Reciprocal responses in the interaction between arabidopsis and the cell-content-feeding chelicerate herbivore spider mite

Plant Physiology

Volumn 164, Issue 1, 2014, Pages 384-399

  Zhurov, Vladimir ^a   Navarro, Marie ^a,b   Bruinsma, Kristie A ^a   Arbona, Vicent ^d   Estrella Santamaria, M ^a,c   Cazaux, Marc ^a,b   Wybouw, Nicky ^e   Osborne, Edward J ^g   Ens, Cherise ^a   Rioja, Cristina ^a,b   Vermeirssen, Vanessa ^e   Rubio Somoza, Ignacio ^h   Krishna, Priti ^a,j   Diaz, Isabel ^c   Schmid, Markus ^h   Gómez Cadenas, Aurelio ^d   Van de Peer, Yves ^e,i,k   Grbić, Miodrag ^a,b   Clark, Richard M ^g   Van Leeuwen, Thomas ^e,f   Grbić, Vojislava ^a,b   more..

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b Ctra Burgos Km 6   (Spain)

^c UNIVERSIDAD POLITÉCNICA DE MADRID   (Spain)

^d UNIVERSITAT JAUME I   (Spain)

^e GHENT UNIVERSITY   (Belgium)

^f UNIVERSITY OF AMSTERDAM   (Netherlands)

^g UNIVERSITY OF UTAH   (United States)

^h MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

ⁱ Vlaams Instituut Voor Biotechnologie   (Belgium)

^j UNIVERSITY OF NEW ENGLAND   (Australia)

^k UNIVERSITY OF PRETORIA   (South Africa)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPENTANE DERIVATIVE; GLUCOSINOLATE; JASMONIC ACID; OXYLIPIN; PHYTOHORMONE;

ANIMAL; ARABIDOPSIS; ARTICLE; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; HERBIVORY; HOST PARASITE INTERACTION; LARVA; META ANALYSIS; METABOLISM; MUTATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; TETRANYCHIDAE;

ANIMALS; ARABIDOPSIS; CYCLOPENTANES; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENETIC VARIATION; GLUCOSINOLATES; HERBIVORY; HOST-PARASITE INTERACTIONS; LARVA; MUTATION; OXYLIPINS; PLANT GROWTH REGULATORS; SIGNAL TRANSDUCTION; TETRANYCHIDAE;

EID: 84891756413     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.231555     Document Type: Article

References (93)

