crops in farming systems is recognised as the most effective and sustainable management strategy for plant-parasitic nematodes. However, breeding for P. thornei resistance in chickpea is limited by the lack of genetic diversity. We deployed a genome-wide association approach to identify genomic regions and candidate genes associated with P. thornei resistance in 285 genetically diverse chickpea accessions. Chickpea accessions were phenotyped for P. thornei resistance in replicated glasshouse experiments performed for two years (2018 and 2020). Whole genome sequencing data comprising 492,849 SNPs were used to implement six multi-locus GWAS models. Fourteen chickpea genotypes were found to be resistant to P. thornei. Of the six multi-locus GWAS methods deployed, FASTmrMLM was found to be the best performing model. In all, 24 significant quantitative trait nucleotides (QTNs) were identified, of which 13 QTNs were associated with lower nematode population density and 11 QTNs with higher nematode population density. These QTNs were distributed across all of the chickpea chromosomes, except chromosome 8. We identified, receptor-linked kinases (RLKs) on chromosomes 1, 4 and 6, GDSL-like Lipase/Acylhydrolase on chromosome 3, Aspartic proteinase-like and Thaumatin-like protein on chromosome 4, AT-hook DNA-binding and HSPRO2 on chromosome 6 as candidate genes for P. thornei resistance in the chickpea reference set. New sources of P. thornei resistant genotypes were identified that can be harnessed into breeding programs and putative candidate P. thornei resistant genes were identified that can be explored further to develop molecular markers and accelerate the incorporation of improved P. thornei resistance into elite chickpea cultivars. Copyright © 2023 Channale, Thompson, Varshney, Thudi and Zwart.
Keywordscandidate resistance genes; chickpea; Cicer arietinum; root-lesion nematode; Pratylenchus thornei; GWAS
ANZSRC Field of Research 2020300407. Crop and pasture nutrition
Byline AffiliationsCentre for Crop Health
Institute for Life Sciences and the Environment
Centre for Crop Health (Research)
Murdoch University
Dr. Rajendra Prasad Central Agricultural University, India
School of Agriculture and Environmental Science
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Thompson, J. P., Rostad, H. E. and Whish, J. P. M.. 2017. "Survival of root-lesion nematodes (Pratylenchus thornei) after wheat growth in a vertisol is influenced by rate of progressive soil desiccation." Annals of Applied Biology. 170 (1), pp. 78-88. https://doi.org/10.1111/aab.12316
Linear modelling of soil temperature effects on root lesion nematode population densities in R [Blog post]
Sparks, Adam H. and Thompson, John P.. 2018. "Linear modelling of soil temperature effects on root lesion nematode population densities in R [Blog post]." Open Plant Pathology Notes. February 2018, pp. 1-24. https://doi.org/10.5281/zenodo.1173391
Predicting the slow decline of root lesion nematodes (Pratylenchus thornei) during host-free fallow to improve farm management
Whish, J. P. M., Thompson, J. P., Clewett, T. G., Wood, J. and Rostad, H. E.. 2017. "Predicting the slow decline of root lesion nematodes (Pratylenchus thornei) during host-free fallow to improve farm management." European Journal of Agronomy. 91, pp. 44-53. https://doi.org/10.1016/j.eja.2017.09.012
Survival of root-lesion nematode Pratylenchus neglectus during progressive soil desiccation after growth of wheat in a vertisol
Thompson, J. P., Rostad, H. E. and Whish, J. P. M.. 2017. "Survival of root-lesion nematode Pratylenchus neglectus during progressive soil desiccation after growth of wheat in a vertisol." Biology and Fertility of Soils. 53 (3), pp. 357-366. https://doi.org/10.1007/s00374-017-1184-2
The first genetic map of pigeon pea based on diversity arrays technology (DArT) markers
Yang, Shi Ying, Saxena, Rachit K., Kulwal, Pawan L., Ash, Gavin J., Dubey, Anuja, Harper, John D. I., Upadhyaya, Hari D., Gothalwal, Ragini, Kilian, Andrzej and Varshney, Rajeev K.. 2011. "The first genetic map of pigeon pea based on diversity arrays technology (DArT) markers." Journal of Genetics. 90 (1), pp. 103-109. https://doi.org/10.1007/s12041-011-0050-5
What is the impact of winter grain crops on Pratylenchus thornei grown in rotation with tolerant and intolerant wheat?
