Characterization of withania somnifera leaf transcriptome and expression analysis of pathogenesis - Related genes during salicylic acid signaling

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Dasgupta, Modhumita Ghosh ^a   George, Blessan Santhosh ^a   Bhatia, Anil ^b   Sidhu, O Prakash ^b  

^a INSTITUTE OF FOREST GENETICS AND TREE BREEDING   (India)

^b CSIR NATIONAL BOTANICAL RESEARCH INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; SALICYLIC ACID; TRANSCRIPTOME; WITHAFERIN A;

ARTICLE; BASE PAIRING; BINDING AFFINITY; CELL ADHESION; CELL COMMUNICATION; CELLULAR DISTRIBUTION; DNA LIBRARY; DOWN REGULATION; GENE; GENE EXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT LEAF; PLANTLET; PR GENE; RNA ISOLATION; SEQUENCE HOMOLOGY; UPREGULATION; WITHANIA SOMNIFERA; WSPR10 GENE;

EID: 84899684531     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094803     Document Type: Article

References (163)

1. Rastogi RP, Mehrotra BN (1998) Compendium of Indian Medicinal Plants. Vol. 6. Central Drug Research Institute & NISCAIR. New Delhi.
2. Bharti SK, Bhatia A, Tewari SK, Sidhu OP, Roy R (2011) Application of HRMAS NMR spectroscopy for studying chemotype variations of Withania somnifera (L. ) Dunal. Magnetic Resonance in Chemistry 49: 659-667.
3. Mishra LC, Singh BB, Dagenais S (2000) Scientific basis for the therapeutic use of Withania somnifera (Ashwagandha): A review. Alternative Medicine Review 5: 334-346. (Pubitemid 30660827)
4. Verma SK, Kumar A (2011) Therapeutic uses of Withania somnifera (ashwagandha) with a note on Withanolides and its pharmacological actions. Asian Journal of Pharmaceutical and Clinical Research 4: 1-4.
5. Siriwardhane AS, Dharmadasa RM, Samarasinghe K (2013) Distribution of Withaferin A, an anticancer potential agent, in different parts of two varieties of Withania somnifera (L. ) Dunal. grown in Sri Lanka. Pakistan Journal of Biological Sciences 16: 141-144.
6. Khedgikar V, Kushwaha P, Gautam J, Verma A, Changkija B, et al. (2013) Withaferin A: a proteasomal inhibitor promotes healing after injury and exerts anabolic effect on osteoporotic bone. Cell Death and Disease 4: e778.
7. Gupta P, Goel R, Pathak S, Srivastava A, Singh SP, et al. (2013b) De novo assembly, functional annotation and comparative analysis of Withania somnifera leaf and root transcriptomes to identify putative genes involved in the withanolides biosynthesis. PLoS ONE 8: e62714.
8. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43: 205-227. (Pubitemid 41318871)
9. De Vos M, Van Oosten VR, Van Poecke RM, Van Pelt JA, Pozo MJ, et al. (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Interact 18: 923-937. (Pubitemid 41170157)
10. Spoel SH, Johnson JS, Dong X (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci USA 104: 18842-18847. (Pubitemid 350210784)
11. Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in plant disease and defense: More than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49: 317-343.
12. Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28: 489-521.
13. Van der Does D, Leon-Reyes A, Koornneef A, Van Verk MC, Rodenburg N, et al. (2013) Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. Plant Cell 25: 744-761.
14. Lee J, Nam J, Park HC, Na G, Miura K, et al. (2007) Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J 49: 79-90. (Pubitemid 44952699)
15. Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase 1002 is required to synthesize salicylic acid for plant defence. Nature 414: 562-565. (Pubitemid 33131541)
16. van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defenserelated proteins in infected plants. Annu Rev Phytopathol 44: 135-162. (Pubitemid 44435701)
17. Reymond P, Farmer EE (1998) Jasmonate and salicylate as global signals for defense gene expression. Curr Opin Plant Biol 1: 404-411. (Pubitemid 128654178)
18. Blanco F, Salinas P, Cecchini N, Jordana X, Van Hummelen P, et al. (2009) Early genomic responses to salicylic acid in Arabidopsis. Plant Mol Biol 70: 79-102.
19. Somssich IE, Hahlbrock K (1998) Pathogen defence in plants-a paradigm of biological complexity. Trends Plant Sci 3: 86-90. (Pubitemid 28118331)
20. Jung JL, Fritig B, Hahne G (1993) Sunflower (Helianthus annuus L. ) Pathogenesis-related proteins (induction by aspirin (acetylsalicylic Acid) and characterization). Plant Physiol 101: 873-880.
