When stress and development go hand in hand: Main hormonal controls of adventitious rooting in cuttings

Frontiers in Plant Science

Volumn 4, Issue MAY, 2013, Pages

  da Costa, Cibele T ^a   de Almeida, Márcia R ^a   Ruedell, Carolina M ^a   Schwambach, Joseli ^b   Maraschin, Felipe S ^a   Fett Neto, Arthur G ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b UNIVERSITY OF CAXIAS DO SUL   (Brazil)

Author keywords

Adventitious rooting; Auxin; Cytokinin; Hormonal crosstalk; Jasmonic acid; MicroRNAs; Nutrition; Receptors

Indexed keywords

EID: 84894609354     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00133     Document Type: Review

References (192)

1. Abu-Abied, M., Szwerdszarf, D., Mordehaev, I., Levy, A., Rogovoy, O., Belausov, E., et al. (2012). Microarray analysis revealed upregulation of nitrate reductase in juvenile cuttings of Eucalyptus grandis, which correlated with increased nitric oxide production and adventitious root formation. Plant J. 71, 787-799.
2. Acosta, M., Oliveros-Valenzuela, M. R., Nicolás, C., and Sánchez-Bravo, J. (2009). Rooting of carnation cuttings. The auxin signal. Plant Signal. Behav. 4, 234-236.
3. Agulló-Antón, M. A., Sánchez-Bravo, J., Acosta, M., and Druege, U. (2011). Auxins or sugars: what makes the difference in the adventitious rooting of stored carnation cuttings? J. Plant Growth Regul. 30, 100-113.
4. Ahkami, A. H., Lischewski, S., Haensch, K. T., Porfirova, S., Hofmann, J., Rolletschek, H., et al. (2009). Molecular physiology of adventitious root formation in Petunia hybrida cuttings: involvement of wound response and primary metabolism. New Phytol. 181, 613-625.
5. Aida, M., Beis, D., Heidstra, R., Willemsen, V., Blilou, I., Galinha, C., et al. (2004). The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119, 109-120.
6. Altamura, M. M. (1996). Root histogenesis in herbaceous and woody explants cultured in vitro. A critical review. Agronomie 16, 589-602.
7. Arena, M. E., Pastur, G. M., Benavides, M. P., Zappacosta, D., Eliasco, E., and Curvetto, N. (2003). Peroxidase and polyamine activity variation during the in vitro rooting of Berberis buxifolia. N. Z. J. Bot. 41, 475-485.
8. Arnaud, C., Bonnot, C., Desnos, T., and Nussaume, L. (2010). The root cap at the forefront. C. R. Biol. 333, 335-343.
9. Assis, T. F., Fett-Neto, A. G., and Alfenas, A. C. (2004). "Current techniques and prospects for the clonal propagation of hardwood with emphasis on Eucalyptus, " in Plantation Forest Biotechnoloy for the 21st Century, eds C. Walter and M. Carson (Kerala: Research Signpost), 304-333.
10. Bak, S., Tax, F. E., Feldmann, K. A., Galbraith, D. W., and Feyereisen, R. (2001). CYP83B1, a cytochrome P450 at the metabolic branch point in auxin and indole glucosinolate biosynthesis in Arabidopsis. Plant Cell 13, 101-111.
11. Barbez, E., and Kleine-Vehn, J. (2012). Divide Et Impera--cellular auxin compartmentalization. Cur. Opin. Plant Biol. 16, 1-7.
12. Barbez, E., Kubes, M., Rolcik, J., Béziat, C., Pencik, A., Wang, B., et al. (2012). A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature 485, 119-122.
13. Barlier, I., Kowalczyk, M., Marchant, A., Ljung, K., Bhalerao, R., Bennett, M., et al. (2000). The SUR2 gene of Arabidopsis thaliana encodes the cytochrome P450 CYP83B1, a modulator of auxin homeostasis. Proc. Natl. Acad. Sci. U.S.A. 97, 14819-14824.
14. Bellamine, J., Penel, C., Greppin, H., and Gaspar, T. (1998). Confirmation of the role of auxin and calcium in the late phases of adventitious root formation. Plant Growth Regul. 26, 191-194.
15. Benkova, E., and Bielach, A. (2010). Lateral root organogenesis--from cell to organ. Cur. Opin. Plant Biol. 13, 677-683.
16. Berleth, T., Scarpella, E., and Prusinkiewicz, P. (2007). Towards the systems biology of auxin-transport-mediated patterning. Trends Plant Sci. 12, 151-159.
17. Blazich, F. A. (1988). "Mineral nutrition and adventitious rooting" in Adventitious Root Formation in Cuttings-Advances in Plant Science, Vol. 2., eds T. D. Davis, B. E. Haissig and N. Sankhla (Portland: Dioscorides Press), 61-69.
18. Blilou, I., Xu, J., Wildwater, M., Willemsen, V., Paponov, I., Friml, J., et al. (2005). The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39-44.
19. Borghi, L., Gutzat, R., Fütterer, J., Laizet, Y., Hennig, L., and Gruissem, W. (2010). Arabidopsis RETINOBLASTOMA-RELATED is required for stem cell maintenance, cell differentiation, and lateral organ production. Plant Cell 22, 1792-1811.
20. Boudolf, V., Inzé, D., and De Veylder, L. (2006). What if higher plants lack a CDC25 phosphatase? Trends Plant Sci. 11, 474-479.
