Plant Cell Reports

, Volume 34, Issue 3, pp 457–468 | Cite as

The Arabidopsis ROP-activated receptor-like cytoplasmic kinase RLCK VI_A3 is involved in control of basal resistance to powdery mildew and trichome branching

  • Tina Reiner
  • Caroline Hoefle
  • Christina Huesmann
  • Dalma Ménesi
  • Attila Fehér
  • Ralph Hückelhoven
Original Paper

Abstract

Key message

TheArabidopsisreceptor-like cytoplasmic kinase AtRLCK VI_A3 is activated by AtROPs and is involved in trichome branching and pathogen interaction.

Abstract

Receptor-like cytoplasmic kinases (RLCKs) belong to the large superfamily of receptor-like kinases, which are involved in a variety of cellular processes like plant growth, development and immune responses. Recent studies suggest that RLCKs of the VI_A subfamily are possible downstream effectors of the small monomeric G proteins of the plant-specific Rho family, called ‘Rho of plants’ (RAC/ROPs). Here, we describe Arabidopsisthaliana AtRLCK VI_A3 as a molecular interactor of AtROPs. In Arabidopsis epidermal cells, transient co-expression of plasma membrane located constitutively activated (CA) AtROP4 or CA AtROP6 resulting in the recruitment of green fluorescent protein-tagged AtRLCK VI_A3 to the cell periphery. Intrinsic kinase activity of AtRLCK VI_A3 was enhanced in the presence of CA AtROP6 in vitro and further suggested a functional interaction between the proteins. In the interaction of the biotrophic powdery mildew fungus Erysiphe cruciferarum (E. cruciferarum) and its host plant Arabidopsis, Atrlck VI_A3 mutant lines supported enhanced fungal reproduction. Furthermore Atrlck VI_A3 mutant lines showed slightly reduced size and an increase in trichome branch number compared to wild-type plants. In summary, our data suggest a role of the AtROP-regulated AtRLCK VI_A3 in basal resistance to E. cruciferarum as well as in plant growth and cellular differentiation during trichome morphogenesis. Results are discussed in the context of literature suggesting a function of RAC/ROPs in both resistance and susceptibility to pathogen infection.

Keywords

Receptor-like cytoplasmic kinase (RLCK) RAC/ROP GTPase Arabidopsis thaliana Erysiphe cruciferarum Trichome 

Notes

Acknowledgments

This work was supported by grants from the German Research Foundation (HU886/3 and SFB924 to R.H.) and the Hungarian Scientific Research Fund (OTKA K101112). The authors gratefully acknowledge the support by the Faculty Graduate Center Weihenstephan of TUM Graduate School at Technische Universität München, Germany.

Conflict of interest

The authors declare no conflict of interest.