21. Görlach J, Volrath S, Knauf-Beiter G, Hengy G, Beckhove U, et al. (1996) Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8: 629-643.
22. Zhang J, Du X, Wang Q, Chen X, Lv D, et al. (2010) Expression of pathogenesis related genes in response to salicylic acid, methyl jasmonate and 1 aminocyclopropane-1-carboxylic acid in Malus hupehensis (Pamp. ) Rehd. BMC Research Notes 3: 208.
23. Lee B, Park YS, Yi HS, Ryu CM (2013) Systemic induction of the small antibacterial compound in the leaf exudate during benzothiadiazole-elicited systemic acquired resistance in pepper. Plant Pathol J 29: 1-6.
24. Niderman T, Genetet I, BruyèreT, Gees R, Stintzi A, et al. (1995) Pathogenesis related PR-1 proteins are antifungal. Plant Physiol 108: 17-27.
25. Taheri P, Tarighi S (2012) The role of pathogenesis-related proteins in the tomato-Rhizoctonia solani interaction. Journal of Botany Doi. org/doi:10. 1155/ 2012/137037
26. Ward ER, Payne GP, Moyer MB, Williams SC, Dincher SS, et al. (1991) Differential regulation of b-l, 3-glucanase messenger RNAs in response to pathogen infection. Plant Physiol 96: 390-397. (Pubitemid 21914025)
27. Kombrink E, Schroder M, Hahlbrock K (1988) Several "pathogenesis- related" proteins in potato are 1,3-,b glucanases and chitinases. Proc Natl Acad Sci 85: 782-786.
28. Zhu B, Chen TH, Li PH (1995) Expression of three osmotin-like protein genes in response to osmotic stress and fungal infection in potato. Plant Mol Biol 28: 17-26.
29. Or?owska E, Fiil A, Kirk HG, Llorente B, Cvitanich C (2012) Differential gene induction in resistant and susceptible potato cultivars at early stages of infection by Phytophthora infestans. Plant Cell Rep 31: 187-203.
30. Soh HC, Park AR, Park S, Back K, Yoon JB, et al. (2012) Comparative analysis of pathogenesis-related protein 10 (PR10) genes between fungal resistant and susceptible peppers. European Journal of Plant Pathology 132: 37-48.
31. Veluthakkal R, Ghosh Dasgupta M (2010) Pathogenesis-related genes and proteins in forest tree species. Trees 24: 993-1006.
32. Wang Z, Zhang JB, Jia CH, Liu JH, Li YQ, et al. (2012) De Novo characterization of the banana root transcriptome and analysis of gene expression under Fusarium oxysporum f. sp. Cubense tropical race 4 infection. BMC Genomics 13: 650.
33. Passos MA, de Cruz VO, Emediato FL, de Teixeira CC, Azevedo VC, et al. (2013) Analysis of the leaf transcriptome of Musa acuminata during interaction with Mycosphaerella musicola: gene assembly, annotation and marker development. BMC Genomics 14: 78.
34. Xiao J, Jin X, Jia X, Wang H, Cao A, et al. (2013) Transcriptome-based discovery of pathways and genes related to resistance against Fusarium head blight in wheat landrace Wangshuibai. BMC Genomics 14: 197.
35. Gao L, Tu ZJ, Millett BP, Bradeen JM (2013) Insights into organ-specific pathogen defense responses in plants: RNA-seq analysis of potato tuber- Phytophthora infestans interactions. BMC Genomics 14: 340.
36. Zhu QH, Stephen S, Kazan K, Jin G, Fan L, et al. (2013) Characterization of the defense transcriptome responsive to Fusarium oxysporum infection in Arabidopsis using RNA-seq. Gene 512: 259-266
37. Socquet-Juglard D, Kamber T, Pothier JF, Christen D, Gessler C, et al. (2013) Comparative RNA-Seq analysis of early-infected peach leaves by the invasive phytopathogen Xanthomonas arboricola pv. pruni. PLoS ONE 8: e54196.
38. De Cremer K, Mathys J, Vos C, Froenicke L, Michelmore RW, et al. (2013) RNAseq-based transcriptome analysis of Lactuca sativa infected by the fungal necrotroph Botrytis cinerea. Plant Cell Environ 36: 1992-2007
39. Martinelli F, Uratsu SL, Albrecht U, Reagan RL, Phu ML, et al. (2012) Transcriptome profiling of citrus fruit response to huanglongbing disease. PLoS ONE 7: e38039.
