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Bio-control agents activate plant immune response and prime susceptible tomato against root-knot nematodes


Autoři: Sergio Molinari aff001;  Paola Leonetti aff001
Působiště autorů: Institute for Sustainable Plant Protection, National Research Council of Italy (IPSP-CNR), Bari, Italy aff001
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0213230

Souhrn

Beneficial microorganisms are generally known to activate plant defense against biotic challenges. However, the molecular mechanisms by which activated plants react more rapidly and actively to pests remain still largely unclear. Tomato plants pre-treated with a mixture of beneficial bio-control agents (BCAs), as soil-drenches, were less sensitive to infection of the root-knot nematode (RKN) Meloidogyne incognita. To unravel the molecular mechanisms of this induced resistance against RKNs, we used qRT-PCR to monitor the expression, in tomato roots and leaves, of 6 key defense genes. Gene transcripts were detected until the 12th day after BCA treatment(3, 7, 8, 12 dpt) and3 and 7 days after nematode inoculation of pre-treated plants. Early after BCA treatment, the salicylic acid (SA)-dependent pathogenesis related gene (PR-gene), PR-1b, marker of the systemic acquired resistance (SAR), was systemically over-expressed. Another PR-gene, PR-5, was over-expressed at later stages of BCA-plant interaction, and only in roots. Activation of defense against RKNs was attested by the early up-regulation of 4 genes (PR-1, PR-3, PR-5, ACO) in pre-treated plants after inoculation. Conversely, the expression of the JA/ET-dependent gene JERF3 did not increase after nematode inoculation in primed plants. A catalase gene (CAT)was highly over-expressed by nematode infection, however, this over-expression was annulled at the earliest stages or limited at the later stages of infection toBCA-treated roots. Enzyme activities, such as glucanase and endochitinase, were enhanced in roots of pre-treated inoculated plants with respect to plants left not inoculated as a control. These findings indicate that BCA interaction with roots primes plants against RKNs. BCA-mediated immunity seems to rely on SA-mediated SAR and to be associated with both the activation of chitinase and glucanase enzyme activities and the inhibition of the plant antioxidant enzyme system. Immunity is triggered at the penetration and movements inside the roots of the invading nematode juveniles but probably acts at the feeding site building stage of nematode infection.

Klíčová slova:

Gene expression – Fungi – Plant fungal pathogens – Tomatoes – Plant defenses – Leaves – Nematode infections – Plant disease resistance


Zdroje

1. Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014). Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52: 347–375. doi: 10.1146/annurev-phyto-082712-102340 24906124

2. Shoresh M, Harman GE, Mastouri F (2010). Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48: 21–43. doi: 10.1146/annurev-phyto-073009-114450 20192757

3. Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Nenerley CM, Monte E, et al. (2011). Trichoderma: the genomics of opportunistic success. Nature Rev 9: 749–759.

4. Cameron DD, Neal AL, van Wees SCM, Ton J (2013). Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci 18: 539–545. doi: 10.1016/j.tplants.2013.06.004 23871659

5. Pineda A, Zheng SJ, van Loon JJA, Pieterse CMJ, Dicke M (2010). Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15: 507–514. doi: 10.1016/j.tplants.2010.05.007 20542720

6. Jones JD, Dangl JL (2006). The plant immune system. Nature 444: 323–329. doi: 10.1038/nature05286 17108957

7. Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209 doi: 10.1146/annurev.phyto.42.040803.140421 15283665

8. Leonetti P, Zonno MC, Molinari S, Altomare C (2017). Induction of SA-signaling pathway and ethylene biosynthesis in Trichoderma harzianum-treated tomato plants after infection of the root-knot nematode Meloidogyne incognita. Plant Cell Rep 36: 621–631. doi: 10.1007/s00299-017-2109-0 28239746

9. Conrath U, Beckers GJM, Langenbach CJG, Jaskiewicz MR (2015). Priming for enhanced defense. Annu Rev Phytopathol 53: 97–119. doi: 10.1146/annurev-phyto-080614-120132 26070330

10. Yedida I, Shoresh M, Kerem K, Benhamou N, Kapulnik Y, Chet I (2003). Concomitant induction of systemic resistant to Pseudomonas syringae pv. lachrymans in cucumber by Trichoderma asperellum (T203) and the accumulation of phytoalexins. Appl Environ Microbiol 69: 7343–7353. doi: 10.1128/AEM.69.12.7343-7353.2003 14660384

11. Pozo MJ, Azcón-Aguilar C (2007). Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10: 393–398. doi: 10.1016/j.pbi.2007.05.004 17658291

