Biologia plantarum 60:299-310, 2016 | DOI: 10.1007/s10535-016-0585-7

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

J. Wang1, Y. Zhang1, Y. Li1, X. Wang1, Z. Liu1, W. Nan2, C. Zhao1, F. Wang1, J. Ma3, Y. Bi1,*
1 School of Life Sciences, Lanzhou University, Lanzhou, P.R. China
2 College of Life Sciences, Chongqing Normal University, Chongqing, P.R. China
3 School of Life Science and Engineering, Lanzhou University of Technology, Lanzhou, P.R. China

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.

Keywords: IAA; LZMBW216; mutants; potato; root elongation
Subjects: auxin transport; mutants; root elongation; growth analysis; plant-microbe interactions; potato
Species: Solanum tuberosum; Arabidopsis thaliana; Stenotrophomonas maltophilia

Received: February 14, 2015; Revised: July 2, 2015; Accepted: August 3, 2015; Published: June 1, 2016Show citation

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Wang, J., Zhang, Y., Li, Y., Wang, X., Liu, Z., Nan, W., ... Bi, Y. (2016). Involvement of polar auxin transport in the inhibition of Arabidopsis seedling growth induced by Stenotrophomonas maltophilia. Biologia plantarum, 60(2), 299-310. doi: 10.1007/s10535-016-0585-7.
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    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. Go to original source...
    2. Alabadí, D., Gil, J., Blázquez, M., García-Martínez, J.: Gibberellins repress photomorphogenesis in darkness. - Plant Physiol. 134: 1050-1057, 2004. Go to original source...
    3. Alström, S., Burns, R.: Cyanide production by rhizobacteria as a possible mechanism of plant growth inhibition. - Biol. Fertil. Soils 7: 232-238, 1989. Go to original source...
    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. Go to original source...
    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. Go to original source...
    6. Badri, D.V., Vivanco, J.M.: Regulation and function of root exudates. - Plant Cell Environ. 32: 666-681, 2009. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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.
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    23. Dharmasiri, N., Dharmasiri, S., Estelle, M.: The F-box protein TIR1 is an auxin receptor. - Nature 435: 441-445, 2005a. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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.
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    31. Glick, B.R.: Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. - FEMS Microbiol. Lett. 251: 1-7, 2005. Go to original source...
    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. Go to original source...
    33. Guilfoyle, T.J., Hagen, G.: Auxin response factors. - Curr Opin Plant Biol. 10: 453-460, 2007. Go to original source...
    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. Go to original source...
    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. Go to original source...
    36. Hirsch, A.M., Fang, Y., Asad, S., Kapulnik, Y.: The role of phytohormones in plant-microbe symbioses. - Plant Soil 194: 171-184, 1997. Go to original source...
    37. Hua, J., Chang, C., Sun, Q., Meyerowitz, EM.: Ethylene insensitivity conferred by Arabidopsis ERS gene. - Science 269: 1712-1714, 1995a. Go to original source...
    38. Hua, J., Meyerowitz, E.M.: Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. - Cell 94: 261-271, 1998. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    45. Lincoln, C., Britton, J.H., Estelle, M.: Growth and development of the axr1 mutants of Arabidopsis. - Plant Cell 2: 1071-1080, 1990. Go to original source...
    46. Lindow, S.E., Brandl, M.T.: Microbiology of the phyllosphere. - Appl. Environ. Microbiol. 69: 1875-1883, 2003.
    47. Ljung K.: Auxin metabolism and homeostasis during plant development. - Development 140: 943-950, 2013. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    53. Misaghi, I., Donndelinger, C.: Endophytic bacteria in symptom-free cotton plants. - Phytopathology 80: 808-811, 1990. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    57. Oldroyd, G.E.D., Downie, J.A.: Coordinating nodule morphogenesis with rhizobial infection in legumes. - Annu. Rev. Plant Biol. 59: 519-546, 2008. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    61. Ping, L., Boland, W.: Signals from the underground: bacterial volatiles promote growth in Arabidopsis. - Trends Plant Sci. 9: 263-266, 2004. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    68. Slankis, V.: Soil factors influencing formation of mycorrhizae. - Annu. Rev. Phytopathol. 12: 437-457, 1974. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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.
    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. Go to original source...
    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.
    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. Go to original source...
    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.
    77. Weise, T., Kai, M., Piechulla, B.: Bacterial ammonia causes significant plant growth inhibition. - PloS ONE 8: e63538, 2013. Go to original source...
    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. Go to original source...
    79. Woodward, A.W., Bartel, B.: Auxin: regulation, action, and interaction. - Ann. Bot. 95: 707-735, 2005. Go to original source...
    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. Go to original source...

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