40. Rodrigues CM, de Souza AA, Takita MA, Kishi LT, Machado MA (2013) RNA-Seq analysis of Citrus reticulata in the early stages of Xylella fastidiosa infection reveals auxin-related genes as a defense response. BMC Genomics 14: 676.
41. Lohse M, Bolger AM, Nagel A, Fernie AR, Lunn JE, et al. (2012) RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Res 40: W622-7.
42. Zerbino DR, Birney E (2008) Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821-829. (Pubitemid 351645072)
43. Schulz MH, Zerbino DR, Vingron M, Birney E (2012) Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 28: 1086-1092.
44. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29. (Pubitemid 30257031)
45. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucl Acids Res 35 (suppl 2): W182-W185.
46. Kozomara A, Griffiths-Jones S (2011) miRBase: integrating microRNA annotation and deep sequencing data. Nucl Acids Res 39 (suppl 1): D152- D157.
47. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalisation of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: 1-11.
48. Andersen CL, Jensen JL, Orntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64: 5245-5250. (Pubitemid 39006544)
49. Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper - Excel-based tool using pair-wise correlations. Biotechnol Lett 26: 509-515. (Pubitemid 38448421)
50. Migocka M, Papierniak A (2010) Identification of suitable reference genes for studying gene expression in cucumber plants subjected to abiotic stress and growth regulators. Mol Breeding 28: 343-357.
51. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCT method. Methods 25: 402-408. (Pubitemid 34164012)
52. Goswami RS, Atenafu EG, Xuan Y, Waldron L, Reis PP, et al. (2013) A microRNA signature obtained from the comparison of aggressive and indolent non-Hodgkin lymphomas: Potential prognostic value in mantle cell lymphoma. J Clin Oncol 31: 2903-2911.
53. Peirson SN, Butler JN, Foster RG (2003) Experimental validation of novel and conventional approaches to quantitative real-time PCR data analysis. Nucleic Acids Research 31: 14 e73.
54. De Bodt S, Maere S, Van de Peer Y (2005) Genome duplication and the origin of angiosperms. Trends Ecol Evol 20: 591-597. (Pubitemid 41502811)
55. Osborn TC, Pires JC, Birchler JA, Auger DL, Chen ZJ, et al. (2003) Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19: 141-147. (Pubitemid 36279181)
56. Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6: 836-846.
57. Yu Z, Habererb G, Matthesa M, Ratteic T, Mayerb KFX, et al. (2013) Impact of natural genetic variation on the transcriptome of autotetraploid Arabidopsis thaliana. Proc Natl Acad Sci USA 107: 17809-17814.
58. Wachholtz M, Heng-Moss T, Twigg P, Baird L, Lu G, et al. (2013) Transcriptome analysis of two buffalograss cultivars. BMC Genomics 14: 613.
59. Singhal VK, Kumar P (2008) Cytomixis during microsporogenesis in the diploid and tetraploid cytotypes of Withania somnifera (L. ) Dunal, (Solanaceae). Comparative Cytogenetics 2: 85-92.
60. Vidya KM, Hegde L, Saraswathi G, Vijay Kumar BM (2013) Evaluation of diploids and autotetraploid genotypes of ashwagandha (Withania somnifera Dunal. ) for growth, yield and quality characters. The Asian J Hort 8: 97-100.
61. Annadurai RS, Jayakumar V, Mugasimangalam RC, Katta MAVSK, Anand S, et al. (2012) Next generation sequencing and de novo transcriptome analysis of Costus pictus D. Don, a non-model plant with potent anti-diabetic properties. BMC Genomics 13: 663.
62. Garg R, Patel RK, Tyagi AK, Jain M (2011) De novo assembly of chickpea transcriptome using short reads for gene discovery and marker identification. DNA Res 18: 53-63.
63. Iorizzo M, Senalik DA, Grzebelus D, Bowman M, Cavagnaro PF, et al. (2011) De novo assembly and characterization of the carrot transcriptome reveals novel genes, new markers, and genetic diversity. BMC Genomics 12: 389
64. Kudapa H, Bharti AK, Cannon SB, Farmer AD, Mulaosmanovic B, et al. (2012) A comprehensive transcriptome assembly of pigeonpea (Cajanus cajan L. ) using sanger and second-generation sequencing platforms. Mol Plant 5: 1020-1028.
65. Barrero RA, Chapman B, Yang Y, Moolhuijzen P, Keeble-Gagnère G, et al. (2011) De novo assembly of Euphorbia fischeriana root transcriptome identifies prostratin pathway related genes. BMC Genomics 12: 600.