12. Song Y, Chen D, Lu K, Sun Z, Zeng R (2015). Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Front Plant Sci 6:786. doi: 10.3389/fpls.2015.00786 26442091

13. Shouteden N, De Waele D, Panis B, Vos CM (2015). Arbuscular Mycorrhizal Fungi for the biocontrol of plant-parasitic nematodes: a review of the mechanisms involved. Front Microbiol 6: 1280. doi: 10.3389/fmicb.2015.01280 26635750

14. Blok VC, Jones JT, Phillips MS, Trudgill DL(2008). Parasitism genes and host range disparities in biotrophic nematodes: the conundrum of polyphagy versus specialisation. Bio Essays 30: 249–259.

15. Williamson VM, Gleason CA(2003). Plant-nematode interactions. Curr Opin Plant Biol 6: 327–333. doi: 10.1016/s1369-5266(03)00059-1 12873526

16. Mantelin S, Thorpe P, Jones JT (2015). Suppression of plant defences by plant-parasitic nematodes. Adv Bot Res 73: 325–337.

17. Molinari S (2016). Systemic acquired resistance activation in Solanaceous crops as a management strategy against root-knot nematodes. Pest ManagSci 72: 888–896. doi: 10.1002/ps.4063 26085141

18. Molinari S (2011). Natural genetic and induced plant resistance, as a control strategy to plant-parasitic nematodes alternative to pesticides. Plant Cell Rep 30:311–323. doi: 10.1007/s00299-010-0972-z 21184231

19. Stirling GR (2011). Biological Control of Plant-Parasitic Nematodes: An Ecological Perspective, a Review of Progress and Opportunities for Further Research. In: Davies K, Spiegel Y, editors. Biological Control of Plant-Parasitic Nematodes: Building Coherence between Microbial Ecology and Molecular Mechanisms. Progress in Biological Control 11: Springer Science + Business Media BV. pp. 1–38.

20. Martínez-Medina A, Fernandez I, Lok GB, Pozo MJ, Pieterse CMJ, Van Wees SCM (2017). Shifting from priming of salicylic acid- to jasmonic acid-regulated defences by Trichiderma protects tomato against the root knot nematode Meloidogyne incognita. New Phytol 213: 1363–1377. doi: 10.1111/nph.14251 27801946

21. Hol WHG, Cook R (2005). An overview of arbuscular mychorrizal fungi-nematode interaction. Basic Appl Ecol 6: 489–503.

22. Siddiqui IA, Shaukat SS (2002). Rhizobacteria-mediated induction of systemic resistance (ISR) in tomato against Meloidogyne javanica. J Phytopathol 150: 469–473.

23. Adam M, Heuer H, Hallmann J (2014). Bacterial antagonists of fungal pathogens also control root-knot nemaotdes by induced systemic resistance of tomato plants. PLoS ONE 9(2): e90402. doi: 10.1371/journal.pone.0090402 24587352

24. Molinari S, Lamberti F, Crozzoli R, Sharma SB, Sanchez Portales L (2005). Isozyme patterns of exotic Meloidogyne spp. populations. Nematol Medit 33: 61–65.

25. Byrd DW Jr, Kirkpatrick T, Barker KR (1983). An improved technique for clearing and staining plant tissue for detection of nematodes. J Nematol 15: 142–143. 19295781

26. Uehara T, Sugiyama S, Matsura H, Arie T, Masuta C (2010). Resistant and susceptible responses in tomato to cyst nematode are differentially regulated by salicylic acid. Plant Cell Physiol 51: 1524–1536. doi: 10.1093/pcp/pcq109 20660227

27. Livak KJ, Schmittgen TD (2001). Analysis of relative gene expression data using real time quantitative PCR and the 2-ΔΔCT method. Methods 25: 402–408. doi: 10.1006/meth.2001.1262 11846609

28. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951). Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265–275. 14907713

29. Reissig JL, Stromenger JL, Leloir LF (1955). A modified colometric method for the estimation of N-acetyl-amino sugars. J Biol Chem 217: 959–966. 13271455

30. Ashwell G (1957). Colorimetric analysis of sugars. Methods Enzymol 3: 73–105.

31. Gerbling KP, Kelly GJ, Fisher KH, Latzko E (1984). Partial purification and properties of soluble ascorbate peroxidase from pea leaves. J Plant Pathol 115: 59–67.

