New genetic tools for plant defense against parasitic nematodes
https://doi.org/10.18699/VJ21.037
Abstract
Nematodes belong to economically important pests. Here we reviewed the recent data on molecular mechanisms of plant resistance to cyst and gall nematodes including the most devastating Globodera rostochiensis, G. pallida, Heterodera schachtii, Meloidogyne chitwoodi, and M. incognita. The Golden Potato Cyst Nematode (G. rostochiensis, GPCN) may be taken as an example of an economically important pest: in Russia, it occurs in 61 regions with a total area of 1.8 million ha and may cause the yield loss from 19 to 90 %. The biological characteristics of sedentary nematodes makes their agrotechnical control problematic, i.e. the GPCN cysts remain dormant in soil for many years until a susceptible host appears, whereas nematicides are either toxic or inefficient. Introgression of resistance genes (R-genes) from related cultivated or wild species is likely to be the most appropriate way for their biocontrol. The life cycle of sedentary nematodes is based on juveniles’ penetration into the host root where they reprogram plant cells into a syncytium or the so-called ‘giant cells’ and inhibit the plant defense response. Molecular mechanisms of plant-nematode interaction are unusual and this phenomenon provides a very interesting model for the investigation of plant morphogenesis control as well as for the development of new genetic instruments of biocontrol. Here we reviewed recent publications on plant parasitic nematode effectors used for hijacking of the plant immune system, data on R-genes and molecular mechanisms of their activities. In addition, host-induced gene silencing (HIGS) is discussed as a perspective mechanism for nematode biocontrol. HIGS is based on the RNA interference in the cells of the host plant addressed against the nematode genes important for their development and productivity. Several recent investigations demonstrated efficiency of HIGS against sedentary nematodes.
Keywords
About the Authors
A. V. KochetovRussian Federation
Novosibirsk
T. A. Gavrilenko
Russian Federation
Novosibirsk,
St. Petersburg
O. S. Afanasenko
Russian Federation
Novosibirsk,
Pushkin, St. Petersburg
References
1. Zinovieva S.V., Chizhov V.N., Pridannikov M.V., Subbotin S.A., Ryss A.Yu., Khusainov R.V. Phytoparasitic nematodes of Russia. KMK Scientific Publishing Association, 2012;374. (in Russian)
2. Kochetov A.V., Sirnik O.A., Rogosin I.B., Glazko G.V., Komarova M.L., Shumny V.K. Contextual features of higher plant mRNA 5’-untranslated regions. Molekulyarnaya Biologiya = Molecular Biology. 2002;36(4):649-656. (in Russian)
3. Kochetov A.V., Titov S.E., Kolodyazhnaia Ia.S., Komarova M., Koval’ V.S., Makarova N.N., Ilinskyi Iu.Iu., Trifonova E.A., Shumny V.K. Tobacco transformants bearing antisense suppressor of proline dehydrogenase gene are characterized by higher proline content and cytoplasm osmotic pressure. Genetika = Genetics. 2004;40(2): 282-285. (in Russian)
4. Handbook on the plant quarantine conditions in CIS member states as of January 1, 2017. Moscow: All-Russia Plant Quarantine Center Publ., 2017;106. (in Russian)
5. Amin R.B., Karegar A., Afsharifar A., Niazi A., Karimi M. Disruption of the pathogenicity and sex ratio of the beet cyst nematode Heterodera schachtii by host-delivered RNA interference. Mol. Plant. Microbe Interact. 2018;31(12):1337-1346. DOI 10.1094/MPMI-0518-0141-R.
6. Bakker E., Achenbach U., Bakker J., van Vliet J., Peleman J., Segers B., van der Heijden S., van der Linde P., Graveland R., Hutten R., van Eck H., Coppoolse E., An der Vossen E., Bakker J., Goverse A. A high-resolution map of the H1 locus harboring resistance to the potato cyst nematode Globodera rostochiensis. Theor. Appl. Genet. 2004;109:146-152. DOI 10.1007/s00122-004-1606-z.