21. Brinker, M., van Zyl, L., Liu, W., Craig, D., Sederoff, R. R., Clapham, D. H., et al. (2004). Microarray analyses of gene expression during adventitious root development in Pinus contorta. Plant Physiol. 135, 1526-1539.
22. Buer, C. S., Imin, N., and Djordjevic, M. A. (2010). Flavonoids: new roles for old molecules. J. Integr. Plant Biol. 52, 98-111.
23. Busov, V., Meilan, R., Pearce, D. W., Rood, S. B., Ma, C., Tschaplinski, T. J., et al. (2006). Transgenic modification of gai or rgl1 causes dwarfing and alters gibberellins, root growth, and metabolite profile in Populus. Planta 224, 288-299.
24. Cambridge, A. P., and Morris, D. A. (1996). Transfer of exogenous auxin from the phloem to the polar auxin transport pathway in pea (Pisum sativum L.). Planta 199, 583-588.
25. Cameron, R., Harrison-Murray, R., Fordham, M., Judd, H., Ford, Y., Marks, T., et al. (2003). Rooting cuttings of Syringa vulgaris cv. Charles Joly and Corylus avellana cv. Aurea: the influence of stock plant pruning and shoot growth. Trees 17, 451-462.
26. Campa, A. (1991). "Biological roles of plant peroxidases: known and potential function" in Peroxidases in Chemistry and Biology, eds J. Everse, K. E. Everse, and M. B. Grisham (Boca Raton: CRC Press), 25-50.
27. Chapman, E. J., and Estelle, M. (2009). Mechanism of auxin-regulated gene expression in plants. Annu. Rev. Gent. 43, 265-285.
28. Corrêa, L. R., Paim, D. C., Schwambach, J., and Fett-Neto, A. G. (2005). Carbohydrates as regulatory factors on the rooting of Eucalyptus saligna Smith and Eucalyptus globulus Labill. Plant Growth Regul. 45, 63-73.
29. Corrêa, L. R., Stein, R. J., and Fett-Neto, A. G. (2012a). Adventitious rooting of detached Arabidopsis thalianaleaves. Biol. Plant. 56, 25-30.
30. Corrêa, L. R., Troleis, J., Mastroberti, A. A., Mariath, J. E., and Fett-Neto, A. G. (2012b). Distinct modes of adventitious rooting in Arabidopsis thaliana. Plant Biol. 14, 100-109.
31. Cui, H., Levesque, M. P., Vernoux, T., Jung, J. W., Paquette, A. J., Gallagher, K. L., et al. (2007). An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316, 421-425.
32. De Klerk, G. J. (2002). Rooting of microcuttings: theory and practice. In Vitro Cell. Dev. Biol. Plant 38, 415-422.
33. De Klerk, G. J., and Hanecakova, J. (2008). Ethylene and rooting of mung bean cuttings. The role of auxin induced synthesis and phase-dependent effects. Plant Growth Regul. 56, 203-209.
34. De Klerk, G. J., Guan, H., Huisman, P., and Marinova, S. (2011). Effects of phenolic compounds on adventitious root formation and oxidative decarboxylation of applied indoleacetic acid in Malus 'Jork 9'. Plant Growth Regul. 63, 175-185.
35. De Klerk, G. J., Van der Krieken, W., and De Jong, J. C. (1999). The formation of adventitious roots: new concepts, new possibilities. In Vitro Cell. Dev. Biol. Plant 35, 189-199.
36. Delarue, M., Prinsen, E., Van Onckelen, H., Caboche, M., and Bellini, C. (1998). Sur2 mutations of Arabidopsis thaliana define a new locus involved in the control of auxin homeostasis. Plant J. 14, 603-611.
37. Delbarre, A., Müller, P., Imhoff, V., and Guern, J. (1996). Comparison of mechanisms controlling uptake and accumulation of 2, 4-dichlorophenoxy acetic acid, naphthalene-1-acetic acid, and indole-3-acetic acid in suspension-cultured tobacco cells. Planta 198, 532-541.
38. Dello Ioio, R., Linhares, F. S., Scacchi, E., Casamitjana-Martinez, E., Heidstra, R., Costantino, P., et al. (2007). Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr. Biol. 17, 678-682.
39. Dello Ioio, R., Nakamura, K., Moubayidin, L., Perilli, S., Taniguchi, M., Morita, M. T., et al. (2008). A genetic framework for the control of cell division and differentiation in the root meristem. Science 322, 1380-1384.
40. Desnos, T. (2008). Root branching responses to phosphate and nitrate. Curr. Opin. Plant Biol. 11, 82-87.
41. De Veylder, L., Beeckman, T., and Inzé, D. (2007). The ins and outs of the plant cell cycle. Nat. Rev. Mol. Cell Biol. 8, 655-665.
42. Dewitte, W., and Murray, J. A. (2003). The plant cell cycle. Annu. Rev. Plant Biol. 54, 235-264.
43. Dharmasiri, N., Dharmasiri, S., and Estelle, M. (2005a). The F-box protein TIR1 is an auxin receptor. Nature 435, 441-445.
44. Dharmasiri, N., Dharmasiri, S., Weijers, D., Lechner, E., Yamada, M., Hobbie, L., et al. (2005b). Plant development is regulated by a family of auxin receptor F box proteins. Dev. Cell 9, 109-119.
45. Díaz-Sala, C., Garrido, G., and Sabater, B. (2002). Age-related loss of rooting capability in Arabidopsis thaliana and its reversal by peptides containing the Arg-Gly-Asp (RGD) motif. Physiol. Plant. 114, 601-607.