References

  1. Afzal AJ, Wood AJ, Lightfoot DA (2008) Plant receptor-like serine threonine kinases: roles in signaling and plant defense. Mol Plant Microbe Interact 21:507–517CrossRefPubMedGoogle Scholar
  2. Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W (2009) Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323:1485–1488CrossRefPubMedGoogle Scholar
  3. Berken A (2006) ROPs in the spotlight of plant signal transduction. Cell Mol Life Sci 63:2446–2459CrossRefPubMedGoogle Scholar
  4. Burr CA, Leslie ME, Orlowski SK, Chen I, Wright CE, Daniels MJ, Liljegren SJ (2011) CAST AWAY, a membrane-associated receptor-like kinase, inhibits organ abscission in Arabidopsis. Plant Physiol 156:1837–1850CrossRefPubMedCentralPubMedGoogle Scholar
  5. Chen L, Shiotani K, Togashi T, Miki D, Aoyama M, Wong HL, Kawasaki T, Shimamoto K (2010) Analysis of the Rac/Rop small GTPase family in rice: expression, subcellular localization and role in disease resistance. Plant Cell Physiol 51:585–595CrossRefPubMedGoogle Scholar
  6. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  7. Dorjgotov D, Jurca ME, Fodor-Dunai C, Szucs A, Ötvös K, Klement É, Bíró J, Fehér A (2009) Plant Rho-type (Rop) GTPase-dependent activation of receptor-like cytoplasmic kinases in vitro. FEBS Lett 583:1175–1182CrossRefPubMedGoogle Scholar
  8. Dörmann P, Kim H, Ott T, Schulze-Lefert P, Trujillo M, Wewer V, Hückelhoven R (2014) Cell-autonomous defense, re-organization and trafficking of membranes in plant-microbe interactions. New Phytol 204:815–822CrossRefPubMedGoogle Scholar
  9. Engelsdorf T, Horst RJ, Pröls R, Pröschel M, Dietz F, Hückelhoven R, Voll LM (2013) Reduced carbohydrate availability enhances the susceptibility of Arabidopsis toward Colletotrichum higginsianum. Plant Physiol 162:225–238CrossRefPubMedCentralPubMedGoogle Scholar
  10. Finer JJ, Vain P, Jones MW, McMullen MD (1992) Development of the particle inflow gun for DNA delivery to plant cells. Plant Cell Rep 11:323–328CrossRefPubMedGoogle Scholar
  11. Fraaije BA, Lovell DJ, Rohel EA, Hollomon DW (1999) Rapid detection and diagnosis of Septoria tritici epidemics in wheat using a polymerase chain reaction/PicoGreen assay. J Appl Microbiol 86:701–708CrossRefGoogle Scholar
  12. Fu Y, Li H, Yang ZB (2002) The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis. Plant Cell 14:777–794CrossRefPubMedCentralPubMedGoogle Scholar
  13. Fu Y, Gu Y, Zheng Z, Wasteneys G, Yang Z (2005) Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 120:687–700CrossRefPubMedGoogle Scholar
  14. Fu Y, Xu T, Zhu L, Wen M, Yang Z (2009) A ROP GTPase signaling pathway controls cortical microtubule ordering and cell expansion in Arabidopsis. Curr Biol 19:1827–1832CrossRefPubMedCentralPubMedGoogle Scholar
  15. Gish LA, Clark SE (2011) The RLK/Pelle family of kinases. Plant J 66:117–127CrossRefPubMedGoogle Scholar
  16. Hoefle C, Hückelhoven R (2008) Enemy at the gates—traffic at the plant cell pathogen interface. Cell Microbiol 10:2400–2407CrossRefPubMedGoogle Scholar
  17. Hoefle C, Huesmann C, Schultheiss H, Bornke F, Hensel G, Kumlehn J, Hückelhoven R (2011) A barley ROP GTPase ACTIVATING PROTEIN associates with microtubules and regulates entry of the barley powdery mildew fungus into leaf epidermal cells. Plant Cell 23:2422–2439CrossRefPubMedCentralPubMedGoogle Scholar
  18. Huesmann C, Hoefle C, Hückelhoven R (2011) ROPGAPs of Arabidopsis limit susceptibility to powdery mildew. Plant Signal Behav 6:1691–1694CrossRefPubMedCentralPubMedGoogle Scholar
  19. Huesmann C, Reiner T, Hoefle C, Preuss J, Jurca ME, Domoki M, Fehér A, Hückelhoven R (2012) Barley ROP binding kinase1 is involved in microtubule organization and in basal penetration resistance to the barley powdery mildew fungus. Plant Physiol 159:311–320CrossRefPubMedCentralPubMedGoogle Scholar
