1932

Abstract

The plant cytoskeleton is a dynamic framework of cytoplasmic filaments that rearranges as the needs of the cell change during growth and development. Incessant turnover mechanisms allow these networks to be rapidly redeployed in defense of host cytoplasm against microbial invaders. Both chemical and mechanical stimuli are recognized as danger signals to the plant, and these are perceived and transduced into cytoskeletal dynamics and architecture changes through a collection of well-recognized, previously characterized players. Recent advances in quantitative cell biology approaches, along with the powerful molecular genetics techniques associated with , have uncovered two actin-binding proteins as key intermediaries in the immune response to phytopathogens and defense signaling. Certain bacterial phytopathogens have adapted to the cytoskeletal-based defense mechanism during the basal immune response and have evolved effector proteins that target actin filaments and microtubules to subvert transcriptional reprogramming, secretion of defense-related proteins, and cell wall–based defenses. In this review, we describe current knowledge about host cytoskeletal dynamics operating at the crossroads of the molecular and cellular arms race between microbes and plants.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-080516-035632
2018-08-25
2024-12-11
Loading full text...

Full text loading...

/deliver/fulltext/phyto/56/1/annurev-phyto-080516-035632.html?itemId=/content/journals/10.1146/annurev-phyto-080516-035632&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Andersson MX, Kourtchenko O, Dangl JL, Mackey D, Ellerström M 2006. Phospholipase-dependent signalling during the AvrRpm1- and AvrRpt2-induced disease resistance responses in Arabidopsis thaliana. . Plant J 47:947–59
    [Google Scholar]
  2. 2.  Bargmann BO, Laxalt AM, Riet Bt, Schouten E, Van Leeuwen W et al. 2006. LePLDβ1 activation and relocalization in suspension-cultured tomato cells treated with xylanase. Plant J 45:358–68
    [Google Scholar]
  3. 3.  Beck M, Zhou JM, Faulkner C, MacLean D, Robatzek S 2012. Spatio-temporal cellular dynamics of the Arabidopsis flagellin receptor reveal activation status–dependent endosomal sorting. Plant Cell 24:4205–19
    [Google Scholar]
  4. 4.  Ben Khaled SB, Postma J, Robatzek S 2015. A moving view: subcellular trafficking processes in pattern recognition receptor-triggered plant immunity. Annu. Rev. Phytopathol. 53:379–402
    [Google Scholar]
  5. 5.  Binet M-N, Humbert C, Lecourieux D, Vantard M, Pugin A 2001. Disruption of microtubular cytoskeleton induced by cryptogein, an elicitor of hypersensitive response in tobacco cells. Plant Physiol 125:564–72
    [Google Scholar]
  6. 6.  Block A, Guo M, Li G, Elowsky C, Clemente TE, Alfano JR 2009. The Pseudomonas syringae type III effector HopG1 targets mitochondria, alters plant development and suppresses plant innate immunity. Cell. Microbiol. 12:318–30
    [Google Scholar]
  7. 7.  Boller T, Felix G 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]
  8. 8.  Boudsocq M, Sheen J 2013. CDPKs in immune and stress signaling. Trends Plant Sci 18:30–40
    [Google Scholar]
  9. 9.  Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L et al. 2010. Differential innate immune signalling via Ca2+ sensor protein kinases. Nature 464:418–22
    [Google Scholar]
