Advertisement

Plant Molecular Biology Reporter

, Volume 37, Issue 1–2, pp 74–86 | Cite as

Overexpression of Wild Arachis Lipocalin Enhances Root-Knot Nematode Resistance in Peanut Hairy Roots

  • Bruna M. Pereira
  • Larissa A. GuimaraesEmail author
  • Nara O. S. Souza
  • Mario A. P. Saraiva
  • Patricia M. Guimaraes
  • Ana C. M. Brasileiro
Original Paper
  • 179 Downloads

Abstract

Plant parasitic root-knot nematodes (RKN) have evolved sophisticated strategies for exploiting plants, and they cause devastating yield losses in many susceptible crops. The RKN Meloidogyne arenaria is the most predominant pathogenic nematode affecting cultivated peanut (Arachis hypogaea L.). Resistance against the M. arenaria has been identified in the wild peanut relative, Arachis stenosperma. Transcriptome studies on A. stenospermaM. arenaria interaction revealed candidate genes potentially involved in the first stages of this resistance response, including a temperature-induced lipocalin (TIL) protein. Plant TILs have a protective role against harmful molecules produced in response to a number of stresses. In this study, the characterization of the RKN-responsive TIL from A. stenosperma (AsTIL) provides new insights into the role of plant lipocalins in nematode resistance. The AsTIL gene has a 2-exon/1-intron structure and encodes a 21.4 kDa polypeptide. It contains three structurally conserved regions, which are a signature for plant lipocalins. Overexpression of AsTIL in transgenic hairy roots from a susceptible peanut cultivar led to the reduction of M. arenaria galls and egg masses 60 days after inoculation. This is the first report of a possible involvement of plant lipocalins in RKN resistance. It also reveals a promising candidate gene for peanut breeding to produce cultivars resistant to M. arenaria.

Keywords

Agrobacterium rhizogenes Arachis hypogaea Arachis stenosperma Biotic stress Meloidogyne arenaria Temperature-induced lipocalin 

Notes

Acknowledgements

We would like to thank Dr. Peggy Ozias-Akins (University of Georgia, USA) for providing the pPZP-201BK-EGFP vector and Dr. Regina Carneiro (Embrapa Cenargen; Brazil) for providing and characterizing RKN M. arenaria.