1. Alexa A, Rahnenführer J, Lengauer T (2006) Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22: 1600-1607
2. Ament K, Kant MR, Sabelis MW, Haring MA, Schuurink RC (2004) Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato. Plant Physiol 135: 2025-2037
3. Ament K, Van Schie CC, Bouwmeester HJ, Haring MA, Schuurink RC (2006) Induction of a leaf specific geranylgeranyl pyrophosphate synthase and emission of (E, E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene in tomato are dependent on both jasmonic acid and salicylic acid signaling pathways. Planta 224: 1197-1208
4. Arbona V, Argamasilla R, Gómez-Cadenas A (2010) Common and divergent physiological, hormonal and metabolic responses of Arabidopsis thaliana and Thellungiella halophila to water and salt stress. J Plant Physiol 167: 1342-1350
5. Beekwilder J, van Leeuwen W, van Dam NM, Bertossi M, Grandi V, Mizzi L, SolovievM, Szabados L, Molthoff JW, Schipper B, et al (2008) The impact of the absence of aliphatic glucosinolates on insect herbivory in Arabidopsis. PLoS ONE 3: e2068
6. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57: 289-300
7. Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, Dangl JL, Weigel D (2007) Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLoS Biol 5: e236
8. Bonaventure G (2012) Perception of insect feeding by plants. Plant Biol (Stuttg) 14: 872-880
9. Böttcher C, Westphal L, Schmotz C, Prade E, Scheel D, Glawischnig E (2009) The multifunctional enzyme CYP71B15 (PHYTOALEXIN DEFICIENT3) converts cysteine-indole-3-acetonitrile to camalexin in the indole-3-acetonitrile metabolic network of Arabidopsis thaliana. Plant Cell 21: 1830-1845
10. Browse J (2009) Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol 60: 183-205
11. Campbell RJ, Grayson RL, Marini RP (1990) Surface and ultrastructural feeding injury to strawberry leaves by the twospotted spider mite. HortScience 25: 948-951
12. Celenza JL, Quiel JA, Smolen GA, Merrikh H, Silvestro AR, Normanly J, Bender J (2005) The Arabidopsis ATR1 Myb transcription factor controls indolic glucosinolate homeostasis. Plant Physiol 137: 253-262
13. Chehab EW, Kaspi R, Savchenko T, Rowe H, Negre-Zakharov F, Kliebenstein D, Dehesh K (2008) Distinct roles of jasmonates and aldehydes in plant-defense responses. PLoS ONE 3: e1904
14. Chung HS, Koo AJK, Gao XL, Jayanty S, Thines B, Jones AD, Howe GA (2008) Regulation and function of Arabidopsis JASMONATE ZIMdomain genes in response to wounding and herbivory. Plant Physiol 146: 952-964
15. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139: 5-17
16. Dearden PK, Donly C, Grbić M (2002) Expression of pair-rule gene homologues in a chelicerate: early patterning of the two-spotted spider mite Tetranychus urticae. Development 129: 5461-5472
17. Dermauw W, Wybouw N, Rombauts S, Menten B, Vontas J, Grbić M, Clark RM, Feyereisen R, Van Leeuwen T (2013) A link between host plant adaptation and pesticide resistance in the polyphagous spider mite Tetranychus urticae. Proc Natl Acad Sci USA 110: E113-E122
18. De Vos M, Van Oosten VR, Van Poecke RMP, Van Pelt JA, Pozo MJ, Mueller MJ, Buchala AJ, Métraux JP, Van Loon LC, Dicke M, et al (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Interact 18: 923-937
19. Dicke M, Takabayashi J, Posthumus MA, Schutte C, Krips OE (1998) Plant-phytoseiid interactions mediated by herbivore-induced plant volatiles: variation in production of cues and in responses of predatory mites. Exp Appl Acarol 22: 311-333
20. Durgbanshi A, Arbona V, Pozo O, Miersch O, Sancho JV, Gómez-Cadenas A (2005) Simultaneous determination of multiple phytohormones in plant extracts by liquid chromatography-electrospray tandem mass spectrometry. J Agric Food Chem 53: 8437-8442
21. Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insectspecific plant reactions. Trends Plant Sci 17: 250-259
22. Fernández-Calvo P, Chini A, Fernández-Barbero G, Chico JM, Gimenez-Ibanez S, Geerinck J, Eeckhout D, Schweizer F, Godoy M, Franco-Zorrilla JM, et al (2011) 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 23: 701-715
