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Planta

, Volume 249, Issue 2, pp 431–444 | Cite as

Transcriptome analysis of root-knot nematode (Meloidogyne incognita)-resistant and susceptible sweetpotato cultivars

  • Il Hwan Lee
  • Donghwan Shim
  • Jea Cheol Jeong
  • Yeon Woo Sung
  • Ki Jung Nam
  • Jung-Wook Yang
  • Joon Ha
  • Jeung Joo Lee
  • Yun-Hee KimEmail author
Original Article

Abstract

Main conclusion

Transcriptome analysis was performed on the roots of susceptible and resistant sweetpotato cultivars infected with the major root-knot nematode species Meloidogyne incognita. In addition, we identified a transcription factor-mediated defense signaling pathway that might function in sweetpotato–nematode interactions.

Root-knot nematodes (RKNs, Meloidogyne spp.) are important sedentary endoparasites of many agricultural crop plants that significantly reduce production in field-grown sweetpotato. To date, no studies involving gene expression profiling in sweetpotato during RKN infection have been reported. Therefore, in the present study, transcriptome analysis was performed on the roots of susceptible (cv. Yulmi) and resistant (cv. Juhwangmi) sweetpotato cultivars infected with the widespread, major RKN species Meloidogyne incognita. Using the Illumina HiSeq 2000 platform, we generated 455,295,628 pair-end reads from the fibrous roots of both cultivars, which were assembled into 74,733 transcripts. A number of common and unique genes were differentially expressed in susceptible vs. resistant cultivars as a result of RKN infection. We assigned the differentially expressed genes into gene ontology categories and used MapMan annotation to predict their functional roles and associated biological processes. The candidate genes including hormonal signaling-related transcription factors and pathogenesis-related genes that could contribute to protection against RKN infection in sweetpotato roots were identified and sweetpotato–nematode interactions involved in resistance are discussed.

Keywords

Defense signaling Root-knot nematodes Sweetpotato Transcriptome 

Abbreviations

DEG

Differentially expressed genes

ET

Ethylene

JA

Jasmonic acid

PR

Pathogenesis-related

RKN

Root-knot nematode

SA

Salicylic acid

TF

Transcription factor

Notes

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).

Supplementary material

425_2018_3001_MOESM1_ESM.pptx (978 kb)
Supplementary material 1 (PPTX 977 kb)
425_2018_3001_MOESM2_ESM.xlsx (14 kb)
Supplementary material 2 (XLSX 13 kb)
425_2018_3001_MOESM3_ESM.xlsx (54 kb)
Supplementary material 3 (XLSX 54 kb)

