Differential gene expression in roots of nematode-resistant and -susceptible peanut (Arachis hypogaea) cultivars in response to early stages of peanut root-knot nematode (Meloidogyne arenaria) parasitization

Journal of Plant Physiology

Volumn 168, Issue 5, 2011, Pages 481-492

  Tirumalaraju, Sivananda V ^a,b   Jain, Mukesh ^a   Gallo, Maria ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b Genetics Institute ^*  (United States)

Author keywords

Arachis hypogaea; Florunner; Giant cell; Meloidogyne; NemaTAM; Root knot nematode; Suppression subtractive hybridization

Indexed keywords

COMPLEMENTARY DNA; PRIMER DNA;

ANIMAL; ARTICLE; GENE EXPRESSION; METABOLISM; NEMATODE; NUCLEOTIDE SEQUENCE; PARASITOLOGY; PEANUT; PHYSIOLOGY; PLANT ROOT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; ARACHIS HYPOGAEA; BASE SEQUENCE; DNA PRIMERS; DNA, COMPLEMENTARY; GENE EXPRESSION; NEMATODA; PLANT ROOTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

ARACHIS HYPOGAEA; MELOIDOGYNE; MELOIDOGYNE ARENARIA; MELOIDOGYNE JAVANICA; NEMATODA;

EID: 79251601217     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2010.08.006     Document Type: Article

References (85)