Owen, K. J., Clewett, T. G. and Thompson, J. P.. 2012. "What is the impact of winter grain crops on Pratylenchus thornei grown in rotation with tolerant and intolerant wheat?" MacLeod, W. J. (ed.) 7th Australasian Soilborne Diseases Symposium. Freemantle, Australia 18 - 20 Sep 2012
Simultaneous selection of wheat plants with resistance to root-lesion nematodes, crown rot and yellow spot
Sheedy, J. G., Thompson, J. P. and Reen, R. A.. 2012. "Simultaneous selection of wheat plants with resistance to root-lesion nematodes, crown rot and yellow spot." MacLeod, W. J. (ed.) 7th Australasian Soilborne Diseases Symposium. Freemantle, Australia 18 - 20 Sep 2012
Yield response in chickpea cultivars and wheat following crop rotations affecting population densities of Pratylenchus thornei and arbuscular mycorrhizal fungi
Reen, R. A., Thompson, J. P., Clewett, T. G., Sheedy, J. G. and Bell, K. L.. 2014. "Yield response in chickpea cultivars and wheat following crop rotations affecting population densities of Pratylenchus thornei and arbuscular mycorrhizal fungi." Crop and Pasture Science. 65 (5), pp. 428-441. https://doi.org/10.1071/CP13441
Microsatellite mapping identifies TTKST-effective stem rust resistance gene in wheat cultivars VL404 and Janz
Bansal, Urmil K., Zwart, Rebecca, Bhavani, Sridhar, Wanyera, Ruth, Gupta, Vidya and Bariana, Harbans S.. 2012. "Microsatellite mapping identifies TTKST-effective stem rust resistance gene in wheat cultivars VL404 and Janz." Molecular Breeding: new strategies in plant improvement. 30 (4), pp. 1757-1765. https://doi.org/10.1007/s11032-012-9759-y
Genomic and functional characterization of coleopteran insectspecific α-amylase inhibitor gene from Amaranthus species
Bhide, A., Channale, Sonal M., Yadav, Yashpal, Bhattacharjee, Kabita, Pawar, Pankaj K., Maheshwari, V. L., Gupta, Vidya S., Ramasamy, Sureshkumar and Giri, Ashok P.. 2017. "Genomic and functional characterization of coleopteran insectspecific α-amylase inhibitor gene from Amaranthus species." Plant Molecular Biology. 94 (3), pp. 319-332. https://doi.org/10.1007/s11103-017-0609-5
Root lesion nematode and crown rot - double trouble!
Daniel, Richard, Simpfendorfer, Steven, McMullen, Guy and Thompson, John. 2011. "Root lesion nematode and crown rot - double trouble!" 2011 GRDC Grains Research Update, Miles. Miles, Australia 01 Mar 2011 Canberra, Australia.
Introgression of resistance to Pratylenchus from wild Cicer species into Australian chickpea cultivars
Reen, R. A., Thompson, J. P. and Knights, E. J.. 2011. "Introgression of resistance to Pratylenchus from wild Cicer species into Australian chickpea cultivars." Tran-Nguyen, Lucy (ed.) 4th Asian Conference on Plant Pathology and the 18th Biennial Australasian Plant Pathology Society Conference (ACPP/APPS 2011): New Frontiers in Plant Pathology for Asia and Oceania. Darwin, Australia 26 - 29 Apr 2011
Cotton stunting corrected by inoculation with arbuscular-mycorrhizal fungal spores
Thompson, J. P., Seymour, N. P. and Clewett, T. G.. 2011. "Cotton stunting corrected by inoculation with arbuscular-mycorrhizal fungal spores." Tran-Nguyen, Lucy (ed.) 4th Asian Conference on Plant Pathology and the 18th Biennial Australasian Plant Pathology Society Conference (ACPP/APPS 2011): New Frontiers in Plant Pathology for Asia and Oceania. Darwin, Australia 26 - 29 Apr 2011
Simultaneous selection of wheat lines with resistance to root lesion nematodes, crown rot and yellow spot
Sheedy, Jason, Reen, Roslyn, Thompson, John and Clewett, Tim. 2011. "Simultaneous selection of wheat lines with resistance to root lesion nematodes, crown rot and yellow spot." Wheat Breeding Assembly 2011. Perth, Australia 24 - 26 Aug 2011 Australia.
