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Oligogalacturonides inhibit growth and induce changes in S6K phosphorylation in maize (Zea mays L. var. Chalqueño)

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Abstract

Cell growth is regulated by the target of rapamycin (TOR) signaling pathway, which integrates environmental cues in eukaryotes. In plants the final organ size is determined by the number and cell size. Several proteins involved in the TOR signaling pathway are conserved in plants, although a differential regulation has been proposed because insensitivity to rapamycin by Arabidopsis thaliana was reported. Reports about the role of auxin in the activation of maize S6 ribosomal protein kinase (S6K), a downstream substrate of TOR, have been published indicating a central role of the TOR pathway in the regulation of plant growth. However, in addition to phytohormones, there are a variety of plant growth regulators, including cell wall fragments called oligogalacturonides (OGs). Here we report the effect of OGs on maize growth and development, as well as on S6K activation. We found that oligogalacturonides inhibit coleoptile growth and modify root architecture of maize seedlings. Western blot analyses indicated a modulation of maize S6K activity from seedlings and embryonic axes in response to OGs treatment. These results show that oligosaccharides regulate growth and development through the modulation of TOR signaling pathway in maize.

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Abbreviations

OGs:

Oligogalacturonides

TOR:

Target of rapamycin

S6rp:

S6 ribosomal protein

S6K:

S6rp kinase

eIF4E:

Eukaryotic translation initiation factor 4E

4EBP1:

eIF4E binding protein

TORC:

TOR complex

FKBP12:

FK506-binding protein

IGF:

Insulin-like growth factor

IAA:

Indole-3-acetic acid

References

  • Agredano-Moreno LT, Reyes de la Cruz H, Martinez-Castilla LP, Sanchez de Jimenez E (2007) Distinctive expression and functional regulation of the maize (Zea mays L.) TOR kinase ortholog. Mol BioSys 3(11):794–802

  • Avruch J, Hara K, Lin Y, Liu M, Long X, Ortiz-Vega S, Yonezawa K (2006) Insulin and amino-acid regulation of mTOR signaling and kinase activity through the Rheb GTPase. Oncogene 25(48):6361–6372

    Article  PubMed  CAS  Google Scholar 

  • Bellincampi D, Salvi G, De Lorenzo G, Cervone F, Marfà V, Eberhard S, Darvill A, Albersheim P (1993) Oligogalacturonides inhibit the formation of roots on tobacco explants. Plant J 4(1):207–213. doi:10.1046/j.1365-313X.1993.04010207.x

    Article  CAS  Google Scholar 

  • Bergmann CW, Ito Y, Singer D, Albersheim P, Darvill AG, Benhamou N, Nuss L, Salvi G, Cervone F, De Lorenzo G (1994) Polygalacturonase-inhibiting protein accumulates in Phaseolus vulgaris L. in response to wounding, elicitors and fungal infection. Plant J 5(5):625–634. doi:10.1111/j.1365-313X.1994.00625.x

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254

    Article  PubMed  CAS  Google Scholar 

  • Burnett PE, Barrow RK, Cohen NA, Snyder SH, Sabatini DM (1998) RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc Natl Acad Sci 95(4):1432–1437

    Article  PubMed  CAS  Google Scholar 

  • Davis KR, Hahlbrock K (1987) Induction of defense responses in cultured parsley cells by plant cell wall fragments. Plant Physiol 84(4):1286–1290. doi:10.1104/pp.84.4.1286

    Article  PubMed  CAS  Google Scholar 

  • García Flores C, Aguilar R, Reyes de la Cruz H, Albores M, Sánchez de Jiménez E (2001) A maize insulin-like growth factor signals to a transduction pathway that regulates protein synthesis in maize. Biochem J 358(1):95–100

    Article  PubMed  Google Scholar 

  • Hahn MG, Darvill AG, Albersheim P (1981) Host-pathogen interactions: XIX. The endogenous elicitor, a fragment of a plant cell wall polysaccharide that elicits phytoalexin accumulation in soybeans. Plant Physiol 68(5):1161–1169. doi:10.1104/pp.68.5.1161

    Article  PubMed  CAS  Google Scholar 

  • Hannan KM, Thomas G, Pearson RB (2003) Activation of S6K1 (p70 ribosomal protein S6 kinase 1) requires an initial calcium-dependent priming event involving formation of a high-molecular-mass signalling complex. Biochem J 370(2):469–477. doi:10.1042/bj20021709

    Article  PubMed  CAS  Google Scholar 

  • Hara K, Maruki Y, Long X, Yoshino K, Oshiro N, Hidayat S, Tokunaga C, Avruch J, Yonezawa K (2002) Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 110(2):177–189

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Hernández-Mata G, Mellado-Rojas M, Richards-Lewis A, López-Bucio J, Beltrán-Peña E, Soriano-Bello E (2010) Plant immunity induced by oligogalacturonides alters root growth in a process involving flavonoid accumulation in Arabidopsis thaliana. J Plant Growth Reg 29(4):441–454. doi:10.1007/s00344-010-9156-x

    Article  Google Scholar 

  • Humphrey TV, Bonetta DT, Goring DR (2007) Sentinels at the wall: cell wall receptors and sensors. New Phytol 176(1):7–21. doi:10.1111/j.1469-8137.2007.02192.x

    Article  PubMed  CAS  Google Scholar 

  • Jastrzebski K, Hannan KM, Tchoubrieva EB, Hannan RD, Pearson RB (2007) Coordinate regulation of ribosome biogenesis and function by the ribosomal protein S6 kinase, a key mediator of mTOR function. Growth Factors 25(4):209–226. doi:10.1080/08977190701779101