66. Temnykh S, DeClerck G, Lukashova A, Lipovich L, Cartinhour S, et al. (2001) Computational and experimental analysis of microsatellites in rice (Oryza sativa L. ): frequency, length variation, transposon associations and genetic marker potential. Genome Res 11: 1441-1452. (Pubitemid 32771552)
67. Thiel T, Michalek W, Varshney RK, Graner A (2003) Exploiting EST 941 databases for the development and characterization of gene derived SSRmarkers in barley (Hordeum vulgare L. ). Theor Appl Genet 106: 411-422. (Pubitemid 36599853)
68. Portis E, Nagy I, Sasva Z, Stagelri A, Barchi L, et al. (2007) The design of Capsicum spp. SSR assays via analysis of in silico DNA sequence, and their potential utility for genetic mapping. Plant Sci 172: 640-648. (Pubitemid 46109087)
69. Varshney RK, Sigmund R, Boerner A, Korzun V, Stein N, et al (2005) Interspecific transferability and comparative mapping of barley EST-SSR markers in wheat, rye, and rice. Plant Sci 168: 195-202. (Pubitemid 39464780)
70. Kantety RV, La Rota M, Matthews DE, Sorrells ME (2002) Data mining for simple sequence repeats in expressed sequence tags from barley, maize, rice, sorghum and wheat. Plant Mol Biol 48: 501-510. (Pubitemid 34415968)
71. Gupta PK, Rustgi S, Sharma S, Singh R, Kumar N, et al. (2003) Transferable EST-SSR markers for the study of polymorphism and genetic diversity in bread wheat. Mol Genet Genome 270: 315-323. (Pubitemid 38085106)
72. Minamiyama Y, Tsuro M, Hirai M (2006) An SSR-based linkage map of Capsicum annuum. Mol Breed 18: 157-169. (Pubitemid 44351272)
73. Cordeiro GM, Casu R, McIntyre CL, Manners JM, Henry RJ (2001) Microsatellite markers from sugarcane (Saccharum spp. ) ESTs cross transferable to Erianthus and Sorghum. Plant Sci 160: 1115-1123. (Pubitemid 32441207)
74. Park YH, Alabady MS, Ulloa M, Sickler B, Wilkins TA, et al. (2005) Genetic mapping of new cotton fiber loci using EST derived microsatellites in an interspecific recombinant inbred line cotton population. Mol Genet Genome 274: 428-441. (Pubitemid 41660779)
75. Kumar S, Shah N, Garg V, Bhatia S (2014) Large scale in-silico identification and characterization of simple sequence repeats (SSRs) from de novo assembled transcriptome of Catharanthus roseus (L. ) G. Don. Plant Cell Rep doi:10. 1007/s00299-014-1569-8
76. Xie F, Burklew CE, Yang Y, Liu M, Xiao P, et al. (2012) De novo sequencing and a comprehensive analysis of purple sweet potato (Ipomoea batatas L. ) transcriptome. Planta 236: 101-113.
77. Chen S, Huang X, Yan X, Liang Y, Wang Y, et al. (2013) Transcriptome Analysis in Sheepgrass (Leymus chinensis): A Dominant Perennial Grass of the Eurasian Steppe. PLoS ONE 8(7): e67974. doi:10. 1371/journal. pone. 0067974
78. Mir BA, Koul S, Kumar A, Kaul MK, Soodan AS, et al. (2011) Assessment and characterization of genetic diversity in Withania somnifera (L. ) Dunal using RAPD and AFLP markers. African Journal of Biotechnology 10: 14746-14756.
79. Tripathi N, Saini N, Kumar S, Tiwari S (2012) Assessment of genetic diversity among Withania somnifera collected from central India using RAPD and ISSR analysis. J Med Arom Plant Sci Biotechnol 6: 133-139.
80. Udayakumar R, Kasthurirengan S, Mariashibu TS, Sudhakar B, Ganapathi A, et al. (2013) Analysis of genetic variation among populations of Withania somnifera (L. ) in South India based on RAPD Markers. European Journal of Medicinal Plants 3: 266-280.
81. Radman R, Saez T, Bucke C, Keshavarz T (2003) Elicitation of plants and microbial cell systems. Biotechnol Appl Biochem 37: 91-102. (Pubitemid 36246350)
82. Ketchum REB, Gibson DM, Croteau RB, Schuler ML (1999) The kinetics of taxoid accumulation in cell suspension cultures of Taxus following elicitation with methyl jasmonate. Biotechnol Bioeng 62: 97-105. (Pubitemid 28562000)
83. Sivanandhan G, Arun M, Mayavan S, Rajesh M, Jeyaraj M, et al. (2012b) Optimization of elicitation conditions with methyl jasmonate and salicylic acid to improve the productivity of withanolides in the adventitious root culture of Withania somnifera (L. ) Dunal. Appl Biochem Biotechnol 168: 681-696.