Estimating number of resistance genes to root-legion nematodes from synthetic hexaploids wheat lines
Thompson, John P., Zwart, Rebecca S. and Butler, David. 2011. "Estimating number of resistance genes to root-legion nematodes from synthetic hexaploids wheat lines." Wheat Breeding Assembly 2011. Perth, Australia 24 - 26 Aug 2011 Australia.
Identifying a non-destructive technique to assess nematode tolerance in wheat variety trials
Whish, Jeremy, Thompson, John, Clewett, Tim and Lawrence, John. 2012. "Identifying a non-destructive technique to assess nematode tolerance in wheat variety trials." 16th Australian Agronomy Conference: Capturing Opportunities and Overcoming Obstacles in Australian Agronomy (ASA 2012). Armidale, Australia 14 - 18 Oct 2012 Australia.
Common QTL and multi-purpose markers for the resistance of five synthetic hexaploids against two species of root lesion nematode
Khoo, Kelvin H. P., Sheedy, Jason, Thompson, John, Hu, Chih-Fang, Vassos, Elysia, Fox, Rebecca, Chalmers, Ken and Mather, Diane E.. 2013. "Common QTL and multi-purpose markers for the resistance of five synthetic hexaploids against two species of root lesion nematode." Wheat Breeding Assembly 2013. Brisbane, Australia 16 - 19 Jul 2013
Highly heritable resistance to root-lesion nematode (Pratylenchus thornei) in Australian chickpea germplasm observed using an optimised glasshouse method and multi-environment trial analysis
Rodda, M. S., Hobson, K. B., Forknall, C. R., Daniel, R. P., Fanning, J. P., Pounsett, D. D., Simpfendorfer, S., Moore, K. J., Owen, K. J., Sheedy, J. G., Thompson, J. P., Hollaway, G. J. and Slater, A. T.. 2016. "Highly heritable resistance to root-lesion nematode (Pratylenchus thornei) in Australian chickpea germplasm observed using an optimised glasshouse method and multi-environment trial analysis." Australasian Plant Pathology. 45 (3), pp. 309-319. https://doi.org/10.1007/s13313-016-0409-4
Modelling population densities of root-lesion nemaotde (Pratylenchus thornei) from soil profile temperatures to choose an optimum sowing date for wheat in a subtropical region
Thompson, J. P.. 2015. "Modelling population densities of root-lesion nemaotde (Pratylenchus thornei) from soil profile temperatures to choose an optimum sowing date for wheat in a subtropical region." Field Crops Research. 183, pp. 50-55. https://doi.org/10.1016/j.fcr.2015.07.005
Characterization of two coleopteran a-amylases and molecular insights into their differential inhibition by synthetic a-amylase inhibitor, acarbose
Channale, Sonal M., Bhide, Amey J., Yadav, Yashpal, Kashyap, Garima, Pawar, Pankaj K., Maheshwari, V. L., Ramasamy, Sureshkumar and Giri, Ashok P.. 2016. "Characterization of two coleopteran a-amylases and molecular insights into their differential inhibition by synthetic a-amylase inhibitor, acarbose." Insect Biochemistry and Molecular Biology. 74, pp. 1-11. https://doi.org/10.1016/j.ibmb.2016.04.009
Temperature response of root-lesion nematode (Pratylenchus thornei) reproduction on wheat cultivars has implications for resistance screening and wheat production