  10. 10.  Branco R, Pearsall E-J, Rundle CA, White RG, Bradby JE, Hardham AR 2017. Quantifying the plant actin cytoskeleton response to applied pressure using nanoindentation. Protoplasma 254:1127–37
    [Google Scholar]
  11. 11.  Bücherl C, Jarsch IK, Schudoma C, Segonzac C, Mbengue M et al. 2017. Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains. eLife 6:e25114
    [Google Scholar]
  12. 12.  Cao Y, Liang Y, Tanaka K, Nguyen CT, Jedrzerjczak RP et al. 2014. The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. eLife 3:e03766
    [Google Scholar]
  13. 13.  Chang X, Nick P 2012. Defence signalling triggered by flg22 and harpin is integrated into a different stilbene output in Vitis cells. PLOS ONE 7:e40446
    [Google Scholar]
  14. 14.  Cheong MS, Kirik A, Kim J-G, Frame K, Kirik V, Mudgett MB 2014. AvrBsT acetylates Arabidopsis ACIP1, a protein that associates with microtubules and is required for immunity. PLOS Pathog 10:e1003952
    [Google Scholar]
  15. 15.  Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T et al. 2007. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500
    [Google Scholar]
  16. 16.  Choi S, Jayaraman J, Segonzac C, Park H-J, Park H et al. 2017. Pseudomonas syringae pv. actinidiae type III effectors localized at multiple cellular compartments activate or suppress innate immune responses in Nicotiana benthamiana. Front. Plant Sci. 8:e2157
    [Google Scholar]
  17. 17.  Cui H, Tsuda K, Parker J 2015. Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66:487–511
    [Google Scholar]
  18. 18.  Dangl JL, Horvath DM, Staskawicz BJ 2013. Pivoting the plant immune system from dissection to deployment. Science 341:746–51
    [Google Scholar]
  19. 19.  Day B, Henty JL, Porter KJ, Staiger CJ 2011. The pathogen-actin connection: a platform for defense signaling in plants. Annu. Rev. Phytopathol. 49:489–506
    [Google Scholar]
  20. 20.  de Jong CF, Laxalt AM, Bargmann BO, de Wit PJ, Joosten MH, Munnik T 2004. Phosphatidic acid accumulation is an early response in the Cf-4/Avr4 interaction. Plant J 39:1–12
    [Google Scholar]
  21. 21.  den Hartog M, Musgrave A, Munnik T 2001. Nod factor–induced phosphatidic acid and diacylglycerol pyrophosphate formation: a role for phospholipase C and D in root hair deformation. Plant J 25:55–66
    [Google Scholar]
  22. 22.  Dou D, Zhou J-M 2012. Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe 12:484–95
    [Google Scholar]
  23. 23.  Ellinger D, Naumann M, Falter C, Zwikowicz C, Jamrow T et al. 2013. Elevated early callose deposition results in complete penetration resistance to powdery mildew in Arabidopsis. . Plant Physiol 161:1433–44
    [Google Scholar]
  24. 24.  Frescatada-Rosa M, Robatzek S, Kuhn H 2015. Should I stay or should I go? Traffic control for plant pattern recognition receptors. Curr. Opin. Plant Biol. 28:23–29
    [Google Scholar]
  25. 25.  Fu Y, Duan X, Tang C, Li X, Voegele RT et al. 2014. TaADF7, an actin-depolymerizing factor, contributes to wheat resistance against Puccinia striiformis f. sp. tritici. Plant J. 78:16–30
    [Google Scholar]
  26. 26.  Gieni RS, Hendzel MJ 2009. Actin dynamics and functions in the interphase nucleus: moving toward an understanding of nuclear polymeric actin. Biochem. Cell Biol. 87:283–306
    [Google Scholar]
  27. 27.  Gómez-Gómez L, Boller T 2000. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. . Cell 5:1003–11
    [Google Scholar]
  28. 28.  Guo M, Kim P, Li G, Elowsky C, Alfano JR 2016. A bacterial effector co-opts calmodulin to target the plant microtubule network. Cell Host Microbe 19:67–78