84. Ciddi V (2006) Withaferin A from cell cultures of Withania somnifera. Indian J Pharm Sci 68: 490-492. (Pubitemid 44599823)
85. Sivanandhan G, Arun M, Mayavan S, Rajesh M, Mariashibu TS, et al. (2012a) Chitosan enhances withanolides production in adventitious root cultures of Withania somnifera (L. ) Dunal. Ind Crop Prod 37: 124-129.
86. Sivanandhan G, Kapil Dev G, Jeyaraj M, Rajesh M, Arjunan A, et al. (2013) Increased production of withanolide A, withanone, and withaferin A in hairy root cultures of Withania somnifera (L. ) Dunal elicited with methyl jasmonate and salicylic acid. Plant Cell Tiss Organ Cult 114: 121-129.
87. Doma M, Abhayankar G, Reddy VD, Kavi Kishor PB (2012) Carbohydrate and elicitor enhanced withanolide (withaferin A and withanolide A) accumulation in hairy root cultures of Withania somnifera (L. ). Indian Journal of Experimental Biology 50: 484-490.
88. Ginzinger DG (2002) Gene quantification using real-time quantitative PCR: an emerging technology hits the mainstream. Exp Hematol 30: 503-512. (Pubitemid 34626648)
89. Huggett J, Dheda K, Bustin S, Zumla A (2005) Real-time RT-PCR normalization; strategies and considerations. Genes Immun 6: 279-284. (Pubitemid 40903399)
90. Gupta P, Akhtar N, Tewari SK, Sangwan RS, Trivedi PK (2011) Differential expression of farnesyl diphosphate synthase gene from Withania somnifera in different chemotypes and in response to elicitors. Plant Growth Regulation 65: 93-100.
91. Gupta P, Agarwal AV, Akhtar N, Sangwan RS, Singh SP, et al. (2013a) Cloning and characterization of 2-C-methyl-D-erythritol-4-phosphate pathway genes for isoprenoid biosynthesis from Indian ginseng, Withania somnifera. Protoplasma 250: 285-295.
92. Nicot N, Hausman J, Hoffmann L, Evers D (2005) Housekeeping gene selection for real time RT-PCR normalization in potato during biotic and abiotic stress. J Exp Bot 56: 2907-2914. (Pubitemid 41507227)
93. Schmidt GW, Delaney SK (2010) Stable internal reference genes for normalization of real-time RT-PCR in tobacco (Nicotiana tabacum) during development and abiotic stress. Mol Genet Genomics 283: 233-241.
94. Wan H, Yuan W, Ruan M, Ye Q, Wang R, et al. (2011) Identification of reference genes for reverse transcription quantitative real-time PCR normalization in pepper (Capsicum annuum L. ). Biochem Biophys Res Commun 416: 24-30.
95. AiméS, Alabouvette C, Steinberg C, Olivain C (2013) The endophytic strain Fusarium oxysporum Fo47: A good candidate for priming the defense responses in tomato roots. Mol Plant-Microbe Interact 26: 918-926.
96. Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47: 177-206.
97. Blanco-Ulate B, Vincenti E, Powell ALT, Cantu D (2013) Tomato transcriptome and mutant analyses suggest a role for plant stress hormones in the interaction between fruit and Botrytis cinerea. Front Plant Sci 4: 142.
98. Hammond-Kosack KE, Jones JD (1996) Resistance gene-dependent plant defense responses. Plant Cell 8: 1773-1791. (Pubitemid 27012404)
99. Ryals J, Neuenschwander UH, Willits MG, Molina A, Steiner H-Y, et al. (1996) Systemic acquired resistance. Plant Cell 8: 1809-1819. (Pubitemid 27012406)
100. Tsuda K, Sato M, Glazebrook J, Cohen JD, Katagiri F (2008) Interplay between MAMP948 triggered and SA-mediated defense responses. Plant J 53: 763-775. (Pubitemid 351495865)
101. Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42: 185-209. (Pubitemid 39308511)
102. Malamy J, Carr JP, Klessig DF, Raskin I (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250: 1002-1004. (Pubitemid 120031810)
103. Métraux J-P, Signer H, Ryals J, Ward E, Wyss-Benz M, et al. (1990) Increase in salicylic acid at the onset of systemic acquired resistance. Science 250: 1004-1006.