1. Afzal A.J., Natarajan A., Saini N., Iqbal M.J., Geisler M., El Shemy H.A., Mungur R., Willmitzer L., Lightfoot D.A. The Nematode resistance allele at the rhg1 locus alters the proteome and primary metabolism of soybean roots. Plant Physiol 2009, 151:1264-1280.
2. Åhman J., Johansson T., Olsson M., Punt P.J., van den Hondel C.A.M.J.J., Tunlid A. Improving the pathogenicity of a nematode-trapping fungus by genetic engineering of a subtilisin with nematotoxic activity. Appl Environ Microbiol 2002, 68:3408-3415.
3. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
4. Barcala M., García A., Cabrera J., Casson S., Lindsey K., Favery B., García-Casado G., Solano R., Fenoll C., Escobar C. Early transcriptomic events in microdissected Arabidopsis nematode-induced giant cells. Plant J 2010, 61:698-712.
5. Bartscha M., Gobbatoa E., Bednareka P., Debeyb S., Schultze J.L., Bautora J., Parkera J.E. Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the Nudix hydrolase NUDT7. Plant Cell 2006, 18:1038-1051.
6. Bendezu I.F., Starr J.L. Mechanism of resistance to Meloidogyne arenaria in the peanut cultivar COAN. J Nematol 2003, 35:115-118.
7. Bhuiyan N.H., Selvaraj G., Wei Y., King J. Gene expression profiling and silencing reveal that monolignol biosynthesis plays a critical role in penetration defense in wheat against powdery mildew invasion. J Exp Bot 2009, 60:509-521.
8. Bopopi J.M., Vandeputte O.M., Himanen K., Mol A., Vaessen Q., El Jaziri M., Baucher M. Ectopic expression of PtaRHE1, encoding a poplar RING-H2 protein with E3 ligase activity, alters plant development and induces defense-related responses. J Exp Bot 2010, 61:297-310.
9. Braam J., Davis R.W. Rain-, wind-, and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell 1990, 60:357-364.
10. Burrows P.R., Barker A.D.P., Newell C.A., Hamilton W.D.O. Plant-derived enzyme inhibitors and lectins for resistance against plant-parasitic nematodes in transgenic crops. Pestic Sci 1998, 52:176-183.
11. Cappelle E.V., Plovie E., Kyndt T., Grunewald W., Cannoot B., Gheysen G. AtCDKA;1 silencing in Arabidopsis thaliana reduces reproduction of sedentary plant-parasitic nematodes. Plant Biotechnol J 2008, 6:749-757.
12. Castagnone-Sereno P. Genetic variability of nematodes: a threat to the durability of plant resistance genes?. Euphytica 2002, 124:193-199.
13. Charlton W.L., Harel H.Y.M., Bakhetia M., Hibbard J.K., Atkinson H.J., McPherson M.J. Additive effects of plant expressed double-stranded RNAs on root-knot nematode development. Int J Parasitol 2010, 40:855-864.
14. Chitwood D.J. Research on plant-parasitic nematode biology conducted by the United States Department of Agriculture-Agricultural Research Service. Pest Manag Sci 2003, 59:748-753.
15. Chiu W.-H., Chandler J., Cnops G., Van Lijsebettens M., Werr W. Mutations in the TORNADO2 gene affect cellular decisions in the peripheral zone of the shoot apical meristem of Arabidopsis thaliana. Plant Mol Biol 2007, 63:731-744.
16. Cho H.-T., Cosgrove D.J. Regulation of root hair initiation and expansin gene expression in Arabidopsis. Plant Cell 2002, 14:3237-3253.
17. Chondrou M.P., Mastellos D., Zarkadis I.K. cDNA cloning and phylogenetic analysis of the sixth complement component in rainbow trout. Mol Immunol 2006, 43:1080-1087.
18. Clough S.J., Fengler K.A., Yu I., Lippok B., Smith R.K., Bent A.F. The Arabidopsis dnd1 'defence, no death' gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci USA 2000, 97:9323-9328.
19. Diachenko L., Lau Y.F., Campbell A.P., Chenchik A., Mogadam F., Huang B., Lukyanov S., Lukyanov K., Gurskaya N., Sverdlov E.D., Siebert D. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 1996, 93:6025-6030.
20. Dickson D.W., DeWaele D. Nematode parasites of peanut. Plant-parasitic nematodes in subtropical and tropical agriculture 2005, 393-436. CAB International. 2nd ed. M. Luc, R.A. Sikora, J. Bridge (Eds.).
21. Dubreuil G., Magliano M., Deleury E., Abad P., Rosso M.N. Transcriptome analysis of root-knot nematode functions induced in the early stages of parasitism. New Phytol 2007, 176:426-436.