    [Google Scholar]
  29. 29.  Haglund CM, Welch MD 2011. Pathogens and polymers: Microbe–host interactions illuminate the cytoskeleton. J. Cell Biol. 195:7–17
    [Google Scholar]
  30. 30.  Hao H, Fan L, Chen T, Li R, Li X et al. 2014. Clathrin and membrane microdomains cooperatively regulated RbohD dynamics and activity in Arabidopsis. . Plant Cell 26:1729–45
    [Google Scholar]
  31. 31.  Hardham AR 2013. Microtubules and biotic interactions. Plant J 75:278–89
    [Google Scholar]
  32. 32.  Hardham AR, Jones DA, Takemoto D 2007. Cytoskeleton and cell wall function in penetration resistance. Curr. Opin. Plant Biol. 10:342–48
    [Google Scholar]
  33. 33.  Hardham AR, Takemoto D, White RG 2008. Rapid and dynamic subcellular reorganization following mechanical stimulation of Arabidopsis epidermal cells mimics responses to fungal and oomycete attack. BMC Plant Biol 8:63
    [Google Scholar]
  34. 34.  Heese A, Hann DR, Gimenez-Ibanez S, Jones AME, He K et al. 2007. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. PNAS 104:12217–22
    [Google Scholar]
  35. 35.  Henty JL, Bledsoe SW, Khurana P, Meagher RB, Day B et al. 2011. Arabidopsis actin depolymerizing factor4 modulates the stochastic dynamic behavior of actin filaments in the cortical array of epidermal cells. Plant Cell 23:3711–26
    [Google Scholar]
  36. 36.  Henty-Ridilla JL, Li J, Blanchoin L, Staiger CJ 2013. Actin dynamics in the cortical array of plant cells. Curr. Opin. Plant Biol. 16:678–87
    [Google Scholar]
  37. 37.  Henty-Ridilla JL, Li J, Day B, Staiger CJ 2014. Actin depolymerizing factor4 regulates actin dynamics during innate immune signaling in Arabidopsis. . Plant Cell 26:340–52
    [Google Scholar]
  38. 38.  Henty-Ridilla JL, Shimono M, Li J, Chang JH, Day B, Staiger CJ 2013. The plant actin cytoskeleton responds to signals from microbe-associated molecular patterns. PLOS Pathog 9:e1003290
    [Google Scholar]
  39. 39.  Higaki T, Goh T, Hayashi T, Kutsuna N, Kadota Y et al. 2007. Elicitor-induced cytoskeletal rearrangement relates to vacuolar dynamics and execution of cell death: in vivo imaging of hypersensitive cell death in tobacco BY-2 cells. Plant Cell Physiol 48:1414–25
    [Google Scholar]
  40. 40.  Higaki T, Kadota A, Goh T, Hayashi T, Kutsuna N et al. 2008. Vacuolar and cytoskeletal dynamics during elicitor-induced programmed cell death in tobacco BY-2 cells. Plant Signal. Behav. 3:700–3
    [Google Scholar]
  41. 41.  Higaki T, Kurusu T, Hasezawa S, Kuchitsu K 2011. Dynamic intracellular reorganization of cytoskeletons and the vacuole in defense responses and hypersensitive cell death in plants. J. Plant Res. 124:315–24
    [Google Scholar]
  42. 42.  Higaki T, Kutsuna N, Sano T, Kondo N, Hasezawa S 2010. Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells. Plant J 61:156–65
    [Google Scholar]
  43. 43.  Hirakawa Y, Nomura T, Hasezawa S, Higaki T 2015. Simplification of vacuole structure during plant cell death triggered by culture filtrates of Erwinia carotovora. J. Int. Plant Biol. 57:127–35
    [Google Scholar]
  44. 44.  Hong Y, Zhao J, Guo L, Kim S-C, Deng X et al. 2016. Plant phospholipases D and C and their diverse functions in stress responses. Prog. Lipid Res. 62:55–74
    [Google Scholar]
  45. 45.  Huang S, Blanchoin L, Kovar DR, Staiger CJ 2003. Arabidopsis capping protein (AtCP) is a heterodimer that regulates assembly at the barbed ends of actin filaments. J. Biol. Chem. 278:44832–42
