Advertisement

Biologia Plantarum

, Volume 60, Issue 2, pp 299–310 | Cite as

Involvement of polar auxin transport in the inhibition of Arabidopsis seedling growth induced by Stenotrophomonas maltophilia

  • J. Wang
  • Y. Zhang
  • Y. Li
  • X. Wang
  • Z. Liu
  • W. Nan
  • C. Zhao
  • F. Wang
  • J. Ma
  • Y. BiEmail author
Original papers

Abstract

A wide range of microorganisms found in the rhizhosphere are able to regulate plant growth and development, but little is known about the mechanism by which epiphytic microbes inhibit plant growth. Here, an epiphytic bacteria Stenotrophomonas maltophilia, named as LZMBW216, were isolated and identified from the potato (Solanum tuberosum L. cv. Da Xi Yang) leaf surface. They could decrease primary root elongation and lateral root numbers in Arabidopsis seedlings. The inhibitory effects of LZMBW216 on plant growth were not due to a reduced indole-3-acetic acid (IAA) content, as exogenously applied IAA did not recover the inhibition. Furthermore, LZMBW216 did not affect the expression of DR5::GUS and CycB1;1::GUS. However, we found that LZMBW216 exhibited little effect on the primary root elongation in the pin2 mutant and on the lateral root numbers in the aux1-7 mutant. Moreover, LZMBW216 decreased expressions of AUX1 and PIN2 proteins. Together, these results suggest that root system architecture alterations caused by LZMBW216 may involve polar auxin transport.

Additional key words

IAA LZMBW216 mutants potato root elongation 

Abbreviations

ACC

1-aminocyclopropane-1-carboxylic acid

ET

ethylene

GFP

green fluorescent protein

IAA

indole-3-acetic acid

GUS

ß-glucuronidase

KB

King’s B medium

MS

Murashige and Skoog

PCR

polymerase chain reaction

YFP

yellow fluorescent protein

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

10535_2016_585_MOESM1_ESM.pdf (347 kb)
Supplementary material, approximately 293 KB.

