TSitologiya i Genetika 2019, vol. 53, no. 4, 60-67
Cytology and Genetics 2019, vol. 53, no. 4, 315–320, doi: https://www.doi.org/10.3103/S0095452719040066

Genetic background of the resistance against plant parasitic nematodes in wheat

Karelov A.V., Pylypenko L.A., Kozub N.A., Sozinov I.A., Blume Ya.B.

SUMMARY. The article describes the state of the art in research on resistance genes in wheat (Triticum aestivum L.) against cereal cyst nematode (Heterodera avenae) and root lesion nematode (Pratylenchus neglectus) and their use in breeding programs. Most of the genes responsible for this resistance are listed and their chromosomal location and their resistance specificity are described. The sources of the genes that are widely used in resistance breeding with the aim of cyst nematode control, are mentioned as well. Finally alternative ways to transfer nematode resistance genes into wheat are indicated.

Keywords: cereal cyst nematode, root lesion nematode, resistance genes, wheat, molecular markers

TSitologiya i Genetika
2019, vol. 53, no. 4, 60-67

Current Issue
Cytology and Genetics
2019, vol. 53, no. 4, 315–320,
doi: 10.3103/S0095452719040066

Full text and supplemented materials

Free full text: PDF  

References

1. Bernard, G., Egnin, M., and Bonsi, C., The impact of plant-parasitic nematodes on agriculture and methods of control, nematology, Concepts Diagn. Control, 2017, vol. 7, pp. 121–151. https://doi.org/10.5772/intechopen.68958

2. Jones, J.T., Haegeman, A., Danchin, E.G., Gaur, H.S., Helder, J., Jones, M.G., Kikuchi, T., Manzanilla-Lopez, R., Palomares-Rius, J.E., Wesemael, W.M., and Perry, R.N., Top 10 plant-parasitic nematodes in molecular plant pathology, Mol. Plant Pathol., 2013, vol. 14, no. 9, pp. 946–961. https://doi.org/10.1111/mpp.12057

3. Toumi, F., Waeyenberge, L., Viaene, N., Dababat, A.A., Nicol, J.M., and Ogbonnaya, F., Cereal cyst nematodes: importance, distribution, identification, quantification, and control, Eur. J. Plant Pathol., 2018, vol. 150, no. 1. https://doi.org/10.1007/s10658-017-1263-0

4. Caboni, P. and Ntalli, N.G., Botanical nematicides, recent findings, in Biopesticides: State of the Art and Future Opportunities, ch. 11, pp. 145–157. https://doi.org/10.1021/bk-2014-1172.ch011

5. Mokrini, F. and Viaene, N., Lieven Waeyenberge L., Dababat A.A., Moens M. Characterization of cereal cyst nematodes (Heterodera spp.) in Morocco based on morphology, morphometrics and rDNA-ITS sequence analysis, J. Plant Protec. Res., 2017, vol. 57, no. 3, pp. 219–227. https://doi.org/10.1515/jppr-2017-0031

6. Mustafa, ImrenM. and Elekcioglu, I.H., Effect of cereal cyst nematode Heterodera avenae (Tylenchida: Heteroderidae) on yield of some spring wheat varieties in Adana Province, Turkey, Turk. J. Agric. For., 2014, vol. 38, pp. 820–823. https://doi.org/10.3906/tar-1312-91

7. Hewezi, T. and Baum, T., Manipulation of plant cells by cyst and root-knot nematode effectors, Mol. Plant–Microbe Interact., 2013, vol. 26, pp. 9–16. https://doi.org/10.1094/MPMI-05-12-0106-FI

8. Kyndt, T., Vieira, P., Gheysen, G., and de Almeida-Engler, J., Nematode feeding sites: unique organs in plant roots, Planta, 2013, vol. 238, no. 5, pp. 807–818. https://doi.org/10.1007/s00425-013-1923-z

9. Absmanner, B., Stadler, R., and Hammes, U.Z., Phloem development in nematode-induced feeding sites: the implications of auxin and cytokinin, Front. Plant Sci., 2013. https://doi.org/10.3389/fpls.2013.00241

10. Okulewicz, A., The impact of global climate change on the spread of parasitic nematodes, Ann. Parasitol., 2017, vol. 63, no. 1, pp. 15–20. https://doi.org/10.17420/ap6301.79

11. Williams, K.J., Fisher, J.M., and Langridg, R., Identification of RFLP markers linked to the cereal cyst nematode resistance gene (Cre) in wheat, Theor. Appl. Genet., 1994, vol. 89, pp. 927–930. https://doi.org/10.1007/BF00224519

12. Ogbonnaya, F.C., Subrahmanyam, N.C., Moullet, O., de Majnik, J., Eagles, H.A., Brown, J.S., Eastwood, R.F., Kollmorgen, J., Appels, R., and Lagudah, E.S., Diagnostic DNA markers for cereal cyst nematode resistance in bread wheat, Aust. J. Agric. Res., 2001, vol. 52, pp. 1367–1374. https://doi.org/10.1071/AR01031