23. Gan XC, Stegle O, Behr J, Steffen JG, Drewe P, Hildebrand KL, Lyngsoe R, Schultheiss SJ, Osborne EJ, Sreedharan VT, et al (2011) Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477: 419-423
24. Grbić M, Khila A, Lee KZ, Bjelica A, Grbić V, Whistlecraft J, Verdon L, Navajas M, Nagy L (2007) Mity model: Tetranychus urticae, a candidate for chelicerate model organism. Bioessays 29: 489-496
25. Grbić M, Van Leeuwen T, Clark RM, Rombauts S, Rouzé P, Grbić V, Osborne EJ, Dermauw W, Ngoc PC, Ortego F, et al (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479: 487-492
26. Heitz T, Widemann E, Lugan R, Miesch L, Ullmann P, Désaubry L, Holder E, Grausem B, Kandel S, Miesch M, et al (2012) Cytochromes P450 CYP94C1 and CYP94B3 catalyze two successive oxidation steps of plant hormone jasmonoyl-isoleucine for catabolic turnover. J Biol Chem 287: 6296-6306
27. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6: 65-70
28. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinformatics 2008: 420747
29. Huffaker A, Pearce G, Veyrat N, Erb M, Turlings TCJ, Sartor R, Shen ZX, Briggs SP, Vaughan MM, Alborn HT, et al (2013) Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense. Proc Natl Acad Sci USA 110: 5707-5712
30. Huffaker A, Ryan CA (2007) Endogenous peptide defense signals in Arabidopsis differentially amplify signaling for the innate immune response. Proc Natl Acad Sci USA 104: 10732-10736
31. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264
32. Jander G, Howe G (2008) Plant interactions with arthropod herbivores: state of the field. Plant Physiol 146: 801-803
33. Jones JD, Dangl JL (2006) The plant immune system. Nature 444: 323-329
34. Kant MR, Ament K, Sabelis MW, Haring MA, Schuurink RC (2004) Differential timing of spider mite-induced direct and indirect defenses in tomato plants. Plant Physiol 135: 483-495
35. Kant MR, Sabelis MW, Haring MA, Schuurink RC (2008) Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences. Proc Biol Sci 275: 443-452
36. Kauffmann A, Gentleman R, Huber W (2009) Array Quality Metrics: a Bioconductor package for quality assessment of microarray data. Bioinformatics 25: 415-416
37. Kempema LA, Cui XP, Holzer FM, Walling LL (2007) Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs: similarities and distinctions in responses to aphids. Plant Physiol 143: 849-865
38. Keogh RC, Deverall BJ, Mcleod S (1980) Comparison of histological and physiological responses to Phakopsora-Pachyrhizi in resistant and susceptible soybean. Trans Br Mycol Soc 74: 329-333
39. Khila A, Grbić M (2007) Gene silencing in the spider mite Tetranychus urticae: dsRNA and siRNA parental silencing of the Distal-less gene. Dev Genes Evol 217: 241-251
40. Kim JH, Jander G (2007) Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. Plant J 49: 1008-1019
41. Kim JH, Lee BW, Schroeder FC, Jander G (2008) Identification of indole glucosinolate breakdown products with antifeedant effects on Myzus persicae (green peach aphid). Plant J 54: 1015-1026
42. Kliebenstein D, Pedersen D, Barker B, Mitchell-Olds T (2002) Comparative analysis of quantitative trait loci controlling glucosinolates, myrosinase and insect resistance in Arabidopsis thaliana. Genetics 161: 325-332
43. Kliebenstein DJ, Kroymann J, Mitchell-Olds T (2005) The glucosinolatemyrosinase system in an ecological and evolutionary context. Curr Opin Plant Biol 8: 264-271
44. Koo AJK, Cooke TF, Howe GA (2011) Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-Lisoleucine. Proc Natl Acad Sci USA 108: 9298-9303
45. Koo AJK, Gao XL, Jones AD, Howe GA (2009) A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. Plant J 59: 974-986
46. Koornneef M, Meinke D (2010) The development of Arabidopsis as a model plant. Plant J 61: 909-921
47. Li CY, Williams MM, Loh YT, Lee GI, Howe GA (2002) Resistance of cultivated tomato to cell content-feeding herbivores is regulated by the octadecanoid-signaling pathway. Plant Physiol 130: 494-503
