Proteomics and transcriptomics of the BABA-induced resistance response in potato using a novel functional annotation approach

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Bengtsson, Therese ^a   Weighill, Deborah ^b   Proux Wéra, Estelle ^a   Levander, Fredrik ^c   Resjö, Svante ^a   Burra, Dharani D ^a   Moushib, Laith I ^c   Hedley, Pete E ^d   Liljeroth, Erland ^a   Jacobson, Dan ^b   Alexandersson, Erik ^a   Andreasson, Erik ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b STELLENBOSCH UNIVERSITY   (South Africa)

^c LUND UNIVERSITY   (Sweden)

^d SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Functional annotation; Mevalonate pathway; Phytophthora infestans; Secretome; Solanum tuberosum; Sterol biosynthesis

Indexed keywords

3 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID; ABSCISIC ACID; PHYTOHORMONE; TRANSCRIPTOME; UNCLASSIFIED DRUG;

AMINO ACID METABOLISM; APOPLAST; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; HOST RESISTANCE; INDUCED RESISTANCE; MICROARRAY ANALYSIS; NONHUMAN; PLANT GENE; PLANT GENOME; PLANT IMMUNITY; PLANT LEAF; PLANT RESPONSE; POTATO; PROTEIN ANALYSIS; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; SEQUENCE ANALYSIS; STEROL SYNTHESIS; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYTOPHTHORA; PROTEOMICS;

PHYTOPHTHORA; PROTEOMICS; SOLANUM TUBEROSUM; TRANSCRIPTOME;

EID: 84899967180     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-315     Document Type: Article

References (71)

