1932

Abstract

Chloroplasts are key players in plant immune signaling, contributing to not only de novo synthesis of defensive phytohormones but also the generation of reactive oxygen and nitrogen species following activation of pattern recognition receptors or resistance (R) proteins. The local hypersensitive response (HR) elicited by R proteins is underpinned by chloroplast-generated reactive oxygen species. HR-induced lipid peroxidation generates important chloroplast-derived signaling lipids essential to the establishment of systemic immunity. As a consequence of this pivotal role in immunity, pathogens deploy effector complements that directly or indirectly target chloroplasts to attenuate chloroplast immunity (CI). Our review summarizes the current knowledge of CI signaling and highlights common pathogen chloroplast targets and virulence strategies. We address emerging insights into chloroplast retrograde signaling in immune responses and gaps in our knowledge, including the importance of understanding chloroplast heterogeneity and chloroplast involvement in intraorganellular interactions in host immunity.

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2021-08-25
2024-04-16
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Literature Cited

  1. 1. 
    Adie BA, Perez-Perez J, Perez-Perez MM, Godoy M, Sanchez-Serrano JJ et al. 2007. ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19:1665–81
    [Google Scholar]
  2. 2. 
    Akimoto-Tomiyama C, Tanabe S, Kajiwara H, Minami E, Ochiai H. 2018. Loss of chloroplast-localized protein phosphatase 2Cs in Arabidopsis thaliana leads to enhancement of plant immunity and resistance to Xanthomonas campestris pv. campestris infection. Mol. Plant Pathol. 19:1184–95
    [Google Scholar]
  3. 3. 
    Andersson MX, Hamberg M, Kourtchenko O, Brunnstrom A, McPhail KL et al. 2006. Oxylipin profiling of the hypersensitive response in Arabidopsis thaliana. Formation of a novel oxo-phytodienoic acid-containing galactolipid, arabidopside E. J. Biol. Chem. 281:31528–37
    [Google Scholar]
  4. 4. 
    Awai K, Maréchal E, Block MA, Brun D, Masuda T et al. 2001. Two types of MGDG synthase genes, found widely in both 16:3 and 18:3 plants, differentially mediate galactolipid syntheses in photosynthetic and nonphotosynthetic tissues in Arabidopsis thaliana. PNAS 98:10960–65
    [Google Scholar]
  5. 5. 
    Ballare CL. 2014. Light regulation of plant defense. Annu. Rev. Plant Biol. 65:335–63
    [Google Scholar]
  6. 6. 
    Bechtold U, Karpinski S, Mullineaux PM. 2005. The influence of the light environment and photosynthesis on oxidative signalling responses in plant–biotrophic pathogen interactions. Plant Cell Environ 28:1046–55
    [Google Scholar]
  7. 7. 
    Beckers GJ, Jaskiewicz M, Liu Y, Underwood WR, He SY et al. 2009. Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21:944–53
    [Google Scholar]
  8. 8. 
    Beckova M, Gardian Z, Yu J, Konik P, Nixon PJ, Komenda J. 2017. Association of Psb28 and Psb27 proteins with PSII-PSI supercomplexes upon exposure of Synechocystis sp. PCC 6803 to High Light. Mol. Plant 10:62–72
    [Google Scholar]
  9. 9. 
    Bennett M, Mehta M, Grant M. 2005. Biophoton imaging: a nondestructive method for assaying R gene responses. Mol. Plant-Microbe Interact. 18:95–102
    [Google Scholar]
  10. 10. 
    Berger S, Benediktyova Z, Matous K, Bonfig K, Mueller MJ et al. 2007. Visualization of dynamics of plant-pathogen interaction by novel combination of chlorophyll fluorescence imaging and statistical analysis: differential effects of virulent and avirulent strains of P. syringae and of oxylipins on A. thaliana. J. Exp. Bot. 58:797–806
    [Google Scholar]
  11. 11. 
    Bhat S, Folimonova SY, Cole AB, Ballard KD, Lei Z et al. 2013. Influence of host chloroplast proteins on Tobacco mosaic virus accumulation and intercellular movement. Plant Physiol 161:134–47
    [Google Scholar]
  12. 12. 
    Bienert GP, Chaumont F. 2014. Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim. Biophys. Acta 1840:1596–604
    [Google Scholar]
  13. 13. 
    Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, DeLucia EH. 2010. Biotic stress globally downregulates photosynthesis genes. Plant Cell Environ 33:1597–613
    [Google Scholar]
  14. 14. 
    Brunkard JO, Burch-Smith TM. 2018. Ties that bind: the integration of plastid signalling pathways in plant cell metabolism. Essays Biochem 62:95–107
    [Google Scholar]
  15. 15. 
    Burger M, Chory J. 2019. Stressed out about hormones: how plants orchestrate immunity. Cell Host Microbe 26:163–72
    [Google Scholar]
  16. 16. 
    Caplan JL, Kumar AS, Park E, Padmanabhan MS, Hoban K et al. 2015. Chloroplast stromules function during innate immunity. Dev. Cell 34:45–57
    [Google Scholar]
  17. 17. 
    Caplan JL, Mamillapalli P, Burch-Smith TM, Czymmek K, Dinesh-Kumar SP. 2008. Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. Cell 132:449–62
    [Google Scholar]
  18. 18. 