7. Bali S., Vining K., Gleason C., Majtahedi H., Brown C.R., Sathuvalli V. Transcriptome profiling of resistance response to Meloidogyne chitwoodi introgressed from wild species Solanum bulbocastanum into cultivated potato. BMC Genomics. 2019;20(1):907. DOI 10.1186/s12864-019-6257-1.
8. Ballvora A., Hesselbach J., Niewöhner J., Leiste D., Salamini F., Gebhardt C. Marker enrichment and high-resolution map of the segment of potato chromosome VII harbouring the nematode resistance gene Gro1. Mol. Gen. Genet. 1995;249:82-90.
9. Banerjee S., Gill S.S., Gawade B.H., Jain P.K., Subramaniam K., Sirohi A. Host Delivered RNAi of Two Cuticle Collagen Genes, Mi-col-1 and Lemmi-5 Hampers Structure and Fecundity in Meloidogyne incognita. Front. Plant Sci. 2018;8:2266. DOI 10.3389/fpls.2017.02266.
10. Barone A., Ritter E., Schachtschabel U., Debener T., Salamini F., Gebhardt C. Localization by restriction fragment length polymorphism mapping in potato of a major dominant gene conferring resistance to the potato cyst nematode Globodera rostochiensis. Mol. Gen. Genet. 1990;224:177-182.
11. Bayless A.M., Zapotocny R.W., Grunwald D.J., Amundson K.K., Diers B.W., Bent A.F. An atypical N-ethylmaleimide sensitive factor enables the viability of nematode-resistant Rhg1 soybeans. Proc. Natl. Acad. Sci USA. 2018;115(19):E4512-E4521.
12. Bournaud C., Gillet F.-X., Murad A.M., Bresso E., Albuquerque E.V.S., Grossi-de-Sá M.F. Meloidogyne incognita PASSE-MURAILLE (MiPM ) gene encodes a cell-penetrating protein that interacts with the CSN5 subunit of the COP9 signalosome. Front. Plant Sci. 2018; 9:904. DOI 10.3389/fpls.2018.00904.
13. Butler K.J., Chen S., Smith J.M., Wang X., Bent A.F. Soybean Resistance Locus Rhg1 Confers Resistance to Multiple Cyst Nematodes in Diverse Plant Species. Phytopathology. 2019;109(12):2107-2115. DOI 10.1094/PHYTO-07-19-0225-R.
14. Chaudhary S., Dutta T.K., Tyagi N., Shivakumara T.N., Papolu P.K., Chobhe K.A., Rao U. Host-induced silencing of Mi-msp-1 confers resistance to root-knot nematode Meloidogyne incognita in eggplant. Transgenic. Res. 2019;28(3-4):327-340. DOI 10.1007/s11248-01900126-5.
15. Dalamu B.V., Umamaheshwari R., Shrama R., Kaushik S.K., Joseph T.A., Singh B.P., Gebhardt C. Potato cyst nematode (PCN) resistance: genes, genotypes and markers – an update. SABRAO J. Breed. Genet. 2012;44:202-228.
16. Dandurand L.M., Zasada I.A., LaMondia J.A. Effect of the trap crop, Solanum sisymbriifolium, on Globodera pallida, Globodera tabacum, and Globodera ellingtonae. J. Nematol. 2019;51:1-11. DOI 10.21307/jofnem-2019-030.
17. Dutta T.K., Papolu P.K., Banakar P., Choudhary D., Sirohi A., Rao U. Tomato transgenic plants expressing hairpin construct of a nematode protease gene conferred enhanced resistance to root-knot nematodes. Front. Microbiol. 2015;6:260. DOI 10.3389/fmicb.2015.00260.
18. Evans K., Trudgill D.L. Pest aspects of potato production. Part 1. The nematode pests of potatoes. In: Harris P. (Ed.). The potato crop. London: Chapman & Hall, 1992.
