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Role of AGC kinases in plant growth and stress responses

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Abstract

AGC kinases are important regulators of cell growth, metabolism, division, and survival in mammalian systems. Mutation or deregulation of members of this family of protein kinases contribute to the pathogenesis of many human diseases, including cancer and diabetes. Although AGC kinases are conserved in the plant kingdom, little is known about their molecular functions and targets. Some of the best-studied plant AGC kinases mediate auxin signaling and are thereby involved in the regulation of growth and morphogenesis. Furthermore, certain members are regulated by lipid-derived signals via the 3-phosphoinositide-dependent kinase 1 (PDK1) and the kinase target of rapamycin (TOR), similar to its animal counterparts. In this review, we discuss recent findings on plant AGC kinases that unravel important roles in the regulation of plant growth, immunity and cell death, and connections to stress-induced mitogen-activated protein kinase signaling cascades.

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References

  1. Pearce LR, Komander D, Alessi DR (2010) The nuts and bolts of AGC protein kinases. Nat Rev Mol Cell Biol 11(1):9–22

    Article  PubMed  CAS  Google Scholar 

  2. Bogre L, Okresz L, Henriques R, Anthony RG (2003) Growth signalling pathways in Arabidopsis and the AGC protein kinases. Trends Plant Sci 8(9):424–431

    Article  PubMed  CAS  Google Scholar 

  3. Devarenne TP, Ekengren SK, Pedley KF, Martin GB (2006) Adi3 is a Pdk1-interacting AGC kinase that negatively regulates plant cell death. EMBO J 25(1):255–265

    Article  PubMed  CAS  Google Scholar 

  4. Lawton MA, Yamamoto RT, Hanks SK, Lamb CJ (1989) Molecular cloning of plant transcripts encoding protein kinase homologs. Proc Natl Acad Sci USA 86(9):3140–3144

    Article  PubMed  CAS  Google Scholar 

  5. Matsui H, Miyao A, Takahashi A, Hirochika H (2010) Pdk1 kinase regulates basal disease resistance through the OsOxi1-OsPti1a phosphorylation cascade in rice. Plant Cell Physiol 51(12):2082–2091

    Article  PubMed  CAS  Google Scholar 

  6. Galvan-Ampudia CS, Offringa R (2007) Plant evolution: AGC kinases tell the auxin tale. Trends Plant Sci 12(12):541–547

    Article  PubMed  CAS  Google Scholar 

  7. Zhang Y, McCormick S (2009) AGCVIII kinases: at the crossroads of cellular signaling. Trends Plant Sci 14(12):689–695

    Article  PubMed  CAS  Google Scholar 

  8. Ding Z, Galvan-Ampudia CS, Demarsy E, Langowski L, Kleine-Vehn J, Fan Y, Morita MT, Tasaka M, Fankhauser C, Offringa R, Friml J (2011) Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nat Cell Biol 13(4):447–452

    Article  PubMed  CAS  Google Scholar 

  9. Robert HS, Offringa R (2008) Regulation of auxin transport polarity by AGC kinases. Curr Opin Plant Biol 11(5):495–502

    Article  PubMed  CAS  Google Scholar 

  10. Rentel MC, Lecourieux D, Ouaked F, Usher SL, Petersen L, Okamoto H, Knight H, Peck SC, Grierson CS, Hirt H, Knight MR (2004) OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427(6977):858–861

    Article  PubMed  CAS  Google Scholar 

  11. Matsui H, Yamazaki M, Kishi-Kaboshi M, Takahashi A, Hirochika H (2010) AGC kinase OsOxi1 positively regulates basal resistance through suppression of OsPti1a-mediated negative regulation. Plant Cell Physiol 51(10):1731–1744

    Article  PubMed  CAS  Google Scholar 

  12. Petersen LN, Ingle RA, Knight MR, Denby KJ (2009) OXI1 protein kinase is required for plant immunity against Pseudomonas syringae in Arabidopsis. J Exp Bot 60(13):3727–3735