    Carella P, Isaacs M, Cameron RK. 2015. Plasmodesmata-located protein overexpression negatively impacts the manifestation of systemic acquired resistance and the long-distance movement of Defective in Induced Resistance1 in Arabidopsis. Plant Biol 17:395–401
    [Google Scholar]
  19. 19. 
    Cecchini NM, Steffes K, Schlappi MR, Gifford AN, Greenberg JT. 2015. Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming. Nat. Commun. 6:7658
    [Google Scholar]
  20. 20. 
    Chan KX, Phua SY, Crisp P, McQuinn R, Pogson BJ. 2016. Learning the languages of the chloroplast: retrograde signaling and beyond. Annu. Rev. Plant Biol. 67:25–53
    [Google Scholar]
  21. 21. 
    Chanda B, Xia Y, Mandal MK, Yu K, Sekine K et al. 2011. Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat. Genet. 43:421–27
    [Google Scholar]
  22. 22. 
    Chen YC, Holmes E, Rajniak J, Kim J-G, Tang S et al. 2018. N-hydroxy-pipecolic acid is a mobile metabolite that induces systemic disease resistance in Arabidopsis. PNAS 115:E4920–29
    [Google Scholar]
  23. 23. 
    Cohen SP, Leach JE. 2019. Abiotic and biotic stresses induce a core transcriptome response in rice. Sci. Rep. 9:6273
    [Google Scholar]
  24. 24. 
    Crawford NM. 2006. Mechanisms for nitric oxide synthesis in plants. J. Exp. Bot. 57:471–78
    [Google Scholar]
  25. 25. 
    Cui H, Gobbato E, Kracher B, Qiu J, Bautor J, Parker JE. 2017. A core function of EDS1 with PAD4 is to protect the salicylic acid defense sector in Arabidopsis immunity. New Phytol 213:1802–17
    [Google Scholar]
  26. 26. 
    de Souza A, Wang JZ, Dehesh K. 2017. Retrograde signals: integrators of interorganellar communication and orchestrators of plant development. Annu. Rev. Plant Biol. 68:85–108
    [Google Scholar]
  27. 27. 
    de Torres Zabala M, Bennett MH, Truman WH, Grant MR 2009. Antagonism between salicylic and abscisic acid reflects early host-pathogen conflict and moulds plant defence responses. Plant J 59:3375–86
    [Google Scholar]
  28. 28. 
    de Torres Zabala M, Littlejohn G, Jayaraman S, Studholme D, Bailey T et al. 2015. Chloroplasts play a central role in plant defence and are targeted by pathogen effectors. Nat Plants 1:15074
    [Google Scholar]
  29. 29. 
    de Torres-Zabala M, Truman W, Bennett MH, Lafforgue G, Mansfield JW et al. 2007. Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J 26:1434–43
    [Google Scholar]
  30. 30. 
    de Vos M, Kriksunov KL, Jander G. 2008. Indole-3-acetonitrile production from indole glucosinolates deters oviposition by Pieris rapae. Plant Physiol 146:916–26
    [Google Scholar]
  31. 31. 
    Desveaux D, Despres C, Joyeux A, Subramaniam R, Brisson N. 2000. PBF-2 is a novel single-stranded DNA binding factor implicated in PR-10a gene activation in potato. Plant Cell 12:1477–89
    [Google Scholar]
  32. 32. 
    Desveaux D, Subramaniam R, Despres C, Mess JN, Levesque C et al. 2004. A “Whirly” transcription factor is required for salicylic acid-dependent disease resistance in Arabidopsis. Dev. Cell 6:229–40
    [Google Scholar]
  33. 33. 
    Ding P, Ding Y. 2020. Stories of salicylic acid: a plant defense hormone. Trends Plant Sci 25:549–65
    [Google Scholar]
  34. 34. 
    Ding P, Rekhter D, Ding Y, Feussner K, Busta L et al. 2016. Characterization of a pipecolic acid biosynthesis pathway required for systemic acquired resistance. Plant Cell 28:2603–15
    [Google Scholar]
  35. 35. 
    Erickson JL, Adlung N, Lampe C, Bonas U, Schattat MH. 2018. The Xanthomonas effector XopL uncovers the role of microtubules in stromule extension and dynamics in Nicotiana benthamiana. Plant J 93:856–70
    [Google Scholar]
  36. 36. 
    Estavillo GM, Crisp PA, Pornsiriwong W, Wirtz M, Collinge D et al. 2011. Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23:3992–4012
    [Google Scholar]
  37. 37. 
    Exposito-Rodriguez M, Laissue PP, Yvon-Durocher G, Smirnoff N, Mullineaux PM. 2017. Photosynthesis-dependent H2O2 transfer from chloroplasts to nuclei provides a high-light signalling mechanism. Nat. Commun. 8:49
    [Google Scholar]
  38. 38. 
    Faris JD, Zhang Z, Lu H, Lu S, Reddy L et al. 2010. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. PNAS 107:13544–49
    [Google Scholar]
  39. 39. 
    Fernandez JC, Burch-Smith TM. 2019. Chloroplasts as mediators of plant biotic interactions over short and long distances. Curr. Opin. Plant Biol. 50:148–55
    [Google Scholar]
  40. 40. 
