Influences of Ipomoea batatas Anti-Cancer Peptide on Tomato Defense Genes


Дәйексөз келтіру

Толық мәтін

Аннотация

Aims:This study investigates the impact of IbACP (Ipomoea batatas anti-cancer peptide) on defense-related gene expression in tomato leaves, focusing on its role in plant defense mechanisms.

Background:IbACP was isolated from sweet potato leaves, and it was identified as a peptide capable of inducing an alkalinization response in tomato suspension culture media. Additionally, IbACP was found to regulate the proliferation of human pancreatic adenocarcinoma cells.

Objective:Elucidate IbACP's molecular influence on defense-related gene expression in tomato leaves using next-generation sequencing analysis.

Methods:To assess the impact of IbACP on defense-related gene expression, transcriptome data were analyzed, encompassing various functional categories such as photosynthesis, metabolic processes, and plant defense. Semi-quantitative reverse-transcription polymerase chain reaction analysis was employed to verify transcription levels of defense-related genes in tomato leaves treated with IbACP for durations ranging from 0 h (control) to 24 h.

Results:IbACP induced jasmonic acid-related genes (LoxD and AOS) at 2 h, with a significant up-regulation of salicylic acid-dependent gene NPR1 at 24 h. This suggested a temporal antagonistic effect between jasmonic acid and salicylic acid during the early hours of IbACP treatment. Downstream ethylene-responsive regulator genes (ACO1, ETR4, and ERF1) were consistently down-regulated by IbACP at all times. Additionally, IbACP significantly up-regulated the gene expressions of suberization-associated anionic peroxidases (TMP1 and TAP2) at all time points, indicating enhanced suberization of the plant cell wall to prevent pathogen invasion.

Conclusion:IbACP enhances the synthesis of defense hormones and up-regulates downstream defense genes, improving the plant's resistance to biotic stresses.

Авторлар туралы

Hsin-Hung Lin

Department of Agronomy, National Chung Hsing University

Email: info@benthamscience.net

Kuan-Hung Lin

Department of Horticulture and Biotechnology, Chinese Culture University

Email: info@benthamscience.net

Yung-Lin Tsai

Department of Biotechnology, National Kaohsiung Normal University

Email: info@benthamscience.net

Rong-Jane Chen

Department of Food Safety/Hygiene and Risk Management, College of Medicine, National Cheng Kung University