    Article  PubMed  CAS  Google Scholar 

  13. Nicaise V, Roux M, Zipfel C (2009) Recent advances in PAMP-triggered immunity against bacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiol 150(4):1638–1647

    Article  PubMed  CAS  Google Scholar 

  14. Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18(2):465–476

    Article  PubMed  CAS  Google Scholar 

  15. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428(6984):764–767

    Article  PubMed  CAS  Google Scholar 

  16. Maekawa T, Kufer TA, Schulze-Lefert P (2011) NLR functions in plant and animal immune systems: so far and yet so close. Nat Immunol 12(9):817–826

    Article  PubMed  CAS  Google Scholar 

  17. Robert-Seilaniantz A, Grant M, Jones JD (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343

    Article  PubMed  CAS  Google Scholar 

  18. Munnik T, Nielsen E (2011) Green light for polyphosphoinositide signals in plants. Curr Opin Plant Biol 14(5):489–497

    Article  PubMed  CAS  Google Scholar 

  19. Testerink C, Munnik T (2011) Molecular, cellular, and physiological responses to phosphatidic acid formation in plants. J Exp Bot 62(7):2349–2361

    Article  PubMed  CAS  Google Scholar 

  20. Mora A, Komander D, van Aalten DM, Alessi DR (2004) PDK1, the master regulator of AGC kinase signal transduction. Semin Cell Dev Biol 15(2):161–170

    Article  PubMed  CAS  Google Scholar 

  21. Komander D, Fairservice A, Deak M, Kular GS, Prescott AR, Peter Downes C, Safrany ST, Alessi DR, van Aalten DM (2004) Structural insights into the regulation of PDK1 by phosphoinositides and inositol phosphates. EMBO J 23(20):3918–3928

    Article  PubMed  CAS  Google Scholar 

  22. McManus EJ, Collins BJ, Ashby PR, Prescott AR, Murray-Tait V, Armit LJ, Arthur JS, Alessi DR (2004) The in vivo role of PtdIns(3,4,5)P3 binding to PDK1 PH domain defined by knocking mutation. EMBO J 23(10):2071–2082

    Article  PubMed  CAS  Google Scholar 

  23. Biondi RM (2004) Phosphoinositide-dependent protein kinase 1, a sensor of protein conformation. Trends Biochem Sci 29(3):136–142

    Article  PubMed  CAS  Google Scholar 

  24. Anthony RG, Henriques R, Helfer A, Meszaros T, Rios G, Testerink C, Munnik T, Deak M, Koncz C, Bogre L (2004) A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J 23(3):572–581

    Article  PubMed  CAS  Google Scholar 

  25. Dittrich AC, Devarenne TP (2012) Characterization of a PDK1 homologue from the moss Physcomitrella patens. Plant Physiol 158(2):1018–1033

    Article  PubMed  CAS  Google Scholar 

  26. Zegzouti H, Anthony RG, Jahchan N, Bogre L, Christensen SK (2006) Phosphorylation and activation of PINOID by the phospholipid signaling kinase 3-phosphoinositide-dependent protein kinase 1 (PDK1) in Arabidopsis. Proc Natl Acad Sci USA 103(16):6404–6409

    Article  PubMed  CAS  Google Scholar 

  27. Zegzouti H, Li W, Lorenz TC, Xie M, Payne CT, Smith K, Glenny S, Payne GS, Christensen SK (2006) Structural and functional insights into the regulation of Arabidopsis AGC VIIIa kinases. J Biol Chem 281(46):35520–35530

    Article  PubMed  CAS  Google Scholar 

  28. Camehl I, Drzewiecki C, Vadassery J, Shahollari B, Sherameti I, Forzani C, Munnik T, Hirt H, Oelmuller R (2011) The OXI1 kinase pathway mediates Piriformospora indica-induced growth promotion in Arabidopsis. PLoS Pathog 7(5):e1002051