46. Diaz-Sala, C., Hutchison, K. W., Goldfarb, B., and Greenwood, M. S. (1996). Maturation-related loss in rooting competence by loblolly pine stem cuttings: the role of auxin transport, metabolism and tissue sensitivity. Physiol. Plant. 97, 481-490.
47. Doerner, P. (1998). Root development: quiescent center not so mute after all. Curr. Biol. 8, 42-44.
48. Druege, U. (2009). "Involvement of carbohydrates in survival and adventitious root formation of cuttings within the scope of global horticulture" in Adventitious Root Formation of Forest Trees and Horticultural Plants-From Genes to Applications, eds K. Niemi and C. Scagel (Kerala: Research Signpost), 187-208.
49. Druege, U., Zerche, S., and Kadner, R. (2004). Nitrogen-and storage-affected carbohydrate partitioning in high-light-adapted Pelargonium cuttings in relation to survival and adventitious root formation under low light. Ann. Bot. 94, 831-842.
50. Druege, U., Zerche, S., Kadner, R., and Ernst, M. (2000). Relationship between nitrogen status, carbohydrate distribution and subsequent rooting of Chrysanthemum cuttings as affected by pre-harvest nitrogen supply and cold-storage. Ann. Bot. 85, 687-701.
51. Dubrovsky, J. G., Sauer, M., Napsucialy-Mendivil, S., Ivanchenko, M., Friml, J., Shishkova, S., et al. (2008). Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc. Natl. Acad. Sci. U.S.A. 105, 8790-8794.
52. Epstein, E., and Ludwig-Müller, J. (1993). Indole-3-butyric acid in plants: occurrence, synthesis, metabolism and transport. Physiol. Plant. 88, 382-389.
53. Fang, W.-C., and Kao, C. H. (2000). Enhanced peroxidase activity in rice leaves in response to excess iron, copper and zinc. Plant Sci. 158, 71-76.
54. Feraru, E., Vosolsobe, S., Feraru, M. I., Petrášek, J., and Kleine-Vehn, J. (2012). Evolution and structural diversification of PILS putative auxin carriers in plants. Front. Plant Sci. 3:227. doi: 10.3389/fpls.2012.00227
55. Fernández-Lorenzo, J. L., Ballester, A., and Rigueiro, A. (2005). Phenolic content of microcuttings of adult chestnut along rooting induction. Plant Cell Tissue Organ Cult. 83, 153-159.
56. Fett-Neto, A. G., Fett, J. P., Goulart, L. W. V., Pasquali, G., Termignoni, R. R., and Ferreira, A. G. (2001). Distinct effects of auxin and light on adventitious root development in Eucalyptus saligna and Eucalyptus globulus. Tree Physiol. 21, 457-464.
57. Fett-Neto, A. G., Teixeira, S. L., Da Silva, E. A. M., and Sant'Anna, R. (1992). Biochemical and morphological changes during in vitro rhizogenesis in cuttings of Sequoia sempervirens (D. Don) Endl. J. Plant Physiol. 140, 720-728.
58. Fleck, J. D., Schwambach, J., Almeida, M. E., Yendo, A. C. A., De Costa, F., Gosmann, G., et al. (2009). Immunoadjuvant saponin production in seedlings and micropropagated plants of Quillaja brasiliensis. In Vitro Cell. Dev. Biol. Plant 45, 715-720.
59. Fogaça, C. M., and Fett-Neto, A. G. (2005). Role of auxin and its modulators in the adventitious rooting of Eucalyptus species differing in recalcitrance. Plant Growth Regul. 45, 1-10.
60. Friml, J., and Palme, K. (2002). Polar auxin transport-old questions and new concepts? Plant Mol. Biol. 49, 273-284.
61. Gaedeke, N., Klein, M., Kolukisaoglu, U., Forestier, C., Muller, A., Ansorge, M., et al. (2001). The Arabidopsis thaliana ABC transporter AtMRP5 controls root development and stomata movement. EMBO J. 20, 1875-1887.
62. Garrido, G., Guerreo, J. R., Cano, E. A., Acosta, M., and Sánchez-Bravo, J. (2002). Origin and basipetal transport of the IAA responsible for rooting of carnation cuttings. Physiol. Plant. 114, 303-312.
63. Geisler, M., and Murphy, A. (2006). The ABC of auxin transport: the role of p-glicoproteins in plant development. FEBS Lett. 580, 1094-1102.
64. Gou, J., Strauss, S. H., Tsai, C. J., Fang, K., Chen, Y., Jiang, X., et al. (2010). Gibberellins regulate lateral root formation in Populus through interactions with auxins and other hormones. Plant Cell 22, 623-639.
65. Gray, W. M., Kepinski, S., Rouse, D., Leyser, O., and Estelle, M. (2001). Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 414, 271-276.
66. Greenham, K., Santner, A., Castillejo, C., Mooney, S., Sairanen, I., Ljung, K., et al. (2011). The AFB4 auxin receptor is a negative regulator of auxin signaling in seedlings. Curr. Biol. 21, 520-525.
67. Greenwood, M. S., Cui, X., and Xu, F. (2001). Response to auxin changes during maturation-related loss of adventitious rooting competence in loblolly pine (Pinus taeda) stem cuttings. Physiol. Plant. 111, 373-380.