  20. Hülskamp M, Miséra S, Jürgens G (1994) Genetic dissection of trichome cell development in Arabidopsis. Cell 76:555–566CrossRefPubMedGoogle Scholar
  21. Ishida T, Kurata T, Okada K, Wada T (2008) A genetic regulatory network in the development of trichomes and root hairs. Annu Rev Plant Biol 59:365–386CrossRefPubMedGoogle Scholar
  22. Joseph RE, Andreotti AH (2008) Bacterial expression and purification of interleukin-2 tyrosine kinase: single step separation of the chaperonin impurity. Protein Expr Purif 60:194–197CrossRefPubMedCentralPubMedGoogle Scholar
  23. Jurca ME, Bottka S, Fehér A (2008) Characterization of a family of Arabidopsis receptor-like cytoplasmic kinases (RLCK class VI). Plant Cell Rep 27:739–748CrossRefPubMedGoogle Scholar
  24. 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 23:2831–2849CrossRefPubMedCentralPubMedGoogle Scholar
  25. Li H, Shen JJ, Zheng ZL, Lin Y, Yang Z (2001) The Rop GTPase switch controls multiple developmental processes in Arabidopsis. Plant Physiol 126:670–684CrossRefPubMedCentralPubMedGoogle Scholar
  26. Lin W, Ma X, Shan L, He P (2013) Big roles of small kinases: the complex functions of receptor-like cytoplasmic kinases in plant immunity and development. J Integr Plant Biol 55:1188–1197CrossRefPubMedGoogle Scholar
  27. Lu D, Wu S, Gao X, Zhang Y, Shan L, He P (2010) A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc Natl Acad Sci USA 107:496–501CrossRefPubMedCentralPubMedGoogle Scholar
  28. Mathur J (2006) Trichome cell morphogenesis in Arabidopsis: a continuum of cellular decisions. Can J Bot 84:604–612CrossRefGoogle Scholar
  29. Mathur J, Chua NH (2000) Microtubule stabilization leads to growth reorientation in Arabidopsis trichomes. Plant Cell 12:465–477CrossRefPubMedCentralPubMedGoogle Scholar
  30. Molendijk AJ, Ruperti B, Singh MK, Dovzhenko A, Ditengou FA, Milia M, Westphal L, Rosahl S, Soellick T-R, Uhrig J, Weingarten L, Huber M, Palme K (2008) A cysteine-rich receptor-like kinase NCRK and a pathogen-induced protein kinase RBK1 are Rop GTPase interactors. Plant J 53:909–923CrossRefPubMedGoogle Scholar
  31. Murase K, Shiba H, Iwano M, Che FS, Watanabe M, Isogai A, Takayama S (2004) A membrane-anchored protein kinase involved in Brassica self-incompatibility signaling. Science 303:1516–1519CrossRefPubMedGoogle Scholar
  32. Nibau C, Wu HM, Cheung AY (2006) RAC/ROP GTPases: ‘hubs’ for signal integration and diversification in plants. Trends Plant Sci 11:309–315CrossRefPubMedGoogle Scholar
  33. Ono E, Wong HL, Kawasaki T, Hasegawa M, Kodama O, Shimamoto K (2001) Essential role of the small GTPase Rac in disease resistance of rice. Proc Natl Acad Sci USA 98:759–764CrossRefPubMedCentralPubMedGoogle Scholar
  34. Pathuri IP, Zellerhoff N, Schaffrath U, Hensel G, Kumlehn J, Kogel KH, Eichmann R, Hückelhoven R (2008) Constitutively activated barley ROPs modulate epidermal cell size, defense reactions and interactions with fungal leaf pathogens. Plant Cell Rep 27:1877–1887CrossRefPubMedGoogle Scholar
  35. Pathuri IP, Imani J, Babaeizad V, Kogel KH, Eichmann R, Hückelhoven R (2009) Ectopic expression of barley constitutively activated ROPs supports susceptibility to powdery mildew and bacterial wildfire in tobacco. Eur J Plant Pathol 125:317–327CrossRefGoogle Scholar
  36. Poraty-Gavra L, Zimmermann P, Haigis S, Bednarek P, Hazak O, Stelmakh OR, Sadot E, Schulze-Lefert P, Gruissem W, Yalovsky S (2013) The Arabidopsis Rho of plants GTPase AtROP6 functions in developmental and pathogen response pathways. Plant Physiol 161:1172–1188CrossRefPubMedCentralPubMedGoogle Scholar