    Article  PubMed  CAS  Google Scholar 

  29. Deak M, Casamayor A, Currie RA, Downes CP, Alessi DR (1999) Characterisation of a plant 3-phosphoinositide-dependent protein kinase-1 homologue which contains a pleckstrin homology domain. FEBS Lett 451(3):220–226

    Article  PubMed  CAS  Google Scholar 

  30. Mahfouz MM, Kim S, Delauney AJ, Verma DP (2006) Arabidopsis target of rapamycin interacts with raptor, which regulates the activity of S6 kinase in response to osmotic stress signals. Plant Cell 18(2):477–490

    Article  PubMed  CAS  Google Scholar 

  31. Otterhag L, Gustavsson N, Alsterfjord M, Pical C, Lehrach H, Gobom J, Sommarin M (2006) Arabidopsis PDK1: identification of sites important for activity and downstream phosphorylation of S6 kinase. Biochimie 88(1):11–21

    Article  PubMed  CAS  Google Scholar 

  32. Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124(3):471–484

    Article  PubMed  CAS  Google Scholar 

  33. Robaglia C, Thomas M, Meyer C (2012) Sensing nutrient and energy status by SnRK1 and TOR kinases. Curr Opin Plant Biol 15(3):301–307

    Article  PubMed  CAS  Google Scholar 

  34. Anderson GH, Veit B, Hanson MR (2005) The Arabidopsis AtRaptor genes are essential for post-embryonic plant growth. BMC Biol 3:12

    Article  PubMed  Google Scholar 

  35. Deprost D, Truong HN, Robaglia C, Meyer C (2005) An Arabidopsis homolog of RAPTOR/KOG1 is essential for early embryo development. Biochem Biophys Res Commun 326(4):844–850

    Article  PubMed  CAS  Google Scholar 

  36. Menand B, Desnos T, Nussaume L, Berger F, Bouchez D, Meyer C, Robaglia C (2002) Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. Proc Natl Acad Sci USA 99(9):6422–6427

    Article  PubMed  CAS  Google Scholar 

  37. Moreau M, Azzopardi M, Clement G, Dobrenel T, Marchive C, Renne C, Martin-Magniette ML, Taconnat L, Renou JP, Robaglia C, Meyer C (2012) Mutations in the Arabidopsis homolog of LST8/GbetaL, a partner of the target of rapamycin kinase, impair plant growth, flowering, and metabolic adaptation to long days. Plant Cell 24(2):463–481

    Article  PubMed  CAS  Google Scholar 

  38. Deprost D, Yao L, Sormani R, Moreau M, Leterreux G, Nicolai M, Bedu M, Robaglia C, Meyer C (2007) The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Rep 8(9):864–870

    Article  PubMed  CAS  Google Scholar 

  39. Hong Y, Pan X, Welti R, Wang X (2008) The effect of phospholipase Dalpha3 on Arabidopsis response to hyperosmotic stress and glucose. Plant Signal Behav 3(12):1099–1100

    Article  PubMed  Google Scholar 

  40. Moritz A, Li Y, Guo A, Villen J, Wang Y, MacNeill J, Kornhauser J, Sprott K, Zhou J, Possemato A, Ren JM, Hornbeck P, Cantley LC, Gygi SP, Rush J, Comb MJ (2010) Akt-RSK-S6 kinase signaling networks activated by oncogenic receptor tyrosine kinases. Sci Signal 3(136):ra64

    Article  PubMed  Google Scholar 

  41. Huang F, Zago MK, Abas L, van Marion A, Galvan-Ampudia CS, Offringa R (2010) Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell 22(4):1129–1142

    Article  PubMed  CAS  Google Scholar 

  42. Anthony RG, Khan S, Costa J, Pais MS, Bogre L (2006) The Arabidopsis protein kinase PTI1-2 is activated by convergent phosphatidic acid and oxidative stress signaling pathways downstream of PDK1 and OXI1. J Biol Chem 281(49):37536–37546