32. Tornero P, Gadea J, Conejero V, Vera P (1997). Two PR-1 genes from tomato are differentially regulated and reveal a novel mode of expression for a Pathogenesis-Related gene during the Hypersensitive Response and development. Mol Plant Microbe Interact 10: 624–634. doi: 10.1094/MPMI.1997.10.5.624 9204567

33. Wang YY, Li BQ, Qin GZ, Li L, Tian SP (2011). Defense response of tomato fruit at different maturity stages to salicylic acid and ethephon. Scientia Hort 129: 183–188.

34. Molinari S, Fanelli E, Leonetti P (2014). Expression of tomato salicylic acid (SA)-responsive pathogenesis-related genes in Mi-1-mediated and SA-induced resistance to root-knot nematodes. Mol Plant Pathol 15: 255–264. doi: 10.1111/mpp.12085 24118790

35. Wubben MJE, Jin J, Baum TJ (2008). Cyst nematode parasitism of Arabidopsis thaliana is inhibited by salicylic acid (SA) and elicits uncoupled SA-independent pathogenesis-related gene expression in roots. Mol Plant Microbe Interact 21: 424–432. doi: 10.1094/MPMI-21-4-0424 18321188

36. Wang H, Huang Z, Chen Q, Zhang Z, Zhang H, Wu Y, et al. (2004). Ectopic overexpression of tomato JERF3 in tobacco activates downstream gene expression and enhances salt tolerance. Plant MolBiol 55, 183–192.

37. Spoel SH, Dong X (2012). How do plants achieve immunity? Defence without specialized immune cells. Nature Rev Immunol 12: 89–100.

38. Fu ZQ, Dong X (2013). Systemic Acquired Resistance: turning local infection into global defense. Annu Rev Plant Biol 64: 839–863. doi: 10.1146/annurev-arplant-042811-105606 23373699

39. Van Loon LC, Rep M, Pieterse CMJ (2006). Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44: 135–162. doi: 10.1146/annurev.phyto.44.070505.143425 16602946

40. Cao H, Bowling SA, Gordon AS, Dong X (1994). Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6: 1583–1592. doi: 10.1105/tpc.6.11.1583 12244227

41. Paszkowski U (2006). Mutualism and parasitism: the yin and yang of plant symbioses. Curr Opin Plant Biol 8: 1–10.

42. Zipfel C, Oldoryd GED (2017). Plant signalling in symbiosis and immunity. Nature 543: 328–336. doi: 10.1038/nature22009 28300100

43. Glazebrook J (2005). Contrasting mechanisms of defense against biotrophic and nectrophic pathogens. Annu Rev Phytopathol 43: 205–227. doi: 10.1146/annurev.phyto.43.040204.135923 16078883

44. Li HY, Yang GD, Shu HR, Yang YT, Ye BX, Nishida I, et al (2006). Colonization by the arbuscular mycorrhizal fungus Glomus versiforme induces a defense response against the root-knot nematode Meloidogyne incognita in the grapevine (Vitis amurensis Rupr.), which includes transcriptional activation of the class III chitin. Plant Cell Physiol 47: 154–163. doi: 10.1093/pcp/pci231 16326755

45. Fudali SL, Wang C, Williamson VM (2013). Ethylene signaling pathway modulates attractiveness of host roots to the root-knot nematode Meloidogyne hapla. Mol Plant Microbe In 26:75–86.

46. Derksen H, Rampitsch C, Daayf F (2013). Signaling cross-talk in plant disease resistance. Plant Sci 207: 79–87. doi: 10.1016/j.plantsci.2013.03.004 23602102

47. Goverse A, Smant G (2017). The activation and suppression of plant innate immunity by parasitic nematodes. Annu Rev Phytopathol 52: 243–265.

48. Vieira P, Gleason C (2019). Plant-parasitic nematode effectors—insights into their diversity and new tools for their identification. Curr Opin Plant Biol 50: 37–43. doi: 10.1016/j.pbi.2019.02.007 30921686

49. Molinari S, Loffredo E (2006). The role of salicylic acid in defense response of tomato to root-knot nematodes. Physiol Mol Plant Pathol 68: 69–78.

50. Molinari S. (2007). New developments in understanding the role of salicylic acid in plant defence. CAB Rev 2: 1–10.

51. Molinari S (2001). Inhibition of H2O2-degrading enzymes in the response of Mi-bearing tomato to root-knot nematodes and salicylic acid treatment. Nematol medit 29: 235–239.

52. Wondafrash M, Van Dam NM, Tytgat TOG (2013). Plant systemic induced responses mediate interactions between root parasitic nematodes and aboveground herbivorous insects. Front Plant Sci 4: 1–15.


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