Indole-3-butyric acid induces lateral root formation via peroxisome-derived indole-3-acetic acid and nitric oxide

New Phytologist

Volumn 200, Issue 2, 2013, Pages 473-482

  Schlicht, Markus ^a   Ludwig Müller, Jutta ^b   Burbach, Christian ^c   Volkmann, Dieter ^c   Baluska, Frantisek ^c  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c UNIVERSITY OF BONN   (Germany)

Author keywords

Arabidopsis; Indole 3 butyric acid (IBA); Lateral root formation; Maize; Nitric oxide (NO); Peroxisomes

Indexed keywords

FLUORESCENCE; MAIZE; MEMBRANE; NITRIC OXIDE; NITROGEN; OXYGEN; PLANT; PLASMA; ROOT ARCHITECTURE; SIGNALING;

ARABIDOPSIS; ZEA MAYS;

INDOLE DERIVATIVE; INDOLEACETIC ACID; INDOLEACETIC ACID DERIVATIVE; INDOLEBUTYRIC ACID; NITRIC OXIDE; PHYTOHORMONE;

ARABIDOPSIS; ARTICLE; GENETICS; GROWTH, DEVELOPMENT AND AGING; INDOLE-3-BUTYRIC ACID (IBA); LATERAL ROOT FORMATION; MAIZE; METABOLISM; MUTATION; NITRIC OXIDE (NO); PEROXISOME; PHENOTYPE; PHYSIOLOGY; PLANT ROOT; SEEDLING; SIGNAL TRANSDUCTION;

ARABIDOPSIS; INDOLE-3-BUTYRIC ACID (IBA); LATERAL ROOT FORMATION; MAIZE; NITRIC OXIDE (NO); PEROXISOMES;

ARABIDOPSIS; INDOLEACETIC ACIDS; INDOLES; MUTATION; NITRIC OXIDE; PEROXISOMES; PHENOTYPE; PLANT GROWTH REGULATORS; PLANT ROOTS; SEEDLING; SIGNAL TRANSDUCTION; ZEA MAYS;

EID: 84884412718     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12377     Document Type: Article

References (95)