    Article  PubMed  CAS  Google Scholar 

  43. Forzani C, Carreri A, de la Fuente van Bentem S, Lecourieux D, Lecourieux F, Hirt H (2011) The Arabidopsis protein kinase Pto-interacting 1–4 is a common target of the oxidative signal-inducible 1 and mitogen-activated protein kinases. FEBS J 278(7):1126–1136

    Article  PubMed  CAS  Google Scholar 

  44. Zhou J, Loh YT, Bressan RA, Martin GB (1995) The tomato gene Pti1 encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response. Cell 83(6):925–935

    Article  PubMed  CAS  Google Scholar 

  45. Sessa G, D’Ascenzo M, Martin GB (2000) The major site of the pti1 kinase phosphorylated by the pto kinase is located in the activation domain and is required for pto-pti1 physical interaction. Eur J Biochem 267(1):171–178

    Article  PubMed  CAS  Google Scholar 

  46. Takahashi A, Agrawal GK, Yamazaki M, Onosato K, Miyao A, Kawasaki T, Shimamoto K, Hirochika H (2007) Rice Pti1a negatively regulates RAR1-dependent defense responses. Plant Cell 19(9):2940–2951

    Article  PubMed  CAS  Google Scholar 

  47. Howden AJ, Salek M, Miguet L, Pullen M, Thomas B, Knight MR, Sweetlove LJ (2010) The phosphoproteome of Arabidopsis plants lacking the oxidative signal-inducible1 (OXI1) protein kinase. New Phytol 190(1):49–56

    Article  Google Scholar 

  48. Dittrich AC, Devarenne TP (2012) An ATP analog-sensitive version of the tomato cell death suppressor protein kinase Adi3 for use in substrate identification. Biochim Biophys Acta 1824(2):269–273

    Article  PubMed  CAS  Google Scholar 

  49. Pitzschke A, Schikora A, Hirt H (2009) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12(4):421–426

    Article  PubMed  CAS  Google Scholar 

  50. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415(6875):977–983

    Article  PubMed  CAS  Google Scholar 

  51. Ichimura K, Casais C, Peck SC, Shinozaki K, Shirasu K (2006) MEKK1 is required for MPK4 activation and regulates tissue-specific and temperature-dependent cell death in Arabidopsis. J Biol Chem 281(48):36969–36976

    Article  PubMed  CAS  Google Scholar 

  52. Gao M, Liu J, Bi D, Zhang Z, Cheng F, Chen S, Zhang Y (2008) MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res 18(12):1190–1198

    Article  PubMed  CAS  Google Scholar 

  53. del Pozo O, Pedley KF, Martin GB (2004) MAPKKKalpha is a positive regulator of cell death associated with both plant immunity and disease. EMBO J 23(15):3072–3082

    Article  PubMed  Google Scholar 

  54. Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earle ED, Tanksley SD (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262(5138):1432–1436

    Article  PubMed  CAS  Google Scholar 

  55. Kim YJ, Lin NC, Martin GB (2002) Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109(5):589–598

    Article  PubMed  CAS  Google Scholar 

  56. Ek-Ramos MJ, Avila J, Cheng C, Martin GB, Devarenne TP (2010) The T-loop extension of the tomato protein kinase AvrPto-dependent Pto-interacting protein 3 (Adi3) directs nuclear localization for suppression of plant cell death. J Biol Chem 285(23):17584–17594

    Article  PubMed  CAS  Google Scholar 

  57. Oh CS, Martin GB (2011) Effector-triggered immunity mediated by the Pto kinase. Trends Plant Sci 16(3):132–140

    Article  PubMed  CAS  Google Scholar 

  58. Vossen JH, Abd-El-Haliem A, Fradin EF, van den Berg GC, Ekengren SK, Meijer HJ, Seifi A, Bai Y, ten Have A, Munnik T, Thomma BP, Joosten MH (2010) Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance. Plant J 62(2):224–239