68. Guan, H., and De Klerk, G. J. (2000). Stem segments of apple microcuttings take up auxin predominantly via the cut surface and not via the epidermal surface. Sci. Hortic. 86, 23-32.
69. Guerrero, J. R., Garrido, G., Acosta, M., and Sánchez-Bravo, J. (1999). Influence of 2, 3, 5-triiodobenzoic acid and 1-N-naphthylphthalamic acid on indoleacetic acid transport in carnation cuttings: relationship with rooting. J. Plant Growth Regul. 18, 183-190.
70. Guo, D., Liang, J., Qiao, Y., Yan, Y., Li, L., and Dai, Y. (2012). Involvement of G1-to-S transition and AhAUX-dependent auxin transport in abscisic acid-induced inhibition of lateral root primodia initiation in Arachis hypogaea L. J. Plant Physiol. 169, 1102-1111.
71. Gutierrez, L., Bussel, J. D., Pacurar, D. I., Schwambach, J., Pacurar, M., and Bellini, C. (2009). Phenotipic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell 21, 3119-3132.
72. Gutierrez, L., Mongelard, G., Floková, K., Pacurard, D. I., Novák, O., Staswick, P., et al. (2012). Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell 24, 2515-2527.
73. Hatzilazarou, S. P., Syrosa, T. D., Yupsanis, T. A., Bosabalidis, A. M., and Economou, A. S. (2006). Peroxidases, lignin, and anatomy during in vitro and ex vitro rooting of gardenia (Gardenia jasminoides Ellis) microshoots. J. Plant Physiol. 163, 827-836.
74. Hayashi, K.-I., Neve, J., Hirose, M., Kuboki, A., Shimada, Y., Kepinski, S., et al. (2012). Rational design of an auxin antagonist of the SCF. ACS Chem. Biol. 7, 590-598.
75. Hayashi, K.-I., Tan, X., Zheng, N., Hatate, T., Kimura, Y., Kepinski, S., et al. (2008). Small-molecule agonists and antagonists of F-box protein-substrate interactions in auxin perception and signaling. Proc. Natl. Acad. Sci. U.S.A. 105, 5632-5637.
76. Hertel, R., Thomson, K. S., and Russo, V. E. A. (1972). In-vitro auxin binding to particulate cell fractions from corn coleoptiles. Planta 107, 325-340.
77. Hoad, S. P., and Leakey, R. R. B. (1996). Effects of pre-severance light quality on the vegetative propagation of Eucalyptus grandis W. Hill ex Maiden. Trees 10, 317-324.
78. Huang, Y., Han, C., Peng, W., Peng, Z., Xiong, X., Zhu, Q., et al. (2010). Brassinosteroid negatively regulates jasmonate inhibition of root growth in Arabidopsis. Plant Signal. Behav. 5, 140-142.
79. Hutchison, K. W., Singer, P. B., McInnis, S., Diaz-Sala, C., and Greenwood, M. S. (1999). Expansins are conserved in conifers and expressed in hypocotyls in response to exogenous auxin. Plant Physiol. 120, 827-831.
80. Husen, A. (2008). Stock-plant etiolation causes drifts in total soluble sugars and anthraquinones, and promotes adventitious root formation in teak (Tectona grandis L. f.) coppice shoots. Plant Growth Regul. 54, 13-21.
81. Husen, A., and Pal, M. (2007). Metabolic changes during adventitious root primordium development in Tectona grandis Linn. f. (teak) cuttings as affected by age of donor plants and auxin (IBA and NAA) treatment. New For. 33, 309-323.
82. Inzé, D., and Veylder, L. D. (2006). Cell cycle regulation in plant development. Annu. Rev. Genet. 40, 77-105.
83. Jaleel, C. A., Riadh, K., Gopi, R., Manivannan, I. J., Al-Juburi, H., Zhao, C. X., et al. (2009). Antioxidant defense response: physiological plasticity in higher plants under abiotic constraints. Acta Physiol. Plant. 31, 427-436.
84. Kenney, G., Sudi, J., and Blackman, G. E. (1969). The uptake of growth substances XIII. Differential uptake of indole-3yl-acetic acid through the epidermal and cut surfaces of etiolated stem segments. J. Exp. Bot. 20, 820-840.
85. Kepinski, S., and Leyser, O. (2005). The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446-451.
86. Kerr, I. D., and Bennett, M. J. (2007). New insight into the biochemical mechanisms regulating auxin transport in plants. Biochem. J. 401, 613-622.
87. Kevers, C., Hausman, J. F., Faivre-Rampant, O., Evers, D., and Gaspar, T. (1997). Hormonal control of adventitious rooting: progress and questions. Angew Botanik 71, 71-79.
88. Kibbler, H., Johnston, M. E., and Williams, R. R. (2004). Adventitious rooting formation in cuttings of Backhousia citriodora F. Muell: 1. Plant genotype, juvenility, and characteristics of cuttings. Sci. Hortic. 102, 133-143.
89. Klopotek, Y., Haensch, K. T., Hause, B., Hajirezaei, M. R., and Druege, U. (2010). Dark exposure of petunia cuttings strongly improves adventitious root formation and enhances carbohydrate availability during rooting in the light. J. Plant Phys. 167, 547-554.
90. Koukourikou-Petridou, M. A., and Bangerth, F. (1997). Effect of changing the endogenous concentration of auxins and cytokinins and the production of ethylene in pea stem cuttings on adventitious root formation. Plant Growth Regul. 22, 101-108.