Thompson, J. P., Clewett, T. G. and O'Reilly, M. M.. 2015. "Temperature response of root-lesion nematode (Pratylenchus thornei) reproduction on wheat cultivars has implications for resistance screening and wheat production." Annals of Applied Biology. 167 (1), pp. 1-10. https://doi.org/10.1111/aab.12187
Optimising initial population density, growth time and nitrogen nutrition for assessing resistance of wheat cutivars to root-lesion nematode (Pratylenchus thornei)
Thompson, J. P., Clewett, T. G. and O'Reilly, M. M.. 2015. "Optimising initial population density, growth time and nitrogen nutrition for assessing resistance of wheat cutivars to root-lesion nematode (Pratylenchus thornei)." Australasian Plant Pathology. 44 (2), pp. 133-147. https://doi.org/10.1007/s13313-015-0347-6
Wheat biomass and yield increased when populations of the root-lesion nematode (Pratylenchus thornei) were reduced through sequential rotation of partially resistant winter and summer crops
Owen, K. J., Clewett, T. G., Bell, K. L. and Thompson, J. P.. 2014. "Wheat biomass and yield increased when populations of the root-lesion nematode (Pratylenchus thornei) were reduced through sequential rotation of partially resistant winter and summer crops." Crop and Pasture Science. 65 (3), pp. 227-241. https://doi.org/10.1071/CP13295
Cereal cultivars can be ranked consistently for resistance to root-lesion nematodes (Pratylenchus thornei & P. neglectus) using diverse procedures
Sheedy, J. G., McKay, A. C., Lewis, J., Vanstone, V. A., Fletcher, S., Kelly, A. and Thompson, J. P.. 2015. "Cereal cultivars can be ranked consistently for resistance to root-lesion nematodes (Pratylenchus thornei & P. neglectus) using diverse procedures." Australasian Plant Pathology. 44 (2), pp. 175-182. https://doi.org/10.1007/s13313-014-0333-4
Root-lesion nematodes - crop rotations and varietal impacts on nematode populations
Owen, Kirsty, Clewett, Tim, Reen, Ros, Sheedy, Jason and Thompson, John. 2011. "Root-lesion nematodes - crop rotations and varietal impacts on nematode populations." 2011 GRDC Advisor Update, Goondiwindi. Goondiwindi, Australia 02 - 03 Mar 2011 Canberra, Australia.
Pre-breeding wheat for resistance to root-lesion nematodes
Thompson, John, Sheedy, Jason, Robinson, Neil, Reen, Ros, Clewett, Tim and Lin, Jing. 2012. "Pre-breeding wheat for resistance to root-lesion nematodes." 2012 GRDC Grains Research Update, Goondiwindi. Goondiwindi, Australia 12 Apr 2012 Canberra, Australia.
Summer crop decisions and root lesion nematodes
Owen, Kirsty, Clewett, Tim and Thompson, John. 2013. "Summer crop decisions and root lesion nematodes." 2013 GRDC Grains Research Update, Bellata and Inglestone. Bellata and Inglestone, Australia 16 Jul 2013 Canberra, Australia.
Latest nematode summer and winter crop rotation results
Owen, Kirsty, Clewett, Tim and Thompson, John. 2014. "Latest nematode summer and winter crop rotation results." 2014 GRDC Grains Research Update, Goondiwindi. Goondiwindi, Australia 04 Mar 2014 Canberra, Australia.
How nematodes reduce yield
Whish, J. P. M., Thompson, J. P., Clewett, T. G., Lawrence, J. L. and Wood, J.. 2014. "How nematodes reduce yield." 2014 GRDC Grains Research Update, Goondiwindi. Goondiwindi, Australia 04 Mar 2014 Canberra, Australia.