References

  1. Abanda-Nkpwatt, D., Müsch, M., Tschiersch, J., Boettner, M., Schwab, W.: Molecular interaction between Methylobacterium extorquens and seedlings: growth promotion, methanol consumption, and localization of the methanol emission site. — J. exp. Bot. 57: 4025–4032, 2006.CrossRefPubMedGoogle Scholar
  2. Alabadí, D., Gil, J., Blázquez, M., García-Martínez, J.: Gibberellins repress photomorphogenesis in darkness. — Plant Physiol. 134: 1050–1057, 2004.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Alström, S., Burns, R.: Cyanide production by rhizobacteria as a possible mechanism of plant growth inhibition. — Biol. Fertil. Soils 7: 232–238, 1989.CrossRefGoogle Scholar
  4. Arase, F., Nishitani, H., Egusa, M., Nishimoto, N., Sakurai, S., Sakamoto, N., Kaminaka, H.: IAA8 involved in lateral root formation interacts with the TIR1 auxin receptor and ARF transcription factors in Arabidopsis. — PloS ONE 7: e43414, 2012.CrossRefGoogle Scholar
  5. Arkhipova, T.N., Veselov, S.U., Melentiev, A.I., Martynenko, E.V., Kudoyarova, G.R.: Ability of bacterium Bacillus subtilis to produce cytokinins and to influence the growth and endogenous hormone content of lettuce plants. — Plant Soil 272: 201–209, 2005.CrossRefGoogle Scholar
  6. Badri, D.V., Vivanco, J.M.: Regulation and function of root exudates. — Plant Cell Environ. 32: 666–681, 2009.CrossRefPubMedGoogle Scholar
  7. Bais, H.P., Weir, T.L., Perry, L.G., Gilroy, S., Vivanco, J.M.: The role of root exudates in rhizosphere interactions with plants and other organisms. — Annu. Rev. Plant Biol. 57: 233–266, 2006.CrossRefPubMedGoogle Scholar
  8. Blom, D., Fabbri, C., Eberl, L., Weisskopf, L.: Volatilemediated killing of Arabidopsis thaliana by bacteria is mainly due to hydrogen cyanide. — Appl. Environ. Microbiol. 77: 1000–1008, 2011.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Boerjan, W., Cervera, M.T., Delarue, M., Beeckman, T., Dewitte, W., Bellini, C., Caboche, M., Van Onckelen, H., Van Montagu, M., Inzé, D.: Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. — Plant Cell 7: 1405–1419, 1995.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Brown, R.L., Kazan, K., McGrath, K.C., Maclean, D.J., Manners, J.M.: A role for the GCC-box in jasmonate-mediated activation of the PDF1.2 gene in Arabidopsis. — Plant Physiol. 132: 1020–1032, 2003.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Calderon Villalobos, L.I., Lee, S., De Oliveira, C., Ivetac, A., Brandt, W., Armitage, L., Sheard, L.B., Tan, X., Parry, G., Mao H.: A combinatorial TIR1/AFB-Aux/IAA co-receptor system for differential sensing of auxin. — Natur. Chem. Biol. 8: 477–485, 2012.CrossRefGoogle Scholar
  12. Camehl, I., Sherameti, I., Venus, Y., Bethke, G., Varma, A., Lee, J., Oelmueller, R. 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: 1062–1073. 2010.CrossRefPubMedGoogle Scholar
  13. Casimiro, I., Marchant, A., Bhalerao, RP., Beeckman, T., Dhooge, S., Swarup, R., Graham, N., Inzé, D., Sandberg, G., Casero, P.J., Bennett, M.: Auxin transport promotes Arabidopsis lateral root initiation. — Plant Cell 13: 843–852, 2001.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Celenza, J.L., Grisafi, P.L., Fink, G.R.: A pathway for lateral root formation in Arabidopsis thaliana. — Genes Dev. 9: 2131–2142, 1995.CrossRefPubMedGoogle Scholar
  15. Cesarz, S., Fender, A.-C., Beyer, F., Valtanen, K., Pfeiffer, B., Gansert, D., Hertel, D., Polle, A., Daniel, R., Leuschner, C.: Roots from beech (Fagus sylvatica L.) and ash (Fraxinus excelsior L.) differentially affect soil microorganisms and carbon dynamics. — Soil Biol. Biochem. 61: 23–32, 2013.CrossRefGoogle Scholar