91. Krogan, T., and Berleth, T. (2007). From genes to patterns: auxin distribution and auxin-dependent gene regulation in plant pattern formation. Can. J. Bot. 85, 355-368.
92. Kusano, T., Berberich, B., Tateda, C., and Takahashi, Y. (2008). Polyamines: essential factors for growth and survival. Planta 228, 367-381.
93. Lanteri, L., Pagnussat, G., Laxalt, A. M., and Lamattina, L. (2009). "Nitric oxide is downstream of auxin and is required for inducing adventitious root formation in herbaceous and woody plants" in Adventitious Root Formation of Forest Trees and Horticultural Plants-from Genes to Applications, eds K. Niemi, and C. Scagel (Kerala: Research Signpost), 222-245.
94. Lewis, D. R., Negi, S., Sukumar, P., and Muday, G. K. (2011). Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. Development 138, 3485-3495.
95. +, cGMP, and MAPKs during adventitious rooting in mung bean seedlings. In Vitro Cell. Dev. Biol. Plant 46, 142-148.
96. Li, S. W., Xue, L., Xu, S., Feng, H., and An, L. (2009a). Mediators, genes and signalling in adventitious rooting. Bot. Rev. 75, 230-247.
97. Li, S. W., Xue, L., Xu, S., Feng, H., and An, L. (2009b). Hydrogen peroxide acts as a signal molecule in the adventitious root formation of mung bean seedlings. Environ. Exp. Bot. 65, 63-71.
98. Li, S. W., Xue, L., Xu, S., Feng, H., and An, L. (2009c). IBA-induced changes in antioxidant enzymes during adventitious rooting in mung bean seedlings: the role of H2O2. Environ. Exp. Bot. 66, 442-450.
99. Li, Y. H., Zou, M. H., Feng, B. H., Huang, X., Zhang, Z., and Sun, G. M. (2012). Molecular cloning and characterization of the genes encoding an auxin efflux carrier and the auxin influx carriers associated with the adventitious root formation in mango (Mangifera indica L.) cotyledon segments. Plant Physiol. Biochem. 55, 33-42.
100. Liao, W., Xiao, H., and Zhang, M. (2009). Role and relationship of nitric oxide and hydrogen peroxide in adventitious root development of marigold. Acta Physiol. Plant. 31, 1279-1289.
101. Liao, W., Xiao, H., and Zhang, M. (2010). Effect of nitric oxide and hydrogen peroxide on adventitious root development from cuttings of ground-cover Chrysanthemum and associated biochemical changes. J. Plant Growth Regul. 29, 338-348.
102. Liu, H. J., and Reid, D. M. (1992). Auxin and ethylene-stimulated adventitious rooting in relation to tissue sensitivity to auxin and ethylene production in sunflower hypocotyls. J. Exp. Bot. 43, 1191-1198.
103. Liu, X., Wu, J., Clark, G., Lundy, S., Lim, M., Arnold, D., et al. (2012). Role for apyrases in auxin polar transport in Arabidopsis. Plant Physiol. 160, 1985-1995.
104. Ljung, K., Hull, A. K., Celenza, J., Yamada, M., Estelle, M., Normanly, J., et al. (2005). Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17, 1090-1104.
105. Loach, K. (1988). "Water relations and adventitious rooting" in Adventitious Root Formation in Cuttings, eds T. D. Davies, B. E. Haissig and N. Sankhla (Portland: Dioscorides Press), 102-116.
106. Ludwig-Müller, J., Jülke, S., Bierfreund, N. M., Decker, E. L., and Reski, R. (2009). Moss (Physcomitrella patens) GH3 proteins act in auxin homeostasis. New Phytol. 181, 323-338.
107. Maraschin, F. S., Memelink, J., and Offringa, R. (2009). Auxin-induced, SCF(TIR1)-mediated poly-ubiquitination marks AUX/IAA proteins for degradation. Plant J. 59, 100-109.
108. Marschner, H. (1995). Mineral Nutrition of Higher Plants. San Diego: Academic Press.
109. Meng, Y., Ma, X., Chen, D., Wu, P., and Chen, M. (2010). MicroRNA-mediated signaling involved in plant root development. Biochem. Biophys. Res. Commun. 393, 345-349.
110. Mensuali-Sodi, A., Panizza, M., and Tognoni, F. (1995). Endogenous ethylene requirement for adventitious root induction and growth in tomato cotyledons and lavandin microcuttings in vitro. Plant Growth Regul. 17, 205-212.
111. Michniewicz, M., Zago, M. K., Abas, L., Weijers, D., Schweighofer, A., Meskiene, I., et al. (2007). Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130, 1044-1056.
112. Mishra, B. S., Singh, M., Aggrawal, P., and Laxmi, A. (2009). Glucose and auxin signaling interaction in controlling Arabidopsis thaliana seedlings root growth and development. PLoS ONE 4:e4502. doi: 10.1371/journal.pone.0004502
113. Miwa, H., Kinoshita, A., Fukuda, H., and Sawa, S. (2009). Plant meristems: CLAVATA3/ESR-related signaling in the shoot apical meristem and the root apical meristem. J. Plant Res. 122, 31-39.
114. Mockaitis, K., and Estelle, M. (2008). Auxin receptors and plant development: a new signaling paradigm. Annu. Rev. Cell Dev. Biol. 24, 55-80.
115. Moe, R., and Andersen, A. S. (1988). "Stockplant environment and subsequent adventitious rooting, " in Adventitious Root Formation in Cuttings-Advances in Plant Science Series, eds T. D. Davis, B. E. Haissig, and N. Sankhla (Portland: Dioscorides Press), 214-234.