13. de Majnik, J., Ogbonnaya, F.C., Moullet, O., and Lagudah, E.S., The Cre1 and Cre3 nematode resistance genes are located at homeologous loci in the wheat genome, Mol. Plant–Microbe Interact., 2003, vol. 16, no. 12, pp. 1129–1134. https://doi.org/10.1094/MPMI.2003.16.12.1129

14. Çalişkan, M., Uranbey, S., Nicol, J., Akar, T., Elekcioğlu, H., and Kaya, G., Indirect selection of Cre1 gene in winter wheat populations, Arch. Biol. Sci., 2011, vol. 63, pp. 49–53. https://doi.org/10.2298/ABS1101049C

15. Delibes, A., Romero, D., Aguaded, S., Duce, A., Mena, M., López- Braña, I., Andrés, M.-F., Martin-Sanchez, J.-A., and García-Olmedo, F., Resistance to the cereal cyst nematode (Heterodera avenae Woll.) transferred from the wild grass Aegilops ventricosa to hexaploid wheat by a “stepping-stone” procedure, Theor. Appl. Genet., 1993, vol. 87, pp. 402–408. https://doi.org/10.1007/BF01184930

16. Ogbonnaya, F.C., Seah, S., Delibes, A., Jahier, J., López- Braña, I., Eastwood, R.F., and Lagudah, E.S., Molecular-genetic characterisation of a new nematode resistance gene in wheat, Theor. Appl. Genet., 2001, vol. 102, pp. 623–629. https://doi.org/10.1007/s001220051689

17. Eastwood, R.F., Lagudah, E.S., and Appels, R., A directed search for DNA sequences tightly linked to cereal cyst nematode resistance genes in Triticum tauschii, Genome, 1994, vol. 37, pp. 311–319. https://doi.org/10.1139/g94-043

18. Jahier, J., Tanguy, A.M., Abelard, P., Dedryver, F., Rivoal, R., Khatkar, S., Bariana, H.S., and Koebner, R., The Aegilops ventricosa segment on chromosome 2AS of the wheat cultivar ‘VPM1’ carries the cereal cyst nematode resistance gene Cre5, Plant Breed., 2001, vol. 120, pp. 125–128. https://doi.org/10.1046/j.1439-0523.2001.00585.x

19. Jahier, J., Tanguy, A.M., Abelard, P., and Rioal, R., Utilization of deletions to localize a gene for resistance to the cereal cyst nematode, Heterodera avenae, on an Aegilops ventricosa chromosome, Plant Breed., 1996, vol. 115, pp. 282–284. https://doi.org/10.1111/j.1439-0523.1996.tb00919.x

20. Montes, M.J., Andres, M.F., Sin, E., López-Braña, I., Martín-Sánchez, J.A., Romero, M.D., and Delibes, A., Cereal cyst nematode resistance conferred by the Cre7 gene from Aegilops triuncialis and its relationship with Cre genes from Australian wheat cultivars, Genome, 2008, vol. 51, pp. 315–319. https://doi.org/10.1139/G08-015

21. Paull, J.G., Chalmers, K.J., Karakousis, A., Kretschmer, J.M., Manning, S., and Langridge, P., Genetic diversity in Australian wheat varieties and breeding material based on RFLP data, Theor. Appl. Genet., 2001, vol. 102, pp. 623–629. https://doi.org/10.1007/s001220050760

22. Jayatilake, D.V., Tucker, E.J., Brueggemann, J., Lewis, J., Garcia, M., Dreisigacker, S., Hayden, M.J., Chalmers, K., and Mather, D.E., Genetic mapping of the Cre8 locus for resistance against cereal cyst nematode (Heterodera avenae Woll.) in wheat, Mol. Breed., 2015, vol. 35, no. 66. https://doi.org/10.1007/s11032-015-0235-3

23. Safari, E., Gororo, N.N., Eastwood, R.F., Lewis, J., Eagles, H.A., and Ogbonnaya, F.C., Impact of Cre1, Cre8 and Cre3 genes on cereal cyst nematode resistance in wheat, Theor. Appl. Genet., 2005, vol. 110, pp. 567–572. https://doi.org/10.1007/s00122-004-1873-8

24. Taylor, C., Shepherd, K.W., and Langridge, P., A molecular genetic map of the long arm of chromosome 6R of rye incorporating the cereal cyst nematode resistance gene, CreR, Theor. Appl. Genet., 1998, vol. 97, pp. 1000–1012. https://doi.org/10.1007/s001220050984

25. Dababat, A.A., Ergnbas-Orakci, G., Toktay, H., Imren, M., Akin, B., Braun, H.-J., Dreisigacker, S., Elekcioglu, I.H., and Morgounov, A., Resistance of winter wheat to Heterodera filipjevi in Turkey, Turk. J. Agric. Forest., 2014, vol. 38, pp. 180–186. https://doi.org/10.3906/tar-1305-47