  16. Chao, Q., Rothenberg, M., Solano, R., Roman, G., Terzaghi, W.: Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. — Cell 89: 1133–1144, 1997.CrossRefPubMedGoogle Scholar
  17. Chang, C., Kwok, S.F., Bleecker, A.B., Meyerowitz, E.M.: Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. — Science 262: 539–544, 1993.CrossRefPubMedGoogle Scholar
  18. Clark, D.G., Gubrium, E.K., Barrett, J.E., Nell, T.A., Klee, H.J.: Root formation in ethylene-insensitive plants. — Plant Physiol. 121: 53–60, 1999.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Colón-Carmona, A., You, R., Haimovitch-Gal, T., Doerner, P.: Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. — Plant J. 20: 503–508, 1999.CrossRefPubMedGoogle Scholar
  20. Contesto, C., Milesi, S., Mantelin, S., Zancarini, A., Desbrosses, G., Varoquaux, F., Bellini, C., Kowalczyk, M., Touraine, B.: The auxin-signaling pathway is required for the lateral root response of Arabidopsis to the rhizobacterium Phyllobacterium brassicacearum. — Planta 232: 1455–1470, 2010.CrossRefPubMedGoogle Scholar
  21. Contreras-Cornejo, H.A., Macías-Rodríguez, L., Cortés-Penagos, C., López-Bucio, J.: Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. — Plant Physiol. 149: 1579–1592, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  22. D'Haeze, W., De Rycke, R., Mathis, R., Goormachtig, S., Pagnotta, S., Verplancke, C., Capoen, W., Holsters, M.: Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semiaquatic legume. — Proc. nat. Acad. Sci. USA 100: 11789–11794, 2003.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Dharmasiri, N., Dharmasiri, S., Estelle, M.: The F-box protein TIR1 is an auxin receptor. — Nature 435: 441–445, 2005a.CrossRefPubMedGoogle Scholar
  24. Dharmasiri, N., Dharmasiri, S., Weijers, D., Lechner, E., Yamada, M., Hobbie, L., Ehrismann, J.S., Jurgens, G., Estelle, M.: Plant development is regulated by a family of auxin receptor F box proteins. — Dev. Cell 9: 109–119, 2005b.CrossRefPubMedGoogle Scholar
  25. Ditengou, F.A., Béguiristain, T., Lapeyrie, F.: Root hair elongation is inhibited by hypaphorine, the indole alkaloid from the ectomycorrhizal fungus Pisolithus tinctorius, and restored by indole-3-acetic acid. — Planta 211: 722–728, 2000.CrossRefPubMedGoogle Scholar
  26. Dreher, KA., Brown, J., Saw, RE., Callis, J.: The Arabidopsis Aux/IAA protein family has diversified in degradation and auxin responsiveness. — Plant Cell 18: 699–714, 2006.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Felten, J., Kohler, A., Morin, E., Bhalerao, R.P., Palme, K., Martin, F., Ditengou, F.A., Legué, V.: The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. — Plant Physiol. 151: 1991–2005, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Friml, J., Yang, X., Michniewicz, M., Weijers, D., Quint, A., Tietz, O., Benjamins, R., Ouwerkerk, P.B., Ljung, K., Sandberg, G.: A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. — Science 306: 862–865, 2004.CrossRefPubMedGoogle Scholar
  29. Fujimoto, S.Y., Ohta, M., Usui, A., Shinshi, H., Ohme-Takagi, M.: Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. — Plant Cell 12: 393–404, 2000.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Fujita, H., Syono, K.: Genetic analysis of the effects of polar auxin transport inhibitors on root growth in Arabidopsis thaliana. — Plant Cell Physiol. 37: 1094–1101, 1996.CrossRefPubMedGoogle Scholar
  31. Glick, B.R.: Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. — FEMS Microbiol. Lett. 251: 1–7, 2005.CrossRefPubMedGoogle Scholar
  32. Gray, E.J., Smith, D.L.: Intracellular and extracellular PGPR: commonalities and distinctions in the plant-bacterium signaling processes. — Soil Biol. Biochem. 37: 395–412, 2005.CrossRefGoogle Scholar