1. Abel S. 2007. Auxin is surfacing. ACS Chemical Biology 2: 380-384.
2. Aloni R, Aloni E, Langhans M, Ullrich CI. 2006. Role of cytokinin and auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Annals of Botany 97: 883-893.
3. Arita NO, Cohen MF, Tokuda G, Yamasaki H. 2006. Fluorometric detection of nitric oxide with diaminofluoresceins (DAFs): applications and limitations for plant NO research. In: Lamattina L, Polacco JC, eds. Nitric oxide in plant growth. Plant cell monogr 6. Heidelberg, Germany: Springer Verlag, 269-280.
4. Bai X, Todd CD, Desikan R, Yang Y, Hu X. 2012. N-3-oxo-decanoyl-L-homoserine-lactone activates auxin-induced adventitious root formation via hydrogen peroxide- and nitric oxide-dependent cyclic GMP signaling in mung bean. Plant Physiology 158: 725-736.
5. Barkawi LS, Tam Y, Tillman JA, Pederson B, Calio J, Al-Amier H, Emerick M, Normanly J, Cohen JD. 2008. A high-throughput method for the quantitative analysis of indole-3-acetic acid and other auxins from plant tissue. Analytical Biochemistry 372: 177-188.
6. Barroso JB, Corpas FJ, Carreras A, Sandalio LM, Valderrama R, Palma JM, Lupianez JA, del Rio LA. 1999. Localization of nitric-oxide synthase in plant peroxisomes. Journal of Biological Chemistry 274: 36729-36733.
7. Bartel B. 1997. Auxin biosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 48: 51-66.
8. Bianco C, Imperlini E, Calogero R, Senatore B, Amoresano A, Carpentieri A, Pucci P, Defez R. 2006b. Indole-3-acetic acid improves Escherichia coli's defences to stress. Archives of Microbiology 185: 373-382.
9. Bianco C, Imperlini E, Calogero R, Senatore B, Pucci P, Defez R. 2006a. Indole-3-acetic acid regulates the central metabolic pathways in Escherichia coli. Microbiology 152: 2421-2431.
10. Bolwell GP, Blee KA, Butt VS, Davies DR, Gardner SL, Gerrish C, Minibayeva F, Rowntree EG, Wojtaszek P. 1999. Recent advances in understanding the origin of the apoplastic oxidative burst in plant cells. Free Radical Research 31(Suppl): S137-S145.
11. Campanella JJ, Ludwig-Müller J, Bakllamaja V, Sharma V, Cartier A. 2003. ILR1 and sILR1 IAA amidohydrolase homologs differ in expression pattern and substrate specificity. Plant Growth Regulation 41: 215-223.
12. Chen X, Naramoto S, Robert S, Tejos R, Löfke C, Lin D, Yang Z, Friml J. 2012. ABP1 and ROP6 GTPase signaling regulate clathrin-mediated endocytosis in Arabidopsis roots. Current Biology 22: 1911-1921.
13. Chhun T, Taketa S, Tsurumi S, Ichii M. 2003. Interaction between two auxin-resistant mutants and their effects on lateral root formation in rice. Journal of Experimental Botany 54: 2701-2708.
14. Christian M, Steffens B, Schenck D, Burmester S, Böttger M, Lüthen H. 2006. How does auxin enhance cell elongation? Roles of auxin-binding proteins and potassium channels in growth control. Plant Biology 8: 346-352.
15. Cluis CP, Mouchel CF, Hardtke CS. 2004. The Arabidopsis transcription factor HY5 integrates light and hormone signaling pathways. Plant Journal 38: 332-347.
16. Cohen JD. 1984. Convenient apparatus for the generation of small amounts of diazomethane. Journal of Chromatography 303: 193-196.
17. Corpas FJ, Hayashi M, Mano S, Nishimura M, Barroso JB. 2009. Peroxisomes are required for in vivo nitric oxide accumulation in the cytosol following salinity stress of Arabidopsis plants. Plant Physiology 151: 2083-2094.
18. Correa-Aragunde N, Graziano M, Lamattina L. 2004. Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218: 900-905.
19. Dahlke RI, Luethen H, Steffens B. 2010. ABP1: an auxin receptor for fast responses at the plasma membrane. Plant Signaling & Behavior 5: 1-3.
20. Dharmasiri N, Dharmasiri S, Estelle M. 2005. The F-box protein TIR1 is an auxin receptor. Nature 435: 441-445.
21. Epstein E, Ludwig-Müller J. 1993. Indole-3-butyric acid in plants: occurrence, synthesis, metabolism, and transport. Physiologia Plantarum 88: 382-389.
22. Felle H, Peters W, Palme K. 1991. The electrical response of maize to auxins. Biochimica et Biophysica Acta 1064: 199-204.
23. Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K. 2002. Lateral redistribution of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415: 806-809.
24. Gas E, Flores-Pérez U, Sauret-Güeto S, Rodríguez-Concepción M. 2009. Hunting for plant nitric oxide synthase provides new evidence of a central role for plastids in nitric oxide metabolism. Plant Cell 21: 18-23.
