1932

Abstract

Many living organisms on Earth have evolved the ability to integrate environmental and internal signals to determine time and thereafter adjust appropriately their metabolism, physiology, and behavior. The circadian clock is the endogenous timekeeper critical for multiple biological processes in many organisms. A growing body of evidence supports the importance of the circadian clock for plant health. Plants activate timed defense with various strategies to anticipate daily attacks of pathogens and pests and to modulate responses to specific invaders in a time-of-day-dependent manner (gating). Pathogen infection is also known to reciprocally modulate clock activity. Such a cross talk likely reflects the adaptive nature of plants to coordinate limited resources for growth, development, and defense. This review summarizes recent progress in circadian regulation of plant innate immunity with a focus on the molecular events linking the circadian clock and defense. More and better knowledge of clock-defense cross talk could help to improve disease resistance and productivity in economically important crops.

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2017-08-04
2024-03-29
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Literature Cited

  1. Almagro L, Gómez Ros LV, Belchi-Navarro S, Bru R, Ros Barceló A, Pedreño MA. 1.  2009. Class III peroxidases in plant defence reactions. J. Exp. Bot. 60:377–90 [Google Scholar]
  2. Atamian HS, Harmer SL. 2.  2016. Circadian regulation of hormone signaling and plant physiology. Plant Mol. Biol. 91:691–702 [Google Scholar]
  3. Banday ZZ, Nandi AK. 3.  2015. Interconnection between flowering time control and activation of systemic acquired resistance. Front. Plant Sci. 6:174 [Google Scholar]
  4. Barneche F, Malapeira J, Mas P. 4.  2014. The impact of chromatin dynamics on plant light responses and circadian clock function. J. Exp. Bot. 65:2895–913 [Google Scholar]
  5. Baudry A, Ito S, Song YH, Strait AA, Kiba T. 5.  et al. 2010. F-box proteins FKF1 and LKP2 act in concert with ZEITLUPE to control Arabidopsis clock progression. Plant Cell 22:606–22 [Google Scholar]
  6. Beattie GA, Lindow SE. 6.  1999. Bacterial colonization of leaves: a spectrum of strategies. Phytopathology 89:353–59 [Google Scholar]
  7. Bechtold DA, Gibbs JE, Loudon AS. 7.  2010. Circadian dysfunction in disease. Trends Pharmacol. Sci. 31:191–98 [Google Scholar]
  8. Bender CL, Alarcon-Chaidez F, Gross DC. 8.  1999. Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol. Mol. Biol. Rev. 63:266–92 [Google Scholar]
  9. Bendix C, Marshall CM, Harmon FG. 9.  2015. Circadian clock genes universally control key agricultural traits. Mol. Plant 8:1135–52 [Google Scholar]
  10. Bhardwaj V, Meier S, Petersen LN, Ingle RA, Roden LC. 10.  2011. Defence responses of Arabidopsis thaliana to infection by Pseudomonas syringae are regulated by the circadian clock. PLOS ONE 6:e26968 [Google Scholar]
  11. Bluhm BH, Burnham AM, Dunkle LD. 11.  2010. A circadian rhythm regulating hyphal melanization in Cercospora kikuchii. . Mycologia 102:1221–28 [Google Scholar]
  12. Boller T, Felix G. 12.  2009. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60:379–406 [Google Scholar]
  13. Brodersen P, Petersen M, Pike HM, Olszak B, Skov S. 13.  et al. 2002. Knockout of Arabidopsis accelerated-cell-death11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev 16:490–502 [Google Scholar]
  14. Campos ML, Kang JH, Howe GA. 14.  2014. Jasmonate-triggered plant immunity. J. Chem. Ecol. 40:657–75 [Google Scholar]
