Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity

Genome Biology

Volumn 14, Issue 12, 2013, Pages

  Rosli, Hernan G ^a,b   Zheng, Yi ^a   Pombo, Marina A ^a   Zhong, Silin ^a,c   Bombarely, Aureliano ^a   Fei, Zhangjun ^a   Collmer, Alan ^d,e   Martin, Gregory B ^a,d,e  

^a United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^b INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^d Department of Obstetrics Gynecology   (United States)

^e KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ENZYME; CELL WALL ASSOCIATED KINASE; FLAGELLIN; PROTEIN KINASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CELL MEMBRANE PROTEIN; PROTEIN AVRPTO; PROTEIN AVRPTOB; PROTEIN SLWAK1; RNA; AVRPTO PROTEIN, PSEUDOMONAS SYRINGAE; VEGETABLE PROTEIN;

ARTICLE; BACTERIAL GROWTH; BACTERIUM IDENTIFICATION; CONTROLLED STUDY; ENZYME REPRESSION; FLAGELLIN INDUCED REPRESSED BY EFFECTOR GENE; GENE; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE SILENCING; IMMUNE RESPONSE; MOLECULAR DYNAMICS; MOLECULAR PHYLOGENY; NONHUMAN; PLANT GENE; PLANT IMMUNITY; PLANT LEAF; PLANT PATHOGEN INTERACTION; PLANT RESPONSE; PROCESS DEVELOPMENT; PSEUDOMONAS SYRINGAE PV. TOMATO; SCREENING TEST; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS; WAK1 GENE; BACTERIAL GENE; FIRE GENE; GENE ONTOLOGY; GENE REPRESSION; GENETIC CODE; GENETIC IDENTIFICATION; HIGH THROUGHPUT SCREENING; MICROORGANISM; PROTEIN FAMILY; PROTEIN FUNCTION; RNA SEQUENCE; TOMATO; VIRUS INDUCTION; CELL WALL; CYTOLOGY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOLECULAR EVOLUTION; PHYLOGENY; PLANT DISEASE; PROCEDURES; PSEUDOMONAS AERUGINOSA;

BACTERIA (MICROORGANISMS); LYCOPERSICON ESCULENTUM; PSEUDOMONAS SYRINGAE PV. TOMATO;

BACTERIAL PROTEINS; CELL WALL; EVOLUTION, MOLECULAR; FLAGELLIN; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; LYCOPERSICON ESCULENTUM; PHYLOGENY; PLANT DISEASES; PLANT IMMUNITY; PLANT PROTEINS; PROTEIN KINASES; PSEUDOMONAS AERUGINOSA; SEQUENCE ANALYSIS, RNA;

EID: 84890505536     PISSN: None     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2013-14-12-r139     Document Type: Article

References (72)