References

  1. Alpizar E, Dechamp E, Espeout S, Royer M, Lecouls AC, Nicole M, Bertrand B, Lashermes P, Etienne H (2006) Efficient production of Agrobacterium rhizogenes-transformed roots and composite plants for studying gene expression in coffee roots. Plant Cell Rep 25:959–967.  https://doi.org/10.1007/s00299-006-0159-9 CrossRefGoogle Scholar
  2. Bertioli DJ, Seijo G, Freitas FO, Valls JFM, Leal-Bertioli SCM, Moretzsohn MC (2011) An overview of peanut and its wild relatives. Plant Genet Resour 9:134–149.  https://doi.org/10.1017/S1479262110000444 CrossRefGoogle Scholar
  3. Boca S, Koestler F, Ksas B, Chevalier A, Leymarie J, Fekete A, Mueller MJ, Havaux M (2014) Arabidopsis lipocalins AtCHL and AtTIL have distinct but overlapping functions essential for lipid protection and seed longevity. Plant Cell Environ 37:368–381.  https://doi.org/10.1111/pce.12159 CrossRefGoogle Scholar
  4. Bosselut N, Ghelder CV, Claverie M, Voisin R, Onesto JP, Rosso MN, Esmenjaud D (2011) Agrobacterium rhizogenes-mediated transformation of Prunus as an alternative for gene functional analysis in hairy-roots and composite plants. Plant Cell Rep 30:1313–1326.  https://doi.org/10.1007/s00299-011-1043-9 CrossRefGoogle Scholar
  5. Branch WD, Culbreath AK (2013) Yield performance and pest resistance among peanut genotypes when grown without fungicides or insecticides. Crop Prot 52:22–25.  https://doi.org/10.1016/j.cropro.2013.05.005 CrossRefGoogle Scholar
  6. Brasileiro ACM, Morgante CV, Araujo ACG, Leal-Bertioli SCM, Silva AK, Martins ACQ, Vinson CC, Santos CMR, Bonfim O, Togawa RC, Saraiva MAP, Bertioli DJ, Guimaraes PM, Silva AK, Vinson CC (2015) Transcriptome profiling of wild Arachis from water-limited environments uncovers drought tolerance candidate genes. Plant Mol Biol Report 33:1876–1892.  https://doi.org/10.1007/s11105-015-0882-x CrossRefGoogle Scholar
  7. Brinker M, Brosché M, Vinocur B, Abo-Ogiala A, Fayyaz P, Janz D, Ottow EA, Cullmann AD, Saborowski J, Kangasjärvi J (2010) Linking the salt transcriptome with physiological responses of a salt-resistant Populus species as a strategy to identify genes important for stress acclimation. Plant Physiol 154:1697–1709.  https://doi.org/10.1104/pp.110.164152 CrossRefGoogle Scholar
  8. Caillaud MC, Dubreuil G, Quentin M, Perfus-Barbeoch L, Lecomte P, de Almeida Engler J, Abad P, Rosso MN, Favery B (2008) Root-knot nematodes manipulate plant cell functions during a compatible interaction. J Plant Physiol 165:104–113.  https://doi.org/10.1016/j.jplph.2007.05.007 CrossRefGoogle Scholar
  9. Charron JBF, Sarhan F (2013) Plant lipocalins. In: Åkerström B, Borregaard N, Flower DR, Salier JP (eds) Lipocalins. USA: Landes Bioscience, Georgetown, TX, pp 41–48Google Scholar
  10. Charron JBF, Breton G, Badawi M, Sarhan F (2002) Molecular and structural analyses of a novel temperature stress-induced lipocalin from wheat and Arabidopsis. FEBS Lett 517:129–132.  https://doi.org/10.1016/S0014-5793(02)02606-6 CrossRefGoogle Scholar
  11. Charron JBF, Ouellet F, Pelletier M, Danyluk J, Chauve C, Sarhan F (2005) Identification, expression, and evolutionary analyses of plant lipocalins. Plant Physiol 139:2017–2028.  https://doi.org/10.1104/pp.105.070466 CrossRefGoogle Scholar
  12. Charron JBF, Ouellet F, Houde M, Sarhan F (2008) The plant apolipoprotein D ortholog protects Arabidopsis against oxidative stress. BMC Plant Biol 12:1–12.  https://doi.org/10.1186/1471-2229-8-86 Google Scholar
  13. Chi WT, Fung RWM, Liu HC, Hsu CC, Charng YY (2009) Temperature-induced lipocalin is required for basal and acquired thermotolerance in Arabidopsis. Plant Cell Environ 32:917–927.  https://doi.org/10.1111/j.1365-3040.2009.01972.x CrossRefGoogle Scholar
  14. Chu Y, Wu CL, Holbrook CC, Tillman BL, Person G, Ozias-Akins P (2011) Marker-assisted selection to pyramid nematode resistance and the high oleic trait in peanut. Plant Genome 4:110–117.  https://doi.org/10.3835/plantgenome2011.01.0001 CrossRefGoogle Scholar