    Foyer CH. 2018. Reactive oxygen species, oxidative signaling and the regulation of photosynthesis. Environ. Exp. Bot. 154:134–42
    [Google Scholar]
  41. 41. 
    Gallie DR, Chen Z. 2019. Chloroplast-localized iron superoxide dismutases FSD2 and FSD3 are functionally distinct in Arabidopsis. PLOS ONE 14:e0220078
    [Google Scholar]
  42. 42. 
    Ganusova EE, Rice JH, Carlew TS, Patel A, Perrodin-Njoku E et al. 2017. Altered expression of a chloroplast protein affects the outcome of virus and nematode infection. Mol. Plant-Microbe Interact. 30:478–88
    [Google Scholar]
  43. 43. 
    Gao Q-M, Yu K, Xia Y, Shine MB, Wang C et al. 2014. Mono- and digalactosyldiacylglycerol lipids function nonredundantly to regulate systemic acquired resistance in plants. Cell Rep 9:1681–91
    [Google Scholar]
  44. 44. 
    Garcia-Molina A, Altmann M, Alkofer A, Epple PM, Dangl JL, Falter-Braun P. 2017. LSU network hubs integrate abiotic and biotic stress responses via interaction with the superoxide dismutase FSD2. J. Exp. Bot. 68:1185–97
    [Google Scholar]
  45. 45. 
    Gohre V, Jones AM, Sklenar J, Robatzek S, Weber AP. 2012. Molecular crosstalk between PAMP-triggered immunity and photosynthesis. Mol. Plant-Microbe Interact. 25:1083–92
    [Google Scholar]
  46. 46. 
    Guirimand G, Guihur A, Perello C, Phillips M, Mahroug S et al. 2020. Cellular and subcellular compartmentation of the 2C-methyl-D-erythritol 4-phosphate pathway in the Madagascar periwinkle. Plants 9:4462
    [Google Scholar]
  47. 47. 
    Guo H, Feng P, Chi W, Sun X, Xu X et al. 2016. Plastid-nucleus communication involves calcium-modulated MAPK signalling. Nat. Commun 7:12173
    [Google Scholar]
  48. 48. 
    Hamel LP, Sekine KT, Wallon T, Sugiwaka Y, Kobayashi K, Moffett P. 2016. The chloroplastic protein THF1 interacts with the coiled-coil domain of the disease resistance protein N′ and regulates light-dependent cell death. Plant Physiol 171:658–74
    [Google Scholar]
  49. 49. 
    Hartmann M, Kim D, Bernsdorff F, Ajami-Rashidi Z, Scholten N et al. 2017. Biochemical principles and functional aspects of pipecolic acid biosynthesis in immunity. Plant Physiol 174:124–53
    [Google Scholar]
  50. 50. 
    Hartmann M, Zeier T, Bernsdorff F, Reichel-Deland V, Kim D et al. 2018. Flavin monooxygenase-generated N-hydroxypipecolic acid is a critical element of plant systemic immunity. Cell 173:456–69.e16
    [Google Scholar]
  51. 51. 
    Havaux M. 2014. Carotenoid oxidation products as stress signals in plants. Plant J 79:597–606
    [Google Scholar]
  52. 52. 
    Havaux M, Triantaphylides C, Genty B. 2006. Autoluminescence imaging: a non-invasive tool for mapping oxidative stress. Trends Plant Sci 11:480–84
    [Google Scholar]
  53. 53. 
    Henfling J, Bostock R, Kuc J. 1980. Effect of abscisic acid on rishitin and lubimin accumulation and resistance to Phytophthora infestans and Cladosporium cucumerinum in potato tuber tissue slices. Phytopathology 70:1074–78
    [Google Scholar]
  54. 54. 
    Huang W, Chen Q, Zhu Y, Hu F, Zhang L et al. 2013. Arabidopsis thylakoid formation 1 is a critical regulator for dynamics of PSII-LHCII complexes in leaf senescence and excess light. Mol. Plant 6:1673–91
    [Google Scholar]
  55. 55. 
    Isemer R, Mulisch M, Schafer A, Kirchner S, Koop HU, Krupinska K. 2012. Recombinant Whirly1 translocates from transplastomic chloroplasts to the nucleus. FEBS Lett 586:85–88
    [Google Scholar]
  56. 56. 
    Jiang C-J, Shimono M, Maeda S, Inoue H, Mori M et al. 2009. Suppression of the rice fatty-acid desaturase gene OsSSI2 enhances resistance to blast and leaf blight diseases in rice. Mol. Plant-Microbe Interact. 22:820–29
    [Google Scholar]
  57. 57. 
    Jones JD, Dangl JL. 2006. The plant immune system. Nature 444:323–29
    [Google Scholar]
  58. 58. 
    Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT. 2009. Priming in systemic plant immunity. Science 324:89–91
    [Google Scholar]
  59. 59. 
    Kachroo A, Fu D-Q, Havens W, Navarre D, Kachroo P, Ghabrial SA. 2008. An oleic acid–mediated pathway induces constitutive defense signaling and enhanced resistance to multiple pathogens in soybean. Mol. Plant-Microbe Interact. 21:564–75
    [Google Scholar]
  60. 60. 