    Article  PubMed  CAS  Google Scholar 

  59. Jacobs S, Zechmann B, Molitor A, Trujillo M, Petutschnig E, Lipka V, Kogel KH, Schafer P (2011) Broad-spectrum suppression of innate immunity is required for colonization of Arabidopsis roots by the fungus Piriformospora indica. Plant Physiol 156(2):726–740

    Article  PubMed  CAS  Google Scholar 

  60. Torres MA, Dangl JL, Jones JD (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99(1):517–522

    Article  PubMed  CAS  Google Scholar 

  61. Zhang J, Shao F, Li Y, Cui H, Chen L, Li H, Zou Y, Long C, Lan L, Chai J, Chen S, Tang X, Zhou JM (2007) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1(3):175–185

    Article  PubMed  CAS  Google Scholar 

  62. Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H, Shibuya N (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64(2):204–214

    Article  PubMed  CAS  Google Scholar 

  63. Hammond RW, Zhao Y (2000) Characterization of a tomato protein kinase gene induced by infection by Potato spindle tuber viroid. Mol Plant Microbe Interact 13(9):903–910

    Article  PubMed  CAS  Google Scholar 

  64. Diaz-Troya S, Perez-Perez ME, Florencio FJ, Crespo JL (2008) The role of TOR in autophagy regulation from yeast to plants and mammals. Autophagy 4(7):851–865

    PubMed  CAS  Google Scholar 

  65. Chen WS, Xu PZ, Gottlob K, Chen ML, Sokol K, Shiyanova T, Roninson I, Weng W, Suzuki R, Tobe K, Kadowaki T, Hay N (2001) Growth retardation and increased apoptosis in mice with homozygous disruption of the Akt1 gene. Genes Dev 15(17):2203–2208

    Article  PubMed  CAS  Google Scholar 

  66. Hofius D, Schultz-Larsen T, Joensen J, Tsitsigiannis DI, Petersen NH, Mattsson O, Jorgensen LB, Jones JD, Mundy J, Petersen M (2009) Autophagic components contribute to hypersensitive cell death in Arabidopsis. Cell 137(4):773–783

    Article  PubMed  CAS  Google Scholar 

  67. Lenz HD, Haller E, Melzer E, Kober K, Wurster K, Stahl M, Bassham DC, Vierstra RD, Parker JE, Bautor J, Molina A, Escudero V, Shindo T, van der Hoorn RA, Gust AA, Nurnberger T (2011) Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens. Plant J 66(5):818–830