1. Walters D, Walsh D, Newton A, Lyon G. Induced resistance for plant disease control: maximizing the efficacy of resistance elicitors. Phytopathology 2005, 95:1368-1373. 10.1094/PHYTO-95-1368, 18943546.
2. Ton J, De Vos M, Robben C, Buchala A, Metraux JP, Van Loon LC, Pieterse CM. Characterization of Arabidopsis enhanced disease susceptibility mutants that are affected in systemically induced resistance. Plant J 2002, 29:11-21. 10.1046/j.1365-313x.2002.01190.x, 12060223.
3. Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD. Systemic acquired resistance. Plant Cell 1996, 8:1809-1819. 10.1105/tpc.8.10.1809, 161316, 12239363.
4. Cohen YR. beta-aminobutyric acid-induced resistance against plant pathogens. Plant Dis 2002, 86:448-457.
5. Justyna P-G, Ewa K. Induction of resistance against pathogens by β-aminobutyric acid. Acta Physiol Plant 2013, 35:1-14.
6. Bengtsson T, Holefors A, Witzell J, Andreasson E, Liljeroth E. Activation of defence responses to Phytophthora infestans in potato by BABA. Plant Pathol 2013, 63(1):193-202.
7. Ton J, Jakab G, Toquin V, Flors V, Iavicoli A, Maeder MN, Metraux J-P, Mauch-Mani B. Dissecting the beta-aminobutyric acid-induced priming phenomenon in arabidopsis. Plant Cell 2005, 17:987-999. 10.1105/tpc.104.029728, 1069713, 15722464.
8. Tsai CH, Singh P, Chen CW, Thomas J, Weber J, Mauch-Mani B, Zimmerli L. Priming for enhanced defence responses by specific inhibition of the Arabidopsis response to coronatine. Plant J 2011, 65:469-479. 10.1111/j.1365-313X.2010.04436.x, 21265899.
9. Zimmerli L, Hou BH, Tsai CH, Jakab G, Mauch-Mani B, Somerville S. The xenobiotic beta-aminobutyric acid enhances Arabidopsis thermotolerance. Plant J 2008, 53:144-156. 10.1111/j.1365-313X.2007.03343.x, 18047473.
10. Singh P, Wu CC, Zimmerli L. beta-aminobutyric acid priming by stress imprinting. Plant Signal Behav 2010, 5:878-880. 10.4161/psb.5.7.11903, 3115037, 20484986.
11. Wu C-C, Singh P, Chen M-C, Zimmerli L. L-Glutamine inhibits beta-aminobutyric acid-induced stress resistance and priming in Arabidopsis. J Exp Bot 2010, 61:995-1002. 10.1093/jxb/erp363, 2826644, 20007686.
12. Singh P, Kuo YC, Mishra S, Tsai CH, Chien CC, Chen CW, Desclos-Theveniau M, Chu PW, Schulze B, Chinchilla D, Boller T, Zimmerli L. The lectin receptor kinase-VI.2 is required for priming and positively regulates Arabidopsis pattern-triggered immunity. Plant Cell 2012, 24:1256-1270. 10.1105/tpc.112.095778, 3336125, 22427336.
13. Li Y, Tian Z, Liu J, Xie C. Comparative cDNA-AFLP analysis reveals that DL-beta-amino-butyric acid induces resistance through early activation of the host-defense genes in potato. Physiol Plant 2009, 136:19-29. 10.1111/j.1399-3054.2009.01209.x, 19508365.
14. Eschen-Lippold L, Altmann S, Rosahl S. DL-beta-aminobutyric acid-induced resistance of potato against Phytophthora infestans requires salicylic acid but not oxylipins. Mol Plant Microbe Interact 2010, 23:585-592. 10.1094/MPMI-23-5-0585, 20367467.
15. Xu X, Pan S, Cheng S, Zhang B, Mu D, Ni P, Zhang G, Yang S, Li R, Wang J, Orjeda G, Guzman F, Torres M, Lozano R, Ponce O, Martinez D, De la Cruz G, Chakrabarti SK, Patil VU, Skryabin KG, Kuznetsov BB, Ravin NV, Kolganova TV, Beletsky AV, Mardanov AV, Di Genova A, Bolser DM, Martin DM, Li G, Yang Y, et al. Genome sequence and analysis of the tuber crop potato. Nature 2011, 475:189-195. 10.1038/nature10158, 21743474.
16. Schwanhausser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M. Global quantification of mammalian gene expression control. Nature 2011, 473:337-342. 10.1038/nature10098, 21593866.
17. Chen F, Mackey AJ, Vermunt JK, Roos DS. Assessing performance of orthology detection strategies applied to eukaryotic genomes. PLoS One 2007, 2:e383. 10.1371/journal.pone.0000383, 1849888, 17440619.
18. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003, 13:2178-2189. 10.1101/gr.1224503, 403725, 12952885.