25. Gerhardt B. 1992. Fatty acid degradation in plants. Progress in Lipid Research 31: 417-446.
26. Godber BL, Doel JJ, Sapkota GP, Blake DR, Stevens CR, Eisenthal R, Harrison R. 2000. Reduction of nitrite to nitric oxide catalyzed by xanthine oxidoreductase. Journal of Biological Chemistry 275: 7757-7763.
27. Guo FQ, Crawford NM. 2005. Arabidopsis nitric oxide synthase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell 17: 3436-3450.
28. Guo FQ, Okamoto M, Crawford NM. 2003. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302: 100-103.
29. Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM. 2005. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Current Biology 15: 1899-1911.
30. Hesse T, Feldwisch J, Balshüsemann D, Bauw G, Puype M, Vandekerckhove J, Löbler M, Klämbt D, Schell J, Palme K. 1989. Molecular cloning and structural analysis of a gene from Zea mays (L.) coding for a putative receptor for the plant hormone auxin. EMBO Journal 8: 2453-2461.
31. Himanen K, Vuylsteke M, Vanneste S, Vercruysse S, Boucheron E, Alard P, Chriqui D, Van Montagu M, Inzé D, Beeckman T. 2004. Transcript profiling of early lateral root initiation. Proceedings of the National Academy of Sciences, USA 101: 5146-5151.
32. Hochholdinger F, Feix G. 1998. Early post-embryonic root formation is specifically affected in the maize mutant lrt1. Plant Journal 16: 247-255.
33. Hu X, Neill SJ, Tang Z, Cai W. 2005. Nitric oxide mediates gravitropic bending in soybean roots. Plant Physiology 137: 663-670.
34. Jentschel K, Thiel D, Rehn F, Ludwig-Müller J. 2007. Arbuscular mycorrhiza enhances auxin levels and alters auxin biosynthesis in Tropaeolum majus during early stages of colonization. Physiologia Plantarum 129: 320-333.
35. Joo JH, Bae YS, Lee JS. 2001. Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiology 126: 1055-1060.
36. Joo JH, Yoo HJ, Hwang I, Lee JS, Nam KH, Bae YS. 2005. Auxin-induced reactive oxygen species production requires the activation of phosphatidylinositol 3kinase. FEBS Letters 579: 1243-1248.
37. Kepinski S, Leyser O. 2005. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435: 446-451.
38. Kindl H. 1993. Fatty acid degradation in plant peroxisomes: function and biosynthesis of the enzymes involved. Biochimie 75: 225-230.
39. Kojima H, Nakatsubo N, Kikuchi K, Kawahara S, Kirino Y, Nagoshi H, Hirata Y, Nagano T. 1998. Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins. Analytical Chemistry 70: 2446-2453.
40. Kolbert Z, Bartha B, Erdei L. 2008. Exogenous auxin-induced NO synthesis is nitrate reductase-associated in Arabidopsis thaliana root primordia. Journal of Plant Physiology 165: 967-975.
41. Kolbert Z, Erdei L. 2008. Involvement of nitrate reductase in auxin-induced NO synthesis. Plant Signaling & Behavior 3: 972-973.
42. Lanteri ML, Laxalt AM, Lamattina L. 2008. Nitric oxide triggers phosphatidic acid accumulation via phospholipase D during auxin-induced adventitious root formation in cucumber. Plant Physiology 147: 188-198.
43. 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. Journal of Experimental Botany 57: 1341-1351.
44. Li J, Jia H. 2013. cGMP modulates Arabidopsis lateral root formation through regulation of polar auxin transport. Plant Physiology and Biochemistry 66: 105-117.
45. Li J, Wang X, Zhang Y, Jia H, Bi Y. 2011. cGMP regulates hydrogen peroxide accumulation in calcium-dependent salt resistance pathway in Arabidopsis thaliana roots. Planta 234: 709-722.
46. Li L, Xu J, Xu ZH, Xue HW. 2005. Brassinosteroids stimulate plant tropisms through modulation of polar auxin transport in Brassica and Arabidopsis. Plant Cell 17: 2738-2753.
47. Loake G, Grant M. 2007. Salicylic acid in plant defence - the players and protagonists. Current Opinion in Plant Biology 10: 466-472.
48. Logan DC, Leaver CJ. 2000. Mitochondria-targeted GFP highlights the heterogeneity of mitochondrial shape, size and movement within living plant cells. Journal of Experimental Botany 346: 865-871.
49. Lombardo MC, Graziano M, Polacco JC, Lamattina L. 2006. Nitric oxide functions as a positive regulator of root hair development. Plant Signaling & Behavior 1: 28-33.
50. Ludwig-Müller J. 2000. Indole-3-butyric acid in plant growth and development. Plant Growth Regulation 32: 219-230.
51. Ludwig-Müller J, Epstein E. 1991. Occurrence and in vivo biosynthesis of indole-3-butyric acid in corn (Zea mays L.). Plant Physiology 97: 765-770.