  15. Chen Z, Agnew JL, Cohen JD, He P, Shan L. 15.  et al. 2007. Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. PNAS 104:20131–36 [Google Scholar]
  16. Chini A, Fonseca S, Fernandez G, Adie B, Chico JM. 16.  et al. 2007. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–71 [Google Scholar]
  17. Clements AN. 17.  1999. The Biology of Mosquitoes: Sensory, Reception and Behaviour 2 Wallingford, UK: CABI740
  18. Coates ME, Beynon JL. 18.  2010. Hyaloperonospora arabidopsidis as a pathogen model. Annu. Rev. Phytopathol. 48:329–45 [Google Scholar]
  19. Cortes T, Ortiz-Rivas B, Martinez-Torres D. 19.  2010. Identification and characterization of circadian clock genes in the pea aphid Acyrthosiphon pisum. Insect Mol. Biol. 19:Suppl. 2123–39 [Google Scholar]
  20. Covington MF, Harmer SL. 20.  2007. The circadian clock regulates auxin signaling and responses in Arabidopsis. . PLOS Biol. 5:e222 [Google Scholar]
  21. Covington MF, Maloof JN, Straume M, Kay SA, Harmer SL. 21.  2008. Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol 9:R130 [Google Scholar]
  22. Dangl JL, Horvath DM, Staskawicz BJ. 22.  2013. Pivoting the plant immune system from dissection to deployment. Science 341:746–51 [Google Scholar]
  23. Dempsey DA, Vlot AC, Wildermuth MC, Klessig DF. 23.  2011. Salicylic acid biosynthesis and metabolism. Arabidopsis Book 9:e0156 [Google Scholar]
  24. de Torres-Zabala M, Truman W, Bennett MH, Lafforgue G, Mansfield JW. 24.  et al. 2007. Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J. 26:1434–43 [Google Scholar]
  25. Devoto A, Nieto-Rostro M, Xie D, Ellis C, Harmston R. 25.  et al. 2002. COI1 links jasmonate signalling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis. . Plant J. 32:457–66 [Google Scholar]
  26. Dodd AN, Salathia N, Hall A, Kevei E, Toth R. 26.  et al. 2005. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–33 [Google Scholar]
  27. Dodds PN, Rathjen JP. 27.  2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11:539–48 [Google Scholar]
  28. Dong MA, Farre EM, Thomashow MF. 28.  2011. CIRCADIAN CLOCK-ASSOCIATED 1 and LATE ELONGATED HYPOCOTYL regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis. PNAS 108:7241–46 [Google Scholar]
  29. Edgar RS, Green EW, Zhao Y, van Ooijen G, Olmedo M. 29.  et al. 2012. Peroxiredoxins are conserved markers of circadian rhythms. Nature 485:459–64 [Google Scholar]
  30. Edwards KD, Anderson PE, Hall A, Salathia NS, Locke JC. 30.  et al. 2006. FLOWERING LOCUS C mediates natural variation in the high-temperature response of the Arabidopsis circadian clock. Plant Cell 18:639–50 [Google Scholar]
  31. Falk A, Feys BJ, Frost LN, Jones JD, Daniels MJ, Parker JE. 31.  1999. EDS1, an essential component of R gene–mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. PNAS 96:3292–97 [Google Scholar]
  32. Fragniere C, Serrano M, Abou-Mansour E, Metraux JP, L'Haridon F. 32.  2011. Salicylic acid and its location in response to biotic and abiotic stress. FEBS Lett 585:1847–52 [Google Scholar]
  33. Fu ZQ, Dong X. 33.  2013. Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 64:839–63 [Google Scholar]
  34. Fu ZQ, Guo M, Jeong BR, Tian F, Elthon TE. 34.  et al. 2007. A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 447:284–88 [Google Scholar]
  35. Gapper C, Dolan L. 35.  2006. Control of plant development by reactive oxygen species. Plant Physiol 141:341–45 [Google Scholar]
  36. Gimenez-Ibanez S, Boter M, Fernández-Barbero G, Chini A, Rathjen JP, Solano R. 36.  2014. The bacterial effector HopX1 targets JAZ transcriptional repressors to activate jasmonate signaling and promote infection in Arabidopsis. PLOS Biol 12:e1001792 [Google Scholar]
