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Transcriptomic changes in sweetpotato peroxidases in response to infection with the root-knot nematode Meloidogyne incognita

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Abstract

A previous transcriptomic analysis of the roots of susceptible and resistant cultivars of sweetpotato (Ipomoea batatas) identified genes that were likely to contribute to protection against infection with the root-knot nematode Meloidogyne incognita. The current study examined the roles of peroxidase genes in sweetpotato defense responses during root-knot nematode infection, using the susceptible (cv. Yulmi) and resistant (cv. Juhwangmi) cultivars. Differentially expressed genes were assigned to gene ontology categories to predict their functional roles and associated biological processes. Comparison with Arabidopsis peroxidases identified a group of genes orthologous to Arabidopsis PEROXIDASE 52 (AtPrx52). An analysis of sweetpotato peroxidase genes determined their roles in protecting plants against root-knot nematode infection and enabled identification of important peroxidases. The interactions involved in sweetpotato resistance to nematode infection are discussed.

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Abbreviations

ROS:

Reactive oxygen species

PR:

Pathogenesis-related

PRX:

Peroxidase

RKN:

Root-knot nematode

DEGs:

Differentially expressed genes

GO:

Gene ontology

TAIR:

Arabidopsis information resource

qRT-PCR:

Quantitative real-time RT-PCR

References

  1. Tognolli M, Penel C, Greppin H, Simon P (2002) Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana. Gene 288:129–138

    Article  CAS  PubMed  Google Scholar 

  2. Passardi F, Longet D, Penel C, Dunand C (2004) The plant peroxidase multigenic family in rice and its evolution in green plants. Phytochemistry 65:1879–1893

    Article  CAS  PubMed  Google Scholar 

  3. Ren LL, Liu YJ, Liu HJ, Qian TT, Qi LW, Wang XR, Zeng QY (2014) Subcellular relocalization and positive selection play key roles in the retention of duplicate genes of populus class III peroxidase family. Plant Cell 26:2404–2419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Shigeto J, Tsutsumi Y (2016) Diverse functions and reactions of class III peroxidases. New Phytol 209:1395–1402

    Article  CAS  PubMed  Google Scholar 

  5. Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a swiss army knife. Plant Cell Rep 24:255–265

    Article  CAS  PubMed  Google Scholar 

  6. Cosio C, Dunand C (2009) Specific functions of individual class III peroxidase genes. J Exp Bot 60:391–408

    Article  CAS  PubMed  Google Scholar 

  7. Almagro L, Gomez Ros LV, Belchi-Navarro S, Bru R, Ros Barcelo A, Pedreno MA (2009) Class III peroxidases in plant defence reactions. J Exp Bot 60:377–390

    Article  CAS  PubMed  Google Scholar 

  8. Van Loon LC, Pierpoint WS, Boller T, Conejero V (1994) Recommendations for naming plant pathogenesis-related proteins. Plant Mol Biol Rep 12:245–264

    Article  Google Scholar 

  9. Bindschedler LV, Dewdney J, Blee KA, Stone JM, Asai T, Plotnikov J, Denoux C, Hayes T, Gerrish C, Davies DR, Ausubel FM, Bolwell GP (2006) Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J 47:851–863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Daudi A, Cheng Z, O’Brien JA, Mammarella N, Khan S, Ausubel FM, Bolwell GP (2012) The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity. Plant Cell 24:275–287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Choi HW, Kim YJ, Lee SC, Hong JK, Hwang BK (2007) Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens. Plant Physiol 145:890–904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Wally O, Punja ZK (2010) Enhanced disease resistance in transgenic carrot (Daucus carota L.) plants over-expressing a rice cationic peroxidase. Planta 232:1229–1239

    Article  CAS  PubMed  Google Scholar 

  13. Coego A, Ramirez V, Ellul P, Mayda E, Vera P (2005) The H2O2-regulated Ep5C gene encodes a peroxidase required for bacterial speck susceptibility in tomato. Plant J 42:283–293

    Article  CAS  PubMed  Google Scholar 

  14. Oliveira JTA, Andrade NC, Martins-Miranda AS, Soares AA, Gondim DMF, Araújo-Filho JH, Freire-Filho FR, Vasconcelos IM (2012) Differential expression of antioxidant enzymes and PR-proteins in compatible and incompatible interactions of cowpea (Vigna unguiculata) and the root-knot nematode Meloidogyne incognita. Plant Physiol Biochem 51:145–152