104. An C, Mou Z (2011) Salicylic Acid and its Function in Plant Immunity Journal of Integrative Plant Biology 53: 412-428.
105. Mateo A, Funck D, Muhlenbock P, Kular B, Mullineaux PM, et al. (2006) Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. J Exp Bot 57: 1795-1807. (Pubitemid 43992229)
106. Holuigue L, Salinas P, Blanco F, Garreto'n V (2007) Salicylic acid and reactive oxygen species in the activation of stress defense genes. In: Hayat S, Ahmad A, editors. Salicylic acid-a plant hormone. Springer, Dordrecht. pp. 197-246.
107. Lu H (2009) Dissection of salicylic acid-mediated defense signaling networks. Plant Signal Behav 4: 713-717.
108. Ng G, Seabolt S, Zhang C, Salimian S, Watkins TA, et al. (2011). Genetic dissection of salicylic acid-mediated defense signaling networks in Arabidopsis. Genetics 189: 851-859.
109. Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5: 325-331. (Pubitemid 34695970)
110. Delaure SL, Hemelrijck WV, Bolle MFCD, Cammue BPA, De Coninck BMA (2008) Building up plant defenses by breaking down proteins. Plant Sci 174: 375-385.
111. Cao H, Bowling SA, Gordon AS, Dong X (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6: 1583-1592. (Pubitemid 24986212)
112. Delaney TP, Friedrich LE, Ryals J (1995) Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc Natl Acad Sci USA 92: 6602-6606.
113. Shah J, Tsui F, Klessig DF (1997) Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA- inducible expression of the tms2 gene. Mol Plant Microbe Interact 10: 69-78. (Pubitemid 27052575)
114. Maleck K, Neuenschwander U, Cade RM, Dietrich RA, Dangl JL, et al. (2002) Isolation and characterization of broad-spectrum disease-resistant Arabidopsis mutants. Genetics 160: 1661-1671. (Pubitemid 34454387)
115. Bowling SA, Guo A, Cao H, Gordon S, Klessig DF, et al. (1994) A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell 6: 1845-1857. (Pubitemid 24986958)
116. Clarke JD, Liu Y, Klessig DF, Dong X (1998) Uncoupling PR gene expression from NPR1 and bacterial resistance: Characterization of the dominant Arabidopsis cpr6-1 mutant. Plant Cell 10: 557-569. (Pubitemid 28542198)
117. Yu IC, Parker J, Bent AF (1998) Gene-for-gene disease response resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc Natl Acad Sci USA 95: 7819-7824.
118. Zhou N, Tootle TL, Tsui F, Klessig DF, Glazebrook J (1998) PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis. Plant Cell 10: 1021-1030. (Pubitemid 28537425)
119. Nawrath C, Métraux JP (1999) Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. The Plant Cell 11: 1393-1404.
120. van Loon LC, van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55: 85-97. (Pubitemid 29402750)
121. Neuhaus JM (1999) Plant Chitinases (PR-3,PR-4,PR-8, PR-11). In: Datta SK, Muthukrishnan, S. CRC Press, Boca Raton. pp. 77-105
122. Davis JM, Wu H, Cooke JE, Reed JM, Luce KS, et al. (2002) Pathogen challenge, salicylic acid, and jasmonic acid regulate expression of chitinase gene homologs in pine. Mol Plant Microbe Interact 15: 380-387. (Pubitemid 34299802)
123. Lawton KA, Beck J, Potter S, Ward E, Ryals J (1994) Regulation of cucumber class III chitinase gene expression. Mol Plant Microbe Interact 7: 48-57. (Pubitemid 2063263)
124. Zhang LY, Zheng XH, Tang HL, Zhu JW, Yang JM (2003) Increase of b-1,3- glucanse and chitinase activities in cotton callus cells treated by salicylic acid and toxin of Verticillium dahlia. Acta Botanica Sinica 45: 802-808.
125. Harfouche AL, Rugini E, Mencarelli F, Botondi R, Muleo R (2008). 721 Salicylic acid induces H2O2 production and endochitinase gene expression but not ethylene biosynthesis in Castanea sativa in vitro model system. J Plant Physiol 165: 734-744. (Pubitemid 351467004)
126. Vidal S, debLeon IP, Denecke J, Tapio Palva E (1997) Salicylic acid and the plant pathogen Erwinia carotovora induce defence genes via antagonistic pathways. Plant Journal 11: 115-123. (Pubitemid 27108362)
127. Yao H J, Tian SP (2005). Effects of pre- and post-harvest application of salicylic acid or methyl jasmonate on inducing disease resistance of cherry fruit in storage. Postharvest Biology and Technology 35: 253-262.