19. Proost S, Van Bel M, Sterck L, Billiau K, Van Parys T, Van de Peer Y, Vandepoele K. PLAZA: a comparative genomics resource to study gene and genome evolution in plants. Plant Cell Online 2009, 21:3718-3731.
20. Smyth GK. "Limma: linear models for microarray data." Bioinformatics and computational biology solutions using R and Bioconductor 2005, 397-420. New York: Springer.
21. Supek F, Bosnjak M, Skunca N, Smuc T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One 2011, 6:e21800. 10.1371/journal.pone.0021800, 3138752, 21789182.
22. Ali A, Moushib LI, Lenman M, Levander F, Olsson K, Carlson-Nilson U, Zoteyeva N, Liljeroth E, Andreasson E. Paranoid potato phytophthora-resistant genotype shows constitutively activated defense. Plant Signal Behav 2012, 7:400-408. 10.4161/psb.19149, 3443922, 22476463.
23. Alexandersson E, Ali A, Resjö S, Andreasson E. Plant secretome proteomics. Front Plant Sci 2013, 4:9. 3561728, 23378846.
24. Kessner D, Chambers M, Burke R, Agus D, Mallick P. ProteoWizard: open source software for rapid proteomics tools development. Bioinformatics 2008, 24:2534-2536. 10.1093/bioinformatics/btn323, 2732273, 18606607.
25. Hakkinen J, Vincic G, Mansson O, Warell K, Levander F. The proteios software environment: an extensible multiuser platform for management and analysis of proteomics data. J Proteome Res 2009, 8:3037-3043. 10.1021/pr900189c, 19354269.
26. Sandin M, Krogh M, Hansson K, Levander F. Generic workflow for quality assessment of quantitative label-free LC-MS analysis. Proteomics 2011, 11:1114-1124. 10.1002/pmic.201000493, 21298787.
27. Bellew M, Coram M, Fitzgibbon M, Igra M, Randolph T, Wang P, May D, Eng J, Fang R, Lin C, Chen J, Goodlett D, Whiteaker J, Paulovich A, McIntosh M. A suite of algorithms for the comprehensive analysis of complex protein mixtures using high-resolution LC-MS. Bioinformatics 2006, 22:1902-1909. 10.1093/bioinformatics/btl276, 16766559.
28. Sandin M, Ali A, Hansson K, Månsson O, Andreasson E, Resjö S, Levander F. An adaptive alignment algorithm for quality-controlled label-free LC-MS. Mol Cell Proteomics 2013, 12:1407-1420. 10.1074/mcp.O112.021907, 3650348, 23306530.
29. Liljeroth E, Bengtsson T, Wiik L, Andreasson E. Induced resistance in potato to Phytphthora infestans-effects of BABA in greenhouse and field tests with different potato varieties. Eur J Plant Pathol 2010, 127:171-183.
30. Yamaguchi S. Gibberellin metabolism and its regulation. Annu Rev Plant Biol 2008, 59:225-251. 10.1146/annurev.arplant.59.032607.092804, 18173378.
31. Fernandez-Calvo P, Chini A, Fernandez-Barbero G, Chico JM, Gimenez-Ibanez S, Geerinck J, Eeckhout D, Schweizer F, Godoy M, Franco-Zorrilla JM, Pauwels L, Witters E, Puga MI, Paz-Ares J, Goossens A, Reymond P, De Jaeger G, Solano R. The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 2011, 23:701-715. 10.1105/tpc.110.080788, 3077776, 21335373.
32. Lorenzo O, Piqueras R, Sanchez-Serrano JJ, Solano R. ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 2003, 15:165-178. 10.1105/tpc.007468, 143489, 12509529.
33. Hossain Z, McGarvey B, Amyot L, Gruber M, Jung J, Hannoufa A. DIMINUTO 1 affects the lignin profile and secondary cell wall formation in Arabidopsis. Planta 2012, 235:485-498. 10.1007/s00425-011-1519-4, 21947665.
34. Tzin V, Galili G. New insights into the shikimate and aromatic amino acids biosynthesis pathways in plants. Mol Plant 2010, 3:956-972. 10.1093/mp/ssq048, 20817774.
35. Moushib LI, Witzell J, Lenman M, Liljeroth E, Andreasson E. Sugar beet extract induces defence against Phytophthora infestans in potato plants. Eur J Plant Pathol 2013, 136(2):261-271.
36. Ogawa T, Ishikawa K, Harada K, Fukusaki E, Yoshimura K, Shigeoka S. Overexpression of an ADP-ribose pyrophosphatase, AtNUDX2, confers enhanced tolerance to oxidative stress in Arabidopsis plants. Plant J 2009, 57:289-301. 10.1111/j.1365-313X.2008.03686.x, 18798872.