    Kachroo A, Kachroo P. 2020. Mobile signals in systemic acquired resistance. Curr. Opin. Plant Biol. 58:41–47
    [Google Scholar]
  61. 61. 
    Kachroo A, Venugopal SC, Lapchyk L, Falcone D, Hildebrand D, Kachroo P 2004. Oleic acid levels regulated by glycerolipid metabolism modulate defense gene expression in Arabidopsis. PNAS 101:5152–57
    [Google Scholar]
  62. 62. 
    Kachroo P, Kachroo A, Lapchyk L, Hildebrand D, Klessig DF. 2003. Restoration of defective cross talk in ssi2 mutants: role of salicylic acid, jasmonic acid, and fatty acids in SSI2-mediated signaling. Mol. Plant-Microbe Interact. 16:1022–29
    [Google Scholar]
  63. 63. 
    Kachroo P, Liu H, Kachroo A. 2020. Salicylic acid: transport and long-distance immune signaling. Curr. Opin. Virol. 42:53–57
    [Google Scholar]
  64. 64. 
    Kachroo P, Shanklin J, Shah J, Whittle EJ, Klessig DF 2001. A fatty acid desaturase modulates the activation of defense signaling pathways in plants. PNAS 98:9448–53
    [Google Scholar]
  65. 65. 
    Kachroo P, Venugopal SC, Navarre DA, Lapchyk L, Kachroo A. 2005. Role of salicylic acid and fatty acid desaturation pathways in ssi2-mediated signaling. Plant Physiol 139:1717–35
    [Google Scholar]
  66. 66. 
    Kang L, Li J, Zhao T, Xiao F, Tang X et al. 2003. Interplay of the Arabidopsis nonhost resistance gene NHO1 with bacterial virulence. PNAS 100:3519–24
    [Google Scholar]
  67. 67. 
    Krause K, Kilbienski I, Mulisch M, Rodiger A, Schafer A, Krupinska K. 2005. DNA-binding proteins of the Whirly family in Arabidopsis thaliana are targeted to the organelles. FEBS Lett 579:3707–12
    [Google Scholar]
  68. 68. 
    Kumar AS, Park E, Nedo A, Alqarni A, Ren L et al. 2018. Stromule extension along microtubules coordinated with actin-mediated anchoring guides perinuclear chloroplast movement during innate immunity. eLife 7:e23625
    [Google Scholar]
  69. 69. 
    Kuzniak E, Kopczewski T. 2020. The chloroplast reactive oxygen species-redox system in plant immunity and disease. Front. . Plant Sci 11:572686
    [Google Scholar]
  70. 70. 
    Lee J-Y, Wang X, Cui W, Sager R, Modla S et al. 2011. A plasmodesmata-localized protein mediates crosstalk between cell-to-cell communication and innate immunity in Arabidopsis. Plant Cell 23:3353–73
    [Google Scholar]
  71. 71. 
    Lemos M, Xiao Y, Bjornson M, Wang JZ, Hicks D et al. 2016. The plastidial retrograde signal methyl erythritol cyclopyrophosphate is a regulator of salicylic acid and jasmonic acid crosstalk. J. Exp. Bot. 67:1557–66
    [Google Scholar]
  72. 72. 
    Lenk M, Wenig M, Bauer K, Hug F, Knappe C et al. 2019. Pipecolic acid is induced in barley upon infection and triggers immune responses associated with elevated nitric oxide accumulation. Mol. Plant-Microbe Interact. 32:1303–13
    [Google Scholar]
  73. 73. 
    Lew TTS, Koman VB, Silmore KS, Seo JS, Gordiichuk P et al. 2020. Real-time detection of wound-induced H2O2 signalling waves in plants with optical nanosensors. Nat. Plants 6:404–15
    [Google Scholar]
  74. 74. 
    Lewis LR, Polanski Z, de Torres Zabala M, Jayaraman S, Bowden L et al. 2015. Transcriptional dynamics driving MAMP-triggered immunity and pathogen effector–mediated immunosuppression in Arabidopsis leaves following infection with Pseudomonas syringae pv tomato DC3000. Plant Cell 27:113038–64
    [Google Scholar]
  75. 75. 
    Lim G-H, Shine MB, de Lorenzo L, Yu K, Cui W et al. 2016. Plasmodesmata localizing proteins regulate transport and signaling during systemic acquired immunity in plants. Cell Host Microbe 19:541–49
    [Google Scholar]
  76. 76. 
    Lin W, Zhang H, Huang D, Schenke D, Cai D et al. 2020. Dual-localized WHIRLY1 affects salicylic acid biosynthesis via coordination of ISOCHORISMATE SYNTHASE1, PHENYLALANINE AMMONIA LYASE1, AND S-ADENOSYL-L-METHIONINE-DEPENDENT METHYLTRANSFERASE1. Plant Physiol 184:1884–99
    [Google Scholar]
  77. 77. 
    Littlejohn GR, Breen S, Smirnoff N, Grant M. 2020. Chloroplast immunity illuminated. New Phytol 229:63088–107
    [Google Scholar]
  78. 78. 