128. Xu X, Tian S (2008) Salicylic acid alleviated pathogen-induced oxidative stress in harvested sweet cherry fruit. Postharvest Biology and Technology 49: 379-385.
129. Derckel JP, Audran JC, Haye B, Lambert B, Legendre L (1998) Characterization, induction by wounding and salicylic acid, and activity against Botrytis cinerea of chitinases and b-1,3 glucanases of ripening grape berries. Physiologia Plantarum 104: 56-64. (Pubitemid 28494477)
130. Salzman RA, Brady JA, Finlayson SA, Buchanan CD, Summaer EJ, et al. (2005) Transcriptional profiling of sorghum induced by methyl jasmonate, salicylic acid, and aminocyclopropane carboxylic acid reveals cooperative regulation and novel gene responses. Plant Physiol 138: 352-368. (Pubitemid 43138134)
131. Veluthakkal R, Ghosh Dasgupta M (2012) Isolation and characterization of pathogen defence related class I chitinase from the actinorhizal tree Casuarina equisetifolia. Forest Pathology 42: 467-480.
132. Ding CK, Wang CY, Gross KC, Smith DL (2002) Jasmonate and salicylate induce the expression of pathogenesis-related-protein genes and increase resistance to chilling injury in tomato fruit. Planta 214: 895-901. (Pubitemid 36059255)
133. Busam C, Kassemeyer HH, Matern U (1997) Differential Expression of Chitinases in Vitis vinifera L. Responding to Systemic Acquired Resistance Activators or Fungal Challenge. Plant Physiol 115: 1029-1038 (Pubitemid 28378761)
134. Klarzynski O, Plesse B, Joubert JM, Yvin JC, Kopp M, et al. (2000) Linear b-1, 3-glucans are elicitors of defense responses in tobacco. Plant physiol 124: 1027-1037.
135. Naidoo R, Ferreira L, Beger DK, Myburg AA, Naidoo S (2013) The identification and differential expression of Eucalyptus grandis pathogenesisrelated genes in response to salicylic acid and methyl jasmonate. Front Plant Sci 4: 43.
136. Ghosh Dasgupta M, Veluthakkal R, Karpaga Raja Sundari B (2013) Characterization of genes expressed in Casuarina equisetifolia in response to elicitation by cell wall components of Trichosporium vesiculosum. Silvae Genetica (In Press).
137. Datta R, Sinha R, Chattopadhyay S (2013) Changes in leaf proteome profile of Arabidopsis thaliana in response to salicylic acid. J Biosci 38: 317-328.
138. Wang YY, Li BQ, Qin GZ, Li L, Tian S (2011) Defense response of tomato fruit at different maturity stages to salicylic acid and ethephon. Scientia Horticulturae 129: 183-188.
139. Xu Y, Chang PFL, Liu D, Narasimhan ML, Raghothama KG, et al. (1994) Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6: 1077-1085.
140. Fernandes CF, Moraes VC, Vasconcelosb IM, Silveirab JA, Oliveira JT (2006) Induction of an anionic peroxidase in cowpea leaves by exogenous salicylic acid. J Plant Physiol 163: 1040-1048. (Pubitemid 44404115)
141. Cag S, Cevahir-Oz G, Sarsag M, Goren-Saglam N (2009) Effect of salicylic acid on pigment, protein content and peroxidase activity in excised sunflower cotyledons. Pak J Bot 41: 2297-2303.
142. Ee SF, Oh JM, Mohd Noor N, Kwon TR, Mohamed-Hussein ZA, et al. (2013) Transcriptome profiling of genes induced by salicylic acid and methyl jasmonate in Polygonum minus. Mol Biol Rep 40: 2231-2241.
143. Gao LJ, Zhang YX (2013) Effects of Salicylic Acid on the Expression of SOD, PPO Isozymes and NPR1 in Pear. Acta Horticulturae Sinica 40: 41-48.
144. Hatfield R, Vermerris W (2001) Lignin formation in plants. The dilemma of linkage specificity. Plant Physiol 126: 1351e7.