  37. Goodspeed D, Chehab EW, Covington MF, Braam J. 37.  2013. Circadian control of jasmonates and salicylates: the clock role in plant defense. Plant Signal. Behav. 8:e23123 [Google Scholar]
  38. Goodspeed D, Chehab EW, Min-Venditti A, Braam J, Covington MF. 38.  2012. Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior. PNAS 109:4674–77 [Google Scholar]
  39. Goodspeed D, Liu JD, Chehab EW, Sheng Z, Francisco M. 39.  et al. 2013. Postharvest circadian entrainment enhances crop pest resistance and phytochemical cycling. Curr. Biol. 23:1235–41 [Google Scholar]
  40. Graf A, Schlereth A, Stitt M, Smith AM. 40.  2010. Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. PNAS 107:9458–63 [Google Scholar]
  41. Green RM, Tingay S, Wang ZY, Tobin EM. 41.  2002. Circadian rhythms confer a higher level of fitness to Arabidopsis plants. Plant Physiol 129:576–84 [Google Scholar]
  42. Greenberg J, Yao N. 42.  2004. The role and regulation of programmed cell death in plant-pathogen interactions. Cell. Microbiol. 6:201–11 [Google Scholar]
  43. Greenham K, Lou P, Puzey JR, Kumar G, Arnevik C. 43.  et al. 2016. Geographic variation of plant circadian clock function in natural and agricultural settings. J. Biol. Rhythms 32:26–34 [Google Scholar]
  44. Greenham K, McClung CR. 44.  2015. Integrating circadian dynamics with physiological processes in plants. Nat. Rev. Genet. 16:598–610 [Google Scholar]
  45. Gutierrez RA, Stokes TL, Thum K, Xu X, Obertello M. 45.  et al. 2008. Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. . PNAS 105:4939–44 [Google Scholar]
  46. Hamdoun S, Liu Z, Gill M, Yao N, Lu H. 46.  2013. Dynamics of defense responses and cell fate change during ArabidopsisPseudomonas syringae interactions. PLOS ONE 8:e83219 [Google Scholar]
  47. Hammond-Kosack KE, Jones JD. 47.  1996. Resistance gene–dependent plant defense responses. Plant Cell 8:1773–91 [Google Scholar]
  48. Hanano S, Domagalska MA, Nagy F, Davis SJ. 48.  2006. Multiple phytohormones influence distinct parameters of the plant circadian clock. Genes Cells 11:1381–92 [Google Scholar]
  49. Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B. 49.  et al. 2000. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290:2110–13 [Google Scholar]
  50. Henriques R, Mas P. 50.  2013. Chromatin remodeling and alternative splicing: pre- and post-transcriptional regulation of the Arabidopsis circadian clock. Semin. Cell Dev. Biol. 24:399–406 [Google Scholar]
  51. Herrera-Vásquez A, Salinas P, Holuigue L. 51.  2015. Salicylic acid and reactive oxygen species interplay in the transcriptional control of defense genes expression. Front. Plant Sci. 6:171 [Google Scholar]
  52. Hevia MA, Canessa P, Muller-Esparza H, Larrondo LF. 52.  2015. A circadian oscillator in the fungus Botrytis cinerea regulates virulence when infecting Arabidopsis thaliana. PNAS 112:8744–49 [Google Scholar]
  53. Hoffman DE, Jonsson P, Bylesjo M, Trygg J, Antti H. 53.  et al. 2010. Changes in diurnal patterns within the Populus transcriptome and metabolome in response to photoperiod variation. Plant Cell Environ 33:1298–313 [Google Scholar]
  54. Hong S, Kim SA, Guerinot ML, McClung CR. 54.  2013. Reciprocal interaction of the circadian clock with the iron homeostasis network in Arabidopsis. Plant Physiol 161:893–903 [Google Scholar]
  55. Hsu PY, Devisetty UK, Harmer SL. 55.  2013. Accurate timekeeping is controlled by a cycling activator in Arabidopsis. . eLife 2:e00473 [Google Scholar]
  56. Hsu PY, Harmer SL. 56.  2014. Wheels within wheels: the plant circadian system. Trends Plant Sci 19:240–49 [Google Scholar]