    Liu NJ, Zhang T, Liu ZH, Chen X, Guo HS et al. 2020. Phytosphinganine affects plasmodesmata permeability via facilitating PDLP5-stimulated callose accumulation in Arabidopsis. Mol. Plant 13:128–43
    [Google Scholar]
  79. 79. 
    Liu Y, Ren D, Pike S, Pallardy S, Gassmann W, Zhang S. 2007. Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade. Plant J 51:941–54
    [Google Scholar]
  80. 80. 
    Lu Y, Tsuda K. 2020. Intimate association of PRR- and NLR-mediated signaling in plant immunity. Mol. Plant-Microbe Interact. 34:13–14
    [Google Scholar]
  81. 81. 
    Lu Y, Yao J. 2018. Chloroplasts at the crossroad of photosynthesis, pathogen infection and plant defense. Int. J. Mol. Sci. 19:3900
    [Google Scholar]
  82. 82. 
    Mackenzie SA, Kundariya H. 2020. Organellar protein multi-functionality and phenotypic plasticity in plants. Philos. Trans. R. Soc. Lond. B 375:20190182
    [Google Scholar]
  83. 83. 
    Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK. 2002. A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419:399–403
    [Google Scholar]
  84. 84. 
    Mandal MK, Chandra-Shekara AC, Jeong R-D, Yu K, Zhu S et al. 2012. Oleic acid–dependent modulation of NITRIC OXIDE ASSOCIATED1 protein levels regulates nitric oxide–mediated defense signaling in Arabidopsis. Plant Cell 24:1654–74
    [Google Scholar]
  85. 85. 
    Manning VA, Hardison LK, Ciuffetti LM. 2007. Ptr ToxA interacts with a chloroplast-localized protein. Mol. Plant-Microbe Interact. 20:168–77
    [Google Scholar]
  86. 86. 
    Manzoor H, Chiltz A, Madani S, Vatsa P, Schoefs B et al. 2012. Calcium signatures and signaling in cytosol and organelles of tobacco cells induced by plant defense elicitors. Cell Calcium 51:434–44
    [Google Scholar]
  87. 87. 
    McDonald MC, Ahren D, Simpfendorfer S, Milgate A, Solomon PS. 2017. The discovery of the virulence gene ToxA in the wheat and barley pathogen Bipolaris sorokiniana. Mol. Plant Pathol. 19:2432–39
    [Google Scholar]
  88. 88. 
    Medina-Puche L, Tan H, Dogra V, Wu M, Rosas-Diaz T et al. 2020. A defense pathway linking plasma membrane and chloroplasts and co-opted by pathogens. Cell 182:1109–24.e25
    [Google Scholar]
  89. 89. 
    Mei Q, Yang Y, Ye S, Liang W, Wang X et al. 2019. H2O2 induces association of RCA with the thylakoid membrane to enhance resistance of Oryza meyeriana to Xanthomonas oryzae pv. oryzae. Plants 8:9351
    [Google Scholar]
  90. 90. 
    Melotto M, Zhang L, Oblessuc PR, He SY. 2017. Stomatal defense a decade later. Plant Physiol 174:561–71
    [Google Scholar]
  91. 91. 
    Meng X, Zhang S. 2013. MAPK cascades in plant disease resistance signaling. Annu. Rev. Phytopathol. 51:245–66
    [Google Scholar]
  92. 92. 
    Metz JG, Pakrasi HB, Seibert M, Arntzer CJ. 1986. Evidence for a dual function of the herbicide-binding D1 protein in photosystem II. FEBS Lett 205:269–74
    [Google Scholar]
  93. 93. 
    Mignolet-Spruyt L, Xu E, Idanheimo N, Hoeberichts FA, Muhlenbock P et al. 2016. Spreading the news: subcellular and organellar reactive oxygen species production and signalling. J. Exp. Bot. 67:3831–44
    [Google Scholar]
  94. 94. 
    Milka K. 2014. NCI-DREAM project, XNAzymes, and galactolipids in plant resistance. Chem. Biol. 21:1597–98
    [Google Scholar]
  95. 95. 
    Mohr PG, Cahill DM. 2003. Abscisic acid influences the susceptibility of Arabidopsis thaliana to Pseudomonas syringae pv. tomato and Peronospora parasitica. Funct. Plant Biol. 30:461–69
    [Google Scholar]
  96. 96. 
    Moire L, Rezzonico E, Goepfert S, Poirier Y. 2004. Impact of unusual fatty acid synthesis on futile cycling through β-oxidation and on gene expression in transgenic plants. Plant Physiol 134:432–42
    [Google Scholar]
  97. 97. 
    Moreau M, Lee GI, Wang Y, Crane BR, Klessig DF. 2008. AtNOS/AtNOA1 is a functional Arabidopsis thaliana cGTPase and not a nitric-oxide synthase. J. Biol. Chem. 283:32957–67
    [Google Scholar]
  98. 98. 
    Mubarakshina MM, Ivanov BN, Naydov IA, Hillier W, Badger MR, Krieger-Liszkay A. 2010. Production and diffusion of chloroplastic H2O2 and its implication to signalling. J. Exp. Bot. 61:3577–87
    [Google Scholar]
  99. 99. 