References

  1. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78Google Scholar
  2. Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479Google Scholar
  3. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–983Google Scholar
  4. Boter M, Ruiz-Rivero O, Abdeen A, Prat S (2004) Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Genes Dev 18:1577–1591Google Scholar
  5. Branch C, Hwang CF, Navarre DA, Williamson VM (2004) Salicylic acid is part of the Mi-1-mediated defense response to root-knot nematode in tomato. Mol Plant Microbe Int 17:351–356Google Scholar
  6. Bridge J, Starr JL (2010) Plant nematodes of agricultural importance a color handbook. Academic Press, San Diego, pp 77–78Google Scholar
  7. Camera SL, Balagué C, Göbel C, Geoffroy P, Legrand M, Feussner I, Roby D, Heitz T (2009) The Arabidopsis patatin-like protein 2 (PLP2) plays an essential role in cell death execution and differentially affects biosynthesis of oxylipins and resistance to pathogens. Mol Plant Microbe Int 22:469–481Google Scholar
  8. Castagnone-Sereno P, Danchin EG, Perfus-Barbeoch L, Abad P (2013) Diversity and evolution of root knot nematodes, genus Meloidogyne: new insights from the genomic era. Annu Rev Phytopathol 51:203–220Google Scholar
  9. Cervantes-Flores JC, Yenchom GC, Pecotam KV, Sosinski B (2008) Detection of quantitative trait loci and inheritance of root-knot nematode resistance in sweetpotato. J Am Soc Hortic Sci 133:844–851Google Scholar
  10. Choi DR, Lee JK, Park BY, Chung MN (2006) Occutrrence of rootknot nematodes in sweet potato fields and resistance screening of sweet potato cultivars. Korean J Appl Entomol 45:211–216Google Scholar
  11. Clark CA, Moyer JW (1998) Compendium of sweetpotato diseases. APS Press, Saint PaulGoogle Scholar
  12. De Vos M, Van Oosten VR, Van Poecke RM, Van Pelt JA, Pozo MJ, Mueller MJ, Buchala AJ, Metraux JP, Van Loon LC, Dicke M, Pieterse CMJ (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe In 18:923–937Google Scholar
  13. Diaz JT, Chinn MS, Truong VD (2014) Simultaneous saccharification and fermentation of industrial sweetpotatoes for ethanol production and anthocyanins extraction. Ind Crops Prod 62:53–60Google Scholar
  14. Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, Fitt GP, Sewelam N, Schenk PM, Manners JM, Kazan K (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225–2245Google Scholar
  15. Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371Google Scholar
  16. Fu L, Niu B, Zhu Z, Wu S, Li W (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28:3150–3152.  https://doi.org/10.1093/bioinformatics/bts565 Google Scholar
  17. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442Google Scholar
  18. Grace MH, Yousef GG, Gustafson SJ, Truong VD, Yencho GC, Lila MA (2014) Phytochemical changes in phenolics, anthocyanins, ascorbic acid, and carotenoids associated with sweetpotato storage and impacts on bioactive properties. Food Chem 145:717–724Google Scholar
  19. Grunewald W, Karimi M, Wieczorek K, Van de Cappelle E, Wischnitzki E, Grundler F, Inzé D, Beeckman T, Gheysen G (2008) A role for AtWRKY23 in feeding site establishment of plant-parasitic nematodes. Plant Physiol 148:358–368Google Scholar
  20. 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.  https://doi.org/10.1007/s11738-017-2560-0 Google Scholar
  21. Hamamouch N, Li C, Seo PJ, Park CM, Davis EL (2011) Expression of Arabidopsis pathogenesis-related genes during nematode infection. Mol Plant Pathol 12:355–364Google Scholar
  22. Han Z, Sun Y, Chai J (2014) Structural insight into the activation of plant receptor kinases. Curr Opin Plant Biol 20:55–63Google Scholar
  23. Holbein J, Grundler FMW, Siddique S (2016) Plant basal resistance to nematodes: an update. J Exp Bot 67:2049–2061Google Scholar
  24. Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329Google Scholar
  25. Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S, Ntoukakis V, Jones JD, Shirasu K, Menke F, Jones A, Zipfel C (2014) Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol Cell 54:43–55Google Scholar
  26. Kazan K, Manners JM (2008) Jasmonate signaling: toward an integrated view. Plant Physiol 146:1459–1468Google Scholar
  27. Kistner MH, Daiber KC, Bester C (1993) The effect of root-knot nematodes (Meloidogyne spp.) and dry land conditions on the production of sweetpotato. JS Afr Soc Hortic Sci 3:108–110Google Scholar
  28. Kreuze J (2002) Molecular studies on the sweetpotato virus disease and its two causal agents. In: Acta Universitatis Agriculturae Sueciae Agraria 335. Department of Plant Biology, Sveriges lantbrukuniversitet, UppsalaGoogle Scholar
  29. Lee JJ, Park KW, Kwak YS, Ahn JY, Jung YH, Lee BH, Jeong JC, Lee HS, Kwak SS (2012) Comparative proteomic study between tuberous roots of light orange- and purple-fleshed sweetpotato cultivars. Plant Sci 193–194:120–129Google Scholar
  30. Li L, Li M, Yu L, Zhou Z, Liang X, Liu Z, Cai G, Gao L, Zhang X, Wang Y, Chen S, Zhou JM (2014) The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15:329–338Google Scholar