  57. Hua J. 57.  2013. Modulation of plant immunity by light, circadian rhythm, and temperature. Curr. Opin. Plant Biol. 16:406–13 [Google Scholar]
  58. Huang H, Nusinow DA. 58.  2016. Into the evening: complex interactions in the Arabidopsis circadian clock. Trends Genet 32:674–86 [Google Scholar]
  59. Huang W, Perez-Garcia P, Pokhilko A, Millar AJ, Antoshechkin I. 59.  et al. 2012. Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science 336:75–79 [Google Scholar]
  60. Ingle RA, Stoker C, Stone W, Adams N, Smith R. 60.  et al. 2015. Jasmonate signalling drives time-of-day differences in susceptibility of Arabidopsis to the fungal pathogen Botrytis cinerea. Plant J. 84:937–48 [Google Scholar]
  61. Izawa T, Mihara M, Suzuki Y, Gupta M, Itoh H. 61.  et al. 2011. Os-GIGANTEA confers robust diurnal rhythms on the global transcriptome of rice in the field. Plant Cell 23:1741–55 [Google Scholar]
  62. Jambunathan N, Siani JM, McNellis TW. 62.  2001. A humidity-sensitive Arabidopsis copine mutant exhibits precocious cell death and increased disease resistance. Plant Cell 13:2225–40 [Google Scholar]
  63. Jiang S, Yao J, Ma KW, Zhou H, Song J. 63.  et al. 2013. Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors. PLOS Pathog 9:e1003715 [Google Scholar]
  64. Karpinski S, Gabrys H, Mateo A, Karpinska B, Mullineaux PM. 64.  2003. Light perception in plant disease defence signalling. Curr. Opin. Plant Biol. 6:390–96 [Google Scholar]
  65. Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA. 65.  2008. COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. PNAS 105:7100–5 [Google Scholar]
  66. Kim JS, Jung HJ, Lee HJ, Kim KA, Goh CH. 66.  et al. 2008. Glycine-rich RNA-binding protein 7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana. . Plant J. 55:455–66 [Google Scholar]
  67. Kim S, Singh P, Park J, Park S, Friedman A. 67.  et al. 2011. Genetic and molecular characterization of a blue light photoreceptor MGWC-1 in Magnaporthe oryzae. . Fungal Genet. Biol. 48:400–7 [Google Scholar]
  68. Kim WY, Fujiwara S, Suh SS, Kim J, Kim Y. 68.  et al. 2007. ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449:356–60 [Google Scholar]
  69. Kinmonth-Schultz HA, Golembeski GS, Imaizumi T. 69.  2013. Circadian clock–regulated physiological outputs: dynamic responses in nature. Semin. Cell Dev. Biol. 24:407–13 [Google Scholar]
  70. Korneli C, Danisman S, Staiger D. 70.  2014. Differential control of pre-invasive and post-invasive antibacterial defense by the Arabidopsis circadian clock. Plant Cell Physiol 55:1613–22 [Google Scholar]
  71. Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G. 71.  2004. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16:3496–507 [Google Scholar]
  72. Kurepa J, Smalle J, Van Montagu M, Inze D. 72.  1998. Oxidative stress tolerance and longevity in Arabidopsis: the late-flowering mutant gigantea is tolerant to paraquat. Plant J. 14:759–64 [Google Scholar]
  73. Lai AG, Doherty CJ, Mueller-Roeber B, Kay SA, Schippers JH, Dijkwel PP. 73.  2012. CIRCADIAN CLOCK-ASSOCIATED 1 regulates ROS homeostasis and oxidative stress responses. PNAS 109:17129–34 [Google Scholar]
  74. Lee K, Singh P, Chung W-C, Ash J, Kim TS. 74.  et al. 2006. Light regulation of asexual development in the rice blast fungus, Magnaporthe oryzae. Fungal Genet. Biol. 43:694–706 [Google Scholar]
  75. Lindow SE, Brandl MT. 75.  2003. Microbiology of the phyllosphere. Appl. Environ. Microbiol. 69:1875–83 [Google Scholar]
  76. Liu T, Carlsson J, Takeuchi T, Newton L, Farre EM. 76.  2013. Direct regulation of abiotic responses by the Arabidopsis circadian clock component PRR7. Plant J 76:101–14 [Google Scholar]
