Activation of a calcium-dependent protein kinase involved in the Azospirillum growth promotion in rice

  • Claudia M. Ribaudo
  • José A. Curá
  • María L. Cantore
Short Communication
  • 379 Downloads

Abstract

Rice seedlings (Oryza sativa) inoculated with the plant growth-promoting rhizobacteria Azospirillum brasilense FT326 showed an enhanced development of the root system 3 days after inoculation. Later on, a remarkable enlargement of shoots was also evident. An increase in the Ca2+-dependent histone kinase activity was also detected as a result of inoculation. The biochemical characterization and Western-blot analysis of the kinase strongly supports the hypothesis that it belongs to a member of the rice CDPK family. The fact that the amount of the protein did not change upon inoculation seems to indicate that a posttranslational activation is responsible for the change in the enzymatic activity. An in-gel kinase experiment identified a 46 kDa CDPK like protein kinase as a putative component of the signal transduction pathway triggered by Azospirillum inoculation. To our knowledge, this is the first report on the possible involvement of a Ca2+-dependent protein kinase in promotion of rice plants growth by A. brasilense.

Keywords

Azospirillum Rice CDPK Lateral roots growth promotion 

References

  1. Abbasi F, Onodera H, Toki S, Tanaka H, Komatsu S (2004) OsCDPK13, a calcium-dependent protein kinase gene from rice, is induced by cold and gibberellin in rice leaf sheath. Plant Mol Biol 55:541–552CrossRefGoogle Scholar
  2. Abo-El-Saad M, Wu R (1995) A rice membrane calcium-dependent protein kinase is induced by gibberellin. Plant Physiol 108:787–793CrossRefGoogle Scholar
  3. Asano T, Hakata M, Nakamura H, Aoki N, Komatsu S, Ichikawa H, Hirochika H, Ohsugi R (2011) Functional characterization of OsCPK21, a calcium-dependent protein kinase that confers salt tolerance in rice. Plant Mol Biol 75:179–191CrossRefGoogle Scholar
  4. Bachmann M, Shiraishi N, Campbell WH, Yoo B-C, Harmos AC, Huber SC (1996) Identification of the major regulatory phosphorylation site as Ser-543 in spinach leaf nitrate reductase and its phosphorylation by a calcium-dependent protein kinase in vitro. Plant Cell 8:505–517CrossRefGoogle Scholar
  5. Baldani VLD, Baldani JI, Döbereiner J (2000) Inoculation of rice plants with endophytic diazotrophs Herbaspirillum seropedicae and Burkholderia spp. Biol Fertil Soils 30:485–491CrossRefGoogle Scholar
  6. Bradford MM (1976) A rapid and sensitive method for the quantitation of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  7. Cassán F, Bottini R, Schneider G, Piccoli P (2001) Azospirillum brasilense and Azospirillum lipoferum hydrolyze conjugates of a GA20 and metabolize the resultant aglycones to GA1 is seedlings of rice dwarf mutants. Plant Physiol 125:2053–2058CrossRefGoogle Scholar
  8. Chen J, Xue B, Xia X, Yin W (2013) A novel calcium-dependent protein kinase gene from Populus euphratica, confers both drought and cold stress tolerance. Biochem Biophys Res Commun 441:630–636CrossRefGoogle Scholar
  9. Cheng SU, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469–485CrossRefGoogle Scholar
  10. Compant S, Clément C, Sessitscha A (2010) Plant growth-promoting bacteria in the rhizo-and endosphere of plants: role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678CrossRefGoogle Scholar
  11. Dodd IC, Zinovkina, NY Safronova VI, Belimov AA (2010) Rhizobacterial mediation of plant hormone status. Ann Appl Biol 157:361–379CrossRefGoogle Scholar