    [Google Scholar]
  46. 46.  Huang S, Gao L, Blanchoin L, Staiger CJ 2006. Heterodimeric capping protein from Arabidopsis is regulated by phosphatidic acid. Mol. Biol. Cell 17:1946–58
    [Google Scholar]
  47. 47.  Inada N 2017. Plant actin depolymerizing factor: actin microfilament disassembly and more. J. Plant Res. 130:227–38
    [Google Scholar]
  48. 48.  Inada N, Higaki T, Hasezawa S 2016. Nuclear function of subclass I actin-depolymerizing factor contributes to susceptibility in Arabidopsis to an adapted powdery mildew fungus. Plant Physiol 170:1420–34
    [Google Scholar]
  49. 49.  Inada N, Higaki T, Hasezawa S 2016. Quantitative analyses on dynamic changes in the organization of host Arabidopsis thaliana actin microfilaments surrounding the infection organ of the powdery mildew fungus Golovinomyces orontii. J. Plant Res. 129:103–10
    [Google Scholar]
  50. 50.  Jelenska J, Kang Y, Greenberg JT 2014. Plant pathogenic bacteria target the actin microfilament network involved in trafficking of disease defense components. BioArchitect 4:149–53
    [Google Scholar]
  51. 51.  Johansson ON, Fahlberg P, Karimi E, Nilsson AK, Ellerström M, Andersson MX 2014. Redundancy among phospholipase D isoforms in resistance triggered by recognition of the Pseudomonas syringae effector AvrRpm1 in Arabidopsis thaliana. Front. Plant Sci. 5:e639
    [Google Scholar]
  52. 52.  Jones JDG, Dangl JL 2006. The plant immune system. Nature 444:323–29
    [Google Scholar]
  53. 53.  Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S et al. 2014. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell 54:43–55
    [Google Scholar]
  54. 54.  Kang Y, Jelenska J, Cecchini NM, Li Y, Lee MW et al. 2014. HopW1 from Pseudomonas syringae disrupts the actin cytoskeleton to promote virulence in Arabidopsis. . PLOS Pathog 10:e1004232
    [Google Scholar]
  55. 55.  Katagiri F, Thilmony R, He SY 2002. The Arabidopsis thalianaPseudomonas syringae interaction. Arabidopsis Book 1:e0039
    [Google Scholar]
  56. 56.  Khan M, Seto D, Subramaniam R, Desveaux D 2017. Oh, the places they'll go! A survey of phytopathogen effectors and their host targets. Plant J 93:651–63
    [Google Scholar]
  57. 57.  Kirik A, Mudgett MB 2009. SOBER1 phospholipase activity suppresses phosphatidic acid accumulation and plant immunity in response to bacterial effector AvrBsT. PNAS 106:20532–37
    [Google Scholar]
  58. 58.  Kobayashi I, Hakuno H 2003. Actin-related defense mechanism to reject penetration attempt by a non-pathogen is maintained in tobacco BY-2 cells. Planta 217:340–45
    [Google Scholar]
  59. 59.  Kobayashi I, Kobayashi Y, Hardham AR 1994. Dynamic reorganization of microtubules and microfilaments in flax cells during the resistance response to flax rust infection. Planta 195:237–47
    [Google Scholar]
  60. 60.  Kobayashi Y, Kobayashi I 2007. Depolymerization of the actin cytoskeleton induces defense responses in tobacco plants. J. Gen. Plant Pathol. 73:360–64
    [Google Scholar]
  61. 61.  Kobayashi Y, Kobayashi I, Funaki Y, Fujimoto S, Takemoto T, Kunoh H 1997. Dynamic reorganization of microfilaments and microtubules is necessary for the expression of non-host resistance in barley coleoptile cells. Plant J 11:525–37
    [Google Scholar]
  62. 62.  Kobayashi Y, Yamada M, Kobayashi I, Kunoh H 1997. Actin microfilaments are required for the expression of nonhost resistance in higher plants. Plant Cell Physiol 38:725–33