    Mueller MJ, Mene-Saffrane L, Grun C, Karg K, Farmer EE. 2006. Oxylipin analysis methods. Plant J 45:472–89
    [Google Scholar]
  100. 100. 
    Mukhtar MS, Carvunis AR, Dreze M, Epple P, Steinbrenner J et al. 2011. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333:596–601
    [Google Scholar]
  101. 101. 
    Mullineaux PM, Exposito-Rodriguez M, Laissue PP, Smirnoff N, Park E 2020. Spatial chloroplast-to-nucleus signalling involving plastid-nuclear complexes and stromules. Philos. Trans. R. Soc. Lond. B 375:20190405
    [Google Scholar]
  102. 102. 
    Mumm R, Burow M, Bukovinszkine'Kiss G, Kazantzidou E, Wittstock U et al. 2008. Formation of simple nitriles upon glucosinolate hydrolysis affects direct and indirect defense against the specialist herbivore, Pieris rapae. J. Chem. Ecol. 34:1311–21
    [Google Scholar]
  103. 103. 
    Mur LA, Aubry S, Mondhe M, Kingston-Smith A, Gallagher J et al. 2010. Accumulation of chlorophyll catabolites photosensitizes the hypersensitive response elicited by Pseudomonas syringae in Arabidopsis. New Phytol 188:161–74
    [Google Scholar]
  104. 104. 
    Nakano M, Mukaihara T. 2018. Ralstonia solanacearum Type III effector RipAL targets chloroplasts and induces jasmonic acid production to suppress salicylic acid-mediated defense responses in plants. Plant Cell Physiol 59:122576–89
    [Google Scholar]
  105. 105. 
    Návarová H, Bernsdorff F, Döring A-C, Zeier J. 2012. Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24:5123–41
    [Google Scholar]
  106. 106. 
    Niemiro A, Cysewski D, Brzywczy J, Wawrzynska A, Sienko M et al. 2020. Similar but not identical—binding properties of LSU (response to low sulfur) proteins from Arabidopsis thaliana. Front. Plant Sci. 11:1246
    [Google Scholar]
  107. 107. 
    Nietzel T, Elsasser M, Ruberti C, Steinbeck J, Ugalde JM et al. 2019. The fluorescent protein sensor roGFP2-Orp1 monitors in vivo H2O2 and thiol redox integration and elucidates intracellular H2O2 dynamics during elicitor-induced oxidative burst in Arabidopsis. New Phytol 221:1649–64
    [Google Scholar]
  108. 108. 
    Nomura H, Komori T, Uemura S, Kanda Y, Shimotani K et al. 2012. Chloroplast-mediated activation of plant immune signalling in Arabidopsis. Nat. Commun 3:926
    [Google Scholar]
  109. 109. 
    Nomura H, Shiina T. 2014. Calcium signaling in plant endosymbiotic organelles: mechanism and role in physiology. Mol. Plant 7:1094–104
    [Google Scholar]
  110. 110. 
    Onkokesung N, Reichelt M, Wright LP, Phillips MA, Gershenzon J, Dicke M. 2019. The plastidial metabolite 2-C-methyl-D-erythritol-2,4-cyclodiphosphate modulates defence responses against aphids. Plant Cell Environ 42:2309–23
    [Google Scholar]
  111. 111. 
    Ori N, Eshed Y, Paran I, Presting G, Aviv D et al. 1997. The I2C family from the wilt disease resistance locus I2 belongs to the nucleotide binding, leucine-rich repeat superfamily of plant resistance genes. Plant Cell 9:521–32
    [Google Scholar]
  112. 112. 
    Park E, Caplan JL, Dinesh-Kumar SP. 2018. Dynamic coordination of plastid morphological change by cytoskeleton for chloroplast-nucleus communication during plant immune responses. Plant Signal. Behav. 13:e1500064
    [Google Scholar]
  113. 113. 
    Peng Z, Hu Y, Zhang J, Huguet-Tapia JC, Block AK et al. 2019. Xanthomonas translucens commandeers the host rate-limiting step in ABA biosynthesis for disease susceptibility. italicPNAS 11620938–46
  114. 114. 
    Pfannschmidt T, Terry MJ, Van Aken O, Quiros PM. 2020. Retrograde signals from endosymbiotic organelles: a common control principle in eukaryotic cells. Philos. Trans. R. Soc. Lond. B 375:20190396
    [Google Scholar]
  115. 115. 
    Ramel F, Birtic S, Ginies C, Soubigou-Taconnat L, Triantaphylides C, Havaux M 2012. Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. PNAS 109:5535–40
    [Google Scholar]
  116. 116. 
    Ren Y, Li Y, Jiang Y, Wu B, Miao Y. 2017. Phosphorylation of WHIRLY1 by CIPK14 shifts its localization and dual functions in Arabidopsis. Mol. Plant 10:749–63
    [Google Scholar]
  117. 117. 
    Robert-Seilaniantz A, Grant M, Jones JD. 2011. Hormone crosstalk in plant disease and defense: more than just JASMONATE-SALICYLATE antagonism. Annu. Rev. Phytopathol. 49:317–43
    [Google Scholar]
  118. 118. 