19. Friedman W. Pests not known to occur in the United States or of limited distribution, No. 68: Golden Nematode. United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine, 1985;10.
20. Gheysen G., Mitchum M.G. Phytoparasitic nematode control of plant hormone pathways. Plant Physiol. 2019;179:1212-1226. DOI 10.1104/pp.18.01067.
21. Hewezi T., Juvale P.S., Piya S., Maier T.R., Rambani A., Rice J.H., Mitchum M.G., Davis E.L., Hussey R.S., Baum T.J. The cyst nematode effector protein 10A07 targets and recruits host posttranslational machinery to mediate its nuclear trafficking and to promote parasitism in Arabidopsis. Plant Cell. 2015;27:891-907. DOI 10.1105/tpc.114.135327.
22. Hu Y., You J., Li C., Pan F., Wang C. The Heterodera glycines effector Hg16B09 is required for nematode parasitism and suppresses plant defense response. Plant Sci. 2019;289:110271. DOI 10.1016/j.plantsci.2019.110271.
23. Iqbal S., Fosu-Nyarko J., Jones M.G.K. Attempt to silence genes of the RNAi pathways of the root-knot nematode, Meloidogyne incognita results in diverse responses including increase and no change in expression of some genes. Front. Plant Sci. 2020;11:328. DOI 10.3389/fpls.2020.00328.
24. Jones L.M., Koehler A.K., Trnka M., Balek J., Challinor A.J., Atkinson H.J., Urwin P.E. Climate change is predicted to alter the current pest status of Globodera pallida and G. rostochiensis in the United Kingdom. Glob. Chang Biol. 2017;23(11):4497-4507. DOI 10.1111/gcb.13676.
25. Joshi I., Kumar A., Singh A.K., Kohli D., Raman K.V., Sirohi A., Chaudhury A., Jain P.K. Development of nematode resistance in Arabidopsis by HD-RNAi-mediated silencing of the effector gene Mi-msp2. Sci. Rep. 2019;9(1):17404. DOI 10.1038/s41598-01953485-8.
26. Kaloshian I., Desmond O.J., Atamian H.S. Disease resistance-genes and defense responses during incompatible interactions. In: Jones J., Gheysen G., Fenoll C. (Eds.). Genomics and molecular genetics of plant–nematode interactions. New York: Springer, 2011;309-324.
27. Kearn J., Lilley C., Urwin P., O’Connor V., Holden-Dye L. Progressive metabolic impairment underlies the novel nematicidal action of fluensulfone on the potato cyst nematode Globodera pallida. Pestic. Biochem. Physiol. 2017;142:83-90. DOI 10.1016/j.pestbp.2017.01.009.
28. Kochetov A.V., Egorova A.A., Glagoleva A.Y., Strygina K.V., Khlestkina E.K., Gerasimova S.V., Shatskaya N.V., Vasilyev G.V., Afonnikov D.A., Shmakov N.A., Antonova O.Y., Alpatyeva N.V., Khiutti A., Afanasenko O.S., Gavrilenko T.A. The mechanism of potato resistance to Globodera rostochiensis: comparison of root transcriptomes of resistant and susceptible Solanum phureja genotypes. BMC Plant Biol. 2020;20(Suppl 1):350. DOI 10.1186/s12870-02002334-2.
29. Kochetov A.V., Glagoleva A.Y., Strygina K.V., Khlestkina E.K., Gerasimova S.V., Ibragimova S.M., Shatskaya N.V., Vasilyev G.V., Afonnikov D.A., Shmakov N.A., Antonova O.Y., Gavrilenko T.A., Alpatyeva N.V., Khiutti A., Afanasenko O.S. Differential expression of NBS-LRR-encoding genes in the root transcriptomes of two Solanum phureja genotypes with contrasting resistance to Globodera rostochiensis. BMC Plant Biol. 2017;17(Suppl 2):251. DOI 10.1186/s12870-017-1193-1.