1. Dodds PN, Rathjen JP. Plant immunity: towards an integrated view of plant--pathogen interactions. Nat Rev Genet 2010, 11:539-548.
2. Schwessinger B, Ronald PC. Plant innate immunity: perception of conserved microbial signatures. Annu Rev Plant Biol 2012, 63:451-482. 10.1146/annurev-arplant-042811-105518, 22404464.
3. Nuhse TS. Cell wall integrity signaling and innate immunity in plants. Front Plant Sci 2012, 3:280. 3518785, 23248636.
4. Segonzac C, Zipfel C. Activation of plant pattern-recognition receptors by bacteria. Curr Opin Microbiol 2011, 14:54-61. 10.1016/j.mib.2010.12.005, 21215683.
5. Lindeberg M, Cunnac S, Collmer A. Pseudomonas syringae type III effector repertoires: last words in endless arguments. Trends Microbiol 2012, 20:199-208. 10.1016/j.tim.2012.01.003, 22341410.
6. Xin XF, He SY. Pseudomonas syringae pv. tomato DC3000: a model pathogen for probing disease susceptibility and hormone signaling in plants. Annu Rev Phytopathol 2013, 51:473-498. 10.1146/annurev-phyto-082712-102321, 23725467.
7. Melotto M, Underwood W, He SY. Role of stomata in plant innate immunity and foliar bacterial diseases. Annu Rev Phytopathol 2008, 46:101-122. 10.1146/annurev.phyto.121107.104959, 2613263, 18422426.
8. Gomez-Gomez L, Boller T. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 2000, 5:1003-1011. 10.1016/S1097-2765(00)80265-8, 10911994.
9. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones JD, Felix G, Boller T. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 2007, 448:497-500. 10.1038/nature05999, 17625569.
10. Zhang J, Li W, Xiang T, Liu Z, Laluk K, Ding X, Zou Y, Gao M, Zhang X, Chen S, Mengiste T, Zhang Y, Zhou JM. Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 2010, 7:290-301. 10.1016/j.chom.2010.03.007, 20413097.
11. Lu D, Wu S, Gao X, Zhang Y, Shan L, He P. A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc Natl Acad Sci USA 2010, 107:496-501. 10.1073/pnas.0909705107, 2806711, 20018686.
12. Cai R, Lewis J, Yan S, Liu H, Clarke CR, Campanile F, Almeida NF, Studholme DJ, Lindeberg M, Schneider D, Zaccardelli M, Setubal JC, Morales-Lizcano NP, Bernal A, Coaker G, Baker C, Bender CL, Leman S, Vinatzer BA. The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity. PLoS Pathog 2011, 7:e1002130. 10.1371/journal.ppat.1002130, 3161960, 21901088.
13. Clarke CR, Chinchilla D, Hind SR, Taguchi F, Miki R, Ichinose Y, Martin GB, Leman S, Felix G, Vinatzer BA. Allelic variation in two distinct Pseudomonas syringae flagellin epitopes modulates the strength of plant immune responses but not bacterial motility. New Phytol 2013, 200:847-860. 10.1111/nph.12408, 23865782.
14. Martin GB. Suppression and activation of the plant immune system by Pseudomonas syringae effectors AvrPto and AvrPtoB. Effectors in Plant-Microbe Interactions 2012, 123-154. London: Wiley-Blackwell, John Wiley and Sons, Martin F, Kamoun S.
15. Yeam I, Nguyen HP, Martin GB. Phosphorylation of the Pseudomonas syringae effector AvrPto is required for FLS2/BAK1-independent virulence activity and recognition by tobacco. Plant J 2010, 61:16-24. 10.1111/j.1365-313X.2009.04028.x, 19793077.
16. Zeng L, Velasquez AC, Munkvold KR, Zhang J, Martin GB. A tomato LysM receptor-like kinase promotes immunity and its kinase activity is inhibited by AvrPtoB. Plant J 2012, 69:92-103. 10.1111/j.1365-313X.2011.04773.x, 3240704, 21880077.
17. Pedley KF, Martin GB. Molecular basis of Pto-mediated resistance to bacterial speck disease in tomato. Annu Rev Phytopathol 2003, 41:215-243. 10.1146/annurev.phyto.41.121602.143032, 14527329.
18. Zhao Y, Thilmony R, Bender CL, Schaller A, He SY, Howe GA. Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant J 2003, 36:485-499. 10.1046/j.1365-313X.2003.01895.x, 14617079.
19. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG, Felix G, Boller T. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 2004, 428:764-767. 10.1038/nature02485, 15085136.
20. Navarro L, Zipfel C, Rowland O, Keller I, Robatzek S, Boller T, Jones JD. The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol 2004, 135:1113-1128. 10.1104/pp.103.036749, 514144, 15181213.
21. Truman W, de Zabala MT, Grant M. Type III effectors orchestrate a complex interplay between transcriptional networks to modify basal defence responses during pathogenesis and resistance. Plant J 2006, 46:14-33. 10.1111/j.1365-313X.2006.02672.x, 16553893.
22. Thilmony R, Underwood W, He SY. Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7. Plant J 2006, 46:34-53. 10.1111/j.1365-313X.2006.02725.x, 16553894.
23. Denoux C, Galletti R, Mammarella N, Gopalan S, Werck D, De Lorenzo G, Ferrari S, Ausubel FM, Dewdney J. Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. Mol Plant 2008, 1:423-445. 10.1093/mp/ssn019, 2954645, 19825551.