    Article  CAS  PubMed  Google Scholar 

  15. Guimaraes PM, Guimaraes LA, Morgante CV, Silva OB, Araujo ACG, Martins ACQ, Mario A, Saraiva P, Thais N, Oliveira Roberto C, Togawa Leal-Bertioli SCM, Bertioli DJ, Brasileiro ACM (2015) Root transcriptome analysis of wild peanut reveals candidate genes for nematode resistance. PLoS ONE 10:e0140937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Portillo M, Cabrera J, Lindsey K, Topping J, Andrés MF, Emiliozzi M, Resnick N, Oliveros JC, Casado GG, Solano R, Koltai H, Fenoll C, Escobar C (2013) Distinct and conserved transcriptomic changes during nematode-induced giant cell development in tomato compared with Arabidopsis: a functional role for gene repression. New Phytol 197:1276–1290

    Article  CAS  PubMed  Google Scholar 

  17. Huh GH, Lee SJ, Bae YS, Liu JR, Kwak SS (1997) Molecular cloning and characterization of cDNAs for anionic and neutral peroxidases from suspension-cultured cells of sweetpotato and their differential expression in response to stress. Mol Gen Genet 255:382–391

    Article  CAS  PubMed  Google Scholar 

  18. Kim KY, Huh GH, Lee HS, Kwon SY, Hur Y, Kwak SS (1999) Molecular characterization of two anionic peroxidase cDNAs isolated from suspension cultures of sweetpotato. Mol Gen Genet 261:941–947

    Article  CAS  PubMed  Google Scholar 

  19. Park SY, Ryu SH, Kwon SY, Lee HS, Kim GK, Kwak SS (2003) Differential expression of six novel peroxidase cDNAs from cell cultures of sweetpotato on response to stress. Mol Gen Genom 269:542–552

    Article  CAS  Google Scholar 

  20. Kim YH, Yang KS, Kim CY, Ryu SH, Song WK, Kwon SY, Lee HS, Bang JW, Kwak SS (2008) Molecular cloning of peroxidase cDNAs from dehydration-treated fibrous roots of sweetpotato and their differential expression in response to stress. BMB Rep 41:259–265

    Article  CAS  PubMed  Google Scholar 

  21. Kim YH, Jeong JC, Lee HS, Kwak SS (2013) Comparative characterization of sweetpotato antioxidant genes from expressed sequence tags of dehydration-treated fibrous roots under different abiotic stress conditions. Mol Biol Rep 40:2887–2896

    Article  CAS  PubMed  Google Scholar 

  22. Jang IC, Park SY, Kim KY, Kwon SY, Kim GK, Kwak SS (2004) Differential expression of 10 sweetpotato peroxidase genes in response to bacterial pathogen, Pectobacterium chrysanthemi. Plant Physiol Biochem 42:451–455

    Article  CAS  PubMed  Google Scholar 

  23. Kim YH, Lim S, Han SH, Lee JC, Song WK, Bang JW, Kwon SY, Lee HS, Kwak SS (2007) Differential expression of 10 sweetpotato peroxidases in response to sulfur dioxide, ozone, and ultraviolet radiation. Plant Physiol Biochem 45:908–914

    Article  CAS  PubMed  Google Scholar 

  24. Kim YH, Lee HS, Kwak SS (2010) Differential responses of sweetpotato peroxidases to heavy metals. Chemosphere 81:79–85

    Article  CAS  PubMed  Google Scholar 

  25. Ha J, Won JC, Jung YH, Yang JW, Lee HU, Nam KJ, Park SC, Jeong JC, Lee SW, Lee DW, Chung JS, Lee JJ, Kim YH (2017) Comparative proteomic analysis of the response of fibrous roots of nematode-resistant and -sensitive sweetpotato cultivars to root-knot nematode Meloidogyne incognita. Acta Physiol Plant 39:262

    Article  CAS  Google Scholar 

  26. Lee IH, Shim D, Jeong JC, Sung YW, Nam KJ, Yang JW, Ha J, Lee JJ, Kim YH (2019) Transcriptome analysis of root-knot nematode (Meloidogyne incognita)-resistant and susceptible sweetpotato cultivars. Planta 249:431–444

    Article  CAS  PubMed  Google Scholar 

  27. Park SC, Kim YH, Ji CY, Park S, Jeong JC, Lee HS, Kwak SS (2012) Stable internal reference genes for the normalization of real-time PCR in different sweetpotato cultivars subjected to abiotic stress conditions. PLoS ONE 7:e51502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  29. Kwak SS, Kim SK, Lee MS, Jung KH, Park IH, Liu JR (1995) Acidic peroxidase from suspension cultures of sweetpotato. Phytochemistry 39:981–984