  33. Guilfoyle, T.J., Hagen, G.: Auxin response factors. — Curr Opin Plant Biol. 10: 453–460, 2007.CrossRefPubMedGoogle Scholar
  34. Hall, A.E., Chen, Q.G., Findell, J.L., Schaller, G.E., Bleecker, A.B.: The relationship between ethylene binding and dominant insensitivity conferred by mutant forms of the ETR1 ethylene receptor. — Plant Physiol. 121: 291–300, 1999.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Hao, D., Ohme-Takagi, M., Sarai, A.: Unique mode of GCC box recognition by the DNA-binding domain of ethylene-responsive element binding factor (ERF domain) in plants. — J. biol. Chem. 273: 26857–26861, 1998.CrossRefPubMedGoogle Scholar
  36. Hirsch, A.M., Fang, Y., Asad, S., Kapulnik, Y.: The role of phytohormones in plant-microbe symbioses. — Plant Soil 194: 171–184, 1997.CrossRefGoogle Scholar
  37. Hua, J., Chang, C., Sun, Q., Meyerowitz, EM.: Ethylene insensitivity conferred by Arabidopsis ERS gene. — Science 269: 1712–1714, 1995a.CrossRefPubMedGoogle Scholar
  38. Hua, J., Meyerowitz, E.M.: Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. — Cell 94: 261–271, 1998.CrossRefPubMedGoogle Scholar
  39. Hua, J., Sakai, H., Nourizadeh, S., Chen, Q.G., Bleecker, A.B., Ecker, J.R., Meyerowitz E.M.: EIN4 and ERS2 are members of the putative ethylene receptor gene family in Arabidopsis. — Plant Cell 10: 1321–1332, 1998b.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Ivanchenko, M.G., Muday, G.K., Dubrovsky, J.G.: Ethylene-auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. — Plant J. 55: 335–347, 2008.CrossRefPubMedGoogle Scholar
  41. Johnson, D., Martin, F., Cairney, J.W.G., Anderson, I.C.: The importance of individuals: intraspecific diversity of mycorrhizal plants and fungi in ecosystems. — New Phytol. 194: 614–628, 2012.CrossRefPubMedGoogle Scholar
  42. Karadeniz, A., Topcuoglu, S.F., Inan, S.: Auxin, gibberellin, cytokinin and abscisic acid production in some bacteria. — World J. Microbiol. Biotechnol. 22: 1061–1064, 2006.CrossRefGoogle Scholar
  43. Kieber, J.J., Rothenberg, M., Roman, G., Feldmann, K.A., Ecker, J.R.: CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. — Cell 72: 427–441, 1993.CrossRefPubMedGoogle Scholar
  44. Lewis, D.R., Negi, S., Sukumar, P., Muday, G.K.: Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. — Development 138: 3485–3495, 2011.CrossRefPubMedGoogle Scholar
  45. Lincoln, C., Britton, J.H., Estelle, M.: Growth and development of the axr1 mutants of Arabidopsis. — Plant Cell 2: 1071–1080, 1990.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Lindow, S.E., Brandl, M.T.: Microbiology of the phyllosphere. — Appl. Environ. Microbiol. 69: 1875–1883, 2003.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Ljung K.: Auxin metabolism and homeostasis during plant development. — Development 140: 943–950, 2013.CrossRefPubMedGoogle Scholar
  48. Long, H.H., Sonntag, D.G., Schmidt, D.D., Baldwin, I.T.: The structure of the culturable root bacterial endophyte community of Nicotiana attenuata is organized by soil composition and host plant ethylene production and perception. - New Phytol. 185: 554–567. 2010.CrossRefPubMedGoogle Scholar
  49. López-Bucio, J., Campos-Cuevas, J.C., Hernández-Calderón, E., Velásquez-Becerra, C., Farías-Rodríguez, R., Macías-Rodríguez, L.I., Valencia-Cantero, E. Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin-and ethylene-independent signaling mechanism in Arabidopsis thaliana. - Mol. Plant-Microbe Interact. 20: 207–217, 2007.CrossRefPubMedGoogle Scholar
  50. López-Bucio, J., Cruz-Ramírez, A., Herrera-Estrella, L.: The role of nutrient availability in regulating root architecture. — Curr. Opin. Plant. Biol. 6: 280–287, 2003.CrossRefPubMedGoogle Scholar