  31. Liu JJ, Ekramoddoullah AKM (2006) The family 10 of plant pathogenesis-related proteins: their structure, regulation, and function in response to biotic and abiotic stresses. Physiol Mol Plant Pathol 68:3–13Google Scholar
  32. Lorenzo O, Chico JM, Sanchez-Serrano JJ, Solano R (2004) JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16:1938–1950Google Scholar
  33. Lu DP, Wu SJ, Gao XQ, Zhang YL, Shan LB, He P (2010) A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc Natl Acad Sci USA 107:496–501Google Scholar
  34. Melillo MT, Leonetti P, Bongiovanni M, Castagnone-Sereno P, Bleve-Zacheo T (2006) Modulation of reactive oxygen species activities and H2O2 accumulation during compatible and incompatible tomato-root knot nematode interactions. New Phytol 170:501–512Google Scholar
  35. Mendy B, Wangombe MW, Radakovic ZS, Holbein J, Ilyas M, Chopra D, Holton N, Zipfel C, Grundler FMW, Siddique S (2017) Arabidopsis leucine-rich repeat receptor-like kinase NILR1 is required for induction of innate immunity to parasitic nematodes. Plos Pathol 13:e1006284Google Scholar
  36. Nahar K, Kyndt T, De Vleesschauwer D, Hofte M, Gheysen G (2011) The jasmonate pathway is a key player in systemically induced defense against root knot nematodes in rice. Plant Physiol 157:305–306Google Scholar
  37. Nandi B, Kundu K, Banerjee N, Babu SPS (2003) Salicylic acid-induced suppression of Meloidogyne incognita infestation of okra and cowpea. Nematology 5:747–752Google Scholar
  38. Palomares-Rius JE, Kikuchi T (2013) Omics fields of study related to plant-parasitic nematodes. J Integr Omics 3:1–10Google Scholar
  39. 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:e51502Google Scholar
  40. Peng HC, Kaloshian I (2014) The tomato leucine-rich repeat receptor-like kinases SISERK3A and SISERK3B have overlapping functions in bacterial and nematode innate immunity. PLoS ONE 9:e93302Google Scholar
  41. Roux M, Schwessinger B, Albrecht C, Chinchilla D, Jones A, Holton N, Malinovsky FG, Tor M, de Vries S, Zipfel C (2011) The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23:2440–2455Google Scholar
  42. Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258Google Scholar
  43. Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P, Pastor V, Flors V (2013) Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. Plant Cell Rep 32:1085–1098Google Scholar
  44. Soriano I, Riley I, Potter M, Bowers W (2004) Phytoecdysteroids: a novel defense against plant-parasitic nematodes. J Chem Ecol 30:1885–1899Google Scholar
  45. Staswick PE, Yuen GY, Lehman CC (1998) Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare. Plant J 15:747–754Google Scholar
  46. Sun YD, Li L, Macho AP, Han ZF, Hu ZH, Zipfel C, Zhou JM, Chai JJ (2013) Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342:624–628Google Scholar
  47. Teixeira MA, Wei L, Kaloshian I (2016) Root-knot nematodes induce pattern- triggered immunity in Arabidopsis thaliana roots. New Phytol 211:279–287Google Scholar
  48. Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue BPA, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95(15107–15):111Google Scholar
  49. Van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Ann Rev Phytopathol 44:135–162Google Scholar
  50. Viaene N, Smol N, Bert W (2012) General techniques in nematology. Academia Press, Gent. Belgium, pp 58–59Google Scholar
  51. Vijayan P, Shockey J, Levesque CA, Cook RJ, Browse J (1998) A role for jasmonate in pathogen defense of Arabidopsis. Proc Natl Acad Sci USA 95:7209–7214Google Scholar
  52. Williamson VM, Kumar A (2006) Nematode resistance in plants: the battle underground. Trends Genet 22:396–403Google Scholar
  53. Woolfe JA (1992) Sweetpotato: an untapped food resource. Cambridge University Press, CambridgeGoogle Scholar
  54. Yeh KW, Lin MI, Tuan SJ, Chen YM, Lin CY, Kao SS (1997) Sweetpotato (Ipomoea batatas) trypsin inhibitors expressed in transgenic tobacco plants confer resistance against Spodoptera litura. Plant Cell Rep 16:696–699Google Scholar
  55. Zipfel C (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20:10–16Google Scholar
  56. Zipfel C (2014) Plant pattern-recognition receptors. Trends Immunol 35:345–351Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Il Hwan Lee
    • 1
  • Donghwan Shim
    • 1
  • Jea Cheol Jeong
    • 2
  • Yeon Woo Sung
    • 3
  • Ki Jung Nam
    • 3
  • Jung-Wook Yang
    • 4
  • Joon Ha
    • 5
  • Jeung Joo Lee
    • 6
  • Yun-Hee Kim
    • 3
    Email author
  1. 1.Department of Forest Genetic ResourcesNational Institute of Forest ScienceSuwonRepublic of Korea
  2. 2.Biological Resource Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)JeongeupRepublic of Korea
  3. 3.Department of Biology Education, IALSGyeongsang National UniversityJinjuRepublic of Korea
  4. 4.Bioenergy Crop Research Institute, National Institute of Crop ScienceRural Development AdministrationMuanRepublic of Korea
  5. 5.Division of Applied Life Science (BK21 Plus)Gyeongsang National UniversityJinjuRepublic of Korea
  6. 6.Department of Plant Medicine, IALSGyeongsang National UniversityJinjuRepublic of Korea

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