116. Morelli, G., and Ruberti, I. (2002). Light and shade in the photocontrol of Arabidopsis growth. Trends Plant Sci. 7, 399-404.
117. Moubayidin, L., Mambro, R. D., and Sabatini, S. (2009). Cytokinin-auxin crosstalk. Trends Plant Sci. 14, 557-562.
118. Moubayidin, L., Perilli, S., Dello Ioio, R., Mambro, R. D., Costantino, P., and Sabatini, S. (2010). The rate of cell differentiation controls the Arabidopsis root meristem growth phase. Curr. Biol. 20, 1138-1143.
119. Muday, G., and DeLong, A. (2001). Polar auxin transport: controlling where and how much. Trends Plant Sci. 6, 535-542.
120. Naija, S., Elloumi, N., Jbir, N., Ammar, S., and Kevers, C. (2008). Anatomical and biochemical changes during adventitious rooting of apple rootstocks MM 106 cultured in vitro. C. R. Biol. 331, 518-525.
121. Navarro, L., Dunoyer, P., Jay, F., Arnold, B., Dharmasiri, N., Estelle, M., et al. (2006). A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436-439.
122. Negi, S., Sukumar, P., Liu, X., Cohen, J. D., and Muday, G. K. (2010). Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. Plant J. 61, 3-15.
123. Negishi, N., Oishi, M., and Kawaoka, A. (2011). Chemical screening for promotion of adventitious root formation in Eucalyptus globulus. BMC Proc. 5(Suppl. 7):P139. doi: 10.1186/1753-6561-5-S7-P139
124. Neil, S. J., Desikanm, R., and Hancock, J. T. (2002). Hydrogen peroxide signaling. Curr. Opin. Plant Biol. 5, 388-395.
125. Neves, C., Santos, H., Vilas-Boas, L., and Amâncio, S. (2002). Involvement of free and conjugated polyamines and free amino acids in the adventitious rooting of micropropagated cork oak and grapevine shoots. Plant Physiol. Biochem. 40, 1071-1080.
126. Nicolás, J. I. L., Acosta, M., and Sánchez-Bravo, J. (2004). Role of basipetal auxin transport and lateral auxin movement in rooting and growth of etiolated lupin hypocotyls. Physiol. Plant. 121, 294-304.
127. Nordström, A. C., and Eliasson, L. (1991). Levels of endogenous indole-3-acetic acid and indole-3-acetylaspartic acid during adventitious root formation in pea cuttings. Physiol. Plant. 82, 599-605.
128. Nordström, A. C., Jacobs, F. A., and Eliasson, L. (1991). Effect of exogenous indole-3-acetic acid and indole-3-butyric acid on internal levels of the respective auxins and their conjugation with aspartic acid during adventitious root formation in pea cuttings. Plant Physiol. 96, 856-861.
129. Oliveros-Valenzuela, M., Reyes, D., Sánchez-Bravo, J., Acosta, M., and Nicolás, C. (2008). Isolation and characterization of a cDNA clone encoding an auxin influx carrier in carnation cuttings. Expression in different organs and cultivars and its relationship with cold storage. Plant Physiol. Biochem. 46, 1071-1076.
130. Ortega-Martínez, O., Pernas, M., Carol, R. J., and Dolan, L. (2007). Ethylene modulates stem cell division in the Arabidopsis thaliana root. Science 317, 507-510.
131. Osmont, K. S., Sibout, R., and Hardtke, C. S. (2007). Hidden branches: developments in root system architecture. Annu. Rev. Plant. Biol. 58, 93-113.
132. Osterc, G. (2009). "A change in perspective: Stockplant qualities that influence adventitious root formation in woody species, " in Adventitious Root Formation of Forest Trees and Horticultural Plants-from Genes to Applications, eds K. Niemi and C. Scagel (Kerala: Research Signpost), 175-186.
133. Osterc, G., and Spethmann, W. (2001). Studies on auxin uptake in Prunus and Malus green cuttings. Propag. Ornam. Plants 1, 3-9.
134. Osterc, G., and Stampar, F. (2011). Differences in endo/exogenous auxin profile in cuttings of different physiological ages. J. Plant Physiol. 168, 2088-2092.
135. Osterc, G., Stefancic, M., and Stampar, F. (2009). Juvenile stockplant material enhances root development through higher endogenous auxin level. Acta Physiol. Plant. 31, 899-903.
136. Overvoorde, P., Fukaki, H., and Beeckman, T. (2010). Auxin control of root development. Cold Spring Harb. Perspect. Biol. 2, a001537.
137. Parry, G., Calderon-Villalobos, L. I., Prigge, M., Peret, B., Dharmasiri, S., Itoh, H., et al. (2009). Complex regulation of the TIR1/AFB family of auxin receptors. Proc. Natl. Acad. Sci. U.S.A. 106, 22540-22545.
138. Peer, W. A., and Murphy, A. S. (2007). Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci. 12, 556-563.
139. Petricka, J., Winter, C. M., and Benfey, P. N. (2012). Control of Arabidopsis root development. Annu. Rev. Plant Biol. 63, 563-950.
140. Pop, T. I., Pamfil D., and Bellini C. (2011). Auxin control in the formation of adventitious rooting. Not. Bot. Hort. Agrobot. Cluj. 39, 307-316.