  15. Chu Y, Guimaraes LA, Wu CL, Timper P, Holbrook CC, Ozias-Akins P (2014) A technique to study Meloidogyne arenaria resistance in Agrobacterium rhizogenes-transformed peanut. Plant Dis 98:1292–1299.  https://doi.org/10.1094/PDIS-12-13-1241-RE CrossRefGoogle Scholar
  16. Claverie M, Dirlewanger E, Bosselut N, Van Ghelder C, Voisin R, Kleinhentz M, Lafargue B, Abad P, Rosso M-N, Chalhoub B, Esmenjaud D (2011) The Ma gene for complete-spectrum resistance to Meloidogyne species in Prunus is a TNL with a huge C-terminal post-LRR region. Plant Physiol 156:779–792.  https://doi.org/10.1104/pp.111.176230 CrossRefGoogle Scholar
  17. Cook DE, Lee TG, Guo X, Melito S, Wang K, Bayless AM, Wang J, Hughes TJ, Willis DK, Clemente TE, Diers BW, Jiang J, Hudson ME, Bent AF (2012) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338:1206–1209CrossRefGoogle Scholar
  18. Culbreath A, Minton N, Brenneman T (1992) Response of Florunner and southern runner peanut cultivars of chemical management of late leaf spot, southern stem rot, and nematodes. Plant Dis 76:1199–1203CrossRefGoogle Scholar
  19. Czosnek H, Eybishtz A, Sade D, Gorovits R, Sobol I, Bejarano E, Rosas-Diaz T, Lozano-Duran R (2013) Discovering host genes involved in the infection by the Tomato yellow leaf curl virus complex and in the establishment of resistance to the virus using Tobacco rattle virus-based post transcriptional gene silencing. Viruses 5:998–1022.  https://doi.org/10.3390/v5030998 CrossRefGoogle Scholar
  20. Dickson DW, Hewlett TE (1989) Effects of bahiagrass and nematicides on Meloidogyne arenaria on peanut. J Nematol 21:671–676Google Scholar
  21. Djian-Caporalino C, Palloix A, Fazari A, Marteu N, Barbary A, Abad P, Sage-Palloix AM, Mateille T, Risso S, Lanza R, Taussig C, Castagnone-Sereno P (2014) Pyramiding, alternating or mixing: comparative performances of deployment strategies of nematode resistance genes to promote plant resistance efficiency and durability. BMC Plant Biol 14:53.  https://doi.org/10.1186/1471-2229-14-53 CrossRefGoogle Scholar
  22. Dong WB, Holbrook CC, Timper P, Brenneman TB, Chu Y, Ozias-Akins P (2008) Resistance in peanut cultivars and breeding lines to three root-knot nematode species. Plant Dis 92:631–638CrossRefGoogle Scholar
  23. Eddaoudi M, Ammati M, Rammah A (1997) Identification of the resistance breaking populations of Meloidogyne on tomatoes in Morocco and their effect on new sources of resistance. Fundam Appl Nematol 20:285–290Google Scholar
  24. Endo M, Shimizu H, Nohales MA, Araki T, Kay SA (2014) Tissue-specific clocks in Arabidopsis show asymmetric coupling. Nature 515:419–422.  https://doi.org/10.1038/nature13919 CrossRefGoogle Scholar
  25. Grzyb J, Latowski D, Strzałka K (2006) Lipocalins—a family portrait. J Plant Physiol 163:895–915.  https://doi.org/10.1016/j.jplph.2005.12.007 CrossRefGoogle Scholar
  26. Guimaraes PM, Brasileiro ACM, Proite K, de Araújo ACG, Leal-Bertioli SCM, Pic-Taylor A, da Silva FR, Morgante CV, Ribeiro GS, Bertioli DJ (2010) A study of gene expression in the nematode resistant wild peanut relative, Arachis stenosperma. Trop Plant Biol 3:183–192.  https://doi.org/10.1007/s12042-010-9056-z CrossRefGoogle Scholar
  27. Guimaraes PM, Brasileiro ACM, Morgante CV et al (2012) Global transcriptome analysis of two wild relatives of peanut under drought and fungi infection. BMC Genomics 13:387.  https://doi.org/10.1186/1471-2164-13-387 CrossRefGoogle Scholar
  28. Guimaraes PM, Guimaraes LA, Morgante CV, Silva OB, Araujo ACG, Martins ACQ, Saraiva MAP, Oliveira TN, Togawa RC, Leal-Bertioli SCM, Bertioli DJ, Brasileiro ACM (2015) Root transcriptome analysis of wild peanut reveals candidate genes for nematode resistance. PLoS One 10:e0140937.  https://doi.org/10.1371/journal.pone.0140937 CrossRefGoogle Scholar
  29. Guimaraes LA, Pereira BM, Araujo ACG, Guimaraes PM, Brasileiro ACM (2017a) Ex vitro hairy root induction in detached peanut leaves for plant–nematode interaction studies. Plant Methods 13:25.  https://doi.org/10.1186/s13007-017-0176-4 CrossRefGoogle Scholar