    Sarma GN, Manning VA, Ciuffetti LM, Karplus PA. 2005. Structure of Ptr ToxA: an RGD-containing host-selective toxin from Pyrenophora tritici-repentis. Plant Cell 17:3190–202
    [Google Scholar]
  119. 119. 
    Sekine KT, Tomita R, Takeuchi S, Atsumi G, Saitoh H et al. 2012. Functional differentiation in the leucine-rich repeat domains of closely related plant virus-resistance proteins that recognize common avr proteins. Mol. Plant-Microbe Interact. 25:1219–29
    [Google Scholar]
  120. 120. 
    Seo S, Okamoto M, Iwai T, Iwano M, Fukui K et al. 2000. Reduced levels of chloroplast FtsH protein in tobacco mosaic virus-infected tobacco leaves accelerate the hypersensitive reaction. Plant Cell 12:917–32
    [Google Scholar]
  121. 121. 
    Shi S, Li S, Asim M, Mao J, Xu D et al. 2018. The Arabidopsis calcium-dependent protein kinases (CDPKs) and their roles in plant growth regulation and abiotic stress responses. Int. J. Mol. Sci. 19:71900
    [Google Scholar]
  122. 122. 
    Shine M, Gao Q-M, Chowda-Reddy R, Singh AK, Kachroo P, Kachroo A. 2019. Glycerol-3-phosphate mediates rhizobia-induced systemic signaling in soybean. Nat. Commun 10:5303
    [Google Scholar]
  123. 123. 
    Smirnoff N, Arnaud D. 2019. Hydrogen peroxide metabolism and functions in plants. New Phytol 221:1197–214
    [Google Scholar]
  124. 124. 
    Stael S, Kmiecik P, Willems P, Van Der Kelen K, Coll NS et al. 2015. Plant innate immunity—sunny side up?. Trends Plant Sci 20:3–11
    [Google Scholar]
  125. 125. 
    Stael S, Wurzinger B, Mair A, Mehlmer N, Vothknecht UC, Teige M. 2012. Plant organellar calcium signalling: an emerging field. J. Exp. Bot. 63:1525–42
    [Google Scholar]
  126. 126. 
    Stonebloom S, Burch-Smith T, Kim I, Meinke D, Mindrinos M, Zambryski P 2009. Loss of the plant DEAD-box protein ISE1 leads to defective mitochondria and increased cell-to-cell transport via plasmodesmata. PNAS 106:17229–34
    [Google Scholar]
  127. 127. 
    Su J, Yang L, Zhu Q, Wu H, He Y et al. 2018. Active photosynthetic inhibition mediated by MPK3/MPK6 is critical to effector-triggered immunity. PLOS Biol 16:e2004122
    [Google Scholar]
  128. 128. 
    Takahashi S, Badger MR. 2011. Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60
    [Google Scholar]
  129. 129. 
    Tang L, Yang G, Ma M, Liu X, Li B et al. 2020. An effector of a necrotrophic fungal pathogen targets the calcium-sensing receptor in chloroplasts to inhibit host resistance. Mol. Plant Pathol. 21:5686–701
    [Google Scholar]
  130. 130. 
    Terashima M, Specht M, Hippler M. 2011. The chloroplast proteome: a survey from the Chlamydomonas reinhardtii perspective with a focus on distinctive features. Curr. Genet. 57:151–68
    [Google Scholar]
  131. 131. 
    Torres MA, Jones JD, Dangl JL. 2006. Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–78
    [Google Scholar]
  132. 132. 
    Unal D, Garcia-Caparros P, Kumar V, Dietz KJ. 2020. Chloroplast-associated molecular patterns as concept for fine-tuned operational retrograde signalling. Philos. Trans. R. Soc. Lond. B 375:20190443
    [Google Scholar]
  133. 133. 
    Vainonen JP, Sakuragi Y, Stael S, Tikkanen M, Allahverdiyeva Y et al. 2008. Light regulation of CaS, a novel phosphoprotein in the thylakoid membrane of Arabidopsis thaliana. FEBS J 275:1767–77
    [Google Scholar]
  134. 134. 
    van der Burgh AM, Joosten M. 2019. Plant immunity: thinking outside and inside the box. Trends Plant Sci 24:587–601
    [Google Scholar]
  135. 135. 
    Venugopal SC, Jeong R-D, Mandal MK, Zhu S, Chandra-Shekara AC et al. 2009. Enhanced disease susceptibility 1 and salicylic acid act redundantly to regulate resistance gene-mediated signaling. PLOS Genet 5:e1000545
    [Google Scholar]
  136. 136. 
    Walley J, Xiao Y, Wang JZ, Baidoo EE, Keasling JD et al. 2015. Plastid-produced interorgannellar stress signal MEcPP potentiates induction of the unfolded protein response in endoplasmic reticulum. PNAS 112:6212–17
    [Google Scholar]
  137. 137. 
    Walley JW, Kliebenstein DJ, Bostock RM, Dehesh K. 2013. Fatty acids and early detection of pathogens. Curr. Opin. Plant Biol. 16:520–26
    [Google Scholar]
  138. 138. 
    Wang C, El-Shetehy M, Shine MB, Yu K, Navarre D et al. 2014. Free radicals mediate systemic acquired resistance. Cell Rep 7:348–55
    [Google Scholar]
  139. 139. 