30. Kochetov A.V., Sarai A. Translational polymorphism as a potential source of plant proteins variety in Arabidopsis thaliana. Bioinformatics. 2004;20:445-447.
31. Kooliyottil R., Dandurand L.-M., Kuhl J.C., Caplan A., Xiao F., Mimee B., Lafond-Lapalme J. Transcriptome analysis of Globodera pallida from the susceptible host Solanum tuberosum or the resistant plant Solanum sisymbriifolium. Sci. Rep. 2019;9(1):13256. DOI 10.1038/s41598-019-49725-6.
32. Kud J., Wang W., Gross R., Fan Y., Huang L., Yuan Y., Gray A., Duarte A., Kuhl J.C., Caplan A., Goverse A., Liu Y., Dandurand L.M., Xiao F. The potato cyst nematode effector RHA1B is a ubiquitin ligase and uses two distinct mechanisms to suppress plant immune signaling. PLoS Pathog. 2019;15(4):e1007720. DOI 10.1371/journal.ppat.1007720.
33. Li X., Xing X., Tian P., Zhang M., Huo Z., Zhao K., Liu C., Duan D., He W., Yang T. Comparative transcriptome profiling reveals defenserelated genes against Meloidogyne incognita invasion in tobacco. Molecules. 2018;23(8):2081. DOI 10.3390/molecules23082081.
34. Limantseva L., Mironenko N., Shuvalov O., Antonova O., Khiutti A., Novikova L., Afanasenko O., Spooner D., Gavrilenko T. Characterization of resistance to Globodera rostochiensis pathotype Ro1 in cultivated and wild potato species accessions from the Vavilov Institute of Plant Industry. Plant Breed. 2014;133:660-665.
35. Lin B., Zhuo K., Hu L., Sun L., Liao J., Zhang L.H., Chen S., Wang X. A novel nematode effector suppresses plant immunity by activating host reactive oxygen species scavenging system. New Phytol. 2016; 209:1159-1173. DOI 10.1111/nph.13701.
36. Mei Y., Wright K.M., Haegeman A., Bauters L., Diaz-Granados A., Goverse A., Gheysen G., T Jones J., Mantelin S. The Globodera pallida SPRYSEC effector GpSPRY-414-2 that suppresses plant defenses targets a regulatory component of the dynamic microtubule network. Front. Plant Sci. 2018;9:1019. DOI 10.3389/fpls.2018.01019.
37. Mejias J., Truong N.M., Abad P., Favery B., Quentin M. Plant proteins and processes targeted by parasitic nematode effectors. Front. Plant Sci. 2019;10:970. DOI 10.3389/fpls.2019.00970.
38. Palomares-Rius J.E., Escobar C., Cabrera J., Vovlas A., Castillo P. Anatomical alterations in plant tissues induced by plant-parasitic nematodes. Front. Plant Sci. 2017;8:1987. DOI 10.3389/fpls.2017.01987.
39. Qiu X., Yang L., Ye J., Wang W., Zhao T., Hu H., Zhou G. Silencing of cyp-33C9 gene affects the reproduction and pathogenicity of the pine wood nematode, Bursaphelenchus xylophilus. Int. J. Mol. Sci. 2019;20(18):4520. DOI 10.3390/ijms20184520.
40. Rodiuc N., Vieira P., Banora M.Y., de Almeida Engler J. On the track of transfer cell formation by specialized plant-parasitic nematodes. Front. Plant Sci. 2014;5:160. DOI 10.3389/fpls.2014.00160.
41. Sabeh M., Lord E., Grenier É., St-Arnaud M., Mimee B. What determines host specificity in hyperspecialized plant parasitic nematodes? BMC Genomics. 2019;20(1):457. DOI 10.1186/s12864-0195853-4.