24. Mysore KS, Crasta OR, Tuori RP, Folkerts O, Swirsky PB, Martin GB. Comprehensive transcript profiling of Pto- and Prf-mediated host defense responses to infection by Pseudomonas syringae pv. tomato. Plant J 2002, 32:299-315. 10.1046/j.1365-313X.2002.01424.x, 12410809.
25. de Torres M, Sanchez P, Fernandez-Delmond I, Grant M. Expression profiling of the host response to bacterial infection: the transition from basal to induced defence responses in RPM1-mediated resistance. Plant J 2003, 33:665-676. 10.1046/j.1365-313X.2003.01653.x, 12609040.
26. Tomato Genome Consortium The tomato genome sequence provides insights into fleshy fruit evolution. Nature 2012, 485:635-641. 10.1038/nature11119, 3378239, 22660326, Tomato Genome Consortium.
27. Cunnac S, Chakravarthy S, Kvitko BH, Russell AB, Martin GB, Collmer A. Genetic disassembly and combinatorial reassembly identify a minimal functional repertoire of type III effectors in Pseudomonas syringae. Proc Natl Acad Sci USA 2011, 108:2975-2980. 10.1073/pnas.1013031108, 3041132, 21282655.
28. Tomato functional genomics database. http://ted.bti.cornell.edu.
29. Chakravarthy S, Velasquez AC, Ekengren SK, Collmer A, Martin GB. Identification of Nicotiana benthamiana genes involved in pathogen-associated molecular pattern-triggered immunity. Mol Plant Microbe Interact 2010, 23:715-726. 10.1094/MPMI-23-6-0715, 20459311.
30. iTAK - Plant Transcription factor and Protein Kinase Identifier and Classifier. http://bioinfo.bti.cornell.edu/cgi-bin/itak/index.cgi.
31. Kohorn BD, Kohorn SL. The cell wall-associated kinases, WAKs, as pectin receptors. Front Plant Sci 2012, 3:88. 3355716, 22639672.
32. Bombarely A, Rosli HG, Vrebalov J, Moffett P, Mueller LA, Martin GB. A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol Plant Microbe Interact 2012, 25:1523-1530. 10.1094/MPMI-06-12-0148-TA, 22876960.
33. Xiao F, He P, Abramovitch RB, Dawson JE, Nicholson LK, Sheen J, Martin GB. The N-terminal region of Pseudomonas type III effector AvrPtoB elicits Pto-dependent immunity and has two distinct virulence determinants. Plant J 2007, 52:595-614. 10.1111/j.1365-313X.2007.03259.x, 2265002, 17764515.
34. Nguyen HP, Yeam I, Angot A, Martin GB. Two virulence determinants of type III effector AvrPto are functionally conserved in diverse Pseudomonas syringae pathovars. New Phytol 2010, 187:969-982. 10.1111/j.1469-8137.2009.03175.x, 20122130.
35. Gimenez-Ibanez S, Hann DR, Ntoukakis V, Petutschnig E, Lipka V, Rathjen JP. AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr Biol 2009, 19:423-429. 10.1016/j.cub.2009.01.054, 19249211.
36. He ZH, Cheeseman I, He D, Kohorn BD. A cluster of five cell wall-associated receptor kinase genes, Wak1-5, are expressed in specific organs of Arabidopsis. Plant Mol Biol 1999, 39:1189-1196. 10.1023/A:1006197318246, 10380805.
37. Verica JA, He ZH. The cell wall-associated kinase (WAK) and WAK-like kinase gene family. Plant Physiol 2002, 129:455-459. 10.1104/pp.011028, 1540232, 12068092.
38. De Lorenzo G, Brutus A, Savatin DV, Sicilia F, Cervone F. Engineering plant resistance by constructing chimeric receptors that recognize damage-associated molecular patterns (DAMPs). FEBS Lett 2011, 585:1521-1528. 10.1016/j.febslet.2011.04.043, 21536040.
39. Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G. A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci USA 2010, 107:9452-9457. 10.1073/pnas.1000675107, 2889104, 20439716.
40. Kohorn BD, Kohorn SL, Todorova T, Baptiste G, Stansky K, McCullough M. A dominant allele of Arabidopsis pectin-binding wall-associated kinase induces a stress response suppressed by MPK6 but not MPK3 mutations. Mol Plant 2012, 5:841-851. 10.1093/mp/ssr096, 3399699, 22155845.
41. Diener AC, Ausubel FM. Resistance to Fusarium oxysporum 1, a dominant Arabidopsis disease-resistance gene, is not race specific. Genetics 2005, 171:305-321. 10.1534/genetics.105.042218, 1456520, 15965251.
42. Li H, Zhou SY, Zhao WS, Su SC, Peng YL. A novel wall-associated receptor-like protein kinase gene, OsWAK1, plays important roles in rice blast disease resistance. Plant Mol Biol 2009, 69:337-346. 10.1007/s11103-008-9430-5, 19039666.
43. Meier S, Ruzvidzo O, Morse M, Donaldson L, Kwezi L, Gehring C. The Arabidopsis wall associated kinase-like 10 gene encodes a functional guanylyl cyclase and is co-expressed with pathogen defense related genes. PLoS One 2010, 5:e8904. 10.1371/journal.pone.0008904, 2811198, 20126659.
44. Lejeune A, Constant S, Delavault P, Simier P, Thalouarn P, Thoiron S. Involvement of a putative Lycopersicon esculentum wall-associated kinase in the early steps of tomato-Orobanche ramosa interaction. Physiol Molec Plant Pathol 2006, 69:3-12.