Biochemical, structural and functional diversity between two digestive α-amylases from Helicoverpa armigera
Bhide, Amey J., Channale, Sonal M., Patil, Sucheta S., Gupta, Vidya S., Ramasamy, Sureshkumar and Giri, Ashok P.. 2015. "Biochemical, structural and functional diversity between two digestive α-amylases from Helicoverpa armigera." Biochimica et Biophysica Acta (BBA): General Subjects. 1850 (9), pp. 1719-1728. https://doi.org/10.1016/j.bbagen.2015.04.008
Resistance to root-lesion nematodes (Pratylenchus thornei and P. neglectus) in synthetic hexaploid wheats and their durum and Aegilops tauschii parents
Thompson, J. P.. 2008. "Resistance to root-lesion nematodes (Pratylenchus thornei and P. neglectus) in synthetic hexaploid wheats and their durum and Aegilops tauschii parents." Australian Journal of Agricultural Research. 59 (5), pp. 432-446. https://doi.org/10.1071/AR07222
Field inoculation with arbuscular-mycorrhizal fungi overcomes phosphorus and zinc deficiencies of linseed (Linum usitatissimum) in a vertisol subject to long-fallow disorder
Thompson, J. P., Clewett, T. G. and Fiske, M. L.. 2013. "Field inoculation with arbuscular-mycorrhizal fungi overcomes phosphorus and zinc deficiencies of linseed (Linum usitatissimum) in a vertisol subject to long-fallow disorder." Plant and Soil: international journal on plant-soil relationships. 371 (1-2), pp. 117-137. https://doi.org/10.1007/s11104-013-1679-z
QTL mapping of multiple foliar disease and root-lesion nematode resistances in wheat
Zwart, R. S., Thompson, J. P., Milgate, A. W., Bansal, U. K., Williamson, P. M., Raman, H. and Bariana, H. S.. 2010. "QTL mapping of multiple foliar disease and root-lesion nematode resistances in wheat." Molecular Breeding: new strategies in plant improvement. 26 (1), pp. 107-124. https://doi.org/10.1007/s11032-009-9381-9
Inheritance of resistance to root-lesion nematodes (Pratylenchus thornei and P. neglectus) in five doubled-haploid populations of wheat
Thompson, John P., Zwart, Rebecca S. and Butler, David. 2012. "Inheritance of resistance to root-lesion nematodes (Pratylenchus thornei and P. neglectus) in five doubled-haploid populations of wheat." Euphytica: international journal on plant breeding. 188 (2), pp. 209-219. https://doi.org/10.1007/s10681-012-0689-x
Crop rotation for the management of root-lesion nematodes in the northern grain region of Australia
Owen, K., Clewett, T. and Thompson, J.. 2008. "Crop rotation for the management of root-lesion nematodes in the northern grain region of Australia." Hodda, Mike (ed.) 5th International Congress of Nematology (5ICN 2008): Nematodes Down Under. Brisbane, Australia 13 - 18 Jul 2008 Canberra, Australia.
Survey for root-lesion and stunt nematodes in the northern Australian grain region
Thompson, J. P., Clewett, T. G., Reen, R. A., Sheedy, J. G. and O'Reilly, M. M.. 2008. "Survey for root-lesion and stunt nematodes in the northern Australian grain region." Hodda, Mike (ed.) 5th International Congress of Nematology (5ICN 2008): Nematodes Down Under. Brisbane, Australia 13 - 18 Jul 2008 Canberra, Australia.
Crop rotation to replace nematicide treatments for assessing chickpea varietal tolerance to Pratylenchus thornei
Reen, R. A., Clewett, T. G. and Thompson, J. P.. 2008. "Crop rotation to replace nematicide treatments for assessing chickpea varietal tolerance to Pratylenchus thornei." Hodda, Mike (ed.) 5th International Congress of Nematology (5ICN 2008): Nematodes Down Under. Brisbane, Australia 13 - 18 Jul 2008 Canberra, Australia.
Evaluating wheat for tolerance and resistance to root-lesion nematodes
Thompson, J. P., Clewett, T. G., Sheedy, J. G. and Seymour, N. P.. 2008. "Evaluating wheat for tolerance and resistance to root-lesion nematodes." Hodda, Mike (ed.) 5th International Congress of Nematology (5ICN 2008): Nematodes Down Under. Brisbane, Australia 13 - 18 Jul 2008 Canberra, Australia.