  77. Liu TL, Newton L, Liu MJ, Shiu SH, Farre EM. 77.  2016. A G-box-like motif is necessary for transcriptional regulation by circadian pseudo-response regulators in Arabidopsis. . Plant Physiol. 170:528–39 [Google Scholar]
  78. Lorrain S, Vailleau F, Balague C, Roby D. 78.  2003. Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants?. Trends Plant Sci 8:263–71 [Google Scholar]
  79. Lu H. 79.  2009. Dissection of salicylic acid–mediated defense signaling networks. Plant Signal. Behav. 4:713–17 [Google Scholar]
  80. Lu H, Rate DN, Song JT, Greenberg JT. 80.  2003. ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response. Plant Cell 15:2408–20 [Google Scholar]
  81. Marcolino-Gomes J, Rodrigues FA, Fuganti-Pagliarini R, Bendix C, Nakayama TJ. 81.  et al. 2014. Diurnal oscillations of soybean circadian clock and drought responsive genes. PLOS ONE 9:e86402 [Google Scholar]
  82. Mas P, Kim WY, Somers DE, Kay SA. 82.  2003. Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. . Nature 426:567–70 [Google Scholar]
  83. Mateo A, Muhlenbock P, Rusterucci C, Chang CC, Miszalski Z. 83.  et al. 2004. LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol 136:2818–30 [Google Scholar]
  84. Matsuzaki J, Kawahara Y, Izawa T. 84.  2015. Punctual transcriptional regulation by the rice circadian clock under fluctuating field conditions. Plant Cell 27:633–48 [Google Scholar]
  85. McClung CR. 85.  2013. Beyond Arabidopsis: the circadian clock in non-model plant species. Semin. Cell Dev. Biol. 24:430–36 [Google Scholar]
  86. McDonald MJ, Rosbash M. 86.  2001. Microarray analysis and organization of circadian gene expression in Drosophila. . Cell 107:567–78 [Google Scholar]
  87. McDowell JM, Simon SA. 87.  2006. Recent insights into R gene evolution. Mol. Plant Pathol. 7:437–48 [Google Scholar]
  88. Meireles-Filho AC, da S Rivas GB, Gesto JS, Machado RC, Britto C. 88.  et al. 2006. The biological clock of an hematophagous insect: locomotor activity rhythms, circadian expression and downregulation after a blood meal. FEBS Lett 580:2–8 [Google Scholar]
  89. Melotto M, Underwood W, Koczan J, Nomura K, He SY. 89.  2006. Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–80 [Google Scholar]
  90. Mendgen K, Hahn M, Deising H. 90.  1996. Morphogenesis and mechanisms of penetration by plant pathogenic fungi. Annu. Rev. Phytopathol. 34:367–86 [Google Scholar]
  91. Menet JS, Pescatore S, Rosbash M. 91.  2014. CLOCK:BMAL1 is a pioneer-like transcription factor. Genes Dev 28:8–13 [Google Scholar]
  92. Michael TP, McClung CR. 92.  2003. Enhancer trapping reveals widespread circadian clock transcriptional control in Arabidopsis. . Plant Physiol. 132:629–39 [Google Scholar]
  93. Michael TP, Mockler TC, Breton G, McEntee C, Byer A. 93.  et al. 2008. Network discovery pipeline elucidates conserved time-of-day-specific cis-regulatory modules. PLOS Genet 4:e14 [Google Scholar]
  94. Michael TP, Salome PA, Yu HJ, Spencer TR, Sharp EL. 94.  et al. 2003. Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302:1049–53 [Google Scholar]
  95. Miller M, Song Q, Shi X, Juenger TE, Chen ZJ. 95.  2015. Natural variation in timing of stress-responsive gene expression predicts heterosis in intraspecific hybrids of Arabidopsis. . Nat. Commun. 6:7453 [Google Scholar]
  96. Montenegro-Montero A, Canessa P, Larrondo LF. 96.  2015. Around the fungal clock: recent advances in the molecular study of circadian clocks in Neurospora and other fungi. Adv. Genet. 92:107–84 [Google Scholar]
  97. Mou Z, Fan W, Dong X. 97.  2003. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–44 [Google Scholar]