45. Ferrari S, Savatin DV, Sicilia F, Gramegna G, Cervone F, Lorenzo GD. Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development. Front Plant Sci 2013, 4:49. 3595604, 23493833.
46. Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, Gwinn ML, Dodson RJ, Deboy RT, Durkin AS, Kolonay JF, Madupu R, Daugherty S, Brinkac L, Beanan MJ, Haft DH, Nelson WC, Davidsen T, Zafar N, Zhou L, Liu J, Yuan Q, Khouri H, Fedorova N, Tran B, Russell D, Berry K, Utterback T, Van Aken SE, Feldblyum TV, D'Ascenzo M, et al. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci USA 2003, 100:10181-10186. 10.1073/pnas.1731982100, 193536, 12928499.
47. Nam KH, Li J. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 2002, 110:203-212. 10.1016/S0092-8674(02)00814-0, 12150928.
48. Veronese P, Nakagami H, Bluhm B, Abuqamar S, Chen X, Salmeron J, Dietrich RA, Hirt H, Mengiste T. The membrane-anchored Botrytis-induced kinase1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens. Plant Cell 2006, 18:257-273. 10.1105/tpc.105.035576, 1323497, 16339855.
49. Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, He P, Bush J, Cheng SH, Sheen J. Differential innate immune signalling via Ca2+ sensor protein kinases. Nature 2010, 464:418-422. 10.1038/nature08794, 2841715, 20164835.
50. Zhong S, Joung JG, Zheng Y, Chen YR, Liu B, Shao Y, Xiang JZ, Fei Z, Giovannoni JJ. High-throughput Illumina strand-specific RNA sequencing library preparation. Cold Spring Harb Protoc 2011, 2011:940-949.
51. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2013, 41:D590-D596. 10.1093/nar/gks1219, 3531112, 23193283.
52. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25. 10.1186/gb-2009-10-3-r25, 2690996, 19261174.
53. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25:1105-1111. 10.1093/bioinformatics/btp120, 2672628, 19289445.
54. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol 2010, 11:R106. 10.1186/gb-2010-11-10-r106, 3218662, 20979621.
55. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc Series B (Methodological) 1995, 57:289-300.
56. Ramskold D, Wang ET, Burge CB, Sandberg R. An abundance of ubiquitously expressed genes revealed by tissue transcriptome sequence data. PLoS Comput Biol 2009, 5:e1000598. 10.1371/journal.pcbi.1000598, 2781110, 20011106.
57. Castruita M, Casero D, Karpowicz SJ, Kropat J, Vieler A, Hsieh SI, Yan W, Cokus S, Loo JA, Benning C, Pellegrini M, Merchant SS. Systems biology approach in Chlamydomonas reveals connections between copper nutrition and multiple metabolic steps. Plant Cell 2011, 23:1273-1292. 10.1105/tpc.111.084400, 3101551, 21498682.
58. SOL genomics network. http://solgenomics.net/.
59. Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 2000, 132:365-386.
60. Liu Y, Schiff M, Dinesh-Kumar SP. Virus-induced gene silencing in tomato. Plant J 2002, 31:777-786. 10.1046/j.1365-313X.2002.01394.x, 12220268.
61. Velasquez AC, Chakravarthy S, Martin GB. Virus-induced gene silencing (VIGS) in Nicotiana benthamiana and tomato. J Vis Exp 2009, 28:e1292.
62. de Hoon MJ, Imoto S, Nolan J, Miyano S. Open source clustering software. Bioinformatics 2004, 20:1453-1454. 10.1093/bioinformatics/bth078, 14871861.
63. Boyle EI, Weng S, Gollub J, Jin H, Botstein D, Cherry JM, Sherlock G. GO::TermFinder - open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 2004, 20:3710-3715. 10.1093/bioinformatics/bth456, 3037731, 15297299.
64. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012, 9:772.
65. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704. 10.1080/10635150390235520, 14530136.
66. Abascal F, Zardoya R, Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105. 10.1093/bioinformatics/bti263, 15647292.
67. Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010, 27:221-224. 10.1093/molbev/msp259, 19854763.
68. FigTree. http://tree.bio.ed.ac.uk/software/figtree/.
69. Oliveros JC. VENNY. An interactive tool for comparing lists with Venn diagrams. 2007, http://bioinfogp.cnb.csic.es/tools/venny/.
70. Bombarely A, Menda N, Tecle IY, Buels RM, Strickler S, Fischer-York T, Pujar A, Leto J, Gosselin J, Mueller LA. The Sol Genomics Network (solgenomics.net): growing tomatoes using Perl. Nucleic Acids Res 2011, 39:D1149-D1155. 10.1093/nar/gkq866, 3013765, 20935049.
71. Nguyen HP, Chakravarthy S, Velasquez AC, McLane HL, Zeng L, Nakayashiki H, Park DH, Collmer A, Martin GB. Methods to study PAMP-triggered immunity using tomato and Nicotiana benthamiana. Mol Plant Microbe Interact 2010, 23:991-999. 10.1094/MPMI-23-8-0991, 20615110.
72. Liu D, Shi L, Han C, Yu J, Li D, Zhang Y. Validation of reference genes for gene expression studies in virus-infected Nicotiana benthamiana using quantitative real-time PCR. PLoS One 2012, 7:e46451. 10.1371/journal.pone.0046451, 3460881, 23029521.