Email: info@benthamscience.net

Yen-Chang Lin

Graduate Institute of Biotechnology, Chinese Culture University

Email: info@benthamscience.net

Yu-Chi Chen

Department of Biotechnology, National Kaohsiung Normal University

Хат алмасуға жауапты Автор.
Email: info@benthamscience.net

Әдебиет тізімі

  1. Sanoubar, R.; Barbanti, L. Fungal diseases on tomato plant under greenhouse condition. Eur. J. Biol. Res., 2017, 7, 299-308. doi: 10.5281/zenodo.1011161
  2. Nisserine, H-K.; Hajira, B.; Soumaya, B.; Mebrouk, K.; Setti, B.; Jamel, E.H. In vitro effect of two fungicides on pathogenic fungi causing root rot on tomato in Algeria. Afr. J. Agric. Res., 2014, 9(33), 2584-2587. doi: 10.5897/AJAR2014.8620
  3. Cole, R.D.; Anderson, G.L.; Williams, P.L. The nematode Caenorhabditis elegans as a model of organophosphate-induced mammalian neurotoxicity. Toxicol. Appl. Pharmacol., 2004, 194(3), 248-256. doi: 10.1016/j.taap.2003.09.013 PMID: 14761681
  4. Ma, J.; Lin, F.; Qin, W.; Wang, P. Differential response of four cyanobacterial and green algal species to triazophos, fentin acetate, and ethephon. Bull. Environ. Contam. Toxicol., 2004, 73(5), 890-897. doi: 10.1007/s00128-004-0510-1 PMID: 15669734
  5. Hua, L.; Yong, C.; Zhanquan, Z.; Boqiang, L.; Guozheng, Q.; Shiping, T. Pathogenic mechanisms and control strategies of Botrytis cinerea causing post-harvest decay in fruits and vegetables. Food Quality and Safety, 2018, 2(3), 111-119. doi: 10.1093/fqsafe/fyy016
  6. Li, T.; Zhang, J.; Tang, J.; Liu, Z.; Li, Y.; Chen, J.; Zou, L. Combined use of Trichoderma atroviride CCTCCSBW0199 and brassinolide to control Botrytis cinerea infection in tomato. Plant Dis., 2020, 104(5), 1298-1304. a doi: 10.1094/PDIS-07-19-1568-RE PMID: 32196417
  7. Li, Z.; Liu, H.; Ding, Z.; Yan, J.; Yu, H.; Pan, R.; Hu, J.; Guan, Y.; Hua, J. Low temperature enhances plant immunity via salicylic acid pathway genes that are repressed by ethylene. Plant Physiol., 2020, 182(1), 626-639. doi: 10.1104/pp.19.01130 PMID: 31694900
  8. Zhao, Y.; Wei, T.; Yin, K.Q.; Chen, Z.; Gu, H.; Qu, L.J.; Qin, G. Arabidopsis RAP2.2 plays an important role in plant resistance to Botrytis cinerea and ethylene responses. New Phytol., 2012, 195(2), 450-460. doi: 10.1111/j.1469-8137.2012.04160.x PMID: 22530619
  9. Broekgaarden, C.; Caarls, L.; Vos, I.A.; Pieterse, C.M.J.; Van Wees, S.C.M. Ethylene: Traffic controller on hormonal crossroads to defense. Plant Physiol., 2015, 169(4), pp.01020.2015. doi: 10.1104/pp.15.01020 PMID: 26482888
  10. Amorim, L.; Santos, R.; Neto, J.; Guida-Santos, M.; Crovella, S.; Benko-Iseppon, A. Transcription factors involved in plant resistance to pathogens. Curr. Protein Pept. Sci., 2017, 18(4), 335-351. doi: 10.2174/1389203717666160619185308 PMID: 27323805
  11. Chen, S.P.; Kuo, C.H.; Lu, H.H.; Lo, H.S.; Yeh, K.W. The sweet potato NAC-Domain transcription factor IbNAC1 is dynamically coordinated by the activator IbbHLH3 and the repressor IbbHLH4 to reprogram the defense mechanism against wounding. PLoS Genet., 2016, 12(10), e1006397. doi: 10.1371/journal.pgen.1006397 PMID: 27780204