42. Schaff J.E., Nielsen D.M., Smith C.P., Scholl E.H., Bird D.M. Comprehensive transcriptome profiling in tomato reveals a role for glycosyltransferase in Mi-mediated nematode resistance. Plant Physiol. 2007;144(2):1079-1092. DOI 10.1104/pp.106.090241.
43. Shivakumara T.N., Chaudhary S., Kamaraju D., Dutta T.K., Papolu P.K., Banakar P., Sreevathsa R., Singh B., Manjaiah K.M., Rao U. Host-induced silencing of two pharyngeal gland genes conferred transcriptional alteration of cell wall-modifying enzymes of Meloidogyne incognita vis-à-vis perturbed nematode infectivity in eggplant. Front. Plant Sci. 2017;8:473. DOI 10.3389/fpls.2017.00473.
44. Shivakumara T.N., Somvanshi V.S., Phani V., Chaudhary S., Hada A., Budhwar R., Shukla R.N., Rao U. Meloidogyne incognita (Nematoda: Meloidogynidae) sterol-binding protein Mi-SBP-1 as a target for its management. Int. J. Parasitol. 2019;49(13-14):1061-1073. DOI 10.1016/j.ijpara.2019.09.002.
45. Strachan S.M., Armstrong M.R., Kaur A., Wright K.M., Lim T.Y., Baker K., Jones J., Bryan G., Blok V., Hein I. Mapping the H2 resistance effective against Globodera pallida pathotype Pa1 in tetraploid potato. Theor. Appl. Genet. 2019;132(4):1283-1294. DOI 10.1007/s00122-019-03278-4.
46. Sugawara T., Trifonova E.A., Kochetov A.V., Kanayama Y. Expression of extracellular ribonuclease gene increases resistance to cucumber mosaic virus in tobacco. BMC Plant Biol. 2016;16(Suppl 3):246. DOI 10.1186/s12870-016-0928-8.
47. Trifonova E.A., Sapotsky M.V., Komarova M.L., Scherban A.B., Shumny V.K., Polyakova A.M., Lapshina L.A., Kochetov A.V., Malinovsky V.I. Protection of transgenic tobacco plants expressing bovine pancreatic ribonuclease against tobacco mosaic virus. Plant Cell Rep. 2007;26:1121-1126. DOI 10.1007/s00299-0060298-z.
48. Trudgill D.L., Blok V.C. Apomictic, polyphagous root-knot nematodes: exceptionally successful and damaging biotrophic rootpathogens. Annu. Rev. Phytopathol. 2001;39:53-77. DOI 10.1146/annurev.phyto.39.1.53.
49. Trudgill D.L., Elliot M.J., Evans K., Phillips M.S. The white potato cyst nematode (Globodera pallida) – a critical analysis of the threat in Britain. Ann. Appl. Biol. 2003;143:73-80.
50. Ventoso I., Kochetov A., Montaner D., Dopazo J., Santoyo J. Extensive translatome remodeling during ER stress response in mammalian cells. PLoS One. 2012;7(5):e35915. DOI 10.1371/journal.pone.0035915.
51. Wang X.R., Moreno Y.A., Wu H.R., Ma C., Li Y.F., Zhang J.A., Yang C., Sun S., Ma W.-J., Geary T.G. Proteomic profiles of soluble proteins from the esophageal gland in female Meloidogyne incognita. Int. J. Parasitol. 2012;42:1177-1183. DOI 10.1016/j.ijpara.2012.10.008.
52. Whitworth J.L., Novy R.G., Zasada I.A., Wang X., Dandurand L.M., Kuhl J.C. Resistance of potato breeding clones and cultivars to three species of potato cyst nematode. Plant Dis. 2018;102(11):21202128. DOI 10.1094/PDIS-12-17-1978-RE.
53. Winslow R.D., Willis R.J. Nematode diseases of potatoes. II. Potato cyst nematode, Heterodera rostochiensis. In: Webster J. (Ed.). Economic Nematology. New York: Acad. Press, 1972;18-34.