22. Fairbairn D.J., Cavallaro A.S., Bernard M., Mahalinga-Iyer J., Graham M.W., Botella J.R. Host-delivered RNAi: an effective strategy to silence genes in plant parasitic nematodes. Planta 2007, 226:1525-1533.
23. Fosu-Nyarko J., Jones M.G.K., Wang Z. Functional characterization of transcripts expressed in early-stage Meloidogyne javanica-induced giant cells isolated by laser microdissection. Mol Plant Pathol 2009, 10:237-248.
24. Fudali S., Janakowski S., Sobczak M., Griesser M., Grundler F.M., Golinowski W. Two tomato alpha-expansins show distinct spatial and temporal expression patterns during development of nematode-induced syncytia. Physiol Planta 2008, 132:370-383.
25. Fudali S., Sobczak M., Janakowski S., Griesser M., Grundler F.M., Golinowski W. Expansins are among plant cell wall modifying agents specifically expressed during development of nematode-induced syncytia. Plant Signal Behav 2008, 3:969-971.
26. Fuller V.L., Lilley C.J., Atkinson H.J., Urwin P.E. Differential gene expression in Arabidopsis following infection by plant-parasitic nematodes Meloidogyne incognita and Heterodera schachtii. Mol Plant Pathol 2007, 8:595-609.
27. Fuller V.L., Lilley C.J., Urwin P.E. Nematode resistance. New Phytol 2008, 180:27-44.
28. Gal T.Z., Aussenberg E.R., Burdman S., Kapulnik Y., Koltai H. Expression of a plant expansin is involved in the establishment of root knot nematode parasitism in tomato. Planta 2006, 224:155-162.
29. Galperin M.Y., Moroz O.V., Wilson K.S., Murzin A.G. House cleaning, a part of good housekeeping. Mol Microbiol 2006, 59:5-19.
30. Gigolashvili T., Berger B., Flügge U.-I. Specific and coordinated control of indolic and aliphatic glucosinolate biosynthesis by R2R3-MYB transcription factors in Arabidopsis thaliana. Phytochem Rev 2009, 8:3-13.
31. Guenther J.F., Roberts D.M. Water-selective and multifunctional aquaporins from Lotus japonicus nodules. Planta 2000, 210:741-748.
32. Hagihara T., Masaru H., Yoji T., Naoto Y. Cloning of soybean genes induced during hypersensitive cell death caused by syringolide elicitor. Planta 2004, 218:606-614.
33. Hammes U.Z., Schachtman D.P., Berg R.H., Nielsen E., Koch W., McIntyre L.M., Taylor C.G. Nematode-induced changes of transporter gene expression in Arabidopsis roots. Mol Plant Microbe Interact 2005, 18:1247-1257.
34. Himelblau E., Mira H., Lin S.J., Culotta V.C., Peñarrubia L., Amasino R.M. Identification of a functional homolog of the yeast copper homeostasis gene ATX1 from Arabidopsis. Plant Physiol 1998, 117:1227-1234.
35. Hofmann J., Hess P.H., Szakasits D., Blochl A., Wieczorek K., Daxbock-Horvath S., Bohlmann H., vanBel A.J.E., Grundler F.M.W. Diversity and activity of sugar transporters in nematode-induced root syncytia. J Exp Bot 2009, 60:3085-3095.
36. Huang G.Z., Allen R., Davis E.L., Baum T.J., Hussey R.S. Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. Proc Natl Acad Sci USA 2006, 103:14302-14306.
37. Hussey R.S., Barker K.R. A comparison of methods of collecting inocula of Meloidogyne spp., including a new technique. Plant Dis Rep 1973, 57:1025-1028.
38. Jain D., Roy N., Chattopadhyay D. CaZF, a plant transcription factor functions through and parallel to HOG and calcineurin pathways in Saccharomyces cerevisiae to provide osmotolerance. PLoS ONE 2009, 4:e5154.
39. Jammes F., Lecomte P., de Almeida-Engler J., Bitton F., Martin-Magniette M.L., Renou J.P., Abad P., Favery B. Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis. Plant J 2005, 44:447-458.
40. Jones M.G.K. Host cell responses to endoparasitic nematode attack: Structure and function of giant cells and syncytia. Ann Appl Biol 1980, 97:353-372.
41. Kaplan D.T., Davis E.L. A bioassay to estimate root penetration by nematodes. J Nematol 1991, 23:446-450.
42. Karahara I., Suda J., Tahara H., Yokota E., Shimmen T., Misaki K., Yonemura S., Staehelin L.A., Mineyuki Y. The preprophase band is a localized center of clathrin-mediated endocytosis in late prophase cells of the onion cotyledon epidermis. Plant J 2009, 57:819-831.
43. Karczmarek A., Overmars H., Helder J., Goverse A. Feeding cell development by cyst and root-knot nematodes involves a similar early, local and transient activation of a specific auxin-inducible promoter element. Mol Plant Pathol 2004, 5:343-346.