  12. Estruch JJ, Kadwell S, Merlin E, Crossland L (1994) Cloning and characterization of a maize pollen-specific calcium-dependent calmodulin-independent protein kinase. Proc Natl Acad Sci USA 91:8837–8841CrossRefGoogle Scholar
  13. Farmer PK, Choi JH (1999) Calcium and phospholipids activation of a recombinant calcium dependent protein kinase (DcCPK1) from carrot (Daucus carota L.). Biochim Biophys Acta 1434:6–17CrossRefGoogle Scholar
  14. Fujiwara S, Tanaka N, Kaneda T, Takayama S, Isogai A, Che F-S (2004) Rice cDNA microarray-based gene expression profiling of the response to flagellin perception in cultured rice cells. Mol Plant Microbe Interact 17:986–998.CrossRefGoogle Scholar
  15. Gargantini PR, Gonzalez-Rizzo S, Chinchilla D, Raices M, Giammaria V, Ulloa RM, Frugier F, Crespi MD (2006) A CDPK isoform participates in the regulation of nodule number in Medicago truncatula. Plant J 48:843–856CrossRefGoogle Scholar
  16. Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica. doi:10.6064/2012/963401 Google Scholar
  17. Grabov A, Blatt MR (1998) Membrane voltage initiates Ca2+ waves and potentiates Ca2+ increases with abscisic acid in stomatal guard cells. Proc Natl Acad Sci USA 95:4779–4783CrossRefGoogle Scholar
  18. Harper JF, Harmon A (2005) Plants, symbiosis and parasites: a calcium signaling connection. Nat Rev Mol Cell Biol 6:555–566CrossRefGoogle Scholar
  19. Kamiyoshihara Y, Iwata M, Fukaya T, Tatsuki M, Mori H (2010) Turnover of LeACS2, a wound-inducible 1-aminocyclopropane-1-carboxylic acid synthase in tomato, is regulated by phosphorylation/dephosphorylation. Plant J 64:140–150Google Scholar
  20. Khan MK, Jan A, Karibe H, Komatsu S (2005) Identification of phosphoproteins regulated by gibberellin in rice leaf sheath. Plant Mol Biol 58:27–40CrossRefGoogle Scholar
  21. Klimecka M, Szczegielniak J, Godecka L, Lewandowska-Gnatowska E, Dobrowolska G, Muszyńska G (2011) Regulation of wound-responsive calcium-dependent protein kinase from maize (ZmCPK11) by phosphatidic acid. Acta Biochim Pol 58:589–595Google Scholar
  22. Komatsu S, Li W, Konishi H, Yoshikawa T, Konishi T, Yang G (2001) Characterization of a Ca2+-dependent protein kinase from rice root: differential response to cold and regulation by abscisic acid. Biol Pharm Bull 24:1316–1319CrossRefGoogle Scholar
  23. Kwak SH, Lee SH (1997) The requirements for Ca2+, protein phosphorylation, and dephosphorylation for ethylene signal transduction in Pisum sativum L. Plant Cell Physiol 38:1142–1149CrossRefGoogle Scholar
  24. Laemmli UK (1970) Cleaveage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefGoogle Scholar
  25. Lanteri ML, Pagnussat GC, Lamattina L (2006) Calcium and calcium-dependent protein kinases are involved in nitric oxide- and auxin-induced adventitious root formation in cucumber. J Exp Bot 57:1341–1351CrossRefGoogle Scholar
  26. Ludwig AA, Saitoh H, Feliz G, Freymark G, Miersch O, Wasternack C, Boller T, Jones JD, Romes T (2005) Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proc Natl Acad Sci USA 102:10736–10741CrossRefGoogle Scholar
  27. Navarro L, Zipfel C, Rowland O, Keller I, Robatzek S, Boller T, Jones JDG (2004) The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol 135:1113–1128CrossRefGoogle Scholar
  28. Okon Y, Labandera-González C (1994) Agronomic application of Azospirillum: an evaluation of 20 years of worldwide field inoculation. Soil Biol Biochem 26:1591–1601CrossRefGoogle Scholar
  29. Patharkar OR, Cushman JC (2000) A stress-induced calcium-dependent protein kinase from Mesembryanthemum crystallinum phophorylates a two-component pseudo-response regulator. Plant J 24:679–691CrossRefGoogle Scholar