Resistance to the root-lesion nematode Pratylenchus thornei in wheat landraces and cultivars from the West Asia and North Africa (WANA) region
Thompson, J. P., O'Reilly, M. M. and Clewett, T. G.. 2009. "Resistance to the root-lesion nematode Pratylenchus thornei in wheat landraces and cultivars from the West Asia and North Africa (WANA) region." Crop and Pasture Science. 60 (12), pp. 1209-1217. https://doi.org/10.1071/CP09159
Root-lesion nematodes (Pratylenchus thornei and P. neglectus): a review of recent progress in managing a significant pest of grain crops in northern Australia
Thompson, J. P., Owen, K. J., Stirling, G. R. and Bell, M. J.. 2008. "Root-lesion nematodes (Pratylenchus thornei and P. neglectus): a review of recent progress in managing a significant pest of grain crops in northern Australia." Australasian Plant Pathology. 37 (3), pp. 235-242. https://doi.org/10.1071/AP08021
Inheritance of resistance to root-lesion nematode (Pratylenchus thornei) in wheat landraces and cultivars from the West Asia and North Africa (WANA) region
Thompson, J. P. and Seymour, N. P.. 2011. "Inheritance of resistance to root-lesion nematode (Pratylenchus thornei) in wheat landraces and cultivars from the West Asia and North Africa (WANA) region." Crop and Pasture Science. 62 (1), pp. 82-93. https://doi.org/10.1071/CP10309
Stunted cotton (Gossypium hirsutum L.) fully recovers biomass and yield of seed cotton after delayed root inoculation with spores of an arbuscular mycorrhizal fungus (Glomus mosseae)
Thompson, J. P., Seymour, N. P. and Clewett, T. G.. 2012. "Stunted cotton (Gossypium hirsutum L.) fully recovers biomass and yield of seed cotton after delayed root inoculation with spores of an arbuscular mycorrhizal fungus (Glomus mosseae)." Australasian Plant Pathology. 41 (4), pp. 431-437. https://doi.org/10.1007/s13313-012-0137-3
Root-lesion nematode (Pratylenchus thornei) reduces nutrient response, biomass and yield of wheat in sorghum-fallow-wheat cropping systems in a subtropical environment
Thompson, J. P., Mackenzie, J. and Sheedy, G. H.. 2012. "Root-lesion nematode (Pratylenchus thornei) reduces nutrient response, biomass and yield of wheat in sorghum-fallow-wheat cropping systems in a subtropical environment." Field Crops Research. 137, pp. 126-140. https://doi.org/10.1016/j.fcr.2012.08.011
Pratylenchus thornei populations reduce water uptake in intolerant wheat cultivars
Whish, J. P. M., Thompson, J. P., Clewett, T. G., Lawrence, J. L. and Wood, J.. 2014. "Pratylenchus thornei populations reduce water uptake in intolerant wheat cultivars." Field Crops Research. 161, pp. 1-10. https://doi.org/10.1016/j.fcr.2014.02.002
Pre-cropping with canola decreased Pratylenchus thornei populations, arbuscular mycorrhizal fungi, and yield of wheat
Owen, K. J., Clewett, T. G. and Thompson, J. P.. 2010. "Pre-cropping with canola decreased Pratylenchus thornei populations, arbuscular mycorrhizal fungi, and yield of wheat." Crop and Pasture Science. 61 (5), pp. 399-410. https://doi.org/10.1071/CP09345
Detection of Polymyxa graminis in a barley crop in Australia
Thompson, J. P., Clewett, T. G., Jennings, R. E., Sheedy, J. G., Owen, K. J. and Persley, D. M.. 2011. "Detection of Polymyxa graminis in a barley crop in Australia." Australasian Plant Pathology. 40 (1), pp. 66-75. https://doi.org/10.1007/s13313-010-0015-9
Hybridisation of Australian chickpea cultivars with wild Cicer spp. increases resistance to root-lesion nematodes (Pratylenchus thornei and P. neglectus)
Thompson, John P., Reen, Roslyn A., Clewett, Timothy G., Sheedy, Jason G., Kelly, Alison M., Gogel, Beverley J. and Knights, Edward J.. 2011. "Hybridisation of Australian chickpea cultivars with wild Cicer spp. increases resistance to root-lesion nematodes (Pratylenchus thornei and P. neglectus)." Australasian Plant Pathology. 40 (6), pp. 601-611. https://doi.org/10.1007/s13313-011-0089-z
First record of stubby-root nematode (Paratrichodorus porosus) associated with barley in Australia
Sheedy, J. G., Clewett, T. G., Hodda, M. and Thompson, J. P.. 2010. "First record of stubby-root nematode (Paratrichodorus porosus) associated with barley in Australia." Australasian Plant Disease Notes. 5 (1), pp. 66-69. https://doi.org/10.1071/DN10024