    [Google Scholar]
  63. 63.  Koh S, André A, Edwards H, Ehrhardt D, Somerville S 2005. Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. Plant J 44:516–29
    [Google Scholar]
  64. 64.  Kurusu T, Higaki T, Kuchitsu K 2015. Programmed cell death in plant immunity: cellular reorganization, signaling, and cell cycle dependence in cultured cells as a model system. Plant Programmed Cell Death AN Gunawardena, PF McCabe 77–96 Switzerland: Springer
    [Google Scholar]
  65. 65.  Laluk K, Luo H, Chai M, Dhawan R, Lai Z, Mengiste T 2011. Biochemical and genetic requirements for function of the immune response regulator BOTRYTIS-INDUCED KINASE1 in plant growth, ethylene signaling, and PAMP-triggered immunity in Arabidopsis. . Plant Cell 23:2831–49
    [Google Scholar]
  66. 66.  Lanteri ML, Laxalt AM, Lamattina L 2008. Nitric oxide triggers phosphatidic acid accumulation via phospholipase D during auxin-induced adventitious root formation in cucumber. Plant Physiol 147:188–98
    [Google Scholar]
  67. 67.  Laxalt AM, Raho N, ten Have A, Lamattina L 2007. Nitric oxide is critical for inducing phosphatidic acid accumulation in xylanase-elicited tomato cells. J. Biol. Chem. 282:21160–68
    [Google Scholar]
  68. 68.  Lee AH-Y, Hurley B, Felsensteiner C, Yea C, Ckurshumova W et al. 2012. A bacterial acetyltransferase destroys plant microtubule networks and blocks secretion. PLOS Pathog 8:e1002523
    [Google Scholar]
  69. 69.  Lee J, Teitzel GM, Munkvold K, del Pozo O, Martin GB et al. 2012. Type III secretion and effectors shape the survival and growth pattern of Pseudomonas syringae on leaf surfaces. Plant Physiol 158:1803–18
    [Google Scholar]
  70. 70.  Leucci MR, Di Sansebastiano G-P, Giganti M, Dalessandro G, Piro G 2007. Secretion marker proteins and cell-wall polysaccharides move through different secretory pathways. Planta 225:1001–17
    [Google Scholar]
  71. 71.  Li J, Blanchoin L, Staiger CJ 2015. Signaling to actin stochastic dynamics. Annu. Rev. Plant Biol. 66:415–40
    [Google Scholar]
  72. 72.  Li J, Cao L, Staiger CJ 2017. Capping protein modulates actin remodeling in response to reactive oxygen species during plant innate immunity. Plant Physiol 173:1125–36
    [Google Scholar]
  73. 73.  Li J, Henty-Ridilla JL, Huang S, Wang X, Blanchoin L, Staiger CJ 2012. Capping protein modulates the dynamic behavior of actin filaments in response to phosphatidic acid in Arabidopsis. . Plant Cell 24:3742–54
    [Google Scholar]
  74. 74.  Li J, Henty-Ridilla JL, Staiger BH, Day B, Staiger CJ 2015. Capping protein integrates multiple MAMP signaling pathways to modulate actin dynamics during plant innate immunity. Nat. Comm. 6:7206
    [Google Scholar]
  75. 75.  Li L, Li M, Yu L, Zhou Z, Liang X et al. 2014. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15:329–38
    [Google Scholar]
  76. 76.  Macho AP 2015. Subversion of plant cellular functions by bacterial type-III effectors: beyond suppression of immunity. New Phytol 210:51–57
    [Google Scholar]
  77. 77.  Macho AP, Zipfel C 2014. Plant PRRs and the activation of innate immune signaling. Mol. Cell 54:263–72
    [Google Scholar]
  78. 78.  Macho AP, Zipfel C 2015. Targeting of plant pattern recognition receptor–triggered immunity by bacterial type-III secretion system effectors. Curr. Opin. Microbiol. 23:14–22
    [Google Scholar]
  79. 79.  Mao H, Nakamura M, Viotti C, Grebe M 2016. A framework for lateral membrane trafficking and polar tethering of the PEN3 ATP-binding cassette transporter. Plant Physiol 172:2245–60