37. Bartsch M, Gobbato E, Bednarek P, Debey S, Schultze JL, Bautor J, Parker JE. 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. 10.1105/tpc.105.039982, 1425861, 16531493.
38. Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu JL, Huckelhoven R, Stein M, Freialdenhoven A, Somerville SC, Schulze-Lefert P. SNARE-protein-mediated disease resistance at the plant cell wall. Nature 2003, 425:973-977. 10.1038/nature02076, 14586469.
39. Schulze-Lefert P, Panstruga R. A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci 2011, 16:117-125. 10.1016/j.tplants.2011.01.001, 21317020.
40. Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D. Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 2005, 310(5751):1180-1183. 10.1126/science.1119409, 16293760.
41. Stein M, Dittgen J, Sánchez-Rodríguez C, Hou B-H, Molina A, Schulze-Lefert P, Lipka V, Somerville S. Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell Online 2006, 18:731-746.
42. Westphal L, Scheel D, Rosahl S. The coi1-16 mutant harbors a second site mutation rendering PEN2 nonfunctional. Plant Cell Online 2008, 20:824-826.
43. Macarisin D, Wisniewski ME, Bassett C, Thannhauser TW. Proteomic analysis of β-aminobutyric acid priming and abscisic acid - induction of drought resistance in crabapple (Malus pumila): effect on general metabolism, the phenylpropanoid pathway and cell wall enzymes. Plant Cell Environ 2009, 32:1612-1631.
44. Kopischke M, Westphal L, Schneeberger K, Clark R, Ossowski S, Wewer V, Fuchs R, Landtag J, Hause G, Dörmann P. Impaired sterol ester synthesis alters the response of Arabidopsis thaliana to Phytophthora infestans. The Plant Journal 2013, 73(3):456-468. 10.1111/tpj.12046, 23072470.
45. Hendrix JW. Sterols in growth and reproduction of fungi. Annu Rev Phytopathol 1970, 8:111-130.
46. Choi D, Bostock RM, Avdiushko S, Hildebrand DF. Lipid-derived signals that discriminate wound- and pathogen-responsive isoprenoid pathways in plants: methyl jasmonate and the fungal elicitor arachidonic acid induce different 3-hydroxy-3-methylglutaryl-coenzyme A reductase genes and antimicrobial isoprenoids in Solanum tuberosum L. Proc Natl Acad Sci 1994, 91:2329-2333. 10.1073/pnas.91.6.2329, 43364, 11607466.
47. Tjamos EC, Kucacute JA. Inhibition of steroid glycoalkaloid accumulation by arachidonic and eicosapentaenoic acids in potato. Science 1982, 217:542-544. 10.1126/science.217.4559.542, 17820543.
48. Choi D, Ward BL, Bostock RM. Differential induction and suppression of potato 3-hydroxy-3-methylglutaryl coenzyme A reductase genes in response to Phytophthora infestans and to its elicitor arachidonic acid. Plant Cell Online 1992, 4:1333-1344.
49. Krits P, Fogelman E, Ginzberg I. Potato steroidal glycoalkaloid levels and the expression of key isoprenoid metabolic genes. Planta 2007, 227:143-150. 10.1007/s00425-007-0602-3, 17701426.
50. Ros B, Thummler F, Wenzel G. Analysis of differentially expressed genes in a susceptible and moderately resistant potato cultivar upon Phytophthora infestans infection. Mol Plant Pathol 2004, 5:191-201. 10.1111/j.1364-3703.2004.00221.x, 20565609.
51. Stermer BA, Bostock RM. Involvement of 3-hydroxy-3-methylglutaryl coenzyme a reductase in the regulation of sesquiterpenoid phytoalexin synthesis in potato. Plant Physiol 1987, 84:404-408. 10.1104/pp.84.2.404, 1056592, 16665452.
52. Bostock RM, Kuc JA, Laine RA. Eicosapentaenoic and arachidonic acids from phytophthora infestans elicit fungitoxic sesquiterpenes in the potato. Science 1981, 212:67-69. 10.1126/science.212.4490.67, 17747631.
53. Bostock RM, Schaeffer DA, Hammerschmidt R. Comparison of elicitor activities of arachidonic acid, fatty acids and glucans from Phytophthora infestans in hypersensitivity expression in potato tuber. Physiol Mol Plant Pathol 1986, 29:349-360.
54. Preisig CL, Kuć JA. Inhibition by salicylhydroxamic acid, BW755C, eicosatetraynoic acid, and disulfiram of hypersensitive resistance elicited by arachidonic acid or poly-l-lysine in potato tuber. Plant Physiol 1987, 84:891-894. 10.1104/pp.84.3.891, 1056690, 16665539.