44. Kawasaki T., Koita H., Nakatsubo T., Hasegawa K., Wakabayashi K., Takahashi H., Umemura K., Umezawa T., Shimamoto K. Cinnamoyl-CoA reductase, a key enzyme in lignin biosynthesis, is an effector of small GTPase Rac in defense signaling in rice. Proc Natl Acad Sci USA 2006, 103:230-235.
45. Klink V.P., Hosseini P., MacDonald M.H., Alkharouf N., Matthews B.F. Population-specific gene expression in the plant pathogenic nematode Heterodera glycines exists prior to infection and during the onset of a resistant or susceptible reaction in the roots of the Glycine max genotype Peking. BMC Genomics 2009, 10:111.
46. Klink V.P., Hosseini P., Matsye P., Alkharouf N.W., Matthews B.F. A gene expression analysis of syncytia laser microdissected from the roots of the Glycine max (soybean) genotype PI 548402 (Peking) undergoing a resistant reaction after infection by Heterodera glycines (soybean cyst nematode). Plant Mol Biol 2009, 71:525-567.
47. Kushiro T., Okamoto M., Nakabayashi K., Yamagishi K., Kitamura S., Asami T., Hirai N., Koshiba T., Kamiya Y., Nambara E. The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′-hydroxylases: key enzymes in ABA catabolism. EMBO J 2004, 23:1647-1656.
48. La Camera S., Geoffroy P., Samaha H., Ndiaye A., Rahim G., Legrand M., Heitz T. A pathogen-inducible patatin-like lipid acyl hydrolase facilitates fungal and bacterial host colonization in Arabidopsis. Plant J 2005, 44:810-825.
49. Levy S., Shoham T. The tetraspanin web modulates immune-signaling complexes. Nat Rev Immunol 2005, 5:136-148.
50. -ΔΔCt method. Methods 2001, 25:402-408.
51. Longemann J., Schell J., Willmitzer L. Improved method for the isolation of RNA from plant tissues. Anal Biochem 1987, 163:16-20.
52. Martin L., Leblanc-Fournier N., Azri W., Lenne1 C., Henry C., Coutand C., Julien J.-L. Characterization and expression analysis under bending and other abiotic factors of PtaZFP2, a poplar gene encoding a Cys2/His2 zinc finger protein. Tree Physiol 2009, 29:125-136.
53. Matos A.R., Gigon A., Laffray D., Pêtres S., Zuily-Fodil Y., Pham-Thi A.T. Effects of progressive drought stress on the expression of patatin-like lipid acyl hydrolase genes in Arabidopsis leaves. Physiol Planta 2008, 134:110-120.
54. McQueen-Mason S.J., Fry S.C., Daniel M., Durachko D.M., Cosgrove D.J. The relationship between xyloglucan endotransglycosylase and in vitro cell wall extension in cucumber hypocotyls. Planta 1993, 190:327-331.
55. Nachin L., Nannmark U., Nystrom T. Differential roles of the universal stress proteins of Escherichia coli in oxidative stress resistance, adhesion, and motility. J Bacteriol 2005, 187:6265-6272.
56. Nah G., Pagliarulo C.L., Mohr P.G., Luo M., Sisneros N., Yu Y., Collura K., Currie J., Goicoechea J.L., Wing R.A., Schumaker K.S. Comparative sequence analysis of the SALT OVERLY SENSITIVE1 orthologous region in Thellungiella halophila and Arabidopsis thaliana. Genomics 2009, 94:196-203.
57. Niebel A., Heungens K., Barthels N., Inzé D., Van Montagu M., Gheysen G. Characterization of a pathogen-induced potato catalase and its systemic expression upon nematode and bacterial infection. Mol Plant Microbe Interact 1995, 8:371-378.
58. Olmos E., Reiss B., Dekke K. The ekeko mutant demonstrates a role for tetraspanin-like protein in plant development. Biochem Biophys Res Commun 2003, 310:1054-1061.
59. Portillo M., Lindsey K., Casson S., García-Casado G., Solano R., Fenoll C., Escobar C. Isolation of RNA from laser-capture-microdissected giant cells at early differentiation stages suitable for differential transcriptome analysis. Mol Plant Pathol 2009, 10:523-535.
60. Qiu J., Hallmann J., Kokalis-Burelle N., Waever D.B., Rodríguez-Kábana R., Tuzun S. Activity and differential induction of chitinase isozymes in soybean cultivars resistant or susceptible to root-knot nematodes. J Nematol 1997, 29:523-530.
61. Radjendirane V., Joseph P., Jaiswal A.K. Gene expression of DT diaphorase (NQO1) in cancer cells. Oxidative Stress and Signal Transduction 1997, 441-475. Chapman and Hall, New York. H.J. Forman, E. Cadenas (Eds.).