141. Puri, S., and Thompson, F. B. (2003). Relationship of water to adventitious rooting in stem cuttings of Populusspecies. Agrofor. Syst. 58, 1-9.
142. Ramírez-Carvajal, G. A., Morse, A. M., Dervinis, C., and Davos, J. M. (2009). The cytokinin type-B response regulator is a negative regulator of adventitious root development in Populus. Plant Physiol. 150, 759-771.
143. Rapaka, V. K., Bessler, B., Schreiner, M., and Druege, U. (2005). Interplay between initial carbohydrate availability, current photosynthesis, and adventitious root formation in Pelargonium cuttings. Plant Sci. 168, 1547-1560.
144. Rashotte, A. M., Poupart, J., Waddell, C. S., and Muday, G. K. (2003). Transport of the two natural auxins, indole-3-butyric acid and indole-3-acetic acid, in Arabidopsis. Plant Physiol. 133, 761-772.
145. Rasmussen, A., Mason, M. G., Cuyper, C. D., Brewer, P. B., Herold, S., Agusti, J., et al. (2012). Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol. 158, 1976-1987.
146. Raven, J. A. (1975). Transport of indole acetic acid in plant cells in relation to pH and eletrical potential gradients, and its significance for polar IAA transport. New Phytol. 74, 163-172.
147. Rein, W. H., Wright, R. D., and Seiler, J. R. (1991). Propagation medium moisture level influences adventitious rooting of woody stem cuttings. J. Am. Soc. Hortic. Sci. 116, 632-636.
148. Rigal, A., Yordanov, Y. S., Perrone, I., Karlberg, A., Tisserant, E., Bellini, C., et al. (2012). The AINTEGUMENTA LIKE1 homeotic transcription factor PtAIL1 controls the formation of adventitious root primordia in poplar. Plant Physiol. 160, 1996-2006.
149. Robert, S., Kleine-Vehn, J., Barbez, E., Sauer, M., Paciorek, T., Baster, P., et al. (2010). ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 143, 111-121.
150. Rolland, F., Baena-Gonzalez, E., and Sheen, J. (2006). Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu. Rev. Plant Biol. 57, 675-709.
151. Rubery, P. H., and Sheldrake, A. R. (1973). Effect of pH and surface charge on cell uptake of auxin. Nat. New Biol. 244, 285-288.
152. Rubio-Somoza, I., and Weigel, D. (2011). MicroRNA networks and developmental plasticity in plants. Trends Plant Sci. 16, 258-264.
153. Ruedell, C. M., De Almeida, M. R., Schwambach, J., Posenato, C., and Fett-Neto, A. G. (2013). Pre and post-severance effects of light quality on carbohydrate dynamics and microcutting adventitious rooting of two Eucalyptus species of contrasting recalcitrance. Plant Growth Regul. 69, 235-245.
154. Sabatini, S., Beis, D., Wolkenfelt, H. T. M., Murfett, J., Guilfoyle, T., Malamy, J., et al. (1999). An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463-472.
155. Sabatini, S., Heidstra, R., Wildwater, M., and Scheres, B. (2003). SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev. 17, 354-358.
156. Sánchez, C., Vielba, J. M., Ferro, E., Covelo, G., Solé, A., Abarca, D., et al. (2007). Two SCARECROW-LIKE genes are induced in response to exogenous auxin in rooting-competent cuttings of distantly related forest species. Tree Physiol. 27, 1459-1470.
157. Santos-Macedo, E., Cardoso, H. C. G., Hernandez, A., Peixe, A. A., Polidoros, A., Ferreira, A., et al. (2009). Physiological responses and gene diversity indicate olive alternative oxidase as a potential source for markers involved in efficient adventitious root induction. Physiol. Plant 137, 532-552.
158. Santos-Macedo, E., Sircar, D., Cardoso, H. G., Peixe, A., and Arnholdt-Schmitt, B. (2012). Involvement of alternative oxidase (AOX) in adventitious rooting of Olea europaea L. microshoots is linked to adaptative phenylpropanoid and lignin metabolism. Plant Cell Rep. 31, 1581-1590.
159. Sarkar, A. K., Luijten, M., Niyashima, S., Lenhard, M., Hashimoto, T., Nakajima, K., et al. (2007). Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446, 811-814.
160. Scherer, G. F. E. (2011). AUXIN-BINDING-PROTEIN1, the second auxin receptor: what is the significance of a two-receptor concept in plant signal transduction? J. Exp. Bot. 62, 3339-3357.
161. Schwambach, J., Fadanelli, C., and Fett-Neto, A. G. (2005). Mineral nutrition and adventitious rooting in microcuttings of Eucalyptus globulus. Tree Physiol. 25, 487-494.
162. Schwambach, J., Ruedell, C. M., De Almeida, M. R., Penchel, R. M., Araújo, E. F., and Fett-Neto, A. G. (2008). Adventitious rooting of Eucalyptus globulus x maidenni mini-cuttings derived from mini-stumps grow in sand bed and intermittent flooding trays: a comparative study. New For. 36, 261-271.
163. Shi, J. H., and Yang, Z. B. (2011). Is ABP1 an auxin receptor yet? Mol. Plant 4, 635-640.
164. Simon, S., and Petrasek, J. (2011). Why plants need more than one type of auxin. Plant Sci. 180, 454-460.
165. Solé, A., Sánchez, C., Vielba, J. M., Valladares, S., Abarca, D., and Díaz-Sala, C. (2008). Characterization and expression of a Pinus radiata putative ortholog to the Arabidopsis SHORT-ROOT gene. Tree Physiol. 28, 1629-1639.