Occurrence of root-lesion nematodes (Pratylenchus thornei and P. neglectus) and stunt nematode (Merlinius brevidens) in the northern grain region of Australia
Thompson, J. P., Clewett, T. G., Sheedy, J. G., Reen, R. A., O'Reilly, M. M. and Bell, K. L.. 2010. "Occurrence of root-lesion nematodes (Pratylenchus thornei and P. neglectus) and stunt nematode (Merlinius brevidens) in the northern grain region of Australia." Australasian Plant Pathology. 39 (3), pp. 254-264. https://doi.org/10.1071/AP09094
Resistance to the root-lesion nematode Pratylenchus thornei of Iranian landrace wheat
Sheedy, J. G. and Thompson, J. P.. 2009. "Resistance to the root-lesion nematode Pratylenchus thornei of Iranian landrace wheat." Australasian Plant Pathology. 38 (5), pp. 478-489. https://doi.org/10.1071/AP09030
Diploid and tetraploid progenitors of wheat are valuable sources of resistance to the root lesion nematode Pratylenchus thornei
Sheedy, J. G., Thompson, J. P. and Kelly, A.. 2012. "Diploid and tetraploid progenitors of wheat are valuable sources of resistance to the root lesion nematode Pratylenchus thornei." Euphytica: international journal on plant breeding. 186 (2), pp. 377-391. https://doi.org/10.1007/s10681-011-0617-5
Evaluation of genetic diversity of Fusarium head blight resistance in European winter wheat
Zwart, Rebecca S., Muylle, Hilde, Van Bockstaele, Erik and Roldán-Ruiz, Isabel. 2008. "Evaluation of genetic diversity of Fusarium head blight resistance in European winter wheat." Theoretical and Applied Genetics: international journal of plant breeding research. 117 (5), pp. 813-828. https://doi.org/10.1007/s00122-008-0822-3
Combining ability analysis of Fusarium head blight resistance in western European wheat lines
Zwart, Rebecca S., Muylle, Hilde, Van Huylenbroeck, Johan, Van Bockstaele, Erik and Roldán-Ruiz, Isabel. 2008. "Combining ability analysis of Fusarium head blight resistance in western European wheat lines." Euphytica: international journal on plant breeding. 162 (3), pp. 449-456. https://doi.org/10.1007/s10681-007-9611-3
Mapping quantitative trait loci for resistance to Pratylenchus thornei from synthetic hexaploid wheat in the International Triticeae Mapping Initiative (ITMI) population
Zwart, R. S., Thompson, J. P., Sheedy, J. G. and Nelson, J.. 2006. "Mapping quantitative trait loci for resistance to Pratylenchus thornei from synthetic hexaploid wheat in the International Triticeae Mapping Initiative (ITMI) population." Australian Journal of Agricultural Research. 57 (5), pp. 525-530. https://doi.org/10.1071/AR05177
Identification of quantitative trait loci for resistance to two species of root-lesion nematode (Pratylenchus thornei and P. neglectus) in wheat
Zwart, R. S., Thompson, J. P. and Godwin, I. D.. 2005. "Identification of quantitative trait loci for resistance to two species of root-lesion nematode (Pratylenchus thornei and P. neglectus) in wheat ." Australian Journal of Agricultural Research. 56 (4), pp. 345-352. https://doi.org/10.1071/AR04223
Genetic analysis of resistance to root-lesion nematode (Pratylenchusthornei) in wheat
Zwart, R. S., Thompson, J. P. and Godwin, I. D.. 2004. "Genetic analysis of resistance to root-lesion nematode (Pratylenchusthornei) in wheat." Plant Breeding. 123 (3), pp. 209-212. https://doi.org/10.1111/j.1439-0523.2004.00986.x
Inheritance and mapping of 11 avirulence genes in Phytophthora sojae
May, K.J., Whisson, S.C., Zwart R.S., Searle, I.R., Irwin, J.A.G., Maclean, D.J., Carroll, B.J. and Drenth, A.. 2002. "Inheritance and mapping of 11 avirulence genes in Phytophthora sojae ." Fungal Genetics and Biology. 37 (1), pp. 1-12. https://doi.org/10.1016/S1087-1845(02)00027-0
Phytotoxicity of fosetyl Al and phosphonic acid to maize during production of vesicular-arbuscular mycorrhizal inoculum
Seymour, N. P., Thompson, J. P. and Fiske M. L.. 1994. "Phytotoxicity of fosetyl Al and phosphonic acid to maize during production of vesicular-arbuscular mycorrhizal inoculum ." Plant Disease: an international journal of applied plant pathology. 78 (5), pp. 441-446. https://doi.org/10.1094/PD-78-0441