  12. Meents, A.K.; Chen, S.P.; Reichelt, M.; Lu, H.H.; Bartram, S.; Yeh, K.W.; Mithöfer, A. Volatile DMNT systemically induces jasmonate-independent direct anti-herbivore defense in leaves of sweet potato (Ipomoea batatas) plants. Sci. Rep., 2019, 9(1), 17431. doi: 10.1038/s41598-019-53946-0 PMID: 31758060
  13. Hua, S.; Chen, Z.; Li, L.; Lin, K.H.; Zhang, Y.; Yang, J.; Chen, S.P. Differences in immunity between pathogen-resistant and -susceptible yam cultivars reveal insights into disease prevention underlying ethylene supplementation. J. Plant Biochem. Biotechnol., 2021, 30(2), 254-264. doi: 10.1007/s13562-020-00582-9
  14. Soto-Suárez, M.; Baldrich, P.; Weigel, D.; Rubio-Somoza, I.; San Segundo, B. The Arabidopsis miR396 mediates pathogen-associated molecular pattern-triggered immune responses against fungal pathogens. Sci. Rep., 2017, 7(1), 44898. doi: 10.1038/srep44898 PMID: 28332603
  15. Xing, X.; Li, X.; Zhang, M.; Wang, Y.; Liu, B.; Xi, Q.; Zhao, K.; Wu, Y.; Yang, T. Transcriptome analysis of resistant and susceptible tobacco ( Nicotiana tabacum) in response to root-knot nematode Meloidogyne incognita infection. Biochem. Biophys. Res. Commun., 2017, 482(4), 1114-1121. doi: 10.1016/j.bbrc.2016.11.167 PMID: 27914810
  16. Chen, Y.L.; Fan, K.T.; Hung, S.C.; Chen, Y.R. The role of peptides cleaved from protein precursors in eliciting plant stress reactions. New Phytol., 2020, 225(6), 2267-2282. doi: 10.1111/nph.16241 PMID: 31595506
  17. Stührwohldt, N.; Schaller, A. Regulation of plant peptide hormones and growth factors by post-translational modification. Plant Biol., 2019, 21(S1)(Suppl. 1), 49-63. doi: 10.1111/plb.12881 PMID: 30047205
  18. Hu, Z.; Zhang, H.; Shi, K. Plant peptides in plant defense responses. Plant Signal. Behav., 2018, 13(8), 1-5. doi: 10.1080/15592324.2018.1475175 PMID: 30067449
  19. Segonzac, C.; Monaghan, J. Modulation of plant innate immune signaling by small peptides. Curr. Opin. Plant Biol., 2019, 51, 22-28. doi: 10.1016/j.pbi.2019.03.007 PMID: 31026543
  20. Pearce, G.; Strydom, D.; Johnson, S.; Ryan, C.A. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science, 1991, 253(5022), 895-897. doi: 10.1126/science.253.5022.895 PMID: 17751827
  21. Chen, Y.C.; Siems, W.F.; Pearce, G.; Ryan, C.A. Six peptide wound signals derived from a single precursor protein in Ipomoea batatas leaves activate the expression of the defense gene sporamin. J. Biol. Chem., 2008, 283(17), 11469-11476. doi: 10.1074/jbc.M709002200 PMID: 18299332
  22. Pearce, G. Systemin, hydroxyproline-rich systemin and the induction of protease inhibitors. Curr. Protein Pept. Sci., 2011, 12(5), 399-408. doi: 10.2174/138920311796391106 PMID: 21418016
  23. Huffaker, A.; Ryan, C.A. Endogenous peptide defense signals in Arabidopsis differentially amplify signaling for the innate immune response. Proc. Natl. Acad. Sci. USA, 2007, 104(25), 10732-10736. doi: 10.1073/pnas.0703343104 PMID: 17566109
  24. Chang, V.H.S.; Yang, D.H.A.; Lin, H.H.; Pearce, G.; Ryan, C.A.; Chen, Y.C. IbACP, a sixteen-amino-acid peptide isolated from Ipomoea batatas leaves, induces carcinoma cell apoptosis. Peptides, 2013, 47, 148-156. doi: 10.1016/j.peptides.2013.02.005 PMID: 23428969