    [Google Scholar]
  80. 80.  Melotto M, Underwood W, Koczan J, Nomura K, He SY 2006. Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–80
    [Google Scholar]
  81. 81.  Melotto M, Zhang L, Oblessuc PR, He SY 2017. Stomatal defense a decade later. Plant Physiol 174:561–71
    [Google Scholar]
  82. 82.  Miklis M, Consonni C, Bhat RA, Lipka V, Schulze-Lefert P, Panstruga R 2007. Barley MLO modulates actin-dependent and actin-independent antifungal defense pathways at the cell periphery. Plant Physiol 144:1132–43
    [Google Scholar]
  83. 83.  Miya A, Albert P, Shinya T, Desaki Y, Ichimura K et al. 2007. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. . PNAS 104:19613–18
    [Google Scholar]
  84. 84.  Opalski KS, Schultheiss H, Kogel K-H, Hückelhoven R 2005. The receptor-like MLO protein and the RAC/ROP family G-protein RACB modulate actin reorganization in barley attacked by the biotrophic powdery mildew fungus Blumeria graminis f.sp. hordei. Plant J. 41:291–303
    [Google Scholar]
  85. 85.  Park J, Gu Y, Lee Y, Yang Z, Lee Y 2004. Phosphatidic acid induces leaf cell death in Arabidopsis by activating the rho-related small G-protein GTPase-mediated pathway of reactive oxygen species generation. Plant Physiol 134:129–36
    [Google Scholar]
  86. 86.  Pinosa F, Buhot N, Kwaaitaal M, Fahlberg P, Thordal-Christensen H et al. 2013. Arabidopsis phospholipase Dδ is involved in basal defense and nonhost resistance to powdery mildew fungi. Plant Physiol 163:896–906
    [Google Scholar]
  87. 87.  Pleskot R, Li J, Žárský V, Potocký M, Staiger CJ 2013. Regulation of cytoskeletal dynamics by phospholipase D and phosphatidic acid. Trends Plant Sci 18:496–504
    [Google Scholar]
  88. 88.  Pleskot R, Pejchar P, Žárský V, Staiger CJ, Potocký M 2012. Structural insights into the inhibition of actin-capping protein by interactions with phosphatidic acid and phosphatidylinositol (4,5)-bisphosphate. PLOS Comput. Biol. 8:e1002765
    [Google Scholar]
  89. 89.  Porter K, Day B 2016. From filaments to function: the role of the plant actin cytoskeleton in pathogen perception, signaling, and immunity. J. Int. Plant Biol. 58:299–311
    [Google Scholar]
  90. 90.  Porter K, Shimono M, Tian M, Day B 2012. Arabidopsis Actin-Depolymerizing Factor-4 links pathogen perception, defense activation and transcription to cytoskeletal dynamics. PLOS Pathog 8:e1003006
    [Google Scholar]
  91. 91.  Qi J, Wang J, Gong Z, Zhou J-M 2017. Apoplastic ROS signaling in plant immunity. Curr. Opin. Plant Biol. 38:92–100
    [Google Scholar]
  92. 92.  Qiao F, Chang X-L, Nick P 2010. The cytoskeleton enhances gene expression in the response to the Harpin elicitor in grapevine. J. Exp. Bot. 61:4021–31
    [Google Scholar]
  93. 93.  Quentin M, Baures I, Hoefle C, Caillaud M-C, Allasia V et al. 2016. The Arabidopsis microtubule-associated protein MAP65-3 supports infection by filamentous biotrophic pathogens by down-regulating salicylic acid–dependent defenses. J. Exp. Bot. 67:1731–43
    [Google Scholar]
  94. 94.  Raho N, Ramirez L, Lanteri ML, Gonorazky G, Lamattina L et al. 2011. Phosphatidic acid production in chitosan-elicited tomato cells, via both phospholipase D and phospholipase C/diacylglycerol kinase, requires nitric oxide. J. Plant Physiol. 168:534–39
    [Google Scholar]