26. Zhang, R., Feng, Y., Li, H., Yuan, H., Dai, J., Cao, A., Xing, L., and Li, H., Cereal cyst nematode resistance gene CreV effective against Heterodera filipjevi transferred from chromosome 6VL of Dasypyrum villosum to bread wheat, Mol. Breed., 2016, vol. 36, p. 122. https://doi.org/10.1007/s11032-016-0549-9

27. Zhai, X.G., Zhao, T., Liu, Y.H., Long, H., Deng, G.B., Pan, Z.F., and Yu, M.Q., Characterization and expression profiling of a novel cereal cyst nematode resistance gene analog in wheat, Mol. Biol., 2008, vol. 42, no. 6, pp. 960–965. https://doi.org/10.1134/S002689330-8060186

28. Kong, L.A., Wu, D.Q., Huang, W.K., Peng, H., Wang, G.-F., Cui, J.-K., Liu, S.-M., Li, Z.-G., Yang, J., and Peng, De-L., Large-scale identification of wheat genes resistant to cereal cyst nematode Heterodera avenae using comparative transcriptomic analysis, BMC Genomics, 2015, vol. 801. https://doi.org/10.1186/s12864-015-2037-8

29. Simonetti, E., Alba, E., Montes, M.J., Delibes, A., and Lopez-Brana, I., Analysis of ascorbate peroxidase genes expressed in resistant and susceptible wheat lines infected by the cereal cyst nematode, Heterodera avenae, Plant Cell Rep., 2010, vol. 29, pp. 1169–1178. https://doi.org/10.1007/s00299-010-0903-z

30. Moatamedi, M., Bazgir, E., Esfahani, M.N., and Darvishnia, M., Genetic variation of bread wheat accessions in response to the cereal cyst nematode, Heterodera filipjevi, Nematology, 2018, vol. 20, no. 9. doi 10.1163/15685411-00003181

31. Yu, Y., Liu, H., Zhu, A., Zhang, G., Zeng, L., and Xue, S., A Review of root lesion nematode: identification and plant resistance, Adv. Microbiol., 2012, vol. 2, no. 4, pp. 411–416. https://doi.org/10.4236/aim.2012.24052

32. Smiley, R.W., Root-lesion nematodes: biology and management in pacific northwest wheat cropping systems, PNW Ext. Bull., 2010, vol. 617, p. 9. https://doi.org/10.1146/annurev-phyto-080615-100257

33. Fosu-Nyarko, J. and Jones, M.G.K., Advances in understanding the molecular mechanisms of root lesion nematode host interactions, Annu. Rev. Phytopathol., 2016, vol. 54, pp. 253–278. https://doi.org/10.1146/annurevphyto-080615-100257

34. Yan, G.P., Plaisance, A., Huang, D., Chowdhury, I.A., and Handoo, Z.A., First report of the new root-lesion nematode Pratylenchus sp. on soybean in North Dakota, Plant Dis., 2017, vol. 101, no. 8, p. 1554. https://doi.org/10.1094/PDIS-04-17-0594-PDN

35. Zwart, R.S., Thompson, J.P., Sheedy, J.G., and Nelson, J.C., Mapping quantitative trait loci for resistance to Pratylenchus thornei from synthetic hexaploid wheat in the international Triticeae mapping initiative (ITMI) population, Austral. J. Agricult. Res., 2006, vol. 57, pp. 525–530. https://doi.org/10.1071/AR05177

36. Zwart, R.S., Thompson, P.J., Milgate, A.W., Bansal, U.K., Williamson, P.M., Raman, H., and Bariana, H.S., QTL mapping of multiple foliar disease and root-lesion nematode resistances in wheat, Mol. Breed, 2010, vol. 26, pp. 107–124. https://doi.org/10.1007/s11032-009-9381-9

37. Williams, K., Taylor, S., Bogacki, P., Pallotta, M., Ba-riana, S., and Wallwork, H., Mapping of the root lesion nematode (Pratylenchus neglectus) resistance gene Rlnn1 in wheat, Theor. Appl. Genet., 2002, vol. 104, pp. 874–879. https://doi.org/10.1007/s00122-001-0839-3

38. Jayatilake, D.V., Tucker, E.J., Bariana, H., Kuchel, H., Edwards, J., McKay, A.C., Chalmers, K., and Mather, D.E., Genetic mapping and marker development for resistance of wheat against the root lesion nematode Pratylenchus neglectus, BMC Plant Biol., 2013, vol. 13, p. 230. https://doi.org/10.1186/1471-2229-13-230

39. Ali, M.A., Azeem, F., Abbas, A., Joyia, F.A., Li, H., and Dababat, A.A., Transgenic strategies for enhancement of nematode resistance in plants, Front. Plant Sci., 2017, vol. 750, no. 2. https://doi.org/10.3389/fpls.2017.00750

40. Karelov, A.V., Kozub, N.A., Sozinov, I.A., Pyly-penko, L.A., and Blume, Ya.B., Allelic state of the Cre8 gene conferring resistance to the nematode Heterodera avenae Woll. in common wheat cultivars of Ukrainian breeding, Factors Exp. Evol. Org. 2016, vol. 18, pp. 89–92.