52. Ludwig-Müller J, Vertocnik A, Town CD. 2005. Analysis of indole-3-butyric acid-induced adventitious root formation on Arabidopsis stem segments. Journal of Experimental Botany 418: 2095-2105.
53. Maurel C, Leblanc N, Barbier-Brygoo H, Perrot-Rechenmann C, Bouvier-Durand M, Guern J. 1994. Alterations of auxin perception in rolB-transformed tobacco protoplasts. Time course of rolB mRNA expression and increase in auxin sensitivity reveal multiple control by auxin. Plant Physiology 105: 1209-1215.
54. Mockaitis K, Howell SH. 2000. Auxin induces mitogenic activated protein kinase (MAPK) activation in roots of Arabidopsis seedlings. Plant Journal 24: 785-796.
55. Modolo LV, Augusto O, Almeida IM, Magalhaes JR, Salgado I. 2005. Nitrite as the major source of nitric oxide production by Arabidopsis thaliana in response to Pseudomonas syringae. FEBS Letters 579: 3814-3820.
56. Moreau M, Lee GI, Wang Y, Crane BR, Klessig DF. 2008. AtNOS/AtNOA1 is functional Arabidopsis thaliana cGTPase and not NO synthase. Journal of Biological Chemistry 283: 32957-32967.
57. Mugnai S, Azzarello E, Baluska F, Mancuso S. 2012. Local root apex hypoxia induces NO-mediated hypoxic acclimation of the entire root. Plant and Cell Physiology 53: 912-920.
58. Murashige T, Skoog F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15: 473-497.
59. Nordström A-C, Jacobs FA, Eliasson L. 1991. Effect of exogenous IAA and IBA on internal levels of the respective auxins and their conjugation with aspartic acid during adventitious root formation in pea cuttings. Plant Physiology 96: 856-861.
60. Oono Y, Chen QG, Overvoorde PJ, Köhler C, Theologis A. 1998. Age mutants of Arabidopsis exhibit altered auxin-regulated gene expression. Plant Cell 10: 1649-1662.
61. Pagnussat GC, Lanteri ML, Lamattina L. 2003. Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiology 132: 1241-1248.
62. Pagnussat GC, Lanteri M, Lombardo M, Lamattina L. 2004. Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiology 135: 279-286.
63. Poupart J, Rashotte AM, Muday GK, Waddell CS. 2005. The rib1 mutant of Arabidopsis has alterations in indole-3-butyric acid transport, hypocotyl elongation, and root architecture. Plant Physiology 139: 1460-1471.
64. Prado AM, Porterfield DM, Feijo JA. 2004. Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 131: 2707-2714.
65. Pufky J, Qiu Y, Rao MV, Hurban P, Jones AM. 2003. The auxin-induced transcriptome for etiolated Arabidopsis seedlings using a structure/function approach. Functional & Integrative Genomics 3: 135-143.
66. Rao RP, Hunter A, Kashpur O, Normanly J. 2010. Aberrant synthesis of indole-3-acetic acid in Saccharomyces cerevisiae triggers morphogenic transition, a virulence trait of pathogenic fungi. Genetics 185: 211-220.
67. Rashotte AM, Poupart J, Waddell CS, Muday GK. 2003. Transport of the two natural auxins, IBA and IAA, in Arabidopsis. Plant Physiology 133: 761-772.
68. del Rio LA, Corpas FJ, Leon AM, Barroso JB, Carreras A, Sandalio LM, Palma JM. 2004. The nitric oxide synthase activity of plant peroxisomes. Free Radical Biology and Medicine 36: 41.
69. Robert S, Kleine-Vehn J, Barbez E, Sauer M, Paciorek T, Baster P, Vanneste S, Zhang J, Simon S, Čovanová M et al. 2010. ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 143: 111-121.
70. Rück A, Plame K, Venis MA, Napier RM, Felle HH. 1993. Patch-clamp analysis establishes a role for an auxin binding protein in the auxin stimulation of plasma membrane current in Zea mays protoplasts. Plant Journal 4: 41-46.
71. Sawa S, Ohgishi M, Goda H, Higuchi K, Shimada Y, Yoshida S, Koshiba T. 2002. The HAT2 gene, a member of the HD-Zip gene family, isolated as an auxin inducible gene by DNA microarray screening, affects auxin response in Arabidopsis. Plant Journal 32: 1011-1022.
72. Spaepen S, Versées W, Gocke D, Pohl M, Steyaert J, Vanderleyden J. 2007. Characterization of phenylpyruvate decarboxylase, involved in auxin production of Azospirillum brasilense. Journal of Bacteriology 189: 7626-7633.
73. Splivallo R, Fischer U, Gobel C, Feussner I, Karlovsky P. 2009. Truffles regulate plant root morphogenesis via the production of auxin and ethylene. Plant Physiology 150: 2018-2029.
74. Strader LC, Culler AH, Cohen JD, Bartel B. 2010. Conversion of endogenous indole-3-butyric acid to indole-3-acetic acid drives cell expansion in Arabidopsis seedlings. Plant Physiology 153: 1577-1586.