    Article  PubMed  CAS  Google Scholar 

  68. Liu Y, Xiong Y, Bassham DC (2009) Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 5(7):954–963

    Article  PubMed  CAS  Google Scholar 

  69. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, Baba M, Baehrecke EH, Bahr BA, Ballabio A, Bamber BA, Bassham DC, Bergamini E, Bi X, Biard-Piechaczyk M, Blum JS, Bredesen DE, Brodsky JL, Brumell JH, Brunk UT, Bursch W, Camougrand N, Cebollero E, Cecconi F, Chen Y, Chin LS, Choi A, Chu CT, Chung J, Clarke PG, Clark RS, Clarke SG, Clave C, Cleveland JL, Codogno P, Colombo MI, Coto-Montes A, Cregg JM, Cuervo AM, Debnath J, Demarchi F, Dennis PB, Dennis PA, Deretic V, Devenish RJ, Di Sano F, Dice JF, Difiglia M, Dinesh-Kumar S, Distelhorst CW, Djavaheri-Mergny M, Dorsey FC, Droge W, Dron M, Dunn WA, Jr., Duszenko M, Eissa NT, Elazar Z, Esclatine A, Eskelinen EL, Fesus L, Finley KD, Fuentes JM, Fueyo J, Fujisaki K, Galliot B, Gao FB, Gewirtz DA, Gibson SB, Gohla A, Goldberg AL, Gonzalez R, Gonzalez-Estevez C, Gorski S, Gottlieb RA, Haussinger D, He YW, Heidenreich K, Hill JA, Hoyer-Hansen M, Hu X, Huang WP, Iwasaki A, Jaattela M, Jackson WT, Jiang X, Jin S, Johansen T, Jung JU, Kadowaki M, Kang C, Kelekar A, Kessel DH, Kiel JA, Kim HP, Kimchi A, Kinsella TJ, Kiselyov K, Kitamoto K, Knecht E, Komatsu M, Kominami E, Kondo S, Kovacs AL, Kroemer G, Kuan CY, Kumar R, Kundu M, Landry J, Laporte M, Le W, Lei HY, Lenardo MJ, Levine B, Lieberman A, Lim KL, Lin FC, Liou W, Liu LF, Lopez-Berestein G, Lopez-Otin C, Lu B, Macleod KF, Malorni W, Martinet W, Matsuoka K, Mautner J, Meijer AJ, Melendez A, Michels P, Miotto G, Mistiaen WP, Mizushima N, Mograbi B, Monastyrska I, Moore MN, Moreira PI, Moriyasu Y, Motyl T, Munz C, Murphy LO, Naqvi NI, Neufeld TP, Nishino I, Nixon RA, Noda T, Nurnberg B, Ogawa M, Oleinick NL, Olsen LJ, Ozpolat B, Paglin S, Palmer GE, Papassideri I, Parkes M, Perlmutter DH, Perry G, Piacentini M, Pinkas-Kramarski R, Prescott M, Proikas-Cezanne T, Raben N, Rami A, Reggiori F, Rohrer B, Rubinsztein DC, Ryan KM, Sadoshima J, Sakagami H, Sakai Y, Sandri M, Sasakawa C, Sass M, Schneider C, Seglen PO, Seleverstov O, Settleman J, Shacka JJ, Shapiro IM, Sibirny A, Silva-Zacarin EC, Simon HU, Simone C, Simonsen A, Smith MA, Spanel-Borowski K, Srinivas V, Steeves M, Stenmark H, Stromhaug PE, Subauste CS, Sugimoto S, Sulzer D, Suzuki T, Swanson MS, Tabas I, Takeshita F, Talbot NJ, Talloczy Z, Tanaka K, Tanaka K, Tanida I, Taylor GS, Taylor JP, Terman A, Tettamanti G, Thompson CB, Thumm M, Tolkovsky AM, Tooze SA, Truant R, Tumanovska LV, Uchiyama Y, Ueno T, Uzcategui NL, van der Klei I, Vaquero EC, Vellai T, Vogel MW, Wang HG, Webster P, Wiley JW, Xi Z, Xiao G, Yahalom J, Yang JM, Yap G, Yin XM, Yoshimori T, Yu L, Yue Z, Yuzaki M, Zabirnyk O, Zheng X, Zhu X, Deter RL (2008) Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4 (2):151–175

    Google Scholar 

  70. Liu Y, Bassham DC (2010) TOR is a negative regulator of autophagy in Arabidopsis thaliana. PLoS One 5(7):e11883

    Article  PubMed  Google Scholar 

  71. Perez-Perez ME, Florencio FJ, Crespo JL (2010) Inhibition of target of rapamycin signaling and stress activate autophagy in Chlamydomonas reinhardtii. Plant Physiol 152(4):1874–1888

    Article  PubMed  CAS  Google Scholar 

  72. Devarenne TP (2011) The plant cell death suppressor Adi3 interacts with the autophagic protein Atg8h. Biochem Biophys Res Commun 412(4):699–703

    Article  PubMed  CAS  Google Scholar 

  73. Liu Y, Schiff M, Czymmek K, Talloczy Z, Levine B, Dinesh-Kumar SP (2005) Autophagy regulates programmed cell death during the plant innate immune response. Cell 121(4):567–577