  25. Lin, H.H.; Lin, K.H.; Wu, K.F.; Chen, Y.C. Identification of Ipomoea batatas anti-cancer peptide (IbACP)-responsive genes in sweet potato leaves. Plant Sci., 2021, 305, 110849. doi: 10.1016/j.plantsci.2021.110849 PMID: 33691955
  26. Zhang, D.; Bao, Y.; Sun, Y.; Yang, H.; Zhao, T.; Li, H.; Du, C.; Jiang, J.; Li, J.; Xie, L.; Xu, X. Comparative transcriptome analysis reveals the response mechanism of Cf-16-mediated resistance to Cladosporium fulvum infection in tomato. BMC Plant Biol., 2020, 20(1), 33. doi: 10.1186/s12870-020-2245-5 PMID: 31959099
  27. Wasternack, C.; Song, S. Jasmonates: Biosynthesis, metabolism, and signaling by proteins activating and repressing transciption. J. Exp. Bot., 2016, 68(6), erw443. doi: 10.1093/jxb/erw443 PMID: 27940470
  28. Zhang, H.; Xie, X.; Xu, Y.; Wu, N. Isolation and functional assessment of a tomato proteinase inhibitor II gene. Plant Physiol. Biochem., 2004, 42(5), 437-444. doi: 10.1016/j.plaphy.2004.03.006 PMID: 15191748
  29. Lefevere, H.; Bauters, L.; Gheysen, G. Salicylic acid biosynthesis in plants. Front. Plant Sci., 2020, 11, 338. doi: 10.3389/fpls.2020.00338 PMID: 32362901
  30. Gaffney, T.; Friedrich, L.; Vernooij, B.; Negrotto, D.; Nye, G.; Uknes, S.; Ward, E.; Kessmann, H.; Ryals, J. Requirement of salicylic Acid for the induction of systemic acquired resistance. Science, 1993, 261(5122), 754-756. doi: 10.1126/science.261.5122.754 PMID: 17757215
  31. Görlach, J.; Volrath, S.; Knauf-Beiter, G.; Hengy, G.; Beckhove, U.; Kogel, K.H.; Oostendorp, M.; Staub, T.; Ward, E.; Kessmann, H.; Ryals, J. Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell, 1996, 8(4), 629-643. doi: 10.1105/tpc.8.4.629 PMID: 8624439
  32. Métraux, J.P.; Signer, H.; Ryals, J.; Ward, E.; Wyss-Benz, M.; Gaudin, J.; Raschdorf, K.; Schmid, E.; Blum, W.; Inverardi, B. Increase in salicylic Acid at the onset of systemic acquired resistance in cucumber. Science, 1990, 250(4983), 1004-1006. doi: 10.1126/science.250.4983.1004 PMID: 17746926
  33. Wildermuth, M.C.; Dewdney, J.; Wu, G.; Ausubel, F.M. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature, 2001, 414(6863), 562-565. doi: 10.1038/35107108 PMID: 11734859
  34. Zhang, Y.; Xu, S.; Ding, P.; Wang, D.; Cheng, Y.T.; He, J.; Gao, M.; Xu, F.; Li, Y.; Zhu, Z.; Li, X.; Zhang, Y. Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proc. Natl. Acad. Sci. USA, 2010, 107(42), 18220-18225. doi: 10.1073/pnas.1005225107 PMID: 20921422
  35. Sun, T.; Zhang, Y.; Li, Y.; Zhang, Q.; Ding, Y.; Zhang, Y. ChIP-seq reveals broad roles of SARD1 and CBP60g in regulating plant immunity. Nat. Commun., 2015, 6(1), 10159. doi: 10.1038/ncomms10159 PMID: 27206545
  36. Delaney, TP; Friedrich, L; Ryals, JA Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc. Natl. Acad. Sci. USA, 1995, 92, 6602-6606. doi: 10.1073/pnas.92.14.6602
  37. Rochon, A.; Boyle, P.; Wignes, T.; Fobert, P.R.; Després, C. The coactivator function of Arabidopsis NPR1 requires the core of its BTB/POZ domain and the oxidation of C-terminal cysteines. Plant Cell, 2007, 18(12), 3670-3685. doi: 10.1105/tpc.106.046953 PMID: 17172357
  38. Ding, Y.; Sun, T.; Ao, K.; Peng, Y.; Zhang, Y.; Li, X.; Zhang, Y. Opposite roles of salicylic acid receptors NPR1 and NPR3/NPR4 in transcriptional regulation of plant immunity. Cell, 2018, 173(6), 1454-1467.e15. doi: 10.1016/j.cell.2018.03.044 PMID: 29656896