  30. Guimaraes LA, Mota APZ, Araujo ACG, de Alencar Figueiredo LF, Pereira BM, de Passos Saraiva MA, Silva RB, Danchin EGJ, Guimaraes PM, Brasileiro ACM (2017b) Genome-wide analysis of expansin superfamily in wild Arachis discloses a stress-responsive expansin-like B gene. Plant Mol Biol 94:79–96.  https://doi.org/10.1007/s11103-017-0594-8 CrossRefGoogle Scholar
  31. Gupta R, Jung E, Brunak S (2004) Prediction of N-glycosylation sites in human proteins. http://www.cbs.dtu.dk/services/NetNGlyc/. Accessed 25 Aug 2017
  32. He X, Sambe MAN, Zhuo C, Tu Q, Guo Z (2015) A temperature induced lipocalin gene from Medicago falcata (MfTIL1) confers tolerance to cold and oxidative stress. Plant Mol Biol 87:645–654.  https://doi.org/10.1007/s11103-015-0304-3 CrossRefGoogle Scholar
  33. Holbrook CC, Noe JP (1992) Resistance to the peanut root-knot nematode (Meloidogyne arenaria) in Arachis hypogaea L. Peanut Sci 19:35–37.  https://doi.org/10.3146/i0095-3679-19-1-9 CrossRefGoogle Scholar
  34. Holbrook CC, Timper P, Culbreath AK, Kvien CK (2008) Registration of “Tifguard” peanut. J Plant Regist 2:92.  https://doi.org/10.3198/jpr2007.12.0662crc CrossRefGoogle Scholar
  35. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  36. Leal-Bertioli SCM, Moretzsohn MC, Roberts PA, Ballen-Taborda C, Borba TCO, Valdisser PA, Vianello RP, Araujo ACG, Guimaraes PM, Bertioli DJ (2016) Genetic mapping of resistance to Meloidogyne arenaria in Arachis stenosperma: a new source of nematode resistance for peanut. G3;Genes Genomes Genet 6:377–390.  https://doi.org/10.1534/g3.115.023044 Google Scholar
  37. Levesque-Tremblay G, Havaux M, Ouellet F (2009) The chloroplastic lipocalin AtCHL prevents lipid peroxidation and protects Arabidopsis against oxidative stress. Plant J 60:691–702.  https://doi.org/10.1111/j.1365-313X.2009.03991.x CrossRefGoogle Scholar
  38. Lin J, Mazarei M, Zhao N, Zhu JJ, Zhuang X, Liu W, Pantalone VR, Arelli PR, Stewart CN Jr, Chen F (2013) Overexpression of a soybean salicylic acid methyltransferase gene confers resistance to soybean cyst nematode. Plant Biotechnol J 11:1135–1145CrossRefGoogle Scholar
  39. Lin J, Wang D, Chen X, Kollner TG, Mazarei M, Guo H, Pantalone VR, Arelli P, Stewart CN Jr, Wang N, Chen F (2017) An (E,E)-alpha-farnesene synthase gene of soybean has a role in defence against nematodes and is involved in synthesizing insect-induced volatiles. Plant Biotechnol J 15:510–519CrossRefGoogle Scholar
  40. Matthews BF, Beard H, MacDonald MH, Kabir S, Youssef RM, Hosseini P, Brewer E (2013) Engineered resistance and hypersusceptibility through functional metabolic studies of 100 genes in soybean to its major pathogen, the soybean cyst nematode. Planta 237:1337–1357.  https://doi.org/10.1007/s00425-013-1840-1 CrossRefGoogle Scholar
  41. Morgante CV, Guimaraes PM, Martins AC, Araújo AC, Leal-Bertioli SC, Bertioli DJ, Brasileiro ACM (2011) Reference genes for quantitative reverse transcription-polymerase chain reaction expression studies in wild and cultivated peanut. BMC Res Notes 4:339.  https://doi.org/10.1186/1756-0500-4-339 CrossRefGoogle Scholar
  42. Morgante CV, Brasileiro ACM, Roberts PA, Guimaraes LA, Araujo ACG, Fonseca LN, Leal-Bertioli SCM, Bertioli DJ, Guimaraes PM (2013) A survey of genes involved in Arachis stenosperma resistance to Meloidogyne arenaria race 1. Funct Plant Biol 40:1298–1309.  https://doi.org/10.1071/FP13096 CrossRefGoogle Scholar
  43. Mota APZ, Vidigal B, Danchin EGJ, Togawa RC, Leal-Bertioli SCM, Bertioli DJ, Araujo ACG, Brasileiro ACM, Guimaraes PM (2018) Comparative root transcriptome of wild Arachis reveals NBS-LRR genes related to nematode resistance. BMC Plant Biol 18:159–175.  https://doi.org/10.1186/s12870-018-1373-7 CrossRefGoogle Scholar
  44. Nelson SC, Simpson CE, Starr JL (1989) Resistance to Meloidogyne arenaria in Arachis spp germoplasm. J Nematol 21:654–660Google Scholar
  45. Pak HK, Sim JS, Rhee Y, Ko HR, Ha SH, Yoon MS, Kang CH, Lee S, Kim YH, Hahn BS (2009) Hairy root induction in oriental melon (Cucumis melo) by Agrobacterium rhizogenes and reproduction of the root-knot nematode (Meloidogyne incognita). Plant Cell Tissue Organ Cult 98:219–228.  https://doi.org/10.1007/s11240-009-9556-4 CrossRefGoogle Scholar