  95. 95.  Robatzek S 2014. Endocytosis: at the crossroads of pattern recognition immune receptors and pathogen effectors. Applied Plant Cell Biology, Plant Cell Monographs 22 P Nick, Z Opartny 273–97 Berlin: Springer-Verlag
    [Google Scholar]
  96. 96.  Robatzek S, Chinchilla D, Boller T 2006. Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. . Genes Dev 20:537–42
    [Google Scholar]
  97. 97.  Roux M, Schwessinger B, Albrecht C, Chinchilla D, Jones A et al. 2011. The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23:2440–55
    [Google Scholar]
  98. 98.  Ruzicka DR, Kandasamy MK, McKinney EC, Burgos-Rivera B, Meagher RB 2007. The ancient subclasses of Arabidopsis ACTIN DEPOLYMERIZING FACTOR genes exhibit novel and differential expression. Plant J 52:460–72
    [Google Scholar]
  99. 99.  Schmidt SM, Panstruga R 2007. Cytoskeletal functions in plant–microbe interactions. Physiol. Mol. Plant Pathol. 71:135–48
    [Google Scholar]
  100. 100.  Shimono M, Higaki T, Kaku H, Shibuya N, Hasezawa S, Day B 2016. Quantitative evaluation of stomatal cytoskeletal patterns during the activation of immune signaling in Arabidopsis thaliana. . PLOS ONE 11:e0159291
    [Google Scholar]
  101. 101.  Shimono M, Lu Y-J, Porter K, Kvitko BH, Henty-Ridilla JL et al. 2016. The Pseudomonas syringae type III effector HopG1 induces actin remodeling to promote symptom development and susceptibility during infection. Plant Physiol 171:2239–55
    [Google Scholar]
  102. 102.  Smith JM, Leslie ME, Robinson SJ, Korasick DA, Zhang T et al. 2014. Loss of Arabidopsis thaliana dynamin-related protein 2B reveals separation of innate immune signaling pathways. PLOS Pathog 10:e1004578
    [Google Scholar]
  103. 103.  Smith JM, Salamango DJ, Leslie ME, Collins CA, Heese A 2014. Sensitivity to flg22 is modulated by ligand-induced degradation and de novo synthesis of the endogenous flagellin-receptor FLAGELLIN-SENSING2. Plant Physiol 164:440–54
    [Google Scholar]
  104. 104.  Staiger CJ 2000. Signaling to the actin cytoskeleton in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51:257–88
    [Google Scholar]
  105. 105.  Staiger CJ, Sheahan MB, Khurana P, Wang X, McCurdy DW, Blanchoin L 2009. Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. J. Cell Biol. 184:269–80
    [Google Scholar]
  106. 106.  Takemoto D, Jones DA, Hardham AR 2003. GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. Plant J 33:775–92
    [Google Scholar]
  107. 107.  Tang D, Wang G, Zhou J-M 2017. Receptor kinases in plant-pathogen interactions: more than pattern-recognition. Plant Cell 29:618–37
    [Google Scholar]
  108. 108.  Tena G, Boudsocq M, Sheen J 2011. Protein kinase signaling networks in plant innate immunity. Curr. Opin. Plant Biol. 14:519–29
    [Google Scholar]
  109. 109.  Tian M, Chaudhry F, Ruzicka DR, Meagher RB, Staiger CJ, Day B 2009. Arabidopsis actin-depolymerizing factor AtADF4 mediates defense signal transduction triggered by the Pseudomonas syringae effector AvrPphB. Plant Physiol 150:815–24
    [Google Scholar]
  110. 110.  Torres MA, Dangl JL, Jones JDG 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]
  111. 111.  Torres MA, Jones JDG, Dangl JL 2006. Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–78
    [Google Scholar]
  112. 112.  Underwood W, Somerville SC 2008. Focal accumulation of defences at sites of fungal pathogen attack. J. Exp. Bot. 59:3501–8
    [Google Scholar]
  113. 113.  Underwood W, Somerville SC 2013. Perception of conserved pathogen elicitors at the plasma membrane leads to relocalization of the Arabidopsis PEN3 transporter. PNAS 110:12492–97