  39. Houben, M.; Van de Poel, B. 1-Aminocyclopropane-1-Carboxylic acid oxidase (ACO): The enzyme that makes the plant hormone ethylene. Front. Plant Sci., 2019, 10, 695. doi: 10.3389/fpls.2019.00695 PMID: 31191592
  40. Gu, Y.Q.; Wildermuth, M.C.; Chakravarthy, S.; Loh, Y.T.; Yang, C.; He, X.; Han, Y.; Martin, G.B. Tomato transcription factors pti4, pti5, and pti6 activate defense responses when expressed in Arabidopsis. Plant Cell, 2002, 14(4), 817-831. doi: 10.1105/tpc.000794 PMID: 11971137
  41. Ouyang, B.; Yang, T.; Li, H.; Zhang, L.; Zhang, Y.; Zhang, J.; Fei, Z.; Ye, Z. Identification of early salt stress response genes in tomato root by suppression subtractive hybridization and microarray analysis. J. Exp. Bot., 2007, 58(3), 507-520. doi: 10.1093/jxb/erl258 PMID: 17210988
  42. Shinozaki, K.; Yamaguchi-Shinozaki, K.; Seki, M. Regulatory network of gene expression in the drought and cold stress responses. Curr. Opin. Plant Biol., 2003, 6(5), 410-417. doi: 10.1016/S1369-5266(03)00092-X PMID: 12972040
  43. Dubouzet, J.G.; Sakuma, Y.; Ito, Y.; Kasuga, M.; Dubouzet, E.G.; Miura, S.; Seki, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J., 2003, 33(4), 751-763. doi: 10.1046/j.1365-313X.2003.01661.x PMID: 12609047
  44. Häffner, E.; Konietzki, S.; Diederichsen, E. Keeping control: The role of senescence and development in plant pathogenesis and defense. Plants, 2015, 4(3), 449-488. doi: 10.3390/plants4030449 PMID: 27135337
  45. He, P.; Warren, R.F.; Zhao, T.; Shan, L.; Zhu, L.; Tang, X.; Zhou, J.M. Overexpression of Pti5 in tomato potentiates pathogen-induced defense gene expression and enhances disease resistance to Pseudomonas syringae pv. tomato. Mol. Plant Microbe Interact., 2001, 14(12), 1453-1457. doi: 10.1094/MPMI.2001.14.12.1453 PMID: 11768541
  46. Wu, C.; Avila, C.A.; Goggin, F.L. The ethylene response factor Pti5 contributes to potato aphid resistance in tomato independent of ethylene signalling. J. Exp. Bot., 2015, 66(2), 559-570. doi: 10.1093/jxb/eru472 PMID: 25504643
  47. Van Breusegem, F.; Vranová, E.; Dat, J.F.; Inzé, D. The role of active oxygen species in plant signal transduction. Plant Sci., 2001, 161(3), 405-414. doi: 10.1016/S0168-9452(01)00452-6
  48. Guida, V.; Criscuolo, G.; Tamburino, R.; Malorni, L.; Parente, A.; Maro, A.D. Purification and enzymatic properties of a peroxidase from leaves of Phytolacca dioica L. (Ombú tree). BMB Rep., 2011, 44(1), 64-69. doi: 10.5483/BMBRep.2011.44.1.64 PMID: 21266109
  49. Mohan, R.; Kolattukudy, P.E. Differential activation of expression of a suberization-associated anionic peroxidase gene in near-isogenic resistant and susceptible tomato lines by elicitors of Verticillium albo-atratrum. Plant Physiol., 1990, 92(1), 276-280. doi: 10.1104/pp.92.1.276 PMID: 16667260
  50. Almagro, L.; Gómez Ros, L.V.; Belchi-Navarro, S.; Bru, R.; Ros Barceló, A.; Pedreño, M.A. Class III peroxidases in plant defence reactions. J. Exp. Bot., 2009, 60(2), 377-390. doi: 10.1093/jxb/ern277 PMID: 19073963

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