  46. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36–e336.  https://doi.org/10.1093/nar/30.9.e36
  47. Proite K, Leal-Bertioli SCM, Bertioli DJ, Moretzsohn MC, da Silva FR, Martins NF, Guimaraes PM, Guimaraes PM (2007) ESTs from a wild Arachis species for gene discovery and marker development. BMC Plant Biol 7:7.  https://doi.org/10.1186/1471-2229-7-7 CrossRefGoogle Scholar
  48. Proite K, Carneiro R, Gomes A, Bertioli D, Falcão R, Gomes A, Leal-Bertioli S, Guimaraes PM, Bertioli D (2008) Post-infection development and histopathology of Meloidogyne arenaria race 1 on Arachis spp. Plant Pathol 57:974–980.  https://doi.org/10.1111/j.1365-3059.2008.01861.x CrossRefGoogle Scholar
  49. Sade D, Eybishtz A, Gorovits R, Sobol I, Czosnek H (2012) A developmentally regulated lipocalin-like gene is overexpressed in Tomato yellow leaf curl virus-resistant tomato plants upon virus inoculation, and its silencing abolishes resistance. Plant Mol Biol 80:273–287.  https://doi.org/10.1007/s11103-012-9946-6 CrossRefGoogle Scholar
  50. Sánchez D, Ganfornina M, Gutierrez G, Gauthier-Jauneau AC, Risler JL, Salier JP (2005) Lipocalin genes and their evolutionary history. In: Åkerström B, Borregaard N, Flower DR, Salier JP (eds) Molecular biology intelligence unit: lipocalins. Landes Bioscience Eurekah.com, Georgetown, TX, pp 5–16
  51. Simon P (2003) Q-Gene: processing quantitative real-time RT-PCR data. Bioinformatics 19:1439–1440.  https://doi.org/10.1093/bioinformatics/btg157 CrossRefGoogle Scholar
  52. Simpson CE, Starr JL (2001) Registration of ‘COAN’ peanut. Crop Sci 41:918CrossRefGoogle Scholar
  53. Simpson CE, Starr JL, Church GT, Burow MD, Paterson AH (2003) Registration of “NemaTAM” peanut. (registrations of cultivars). Crop Sci 43:1561–1562CrossRefGoogle Scholar
  54. Simpson CE, Starr JL, Baring MR, Burow MD, Cason JM, Wilson JN (2013) Registration of “Webb” peanut. J Plant Regist 7:265–268.  https://doi.org/10.3198/jpr2013.01.0005crc CrossRefGoogle Scholar
  55. Solovyev V (2007) Statistical approaches in eukaryotic gene prediction. In: Handbook of statistical genetics. John Wiley & Sons, Ltd, pp 97–159Google Scholar
  56. Subramanian S (2017) Hairy root composite plant systems in root-microbe interaction research. Prod Plant Deriv Nat Compd through Hairy Root Cult 17–44.  https://doi.org/10.1007/978-3-319-69769-7_2
  57. Tzortzakakis EA, Conceição I, Dias AM, Simoglou KB, Abrantes I (2014) Occurrence of a new resistant breaking pathotype of Meloidogyne incognita on tomato in Greece. J Plant Dis Prot 121:184–186.  https://doi.org/10.1007/BF03356508 CrossRefGoogle Scholar
  58. Vinson CC, Mota APZ, Oliveira TN, Guimaraes LA, Leal-Bertioli SCM, Williams TCR, Nepomuceno AL, Saraiva MAP, Araujo ACG, Guimaraes PM, Brasileiro ACM (2018) Early responses to dehydration in contrasting wild Arachis species. PLoS One 13(5):e0198191.  https://doi.org/10.1371/journal.pone.0198191 CrossRefGoogle Scholar
  59. Vos P, Simons G, Jesse T, Wijbrandi J, Heinen L, Hogers R, Frijters A, Groenendijk J, Diergaarde P, Reijans M, Fierens-Onstenk J, de Both M, Peleman J, Liharska T, Hontelez J, Zabeau M (1998) The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nat Biotechnol 16:1365–1369.  https://doi.org/10.1038/4350 CrossRefGoogle Scholar
  60. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697.  https://doi.org/10.1093/aob/mcm079 CrossRefGoogle Scholar
  61. Zhao S, Fernald RD, Fernald ZS, Rd ZSF, Zhao S, Fernald RD, Rd ZSF, Liebert MA, Reaction RPC (2005) Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 12:1047–1064.  https://doi.org/10.1089/cmb.2005.12.1047.Comprehensive CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Embrapa Recursos Genéticos e BiotecnologiaBrasiliaBrazil
  2. 2.Universidade de BrasíliaBrasiliaBrazil
  3. 3.Department of Horticulture and Institute of Plant Breeding, Genetics & GenomicsThe University of GeorgiaTiftonUSA

Personalised recommendations