  51. López-Bucio, J., Hernández-Abreu, E., Sánchez-Calderón, L., Nieto-Jacobo, M.F., Simpson, J., Herrera-Estrella, L.: Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. — Plant Physiol. 129: 244–256, 2002.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Meldau, D.G., Long, H.H., Baldwin, I.T.: A native plant growth promoting bacterium, Bacillus sp. B55, rescues growth performance of an ethylene-insensitive plant genotype in nature. — Front. Plant Sci. 3: 1–13, 2012.CrossRefGoogle Scholar
  53. Misaghi, I., Donndelinger, C.: Endophytic bacteria in symptom-free cotton plants. — Phytopathology 80: 808–811, 1990.CrossRefGoogle Scholar
  54. Morgan, J.A.W., Bending, G.D., White, P.J.: Biological costs and benefits to plant-microbe interactions in the rhizosphere. — J. exp. Bot. 56: 1729–1739, 2005.CrossRefPubMedGoogle Scholar
  55. Negi, S., Ivanchenko, M.G., Muday, G.K.: Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana. — Plant J. 55: 175–187, 2008.CrossRefPubMedPubMedCentralGoogle Scholar
  56. Ohta, M., Ohme-Takagi, M., Shinshi, H.: Three ethylene-responsive transcription factors in tobacco with distinct transactivation functions. — Plant J. 22: 29–38, 2000.CrossRefPubMedGoogle Scholar
  57. Oldroyd, G.E.D., Downie, J.A.: Coordinating nodule morphogenesis with rhizobial infection in legumes. — Annu. Rev. Plant Biol. 59: 519–546, 2008.CrossRefPubMedGoogle Scholar
  58. O'Malley, R.C., Rodriguez, F.I., Esch, J.J., Binder, B.M., O'Donnell, P., Klee, H.J., Bleecker, A.B.: Ethylene-binding activity, gene expression levels, and receptor system output for ethylene receptor family members from Arabidopsis and tomato. — Plant J. 41: 651–659, 2005.CrossRefPubMedGoogle Scholar
  59. Perrine-Walker, F.M., Jublanc, E.: The localization of auxin transporters PIN3 and LAX3 during lateral root development in Arabidopsis thaliana. — Biol. Plant. 58: 778–782, 2014.CrossRefGoogle Scholar
  60. Persello-Cartieaux, F., David, P., Sarrobert, C., Thibaud, M.C., Achouak, W., Robaglia, C., Nussaume, L.: Utilization of mutants to analyze the interaction between Arabidopsis thaliana and its naturally root-associated Pseudomonas. — Planta 212: 190–198, 2001.CrossRefPubMedGoogle Scholar
  61. Ping, L., Boland, W.: Signals from the underground: bacterial volatiles promote growth in Arabidopsis. — Trends Plant Sci. 9: 263–266, 2004.CrossRefPubMedGoogle Scholar
  62. Ruegger, M., Dewey, E., Gray, W.M., Hobbie, L., Turner, J., Estelle, M.: The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast grr1p. — Genes Dev. 12: 198–207, 1998.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Ružicka, K., Ljung, K., Vanneste, S., Podhorská, R., Beeckman, T., Friml, J., Benková, E.: Ethylene regulates root growth through effects on auxin biosynthesis and transportdependent auxin distribution. — Plant Cell 19: 2197–2212, 2007.CrossRefPubMedPubMedCentralGoogle Scholar
  64. Ryu, C.M., Farag, M.A., Hu, C.H., Reddy, M.S., Wei, H.X., Paré, P.W., Kloepper, J.W.: Bacterial volatiles promote growth in Arabidopsis. — Proc. nat. Acad. Sci. USA 100: 4927–4932, 2003.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Ryu, C.M., Hu, C.H., Locy, R., Kloepper, J.: Study of mechanisms for plant growth promotion elicited by rhizobacteria in Arabidopsis thaliana. — Plant Soil 268: 285–292, 2005.CrossRefGoogle Scholar
  66. Sakai, H., Hua, J., Chen, Q.G., Chang, C., Medrano, L.J., Bleecker, A.B., Meyerowitz, E.M.: ETR2 is an ETR1-like gene involved in ethylene signaling in Arabidopsis. — Proc. nat. Acad. Sci. USA. 95: 5812–5817, 1998.CrossRefPubMedPubMedCentralGoogle Scholar