62. Rebrikov D.V., Britanova O.V., Gurskaya N.G., Lukyanov K.A., Tarabykin V.S., Lukyanov S.A. Mirror orientation selection (MOS)-a method for eliminating false positive clones from libraries generated by suppression subtractive hybridization. Nucleic Acid Res 2000, 28:e90.
63. Ripoll C., Favery B., Lecomte P., Van Damme E., Peumans W., Abad P., Jouanin L. Evaluation of the ability of lectin from snowdrop (Galanthus nivalis) to protect plants against root-knot nematodes. Plant Sci 2003, 164:517-523.
64. Rosso M.N., Jones J.T., Abad P. RNAi and functional genomics in plant parasitic nematodes. Annu Rev Phytopathol 2009, 47:207-232.
65. Sambrook J., Fritsch E.F., Maniatis T., Molecular Cloning: A laboratory manual 1989, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York. 2nd ed.
66. Sano T., Nagata T. The possible involvement of a phosphate-induced transcription factor encoded by Phi-2 gene from tobacco in ABA-signaling pathways. Plant Cell Physiol 2002, 43:12-20.
67. Sasser J.N. Plant-parasitic nematodes: the farmer's hidden enemy 1990, North Carolina State University Press, Raleigh, NC, p. 47-8.
68. Schaff J.E., Nielsen D.M., Smith C.P., Scholl E.H., Bird D.Mc.K. Comprehensive transcriptome profiling in tomato reveals a role for glycosyltransferase in Mi-mediated nematode resistance. Plant Physiol 2007, 144:1079-1092.
69. Simpson C.E., Nelson S.C., Starr J.L., Woodard K.E., Smith O.O. Registration of TxAG-6 and TXAG-7 peanut germplasm lines. Crop Sci 1993, 33:1418.
70. Simpson C.E., Starr J.L., Church G.T., Burow M.D., Paterson A.H. Registration of 'NemaTAM' peanut. Crop Sci 2003, 43:1561.
71. Simpson C.E., Starr J.L. Registration of 'COAN' peanut. Crop Sci 2001, 41:918.
72. Sindhu A.S., Maier T.R., Mitchum M.G., Hussey R.S., Davis E.L., Baum T.J. Effective and specific in planta RNAi in cyst nematodes: expression interference of four parasitism genes reduces parasitic success. J Exp Bot 2009, 60:315-324.
73. Sweetlove L.J., Heazlewood J.L., Herald V., Holtzapffel R., Day D.A., Millar A.H. The impact of oxidative stress on Arabidopsis mitochondria. Plant J 2002, 32:891-904.
74. Swiecicka M., Filipecki M., Lont D.J., Van Vliet J., Qin L., Goverse A., Bakker J., Helder J. Dynamics in the tomato root transcriptome on infection with the potato cyst nematode Globodera rostochiensis. Mol Plant Pathol 2009, 10:487-500.
75. Tucker M.L., Burke A., Murphy C.A., Thai V.K., Ehrenfried M.L. Gene expression profiles for cell wall-modifying proteins associated with soybean cyst nematode infection, petiole abscission, root tips, flowers, apical buds, and leaves. J Exp Bot 2007, 58:3395-3406.
76. Upchurch R.G., Rose M.S., Eweida M., Zuo W. Expression of the cercosporin transporter, CFP, in tobacco reduces frog-eye lesion size. Biotechnol Lett 2005, 27:1543-1550.
77. Urwin P.E., Green J., Atkinson H.J. Expression of a plant cystatin confers partial resistance to Globodera, full resistance is achieved by pyramiding a cystatin with natural resistance. Mol Breed 2003, 12:263-269.
78. Wieczorek K., Grundler F.M. Expanding nematode-induced syncytia: the role of expansins. Plant Signal Behav 2006, 1:223-224.
79. Wuyts N., Lognay G., Swennen R., De Waele D. Nematode infection and reproduction in transgenic and mutant Arabidopsis and tobacco with an altered phenylpropanoid metabolism. J Exp Bot 2006, 57:2825-2835.
80. Xiao S., Dai L., Liu F., Wang Z., Peng W., Xie D. COS1: an Arabidopsis coronatine insensitive1 suppressor essential for regulation of jasmonate-mediated plant defense and senescence. Plant Cell 2004, 16:1132-1142.
81. Xu W., Purugganan M.M., Polisensky D.H., Antosiewicz D.M., Fry S.C., Braam J. Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase. Plant Cell 1995, 7:1555-1567.
82. Yadav B.C., Veluthambi K., Subramaniam K. Host-generated double stranded RNA induces RNAi in plant-parasitic nematodes and protects the host from infection. Mol Biochem Parasitol 2006, 148:219-222.
83. pro-1 in Chinese domesticated and wild soybeans. Mol Breed 2008, 22:593-602.
84. Zanelli C.F., Valentini S.R. Is there a role for eIF5A in translation?. Amino Acids 2007, 33:351-358.
85. Zinoveva S.V., Vasyukova N.I., Ozeretskovskaya O.L. Biochemical aspects of plant interactions with phytoparasitic nematodes: a review. Appl Biochem Microbiol 2004, 40:111-119.