48. Li L, Zhao YF, McCaig BC, Wingerd BA, Wang JH, WhalonME, Pichersky E, Howe GA (2004) The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonatesignaled defense responses, and glandular trichome development. Plant Cell 16: 126-143
49. Li L, Zhao YF, McCaig BC, Wingerd BA, Wang JH, Whalon ME, Pichersky E, Howe GA (2004) Plant Cell 16: 783
50. Li Q, Xie QG, Smith-Becker J, Navarre DA, Kaloshian I (2006) Mi-1-mediated aphid resistance involves salicylic acid and mitogenactivated protein kinase signaling cascades. Mol Plant Microbe Interact 19: 655-664
51. Li X, Schuler MA, Berenbaum MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52: 231-253
52. Malitsky S, Blum E, Less H, Venger I, Elbaz M, Morin S, Eshed Y, Aharoni A (2008) The transcript and metabolite networks affected by the two clades of Arabidopsis glucosinolate biosynthesis regulators. Plant Physiol 148: 2021-2049
53. McDanell R, McLean AEM, Hanley AB, Heaney RK, Fenwick GR (1988) Chemical and biological properties of indole glucosinolates (glucobrassicins): a review. Food Chem Toxicol 26: 59-70
54. McGurl B, Pearce G, Orozco-Cardenas M, Ryan CA (1992) Structure, expression, and antisense inhibition of the systemin precursor gene. Science 255: 1570-1573
55. Mewis I, Appel HM, Hom A, Raina R, Schultz JC (2005) Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiol 138: 1149-1162
56. Mewis I, Tokuhisa JG, Schultz JC, Appel HM, Ulrichs C, Gershenzon J (2006) Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways. Phytochemistry 67: 2450-2462
57. Migeon A, Dorkeld F (2013) Spider Mites Web: a comprehensive database for the Tetranychidae. http://www.montpellier.inra.fr/CBGP/spmweb (October 21, 2013)
58. Müller R, de Vos M, Sun JY, Sønderby IE, Halkier BA, Wittstock U, Jander G (2010) Differential effects of indole and aliphatic glucosinolates on lepidopteran herbivores. J Chem Ecol 36: 905-913
59. Park JH, Halitschke R, Kim HB, Baldwin IT, Feldmann KA, Feyereisen R (2002) A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant J 31: 1-12
60. Pearce G, Strydom D, Johnson S, Ryan CA (1991) A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253: 895-897
61. Pfalz M, Vogel H, Kroymann J (2009) The gene controlling the indole glucosinolate modifier1 quantitative trait locus alters indole glucosinolate structures and aphid resistance in Arabidopsis. Plant Cell 21: 985-999
62. Ratzka A, Vogel H, Kliebenstein DJ, Mitchell-Olds T, Kroymann J (2002) Disarming the mustard oil bomb. Proc Natl Acad Sci USA 99: 11223-11228
63. Reymond P, Bodenhausen N, Van Poecke RMP, Krishnamurthy V, Dicke M, Farmer EE (2004) A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16: 3132-3147
64. Rieu I, Powers SJ (2009) Real-time quantitative RT-PCR: design, calculations, and statistics. Plant Cell 21: 1031-1033
65. Ritchie ME, Silver J, Oshlack A, Holmes M, Diyagama D, Holloway A, Smyth GK (2007) A comparison of background correction methods for two-colour microarrays. Bioinformatics 23: 2700-2707
66. Robert-Seilaniantz A, Grant M, Jones JD (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49: 317-343
67. Santamaria ME, Cambra I, Martinez M, Pozancos C, González-Melendi P, Grbić V, Castañera P, Ortego F, Diaz I (2012) Gene pyramiding of peptidase inhibitors enhances plant resistance to the spider mite Tetranychus urticae. PLoS ONE 7: e43011
68. Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J, Chourey PS, Alborn HT, Teal PEA (2006) Fragments of ATP synthase mediate plant perception of insect attack. Proc Natl Acad Sci USA 103: 8894-8899
69. Schramm K, Vassão DG, Reichelt M, Gershenzon J, Wittstock U (2012) Metabolism of glucosinolate-derived isothiocyanates to glutathione conjugates in generalist lepidopteran herbivores. Insect Biochem Mol Biol 42: 174-182
70. Schweighofer A, Kazanaviciute V, Scheikl E, Teige M, Doczi R, Hirt H, Schwanninger M, Kant M, Schuurink R, Mauch F, et al (2007) The PP2C-type phosphatase AP2C1, which negatively regulates MPK4 and MPK6, modulates innate immunity, jasmonic acid, and ethylene levels in Arabidopsis. Plant Cell 19: 2213-2224