75. Strader LC, Wheeler DL, Christensen SE, Berens JC, Cohen JD, Rampey RA, Bartel B. 2011. Multiple facets of Arabidopsis seedling development require indole-3-butyric acid-derived auxin. Plant Cell 23: 984-999.
76. Teale WD, Paponov IA, Ditengou F, Palme K. 2005. Auxin and the developing root of Arabidopsis thaliana. Physiologia Plantarum 123: 130-138.
77. Teale WD, Paponov IA, Palme K. 2006. Auxin in action: signalling, transport and the control of plant growth and development. Nature Reviews in Molecular Cell Biology 7: 847-859.
78. Tognetti VB, Van Aken O, Morreel K, Vandenbroucke K, van de Cotte B, De Clercq I, Chiwocha S, Fenske R, Prinsen E, Boerjan W et al. 2010. Perturbation of indole-3-butyric acid homeostasis by the UDP-glucosyltransferase UGT74E2 modulates Arabidopsis architecture and water stress tolerance. Plant Cell 22: 2660-2679.
79. Tromas A, Paponov I, Perrot-Rechenmann C. 2010. AUXIN BINDING PROTEIN 1: functional and evolutionary aspects. Trends in Plant Science 15: 36-46.
80. Ulrich JM. 1960. Auxin production by mycorrhizal fungi. Physiologia Plantarum 13: 429-443.
81. Wan Y, Jasik J, Wang L, Hao H, Volkmann D, Menzel D, Mancuso S, Baluška F, Lin J. 2012. The signal transducer NPH3 integrates the phototropin1 photosensor with PIN2-based polar auxin transport in Arabidopsis root phototropism. Plant Cell 24: 551-565.
82. Wang BL, Tang XY, Cheng LY, Zhang AZ, Zhang WH, Zhang FS, Liu JQ, Cao Y, Allan DL, Vance CP et al. 2010. Nitric oxide is involved in phosphorus deficiency-induced cluster-root development and citrate exudation in white lupin. New Phytologist 187: 1112-1123.
83. Wang C, Yan X, Chen Q, Jiang N, Fu W, Ma B, Liu J, Li C, Bednarek SY, Pan J. 2013. Clathrin light chains regulate clathrin-mediated trafficking, auxin signaling, and development in Arabidopsis. Plant Cell 25: 499-516.
84. Wiszniewski AA, Zhou W, Smith SM, Bussell JD. 2008. Identification of two Arabidopsis genes encoding a peroxisomal oxidoreductase-like protein and an acyl-CoA synthetase-like protein that are required for responses to pro-auxins. Plant Molecular Biology 69: 503-515.
85. Woodward AW, Bartel B. 2005a. Auxin: regulation, action, and interaction. Annals of Botany 95: 707-735.
86. Woodward AW, Bartel B. 2005b. The Arabidopsis peroxisomal targeting signal type 2 receptor PEX7 is necessary for peroxisome function and dependent on PEX5. Molecular Biology of the Cell 16: 573-583.
87. 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: 99-110.
88. Yadav S, David A, Baluška F, Bhatla SC. 2013. Rapid auxin-induced nitric oxide accumulation and subsequent tyrosine nitration of proteins during adventitious root formation in sunflower hypocotyls. Plant Signaling & Behavior 8: e23196.
89. Yamazoe A, Hayashi K, Kepinski S, Leyser O, Nozaki H. 2005. Characterization of terfestatin A, a new specific inhibitor for auxin signaling. Plant Physiology 139: 779-789.
90. Zhang Z, Naughton D, Winyard PG, Benjamin N, Blake DR, Symons MCR. 1998. Generation of nitric oxide by a nitrite reductase activity of xanthine oxidase: a potential pathway for nitric oxide formation in the absence of nitric oxide synthase activity. Biochemical and Biophysical Research Communications 249: 767.
91. Zolman BK, Bartel B. 2004. An Arabidopsis indole-3-butyric acid-response mutant defective in PEROXIN6, an apparent ATPase implicated in peroxisomal function. Proceedings of the National Academy of Sciences, USA 101: 1786-1791.
92. Zolman BK, Martinez N, Millius A, Adham AR, Bartel B. 2008. Identification and characterization of Arabidopsis indole-3-butyric acid response mutants defective in novel peroxisomal enzymes. Genetics 180: 237-251.
93. Zolman BK, Monroe-Augustus M, Thompson B, Hawes JW, Krukenberg KA, Matsuda SP, Bartel B. 2001b. chy1, an Arabidopsis mutant with impaired beta-oxidation, is defective in a peroxisomal beta-hydroxyisobutyryl-CoA hydrolase. Journal of Biological Chemistry 276: 31037-31046.
94. Zolman BK, Silva ID, Bartel B. 2001a. The Arabidopsis pxa1 mutant is defective in an ATP-binding cassette transporter-like protein required for peroxisomal fatty acid beta-oxidation. Plant Physiology 127: 1266-1278.
95. Zolman BK, Yoder A, Bartel B. 2000. Genetic analysis of indole-3-butyric acid responses in Arabidopsis thaliana reveals four mutant classes. Genetics 156: 1323-1337.