145. Liu JJ, Ekramoddoullah AKM, Yu X (2003) Differential expression of multiple PR10 proteins in western white pine following wounding, fungal infection and cold-hardening. Physiol Plantarum 119: 544-553. (Pubitemid 37496597)
146. Takeuchi K, Gyohda A, Tominaga M, Kawakatsu M, Hatakeyama A, et al. (2011) RSOsPR10 Expression in response to environmental stresses is regulated antagonistically by jasmonate/ethylene and salicylic acid signaling pathways in rice roots. Plant Cell Physiol 52: 1686-1696.
147. Crowell DN, John MF, Russell D, Amasino RM (1992) Characterization of a stress-induced, developmentally regulated gene family from soybean. Plant Mol Biol 18: 459-466.
148. Warner SA, Gill A, Draper J (1994) The developmental expression of the asparagus intracellular PR protein (AoPR1) gene correlates with sites of phenylpropanoid biosynthesis. Plant J 6: 31-43.
149. Breda C, Sallaud C, el-Turk J, Buffard D, de Kozak I, et al. (1996) Defense reaction in Medicago sativa: a gene encoding a class 10 PR protein is expressed in vascular bundles, Mol. Plant Microbe Interact 9: 713-719. (Pubitemid 26407134)
150. Walter MH, Liu JW, Wunn J, Hess D (1996) Bean ribonuclease-like pathogenesis-related protein genes (Ypr10) display complex patterns of developmental dark-induced and exogenous-stimulus-dependent expression. Eur J Biochem 239: 281-293. (Pubitemid 26246531)
151. Jwa NS, Agrawal GK, Rakwal R, Park CH, Agrawal VP (2001) Molecular cloning and characterization of a novel jasmonate inducible pathogenesisrelated class 10 protein gene, JIOsPR10, from rice (Oryza sativa L. ) seedling leaves. Biochem Biophys Res Commun 286: 973-983. (Pubitemid 32924868)
152. Hwang SH, Lee IA, Yie SW, Hwang DJ (2008) Identification of an OsPR10a promoter region responsive to salicylic acid. Planta 227: 1141-1150.
153. McGee JD, Hamer JE, Hodges TK (2001) Characterization of a PR-10 pathogenesis-related gene family induced in rice during infection with Magnaporthe grisea. Mol Plant Microbe Interact 14: 877-886. (Pubitemid 32575665)
154. Hwang HJ, Kima H, Yu HJ, Oh MH, Lee I, et al. (2003) Gene encoding
155. Jayaraj J, Muthukrishnan S, Liang GH, Velazhahan R (2004) Jasmonic acid and salicylic acid induce accumulation of b-1,3-glucanase and thaumatin-like proteins in wheat and enhance resistance against Stagonospora nodorum. Biol Plant 48: 425-430. (Pubitemid 39225089)
156. Singh NK, Kumar KRR, Kumar D, Shukla P, Kirti PB (2013) Characterization of a pathogen induced thaumatin-like protein gene AdTLP from Arachis diogoi, a wild peanut. PLoS ONE 8(12): e83963. doi:10. 1371/journal. pone. 0083963
157. Han Q, Feng H, Zhao H, Huang L, Wang X, et al. (2013) Effect of a benzothiadiazole on inducing resistance of soybean to Phytophthora sojae. Protoplasma 250: 471-481.
158. Bovie C, Ongena M, Thonart P, Dommes J (2004) Cloning and expression analysis of cDNAs corresponding to genes activated in cucumber showing systemic acquired resistance after BTH treatment. BMC Plant Biol 26: 4-15.
159. Dao TTH, Puig RC, Kima HK, Erkelens C, Lefeber AWM, et al. (2009) Effect of benzothiadiazole on the metabolome of Arabidopsis thaliana. Plant Physiol Biochem 47: 146-152.
160. Burketova L, Sindelarova M, Sindelarov L (1999) Benzothiadiazole as an inducer of b-1,3- glucanase and chitinase isozymes in sugar beet. Biol Plant 42: 423-430.
161. Ma BC, Tang WL, Ma LY, Li LL, Zhang LB, et al. (2009) The role of chitinase gene expression in the defense of harvested banana against anthracnose disease. J Amer Soc Hort Sci 134: 379-386.
162. Kogel KH, Beckhove U, Dreschers J, Münch S, Romm'e Y (1994) Acquired resistance in barley: the resistance mechanism induced by 2,6- dichloroisonicotinic acid is a phenocopy of a genetically based mechanism governing racespecific powdery mildew resistance. Plant Physiol 106: 1269-1277. (Pubitemid 24986551)
163. Morris SW, Vernooij B, Titatarn S, Starrett M, Thomas S, et al. 1998 Induced resistance responses in maize. Mol Plant Microbe Interact 11: 643-658. (Pubitemid 28417754)