  98. Muller NA, Wijnen CL, Srinivasan A, Ryngajllo M, Ofner I. 98.  et al. 2016. Domestication selected for deceleration of the circadian clock in cultivated tomato. Nat. Genet. 48:89–93 [Google Scholar]
  99. Nagel DH, Doherty CJ, Pruneda-Paz JL, Schmitz RJ, Ecker JR, Kay SA. 99.  2015. Genome-wide identification of CCA1 targets uncovers an expanded clock network in Arabidopsis. . PNAS 112:E4802–10 [Google Scholar]
  100. Nakamichi N, Kiba T, Kamioka M, Suzuki T, Yamashino T. 100.  et al. 2012. Transcriptional repressor PRR5 directly regulates clock-output pathways. PNAS 109:17123–28 [Google Scholar]
  101. Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N. 101.  et al. 2006. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–39 [Google Scholar]
  102. Nawrath C, Heck S, Parinthawong N, Metraux JP. 102.  2002. EDS5, an essential component of salicylic acid–dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell 14:275–86 [Google Scholar]
  103. Nawrath C, Metraux JP. 103.  1999. Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11:1393–404 [Google Scholar]
  104. Ng G, Seabolt S, Zhang C, Salimian S, Watkins TA, Lu H. 104.  2011. Genetic dissection of salicylic acid–mediated defense signaling networks in Arabidopsis. Genetics 189:851–59 [Google Scholar]
  105. Ni Z, Kim ED, Ha M, Lackey E, Liu J. 105.  et al. 2009. Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457:327–31 [Google Scholar]
  106. Nicaise V, Joe A, Jeong BR, Korneli C, Boutrot F. 106.  et al. 2013. Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. EMBO J 32:701–12 [Google Scholar]
  107. Nohales MA, Kay SA. 107.  2016. Molecular mechanisms at the core of the plant circadian oscillator. Nat. Struct. Mol. Biol. 23:1061–69 [Google Scholar]
  108. Palaksha, Kouser S, Shakunthala V. 108.  2013. Circadian regulation of oviposition rhythm in Drosophilaagumbensis and Drosophila nagarholensis (Diptera). Biol. Rhythm Res. 44:325–32 [Google Scholar]
  109. Panda S, Antoch MP, Miller BH, Su AI, Schook AB. 109.  et al. 2002. Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109:307–20 [Google Scholar]
  110. Paulitz T. 110.  1996. Diurnal release of ascospores by Gibberella zeae in inoculated wheat plots. Plant Dis 80:674–78 [Google Scholar]
  111. Rawat R, Schwartz J, Jones MA, Sairanen I, Cheng Y. 111.  et al. 2009. REVEILLE1, a Myb-like transcription factor, integrates the circadian clock and auxin pathways. PNAS 106:16883–88 [Google Scholar]
  112. Robert-Seilaniantz A, Grant M, Jones JD. 112.  2011. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu. Rev. Phytopathol. 49:317–43 [Google Scholar]
  113. Roden LC, Ingle RA. 113.  2009. Lights, rhythms, infection: the role of light and the circadian clock in determining the outcome of plant-pathogen interactions. Plant Cell 21:2546–52 [Google Scholar]
  114. Rodriguez MC, Petersen M, Mundy J. 114.  2010. Mitogen-activated protein kinase signaling in plants. Annu. Rev. Plant Biol. 61:621–49 [Google Scholar]
  115. Rosato E, Tauber E, Kyriacou CP. 115.  2006. Molecular genetics of the fruit-fly circadian clock. Eur. J. Hum. Genet. 14:729–38 [Google Scholar]
  116. Rugnone ML, Faigon Soverna A, Sanchez SE, Schlaen RG, Hernando CE. 116.  et al. 2013. LNK genes integrate light and clock signaling networks at the core of the Arabidopsis oscillator. PNAS 110:12120–25 [Google Scholar]
  117. Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD. 117.  1996. Systemic acquired resistance. Plant Cell 8:1809–19 [Google Scholar]
  118. Salichos L, Rokas A. 118.  2010. The diversity and evolution of circadian clock proteins in fungi. Mycologia 102:269–78 [Google Scholar]
  119. Salomé PA, McClung CR. 119.  2005. What makes the Arabidopsis clock tick on time? A review on entrainment. Plant Cell Environ 28:21–38 [Google Scholar]