    Article  PubMed  CAS  Google Scholar 

  • Kollárová K, Vatehová Z, Slováková L, Lisková D (2010) Interaction of galactoglucomannan oligosaccharides with auxin in mung bean primary root. Plant Physiol Biochem 48(6):401–406

    Article  PubMed  Google Scholar 

  • Loewith R, Jacinto E, Wullschleger S, Lorberg A, Crespo JL, Bonenfant D, Oppliger W, Jenoe P, Hall MN (2002) Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol Cell 10(3):457–468

    Article  PubMed  CAS  Google Scholar 

  • Marfà V, Gollin DJ, Eberhard S, Mohnen D, Darvill A, Albersheim P (1991) Oligogalacturonides are able to induce flowers to form on tobacco explants. Plant J 1(2):217–225. doi:10.1111/j.1365-313X.1991.00217.x

    Article  Google Scholar 

  • 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 99(9):6422–6427. doi:10.1073/pnas.092141899

    Article  PubMed  CAS  Google Scholar 

  • Menand B, Meyer C, Robaglia C, Thomas G, Sabatini DM, Hall MN (2004) Plant growth and the TOR pathway. Curr Top Microbiol Immunol 279:97–113. doi:10.1007/978-3-642-18930-2_7

    Article  PubMed  CAS  Google Scholar 

  • Messiaen J, Van Cutsem P (1994) Pectic signal transduction in carrot cells: membrane, cytosolic and nuclear responses induced by oligogalacturonides. Plant Cell Physiol 35(4):677–689

    CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15(3):473–497. doi:10.1111/j.1399-3054.1962.tb08052.x

    Article  CAS  Google Scholar 

  • Nothnagel EA, McNeil M, Albersheim P, Dell A (1983) Host-pathogen interactions: XXII. A galacturonic acid oligosaccharide from plant cell walls elicits phytoalexins. Plant Physiol 71(4):916–926. doi:10.1104/pp.71.4.916

    Article  PubMed  CAS  Google Scholar 

  • O’Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250(10):4007–4021

    PubMed  Google Scholar 

  • Reyes de la Cruz H, Aguilar R, Sánchez de Jiménez E (2004) Functional characterization of a maize ribosomal S6 protein kinase (ZmS6K), a plant ortholog of metazoan p70S6K. Biochemistry 43(2):533–539. doi:10.1021/bi035222z

    Article  PubMed  CAS  Google Scholar 

  • Ridley BL, O’Neill MA, Mohnen D (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochem 57(6):929–967

    Article  CAS  Google Scholar 

  • Rodriguez-Lopez CD, Rodriguez-Romero A, Aguilar R, Sanchez de Jimenez E (2011) Biochemical characterization of a new maize (Zea mays L.) Peptide growth factor. Prot Pept Lett 18(1):84–91. doi:10.2174/092986611794328636

    Google Scholar 

  • Sánchez de Jiménez E, Beltrán-Peña E, Ortíz-López A (1999) Insulin-stimulated ribosomal protein synthesis in maize embryonic axes during germination. Physiol Plant 105(1):148–154. doi:10.1034/j.1399-3054.1999.105122.x

    Article  Google Scholar 

  • Sánchez-Rodríguez C, Rubio-Somoza I, Sibout R, Persson S (2010) Phytohormones and the cell wall in Arabidopsis during seedling growth. Trends Plant Sci 15(5):291–301

    Article  PubMed  Google Scholar 

  • Turck F, Kozma SC, Thomas G, Nagy F (1998) A heat-sensitive Arabidopsis thaliana kinase substitutes for human p70s6k function in vivo. Mol Cell Biol 18(4):2038–2044

    PubMed  CAS  Google Scholar 

  • Turck F, Zilbermann F, Kozma SC, Thomas G, Nagy F (2004) Phytohormones participate in an S6 kinase signal transduction pathway in Arabidopsis. Plant Physiol 134(4):1527–1535. doi:10.1104/pp.103.035873

    Article  PubMed  CAS  Google Scholar 

  • Wang M-L, Panasyuk G, Gwalter J, Nemazanyy I, Fenton T, Filonenko V, Gout I (2008) Regulation of ribosomal protein S6 kinases by ubiquitination. Biochemi Biophys Res Commun 369(2):382–387

    Article  CAS  Google Scholar 

  • Williams AJ, Werner-Fraczek J, Chang I-F, Bailey-Serres J (2003) Regulated phosphorylation of 40S ribosomal protein S6 in root tips of maize. Plant Physiol 132(4):2086–2097. doi:10.1104/pp.103.022749

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yang Q, Guan K-L (2007) Expanding mTOR signaling. Cell Res 17(8):666–681

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by The CONACyT Grant no. 25540 and CIC-UMSNH Grant no. 2.27. Peña-Uribe was recipient of CONACyT fellowship no. 22066.

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Correspondence to Homero Reyes de la Cruz.

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Peña-Uribe, C.A., García-Pineda, E., Beltrán-Peña, E. et al. Oligogalacturonides inhibit growth and induce changes in S6K phosphorylation in maize (Zea mays L. var. Chalqueño). Plant Growth Regul 67, 151–159 (2012). https://doi.org/10.1007/s10725-012-9672-8

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  • DOI: https://doi.org/10.1007/s10725-012-9672-8

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