  67. Shkolnik-Inbar, D., Bar-Zvi, D.: ABI4 mediates abscisic acid and cytokinin inhibition of lateral root formation by reducing polar auxin transport in Arabidopsis. — Plant Cell 22: 3560–3573, 2010.CrossRefPubMedPubMedCentralGoogle Scholar
  68. Slankis, V.: Soil factors influencing formation of mycorrhizae. — Annu. Rev. Phytopathol. 12: 437–457, 1974.CrossRefGoogle Scholar
  69. Stepanova, A.N., Hoyt, J.M., Hamilton, A.A., Alonso, J.M.: A link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. — Plant Cell 17: 2230–2242, 2005.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Sturz, AV., Christie, B.R., Nowak, J. Bacterial endophytes: potential role in developing sustainable systems of crop production. - Crit. Rev. Plant Sci. 19: 1–30, 2000.CrossRefGoogle Scholar
  71. Sukumar, P., Legue, V., Vayssieres, A., Martin, F., Tuskan, G.A., Kalluri, U.C.: Involvement of auxin pathways in modulating root architecture during beneficial plantmicroorganism interactions. — Plant Cell Environ. 36: 909–919, 2013.CrossRefPubMedGoogle Scholar
  72. Swarup, K., Benkova, E., Swarup, R., Casimiro, I., Peret, B., Yang, Y., Parry, G., Nielsen, E., De Smet, I., Vanneste, S., Levesque, M.P., Carrier, D., James, N., Calvo, V., Ljung, K., Kramer, E., Roberts, R., Graham, N., Marillonnet, S., Patel, K., Jones, J.D.G., Taylor, C.G., Schachtman, D.P., May, S., Sandberg, G., Benfey, P., Friml, J., Kerr, I., Beeckman, T., Laplaze, L., Bennett, M.J.: The auxin influx carrier LAX3 promotes lateral root emergence. — Natur. Cell Biol. 10: 946–954, 2008.CrossRefGoogle Scholar
  73. Tiwari, S,B., Hagen, G., Guilfoyle, T.: The roles of auxin response factor domains in auxin-responsive transcription. — Plant Cell. 15: 533–543, 2003.CrossRefPubMedPubMedCentralGoogle Scholar
  74. Ulmasov, T., Murfett, J., Hagen, G., Guilfoyle, T.J.: Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. — Plant Cell 9: 1963–1971, 1997.CrossRefPubMedPubMedCentralGoogle Scholar
  75. Wang, J., Zhang, Y., Li, Y., Wang, X., Nan, W., Hu, Y., Zhang, H., Zhao, C., Wang, F., Li, P., Shi, H., Bi, Y.: Endophytic microbes Bacillus sp. LZR216-regulated root development is dependent on polar auxin transport in Arabidopsis seedlings. — Plant Cell Rep. 34: 1075–1087, 2015.CrossRefPubMedGoogle Scholar
  76. Weijers, D., Benkova, E., Jager, K.E., Schlereth, A., Hamann, T., Kientz, M., Wilmoth, J.C., Reed, J.W., Jurgens, G.: Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. — EMBO J. 24: 1874–1885, 2005.CrossRefPubMedPubMedCentralGoogle Scholar
  77. Weise, T., Kai, M., Piechulla, B.: Bacterial ammonia causes significant plant growth inhibition. — PloS ONE 8: e63538, 2013.CrossRefGoogle Scholar
  78. Wilmoth, J.C., Wang, S., Tiwari, S.B., Joshi, A.D., Hagen, G., Guilfoyle, T.J., Alonso, J.M., Ecker, J.R., Reed, J.W.: NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. — Plant J. 43: 118–130, 2005.CrossRefPubMedGoogle Scholar
  79. Woodward, A.W., Bartel, B.: Auxin: regulation, action, and interaction. — Ann. Bot. 95: 707–735, 2005.CrossRefPubMedPubMedCentralGoogle Scholar
  80. Zamioudis, C., Mastranesti, P., Dhonukshe, P., Blilou, I., Pieterse, C.: Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. — Plant Physiol. 162: 304–318, 2013.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • J. Wang
    • 1
  • Y. Zhang
    • 1
  • Y. Li
    • 1
  • X. Wang
    • 1
  • Z. Liu
    • 1
  • W. Nan
    • 2
  • C. Zhao
    • 1
  • F. Wang
    • 1
  • J. Ma
    • 3
  • Y. Bi
    • 1
    Email author
  1. 1.School of Life SciencesLanzhou UniversityLanzhouP.R. China
  2. 2.College of Life SciencesChongqing Normal UniversityChongqingP.R. China
  3. 3.School of Life Science and EngineeringLanzhou University of TechnologyLanzhouP.R. China

Personalised recommendations