  120. Scheiermann C, Kunisaki Y, Frenette PS. 120.  2013. Circadian control of the immune system. Nat. Rev. Immunol. 13:190–98 [Google Scholar]
  121. Seo PJ, Mas P. 121.  2014. Multiple layers of posttranslational regulation refine circadian clock activity in Arabidopsis. . Plant Cell 26:79–87 [Google Scholar]
  122. Serrano M, Wang B, Aryal B, Garcion C, Abou-Mansour E. 122.  et al. 2013. Export of salicylic acid from the chloroplast requires the multidrug and toxin extrusion–like transporter EDS5. Plant Physiol 162:1815–21 [Google Scholar]
  123. Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G. 123.  et al. 2010. Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468:400–5 [Google Scholar]
  124. Shin J, Heidrich K, Sanchez-Villarreal A, Parker JE, Davis SJ. 124.  2012. TIME FOR COFFEE represses accumulation of the MYC2 transcription factor to provide time-of-day regulation of jasmonate signaling in Arabidopsis. . Plant Cell 24:2470–82 [Google Scholar]
  125. Somers DE, Webb AA, Pearson M, Kay SA. 125.  1998. The short-period mutant, toc1-1, alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana. Development 125:485–94 [Google Scholar]
  126. Spoel SH, Dong X. 126.  2008. Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe 3:348–51 [Google Scholar]
  127. Spoel SH, van Ooijen G. 127.  2014. Circadian redox signaling in plant immunity and abiotic stress. Antioxid. Redox Signal. 20:3024–39 [Google Scholar]
  128. Staiger D, Shin J, Johansson M, Davis SJ. 128.  2013. The circadian clock goes genomic. Genome Biol 14:208 [Google Scholar]
  129. Staiger D, Zecca L, Wieczorek Kirk DA, Apel K, Eckstein L. 129.  2003. The circadian clock regulated RNA-binding protein AtGRP7 autoregulates its expression by influencing alternative splicing of its own pre-mRNA. Plant J 33:361–71 [Google Scholar]
  130. Strawn MA, Marr SK, Inoue K, Inada N, Zubieta C, Wildermuth MC. 130.  2007. Arabidopsis isochorismate synthase functional in pathogen-induced salicylate biosynthesis exhibits properties consistent with a role in diverse stress responses. J. Biol. Chem. 282:5919–33 [Google Scholar]
  131. Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Dong X. 131.  2008. Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–56 [Google Scholar]
  132. Tanaka S, Han X, Kahmann R. 132.  2015. Microbial effectors target multiple steps in the salicylic acid production and signaling pathway. Front. Plant Sci. 6:349 [Google Scholar]
  133. Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS. 133.  et al. 2003. Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317–30 [Google Scholar]
  134. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A. 134.  et al. 2007. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661–65 [Google Scholar]
  135. Torres MA, Dangl JL, Jones JD. 135.  2002. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. PNAS 99:517–22 [Google Scholar]
  136. Torres MA, Jones JD, Dangl JL. 136.  2005. Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. . Nat. Genet. 37:1130–4 [Google Scholar]
  137. Toruno TY, Stergiopoulos I, Coaker G. 137.  2016. Plant-pathogen effectors: cellular probes interfering with plant defenses in spatial and temporal manners. Annu. Rev. Phytopathol. 54:419–41 [Google Scholar]
  138. Tsuda K, Sato M, Glazebrook J, Cohen JD, Katagiri F. 138.  2008. Interplay between MAMP-triggered and SA-mediated defense responses. Plant J 53:763–75 [Google Scholar]
  139. Underwood W, Melotto M, He SY. 139.  2007. Role of plant stomata in bacterial invasion. Cell. Microbiol. 9:1621–29 [Google Scholar]