166. Sorin, C., Bussell, J. D., Camus, I., Ljung, K., Kowalkzyc, N., Geiss, G., et al. (2005). Auxin and light control of adventitious rooting in Arabidopsis require ARGONAUTE1. Plant Cell 17, 1343-1359.
167. Stahl, Y., Wink, R. H., Ingram, G. C., and Simon, R. (2009). A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr. Biol. 19, 909-914.
168. Staswick, P. E., Serban, B., Rowe, M., Tiryaki, I., Maldonado, M. T., Maldonado, M. C., et al. (2005). Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17, 616-627.
169. Steffens, B., Wang, J., and Sauter, M. (2006). Interactions between ethylene, gibberellin and abscisic acid regulate emergence and growth rate of adventitious roots in deepwater rice. Planta 223, 604-612.
170. Strader, L. C., and Bartel, B. (2011). Transport and metabolism of the endogenous auxin precursor indole-3-butyric acid. Mol. Plant 4, 477-486.
171. Svenson, S. E., Davies, F. T. Jr., and Duray, S. A. (1995). Gas exchange, water relations, and dry weight partitioning during root initiation and development of Poinsettia cuttings. J. Am. Soc. Hortic. Sci. 120, 454-459.
172. Tan, X., Calderon-Villalobos, L. I. A., Sharon, M., Zheng, C., Robinson, C. V., Estelle, M., et al. (2007). Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446, 640-645.
173. Tao, Y., Ferrer, J.-L., Ljung, K., Pojer, F., Hong, F., Long, J. A., et al. (2008). Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133, 164-176.
174. Terrile, M. C., Paris, R., Calderon-Villalobos, L. I. A., Iglesias, M. J., Lamattina, L., Estelle, M., et al. (2012). Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. Plant J. 70, 492-500.
175. Tian, Q., Uhlir, N. J., and Reed, J. W. (2002). Arabidopsis SHY2/IAA3 inhibits auxin-regulated gene expression. Plant Cell 14, 301-319.
176. Ticconi, C., Luceroa, R. D., Sakhonwaseea, S., Adamson, A. W., Creffb, A., Nussaumeb, L., et al. (2009). ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proc. Natl. Acad. Sci. 106, 14174-14179.
177. Tromas, A., Paponov, I., and Perrot-Rechenmann, C. (2010). AUXIN BINDING PROTEIN 1: functional and evolutionary aspects. Trends Plant Sci. 15, 436-446.
178. Ueda, J., Miyamoto, K., Uheda, E., and Oka, M. (2011). Auxin transport and graviresponse in plants: relevance to ABC proteins. Biol. Sci. Space 25, 69-75.
179. Van den Berg, C., Willemsen, V., Hendriks, G., Weisbeek, P., and Scheres, B. (1997). Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390, 287-289.
180. Vanneste, S., and Friml, J. (2009). Auxin: a trigger for change in plant development. Cell 136, 1005-1016.
181. Veierskov, B. (1988). "Relations between carbohydrates and adventitious root formation" in Adventitious Root Formation in Cuttings. Advances in Plant Science, vol. 2, eds T. D. Davis, B. E. Haissig, and N. Sankhla (Portland: Discorides Press), 70-77.
182. Vidoz, M. L., Loreti, E., Mensuali, A., Alpi, A., and Perata, P. (2010). Hormonal interplay during adventitious root formation in flooded tomato plants. Plant J. 63, 551-562.
183. Vielba, J. M., Díaz-Sala, C., Ferro, E., Rico, S., Lamprecht, M., Abarca, D., et al. (2011). CsSCL1 is differentially regulated upon maturation in chestnut microshoots, and is specifically expressed in rooting-competent cells. Tree Physiol. 31, 1152-1160.
184. Vieten, A., Sauer, M., Brewer, P. B., and Friml, J. (2007). Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci. 12, 160-168.
185. Wildwater, M., Campilho, A., Perez-Perez, J. M., Heidstra, R., Blilou, I., Korthout, H., et al. (2005). The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123, 1337-1349.
186. Wolters, H., and Jürgens, G. (2009). Survival of the flexible: hormonal growth control and adaptation in plant development. Nat. Rev. Genet. 10, 305-317.
187. Woodward, A. W., and Bartel, B. (2005). Auxin: regulation, action, and interaction. Ann. Bot. 95, 707-735.
188. Xu, M., Zhu, L., Shou, H., and Wu, P. (2005). A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol. 46, 1674-1681.
189. Yadav, S., David, A., and Bhatla, S. C. (2010). Nitric oxide modulates specific steps of auxin-induced adventitious rooting in sunflower. Plant Signal. Behav. 5, 1163-1166.
190. Yang, Y., Hammes, U. Z., Taylor, C. G., Schachtman, D. P., and Nielsen, E. (2006). High-affinity auxin transport by the AUX1 influx carrier protein. Curr. Biol. 16, 1123-1127.
191. Zazimalová, E., Murphy, A. S., Yang, H., Klára, H., and Hošek, P. (2010). Auxin transporters-why so many? Cold Spring Harb. Perspect. Biol. 2, a001552.
192. Zerche, S., and Druege, U. (2009). Nitrogen content determines adventitious rooting in Euphorbia pulcherrimaunder adequate light independently of pre-rooting carbohydrate depletion of cuttings. Sci. Hortic. 121, 340-347.