    [Google Scholar]
  114. 114.  van der Luit AH, Piatti T, van Doorn A, Musgrave A, Felix G et al. 2000. Elicitation of suspension-cultured tomato cells triggers the formation of phosphatidic acid and diacylglycerol pyrophosphate. Plant Physiol 123:1507–15
    [Google Scholar]
  115. 115.  Voigt CA 2014. Callose-mediated resistance to pathogenic intruders in plant defense-related papillae. Front. Plant Sci. 5:e168
    [Google Scholar]
  116. 116.  Wan J, Tanaka K, Zhang X-C, Son GH, Brechenmacher L et al. 2012. LYK4, a LysM receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. . Plant Physiol 160:396–406
    [Google Scholar]
  117. 117.  Wan J, Zhang X-C, Neece D, Ramonell KM, Clough S et al. 2008. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. . Plant Cell 20:471–81
    [Google Scholar]
  118. 118.  Wang W, Wen Y, Berkey R, Xiao S 2009. Specific targeting of the Arabidopsis resistance protein RPW8.2 to the interfacial membrane encasing the fungal haustorium renders broad-spectrum resistance to powdery mildew. Plant Cell 21:2898–913
    [Google Scholar]
  119. 119.  Wang X, Richards J, Gross T, Druka A, Kleinhofs A et al. 2013. The rpg4-mediated resistance to wheat stem rust (Puccinia graminis) in barley (Hordeum vulgare) requires Rpg5, a second NBS-LRR gene, and an actin depolymerization factor. Mol. Plant-Microbe Interact. 26:407–18
    [Google Scholar]
  120. 120.  Xu J-R, Staiger CJ, Hamer JE 1998. Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. PNAS 95:12713–18
    [Google Scholar]
  121. 121.  Yamaguchi T, Minami E, Shibuya N 2003. Activation of phospholipases by N-acetylchitooligosaccharide elicitor in suspension-cultured rice cells mediates reactive oxygen generation. Physiol. Plant. 118:361–70
    [Google Scholar]
  122. 122.  Yamaguchi T, Minami E, Ueki J, Shibuya N 2005. Elicitor-induced activation of phospholipases plays an important role for the induction of defense responses in suspension-cultured rice cells. Plant Cell Physiol 46:579–87
    [Google Scholar]
  123. 123.  Yang L, Qing L, Liu G, Peremyslov VV, Dolja VV, Wei Y 2014. Myosins XI modulate host cellular responses and penetration resistance to fungal pathogens. PNAS 111:13996–4001
    [Google Scholar]
  124. 124.  Zhang B, Hua Y, Wang J, Huo Y, Shimono M et al. 2017. TaADF4, an actin-depolymerizing factor from wheat, is required for resistance to the stripe rust pathogen Puccinia striiformis f. sp. tritici. Plant J. 89:1210–24
    [Google Scholar]
  125. 125.  Zhao J 2015. Phospholipase D and phosphatidic acid in plant defence response: from protein–protein and lipid–protein interactions to hormone signalling. J. Exp. Bot. 66:1721–36
    [Google Scholar]
  126. 126.  Zhao J, Devaiah SP, Wang C, Li M, Welti R, Wang X 2013. Arabidopsis phospholipase Dβ1 modulates defense responses to bacterial and fungal pathogens. New Phytol 199:228–40
    [Google Scholar]
  127. 127.  Zheng B, Han M, Bernier M, Wen JK 2009. Nuclear actin and actin-binding proteins in the regulation of transcription and gene expression. FEBS J 276:2669–85
    [Google Scholar]
  128. 128.  Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG et al. 2006. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–60
    [Google Scholar]
/content/journals/10.1146/annurev-phyto-080516-035632
Loading
/content/journals/10.1146/annurev-phyto-080516-035632
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error