    Wang C, Liu R, Lim G-H, de Lorenzo L, Yu K et al. 2018. Pipecolic acid confers systemic immunity by regulating free radicals. Sci. Adv. 4:eaar4509
    [Google Scholar]
  140. 140. 
    Wang JZ, Li B, Xiao Y, Ni Y, Ke H et al. 2017. Initiation of ER body formation and indole glucosinolate metabolism by the plastidial retrograde signaling metabolite, MEcPP. Mol. Plant 10:1400–16
    [Google Scholar]
  141. 141. 
    Wang X, Sager R, Cui W, Zhang C, Lu H, Lee JY. 2013. Salicylic acid regulates plasmodesmata closure during innate immune responses in Arabidopsis. Plant Cell 25:2315–29
    [Google Scholar]
  142. 142. 
    Wang Y, Schuck S, Wu J, Yang P, Döring A-C et al. 2018. A MPK3/6-WRKY33-ALD1-pipecolic acid regulatory loop contributes to systemic acquired resistance. Plant Cell 30:2480–94
    [Google Scholar]
  143. 143. 
    Weinl S, Held K, Schlucking K, Steinhorst L, Kuhlgert S et al. 2008. A plastid protein crucial for Ca2+-regulated stomatal responses. New Phytol 179:675–86
    [Google Scholar]
  144. 144. 
    Wendehenne D, Gao Q-M, Kachroo A, Kachroo P. 2014. Free radical-mediated systemic immunity in plants. Curr. Opin. Plant Biol. 20:127–34
    [Google Scholar]
  145. 145. 
    Wittek F, Hoffmann T, Kanawati B, Bichlmeier M, Knappe C et al. 2014. Arabidopsis ENHANCED DISEASE SUSCEPTIBILITY1 promotes systemic acquired resistance via azelaic acid and its precursor 9-oxo nonanoic acid. J. Exp. Bot. 65:5919–31
    [Google Scholar]
  146. 146. 
    Xia Y, Gao Q-M, Yu K, Lapchyk L, Navarre D et al. 2009. An intact cuticle in distal tissues is essential for the induction of systemic acquired resistance in plants. Cell Host Microbe 5:151–65
    [Google Scholar]
  147. 147. 
    Xia Y, Yu K, Navarre D, Seebold K, Kachroo A, Kachroo P. 2010. The glabra1 mutation affects cuticle formation and plant responses to microbes. Plant Physiol 154:833–46
    [Google Scholar]
  148. 148. 
    Xiao Y, Savchenko T, Baidoo EE, Chehab WE, Hayden DM et al. 2012. Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes. Cell 149:1525–35
    [Google Scholar]
  149. 149. 
    Yaeno T, Matsuda O, Iba K. 2004. Role of chloroplast trienoic fatty acids in plant disease defense responses. Plant J 40:931–41
    [Google Scholar]
  150. 150. 
    Yamada K, Hara-Nishimura I, Nishimura M. 2011. Unique defense strategy by the endoplasmic reticulum body in plants. Plant Cell Physiol 52:2039–49
    [Google Scholar]
  151. 151. 
    Yamburenko MV, Zubo YO, Borner T. 2015. Abscisic acid affects transcription of chloroplast genes via protein phosphatase 2C-dependent activation of nuclear genes: repression by guanosine-3′-5′-bisdiphosphate and activation by sigma factor 5. Plant J 82:1030–41
    [Google Scholar]
  152. 152. 
    Yu K, Soares JM, Mandal MK, Wang C, Chanda B et al. 2013. A feedback regulatory loop between G3P and lipid transfer proteins DIR1 and AZI1 mediates azelaic-acid-induced systemic immunity. Cell Rep 3:1266–78
    [Google Scholar]
  153. 153. 
    Yun BW, Feechan A, Yin M, Saidi NB, Le Bihan T et al. 2011. S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478:264–68
    [Google Scholar]
  154. 154. 
    Yun BW, Skelly MJ, Yin M, Yu M, Mun BG et al. 2016. Nitric oxide and S-nitrosoglutathione function additively during plant immunity. New Phytol 211:516–26
    [Google Scholar]
  155. 155. 
    Zaninotto F, La Camera S, Polverari A, Delledonne M 2006. Cross talk between reactive nitrogen and oxygen species during the hypersensitive disease resistance response. Plant Physiol 141:379–83
    [Google Scholar]
  156. 156. 
    Zechmann B. 2019. Ultrastructure of plastids serves as reliable abiotic and biotic stress marker. PLOS ONE 14:e0214811
    [Google Scholar]
  157. 157. 
    Zoeller M, Stingl N, Krischke M, Fekete A, Waller F et al. 2012. Lipid profiling of the Arabidopsis hypersensitive response reveals specific lipid peroxidation and fragmentation processes: biogenesis of pimelic and azelaic acid. Plant Physiol 160:365–78
    [Google Scholar]
  158. 158. 
    Zurbriggen MD, Carrillo N, Tognetti VB, Melzer M, Peisker M et al. 2009. Chloroplast-generated reactive oxygen species play a major role in localized cell death during the non-host interaction between tobacco and Xanthomonas campestris pv. vesicatoria. Plant J 60:962–73
    [Google Scholar]
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