  30. Patten CL, Glick B (2002) Role of Pseudomonas putida indole acetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801CrossRefGoogle Scholar
  31. Putnam-Evans CL, Harmon AC, Palevitz BA, Fechheimer M, Cormier MJ (1989) Calcium-dependent protein kinase is localized with F-actin in plant cells. Cell Motil Cytoskelet 12:12–22CrossRefGoogle Scholar
  32. Raíces M, Chico JM, Téllez-Iñón MT, Ulloa RM (2001) Molecular characterization of StCDPK1 a calcium-dependent protein kinase from Solanum tuberosum that is induced at the onset of tuber development. Plant Mol Biol 46:591–601CrossRefGoogle Scholar
  33. Ribaudo C, Krumpholz E, Cassán F, Bottini R, Cantore ML, Curá J (2006) Azospirillum sp. promotes root hair development in tomato plants through a mechanism that involves ethylene. J Plant Growth Regul 24:175–185CrossRefGoogle Scholar
  34. Romeis T, Ludwig AA, Martin R, Jones JDG (2001) Calcium-dependent protein kinase play an essential role in a plant defense response. EMBO J 20:5556–5567CrossRefGoogle Scholar
  35. Roskoski R (1983) Assay of protein kinase. In: Corbin JD, Hardman JG (eds) Methods in enzimology. Academic Press, San Diego, pp 3–6Google Scholar
  36. Rutschmann F, Stalder U, Piotrowski M, Oecking C, Schaller A (2002) LeCPK1, a calcium-dependent protein kinase from tomato. Plasma membrane targeting and biochemical characterization. Plant Physiol 129:156–186CrossRefGoogle Scholar
  37. Ryu CM, Murphy JF, Mysore KS, Kloepper JW (2004) Plant growth-promoting rhizobacteria systematically protect Arabidopsis thaliana against Cucumber mosaic virus by a salicylic acid and NPR1-independent and jasmonic acid-dependent signaling pathway. Plant J 39:381–392CrossRefGoogle Scholar
  38. Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K (2000) Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23:319–327CrossRefGoogle Scholar
  39. Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14:S401–S417Google Scholar
  40. Sharifi RS (2011) Grain yield and physiological growth indices in maize (Zea mays L.) hybrids under seed biopriming with plant growth promoting rhizobacteria (PGPR). J Food Agric Environ 9:393–397Google Scholar
  41. Szczegielniak J, Borkiewicz L, Szurmak B, Lewandowska-Gnatowska E, Statkiewicz M, Klimecka M, Cieśla J, Muszyńska G (2012) Maize calcium-dependent protein kinase (ZmCPK11): local and systemic response to wounding, regulation by touch and components of jasmonate signaling. Physiol Plant 146:1–14CrossRefGoogle Scholar
  42. Yang G, Komatsu S (2000) Involvement of calcium-dependent protein kinase in rice (Oryza sativa L.) lamina inclination caused by brassinolide. Plant Cell Physiol 41:1243–1250CrossRefGoogle Scholar
  43. Yang DH, Hettenhausen C, Baldwin IT, Wu J (2012) Silencing Nicotiana attenuata calcium-dependent protein kinases, CDPK4 and CDPK5, strongly up-regulates wound- and herbivory-induced jasmonic acid accumulations. Plant Physiol 159:1591–1607CrossRefGoogle Scholar
  44. Zhang XQ, Lund AA, Sarath G, Cerny RL, Roberts DM, Chollet R (1999) Soybean nodule sucrose synthase (nodulin-100): further analysis of its phosphorylation using recombinant and authentic root-nodule enzymes. Arch Biochem Biophys 371:70–82CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Claudia M. Ribaudo
    • 1
  • José A. Curá
    • 1
  • María L. Cantore
    • 1
  1. 1.Cátedra de Bioquímica, Facultad de AgronomíaUniversidad de Buenos AiresCiudad Autónoma de Buenos AiresArgentina

Personalised recommendations