    Article  CAS  Google Scholar 

  30. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  Google Scholar 

  31. Kim SK, Kwak SS, Jung KH, Min SR, Park IH, Liu JR (1994) Selection of plant cell lines for high yields of peroxidase. J Biochem Mol Biol 27:132–137

    CAS  Google Scholar 

  32. Ludwikow A, Gallois P, Sadowski J (2004) Ozone-induced oxidative stress response in Arabidopsis: transcription profiling by microarray approach. Cell Mol Biol Lett 9:829–842

    CAS  PubMed  Google Scholar 

  33. Little D, Gouhier-Darimont C, Bruessow F, Reymond P (2007) Oviposition by pierid butterflies triggers defense responses in Arabidopsis. Plant Physiol 143:784–800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Mohr PG, Cahill DM (2007) Suppression by ABA of salicylic acid and lignin accumulation and the expression of multiple genes, in Arabidopsis infected with Pseudomonas syringae pv. tomato. Funct Integr Genom 7:181–191

    Article  CAS  Google Scholar 

  35. Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 116:409–418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Cheong YH, Chang HS, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129:661–677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Narusaka Y, Narusaka M, Seki M, Ishida J, Shinozaki K, Nan Y, Park P, Shiraishi T, Kobayashi M (2005) Cytological and molecular analyses of non-host resistance of Arabidopsis thaliana to Alternaria alternata. Mol Plant Pathol 6:615–627

    Article  CAS  PubMed  Google Scholar 

  38. Weber M, Trampczynska A, Clemens S (2006) Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2+-hypertolerant facultative metallophyte Arabidopsis halleri. Plant Cell Environ 29:950–963

    Article  CAS  PubMed  Google Scholar 

  39. Chassot C, Nawrath C, Metraux JP (2007) Cuticular defects lead to full immunity to a major plant pathogen. Plant J 49:972–980

    Article  CAS  PubMed  Google Scholar 

  40. Abercrombie J, Halfhill M, Ranjan P, Rao MR, Saxton AM, Yuan JS, Stewart CNJ (2008) Transcriptional responses of Arabidopsis thaliana plants to As (V) stress. BMC Plant Biol 8:87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Kumari M, Taylor GJ, Deyholos MK (2008) Transcriptomic responses to aluminum stress in roots of Arabidopsis thaliana. Mol Genet Genom 279:339–357

    Article  CAS  Google Scholar 

  42. Vercauteren I, Van Der Schueren E, Van Montagu M, Gheysen G (2001) Arabidopsis thaliana genes expressed in the early compatible interaction with root-knot nematodes. Mol Plant Microbe Inter 14:288–299

    Article  CAS  Google Scholar 

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Acknowledgements

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT, and Future Planning (2018R1A1A1A05018446).

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Author notes

  1. Yeon Woo Sung, Il Hwan Lee and Donghwan Shim have contributed equally to this work.

Authors and Affiliations

  1. Department of Biology Education, IALS, Gyeongsang National University, Jinju, 660-701, Republic of Korea

    Yeon Woo Sung, Kang-Lok Lee, Ki Jung Nam & Yun-Hee Kim

  2. Division of Applied Life Science (BK21 Plus), Gyeongsang National University, Jinju, Republic of Korea

    Yeon Woo Sung

  3. Department of Forest Bio-resources, National Institute of Forest Science, Suwon, Republic of Korea

    Il Hwan Lee & Donghwan Shim

  4. National Institute of Crop Science, Rural Development Administration, Suwon, Republic of Korea

    Jung-Wook Yang

  5. Department of Plant Medicine, IALS, Gyeongsang National University, Jinju, Republic of Korea

    Jeung Joo Lee

  6. Plant Systems Engineering Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB), Daejeon, Republic of Korea

    Sang-Soo Kwak

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  1. Yeon Woo Sung
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Contributions

YHK, YWS, IHL and DS conceived and designed the experiments. YWS, IHL and YHK performed the experiments. KLL and KJN analyzed the data. JWY, JJL and SSK contributed to the analysis and provided materials and reagent tools. YHK, YWS, IHL and DS wrote the paper.

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Correspondence to Yun-Hee Kim.

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Sung, Y.W., Lee, I.H., Shim, D. et al. Transcriptomic changes in sweetpotato peroxidases in response to infection with the root-knot nematode Meloidogyne incognita. Mol Biol Rep 46, 4555–4564 (2019). https://doi.org/10.1007/s11033-019-04911-7

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