    Article  PubMed  CAS  Google Scholar 

  74. Qiang X, Weiss M, Kogel KH, Schafer P (2011) Piriformospora indica-a mutualistic basidiomycete with an exceptionally large plant host range. Mol Plant Pathol 13(5):508–518

    Article  PubMed  Google Scholar 

  75. Vadassery J, Ranf S, Drzewiecki C, Mithofer A, Mazars C, Scheel D, Lee J, Oelmuller R (2009) A cell wall extract from the endophytic fungus Piriformospora indica promotes growth of Arabidopsis seedlings and induces intracellular calcium elevation in roots. Plant J 59(2):193–206

    Article  PubMed  CAS  Google Scholar 

  76. Shahollari B, Vadassery J, Varma A, Oelmuller R (2007) A leucine-rich repeat protein is required for growth promotion and enhanced seed production mediated by the endophytic fungus Piriformospora indica in Arabidopsis thaliana. Plant J 50(1):1–13

    Article  PubMed  CAS  Google Scholar 

  77. Stein E, Molitor A, Kogel KH, Waller F (2008) Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1. Plant Cell Physiol 49(11):1747–1751

    Article  PubMed  CAS  Google Scholar 

  78. Schafer P, Pfiffi S, Voll LM, Zajic D, Chandler PM, Waller F, Scholz U, Pons-Kuhnemann J, Sonnewald S, Sonnewald U, Kogel KH (2009) Phytohormones in plant root-Piriformospora indica mutualism. Plant Signal Behav 4(7):669–671

    Article  PubMed  Google Scholar 

  79. Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B, Novak O, Strnad M, Ludwig-Muller J, Oelmuller R (2008) The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. Mol Plant Microbe Interact 21(10):1371–1383

    Article  PubMed  CAS  Google Scholar 

  80. Camehl I, Sherameti I, Venus Y, Bethke G, Varma A, Lee J, Oelmuller R (2010) Ethylene signalling and ethylene-targeted transcription factors are required to balance beneficial and nonbeneficial traits in the symbiosis between the endophytic fungus Piriformospora indica and Arabidopsis thaliana. New Phytol 185(4):1062–1073

    Article  PubMed  CAS  Google Scholar 

  81. Henriques R, Magyar Z, Monardes A, Khan S, Zalejski C, Orellana J, Szabados L, de la Torre C, Koncz C, Bogre L (2010) Arabidopsis S6 kinase mutants display chromosome instability and altered RBR1-E2F pathway activity. EMBO J 29(17):2979–2993

    Article  PubMed  CAS  Google Scholar 

  82. Dhonukshe P, Huang F, Galvan-Ampudia CS, Mahonen AP, Kleine-Vehn J, Xu J, Quint A, Prasad K, Friml J, Scheres B, Offringa R (2010) Plasma membrane-bound AGC3 kinases phosphorylate PIN auxin carriers at TPRXS (N/S) motifs to direct apical PIN recycling. Development 137(19):3245–3255

    Article  PubMed  CAS  Google Scholar 

  83. Zourelidou M, Muller I, Willige BC, Nill C, Jikumaru Y, Li H, Schwechheimer C (2009) The polarly localized D6 protein kinase is required for efficient auxin transport in Arabidopsis thaliana. Development 136(4):627–636

    Article  PubMed  CAS  Google Scholar 

  84. Pflieger D, Bigeard J, Hirt H (2011) Isolation and characterization of plant protein complexes by mass spectrometry. Proteomics 11(9):1824–1833

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The project is supported by funding from the following projects: ANR MAPK, EU ADYSARC, and Systems Biology SHIPREC. Due to space limitations, we apologize to all colleagues whose work has not been included in the review.

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Garcia, A.V., Al-Yousif, M. & Hirt, H. Role of AGC kinases in plant growth and stress responses. Cell. Mol. Life Sci. 69, 3259–3267 (2012). https://doi.org/10.1007/s00018-012-1093-3

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