  37. Sambade A, Findlay K, Schäffner AR, Lloyd CW, Buschmann H (2014) Actin-dependent and -independent functions of cortical microtubules in the differentiation of Arabidopsis leaf trichomes. Plant Cell 26:1629–1644CrossRefPubMedGoogle Scholar
  38. Schellmann S, Hülskamp M (2005) Epidermal differentiation: trichomes in Arabidopsis as a model system. Int J Dev Biol 49:579–584CrossRefPubMedGoogle Scholar
  39. Schultheiss H, Dechert C, Kogel KH, Hückelhoven R (2002) A small GTP-binding host protein is required for entry of powdery mildew fungus into epidermal cells of barley. Plant Physiol 128:1447–1454CrossRefPubMedCentralPubMedGoogle Scholar
  40. Schultheiss H, Dechert C, Kogel KH, Hückelhoven R (2003) Functional analysis of barley RAC/ROP G-protein family members in susceptibility to the powdery mildew fungus. Plant J 36(5):589–601CrossRefPubMedGoogle Scholar
  41. Schweizer P, Pokorny J, Abderhalden O, Dudler R (1999) A transient assay system for the functional assessment of defense-related genes in wheat. Mol Plant Microbe Interact 12:647–654CrossRefGoogle Scholar
  42. Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, Li WH (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220–1234CrossRefPubMedCentralPubMedGoogle Scholar
  43. Singh MK, Ren F, Giesemann T, Bosco CD, Pasternak TP, Blein T, Ruperti B, Schmidt G, Aktories K, Molendijk AJ, Palme K (2013) Modification of plant Rac/Rop GTPase signalling using bacterial toxin transgenes. Plant J 73:314–324Google Scholar
  44. Sreeramulu S, Mostizky Y, Sunitha S, Shani E, Nahum H, Salomon D, Hayun LB, Gruetter C, Rauh D, Ori N, Sessa G (2013) BSKs are partially redundant positive regulators of brassinosteroid signaling in Arabidopsis. Plant J 74:905–919CrossRefPubMedGoogle Scholar
  45. Swiderski MR, Innes RW (2001) The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. Plant J 26:101–112CrossRefPubMedGoogle Scholar
  46. Szymanski DB (2005) Breaking the WAVE complex: the point of Arabidopsis trichomes. Curr Opin Plant Biol 8:103–112CrossRefPubMedGoogle Scholar
  47. Tang W, Kim TW, Oses-Prieto JA, Sun Y, Deng Z, Zhu S, Wang R, Burlingame AL, Wang ZY (2008) BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321:557–560CrossRefPubMedCentralPubMedGoogle Scholar
  48. Veronese P, Nakagami H, Bluhm B, AbuQamar S, Chen X, Salmeron J, Dietrich RA, Hirt H, Mengiste T (2006) The membrane-anchored BOTRYTIS-INDUCED KINASE1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens. Plant Cell 18:257–273CrossRefPubMedCentralPubMedGoogle Scholar
  49. Weis C, Hückelhoven R, Eichmann R (2013) LIFEGUARD proteins support plant colonization by biotrophic powdery mildew fungi. J Exp Bot 64:3855–3867CrossRefPubMedCentralPubMedGoogle Scholar
  50. Winge P, Brembu T, Kristensen R, Bones AM (2000) Genetic structure and evolution of RAC-GTPases in Arabidopsis thaliana. Genetics 156:1959–1971PubMedCentralPubMedGoogle Scholar
  51. Xu T, Wen M, Nagawa S, Fu Y, Chen JG, Wu MJ, Perrot-Rechenmann C, Friml J, Jones AM, Yang Z (2010) Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143:99–110CrossRefPubMedCentralPubMedGoogle Scholar
  52. Zhang J, Li W, Xiang T, Liu Z, Laluk K, Ding X, Zou Y, Gao M, Zhang X, Chen S, Mengiste T, Zhang Y, Zhou JM (2010) Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7:290–301CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Tina Reiner
    • 1
  • Caroline Hoefle
    • 1
  • Christina Huesmann
    • 1
  • Dalma Ménesi
    • 2
  • Attila Fehér
    • 2
  • Ralph Hückelhoven
    • 1
  1. 1.Lehrstuhl für Phytopathologie, Technische Universität MünchenFreising-WeihenstephanGermany
  2. 2.Laboratory of Functional Cell Biology, Biological Research Centre, Institute of Plant BiologyHungarian Academy of SciencesSzegedHungary

Personalised recommendations