71. Smith CA, Want EJ, O'Maille G, Abagyan R, Siuzdak G (2006) XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal Chem 78: 779-787
72. Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: e3
73. Smyth GK, Speed T (2003) Normalization of cDNA microarray data. Methods 31: 265-273
74. Sønderby IE, Hansen BG, Bjarnholt N, Ticconi C, Halkier BA, Kliebenstein DJ (2007) A systems biology approach identifies a R2R3 MYB gene subfamily with distinct and overlapping functions in regulation of aliphatic glucosinolates. PLoS ONE 2: e1322
75. Stintzi A, Weber H, Reymond P, Browse J, Farmer EE (2001) Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc Natl Acad Sci USA 98: 12837-12842
76. Sun JY, Sønderby IE, Halkier BA, Jander G, de Vos M (2009) Non-volatile intact indole glucosinolates are host recognition cues for ovipositing Plutella xylostella. J Chem Ecol 35: 1427-1436
77. Suzuki R, Shimodaira H (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22: 1540-1542
78. Tanigoshi LK, Davis RW (1978) An ultrastructural study of Tetranychus mcdanieli feeding injury to the leaves of 'Red Delicious' apple (Acari: Tetranychidae). Int J Acarol 4: 47-51
79. Truman W, Bennett MH, Kubigsteltig I, Turnbull C, Grant M (2007) Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc Natl Acad Sci USA 104: 1075-1080
80. Van Leeuwen T, Demaeght P, Osborne EJ, Dermauw W, Gohlke S, Nauen R, Grbić M, Tirry L, Merzendorfer H, Clark RM (2012) Population bulk segregant mapping uncovers resistance mutations and the mode of action of a chitin synthesis inhibitor in arthropods. Proc Natl Acad Sci USA 109: 4407-4412
81. Van Leeuwen T, Dermauw W, Grbić M, Tirry L, Feyereisen R (2013) Spider mite control and resistance management: does a genome help? Pest Manag Sci 69: 156-159
82. Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L (2010) Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: a review. Insect Biochem Mol Biol 40: 563-572
83. Wheat CW, Vogel H, Wittstock U, Braby MF, Underwood D, Mitchell-Olds T (2007) The genetic basis of a plant-insect coevolutionary key innovation. Proc Natl Acad Sci USA 104: 20427-20431
84. Whiteman NK, Gloss AD, Sackton TB, Groen SC, Humphrey PT, Lapoint RT, Sønderby IE, Halkier BA, Kocks C, Ausubel FM, et al (2012) Genes involved in the evolution of herbivory by a leaf-mining, drosophilid fly. Genome Biol Evol 4: 900-916
85. Wittstock U, Agerbirk N, Stauber EJ, Olsen CE, Hippler M, Mitchell-Olds T, Gershenzon J, Vogel H (2004) Successful herbivore attack due to metabolic diversion of a plant chemical defense. Proc Natl Acad Sci USA 101: 4859-4864
86. Wu J, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44: 1-24
87. Yamaguchi Y, Huffaker A (2011) Endogenous peptide elicitors in higher plants. Curr Opin Plant Biol 14: 351-357
88. Zhang PJ, Zheng SJ, van Loon JJA, Boland W, David A, Mumm R, Dicke M (2009) Whiteflies interfere with indirect plant defense against spider mites in lima bean. Proc Natl Acad Sci USA 106: 21202-21207
89. Zhao YD, Hull AK, Gupta NR, Goss KA, Alonso J, Ecker JR, Normanly J, Chory J, Celenza JL (2002) Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes Dev 16: 3100-3112
90. Zheng SJ, van Dijk JP, Bruinsma M, Dicke M (2007) Sensitivity and speed of induced defense of cabbage (Brassica oleracea L.): dynamics of Bo-LOX expression patterns during insect and pathogen attack. Mol Plant Microbe Interact 20: 1332-1345
91. Zhou N, Tootle TL, Glazebrook J (1999) Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. Plant Cell 11: 2419-2428
92. Zhu-Salzman K, Luthe DS, Felton GW (2008) Arthropod-inducible proteins: broad spectrum defenses against multiple herbivores. Plant Physiol 146: 852-858
93. Züst T, Heichinger C, Grossniklaus U, Harrington R, Kliebenstein DJ, Turnbull LA (2012) Natural enemies drive geographic variation in plant defenses. Science 338: 116-119