55. Cacas J-L, Vailleau F, Davoine C, Ennar N, Agnel J-P, Tronchet M, Ponchet M, Blein J-P, Roby D, Triantaphylides C, Montillet J-L. The combined action of 9 lipoxygenase and galactolipase is sufficient to bring about programmed cell death during tobacco hypersensitive response. Plant Cell Environ 2005, 28:1367-1378.
56. Cacas J-L, Marmey P, Montillet J-L, Sayegh-Alhamdia M, Jalloul A, Rojas-Mendoza A, Clérivet A, Nicole M. A novel patatin-like protein from cotton plant, GhPat1, is co-expressed with GhLox1 during Xanthomonas campestris-mediated hypersensitive cell death. Plant Cell Rep 2009, 28:155-164. 10.1007/s00299-008-0622-x, 18850102.
57. Berkowitz O, Jost R, Kollehn DO, Fenske R, Finnegan PM, O'Brien PA, Hardy GE, Lambers H. Acclimation responses of Arabidopsis thaliana to sustained phosphite treatments. J Exp Bot 2013, 64:1731-1743. 10.1093/jxb/ert037, 3617837, 23404904.
58. Alcazar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF. Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 2010, 231:1237-1249. 10.1007/s00425-010-1130-0, 20221631.
59. Lazzarato L, Trebbi G, Pagnucco C, Franchin C, Torrigiani P, Betti L. Exogenous spermidine, arsenic and beta-aminobutyric acid modulate tobacco resistance to tobacco mosaic virus, and affect local and systemic glucosylsalicylic acid levels and arginine decarboxylase gene expression in tobacco leaves. J Plant Physiol 2009, 166:90-100. 10.1016/j.jplph.2008.01.011, 18462831.
60. Halim VA, Eschen-Lippold L, Altmann S, Birschwilks M, Scheel D, Rosahl S. Salicylic acid is important for basal defense of solanum tuberosum against Phytophthora infestans. Mol Plant-Microbe Interact 2007, 20:1346-1352.
61. Navarro L, Bari R, Achard P, Lisón P, Nemri A, Harberd NP, Jones JD. DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr Biol 2008, 18:650-655.
62. Wang D, Pajerowska-Mukhtar K, Culler AH, Dong X. Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr Biol 2007, 17:1784-1790. 10.1016/j.cub.2007.09.025, 17919906.
63. Ding X, Cao Y, Huang L, Zhao J, Xu C, Li X, Wang S. Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in rice. Plant Cell 2008, 20:228-240. 10.1105/tpc.107.055657, 2254934, 18192436.
64. van Loon LC, Rep M, Pieterse CM. Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 2006, 44:135-162. 10.1146/annurev.phyto.44.070505.143425, 16602946.
65. Dhaubhadel S, Kuflu K, Romero MC, Gijzen M. A soybean seed protein with carboxylate-binding activity. J Exp Bot 2005, 56:2335-2344. 10.1093/jxb/eri226, 16061511.
66. Mika A, Minibayeva F, Beckett R, Lüthje S. Possible functions of extracellular peroxidases in stress-induced generation and detoxification of active oxygen species. Phytochem Rev 2004, 3:173-193.
67. Baysal T, Gu{double grave}rsoy YZ, Örnek H, Duru A. Induction of oxidants in tomato leaves treated with DL-b-Amino butyric acid (BABA) and infected with Clavibacter michiganensis ssp. Eur J Plant Pathol 2005, 112:361-369.
68. Almasia NI, Bazzini AA, Hopp HE, Vazquez-Rovere C. Overexpression of snakin-1 gene enhances resistance to Rhizoctonia solani and Erwinia carotovora in transgenic potato plants. Mol Plant Pathol 2008, 9:329-338. 10.1111/j.1364-3703.2008.00469.x, 18705874.
69. Segura A, Moreno M, Madueno F, Molina A, Garcia-Olmedo F. Snakin-1, a peptide from potato that is active against plant pathogens. Mol Plant-Microbe Interact 1999, 12:16-23.
70. Nahirnak V, Almasia NI, Fernandez PV, Hopp HE, Estevez JM, Carrari F, Vazquez-Rovere C. Potato snakin-1 gene silencing affects cell division, primary metabolism, and cell wall composition. Plant Physiol 2012, 158:252-263. 10.1104/pp.111.186544, 3252113, 22080603.
71. Olivieri FP, Lobato MC, Gonzalez Altamiranda E, Daleo GR, Huarte M, Guevara MG, Andreu AB. BABA effects on the behaviour of potato cultivars infected by Phytophthora infestans and Fusarium solani. Eur J Plant Pathol 2009, 123:47-56.