  140. Wang GF, Seabolt S, Hamdoun S, Ng G, Park J, Lu H. 140.  2011. Multiple roles of WIN3 in regulating disease resistance, cell death, and flowering time in Arabidopsis. . Plant Physiol. 156:1508–19 [Google Scholar]
  141. Wang GY, Shi JL, Ng G, Battle SL, Zhang C, Lu H. 141.  2011. Circadian clock–regulated phosphate transporter PHT4;1 plays an important role in Arabidopsis defense. Mol. Plant 4:516–26 [Google Scholar]
  142. Wang L, Tsuda K, Truman W, Sato M, Nguyen LV. 142.  et al. 2011. CBP60g and SARD1 play partially redundant critical roles in salicylic acid signaling. Plant J 67:1029–41 [Google Scholar]
  143. Wang W, Barnaby JY, Tada Y, Li H, Tor M. 143.  et al. 2011. Timing of plant immune responses by a central circadian regulator. Nature 470:110–14 [Google Scholar]
  144. Webb AA. 144.  2003. The physiology of circadian rhythms in plants. New Phytol 160:281–303 [Google Scholar]
  145. Wildermuth MC, Dewdney J, Wu G, Ausubel FM. 145.  2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–65 [Google Scholar]
  146. Williamson B, Tudzynski B, Tudzynski P, van Kan JA. 146.  2007. Botrytis cinerea: the cause of grey mould disease. Mol. Plant Pathol. 8:561–80 [Google Scholar]
  147. Windram O, Madhou P, McHattie S, Hill C, Hickman R. 147.  et al. 2012. Arabidopsis defense against Botrytis cinerea: chronology and regulation deciphered by high-resolution temporal transcriptomic analysis. Plant Cell 24:3530–57 [Google Scholar]
  148. Woelfle MA, Johnson CH. 148.  2006. No promoter left behind: global circadian gene expression in cyanobacteria. J. Biol. Rhythms 21:419–31 [Google Scholar]
  149. Wu Y, Zhang D, Chu JY, Boyle P, Wang Y. 149.  et al. 2012. The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 1:639–47 [Google Scholar]
  150. Xia XJ, Zhou YH, Shi K, Zhou J, Foyer CH, Yu JQ. 150.  2015. Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J. Exp. Bot. 66:2839–56 [Google Scholar]
  151. Xie Q, Wang P, Liu X, Yuan L, Wang L. 151.  et al. 2014. LNK1 and LNK2 are transcriptional coactivators in the Arabidopsis circadian oscillator. Plant Cell 26:2843–57 [Google Scholar]
  152. Yamasaki K, Motomura Y, Yagi Y, Nomura H, Kikuchi S. 152.  et al. 2013. Chloroplast envelope localization of EDS5, an essential factor for salicylic acid biosynthesis in Arabidopsis thaliana. . Plant Signal. Behav. 8:e23603 [Google Scholar]
  153. Yan S, Dong X. 153.  2014. Perception of the plant immune signal salicylic acid. Curr. Opin. Plant Biol. 20:64–68 [Google Scholar]
  154. Yoshioka K, Kachroo P, Tsui F, Sharma SB, Shah J, Klessig DF. 154.  2001. Environmentally sensitive, SA-dependent defense responses in the cpr22 mutant of Arabidopsis. . Plant J. 26:447–59 [Google Scholar]
  155. Zhang C, Xie Q, Anderson RG, Ng G, Seitz NC. 155.  et al. 2013. Crosstalk between the circadian clock and innate immunity in Arabidopsis. . PLOS Pathog. 9:e1003370 [Google Scholar]
  156. Zhang Y, Xu S, Ding P, Wang D, Cheng YT. 156.  et al. 2010. Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. PNAS 107:18220–25 [Google Scholar]
  157. Zheng XY, Zhou M, Yoo H, Pruneda-Paz JL, Spivey NW. 157.  et al. 2015. Spatial and temporal regulation of biosynthesis of the plant immune signal salicylic acid. PNAS 112:9166–73 [Google Scholar]
  158. Zhou M, Wang W, Karapetyan S, Mwimba M, Marques J. 158.  et al. 2015. Redox rhythm reinforces the circadian clock to gate immune response. Nature 523:472–76 [Google Scholar]
  159. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD. 159.  et al. 2004. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–67 [Google Scholar]
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