Adventitious roots and lateral roots: Similarities and differences

Annual Review of Plant Biology

Volumn 65, Issue , 2014, Pages 639-666

  Bellini, Catherine ^a,b   Pacurar, Daniel I ^a   Perrone, Irene ^a  

^a Umea Plant Science Center   (Sweden)

^b INSTITUT JEAN PIERRE BOURGIN   (France)

Author keywords

dicotyledons; environment; monocotyledons; phytohormones; roots; vegetative propagation

Indexed keywords

WATER;

CLASSIFICATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; PLANT ROOT; REVIEW;

PLANT ROOTS; WATER;

EID: 84898538675     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-050213-035645     Document Type: Review

References (199)

1. Ahkami AH, Lischewski S, Haensch KT, Porfirova S, Hofmann J, et al. 2009. Molecular physiology of adventitious root formation in Petunia hybrida cuttings: involvement of wound response and primary metabolism. New Phytol. 181:613-25
2. Arikita FN, Azevedo MS, Scotton DC, Pinto MDS, Figueira A, Peres LE. 2013. Novel natural genetic variation controlling the competence to form adventitious roots and shoots from the tomato wild relative Solanum pennellii. Plant Sci. 199-200:121-30
3. Axtell MJ, Bowman JL. 2008. Evolution of plantmicroRNAs and their targets. Trends Plant Sci. 13:343-49
4. Azevedo JL, Araujo WL. 2007. Diversity and applications of endophytic fungi isolated from tropical plants. In Fungi: Multifaceted Microbes, ed. BN Guangui, SK Deshmukh, pp. 189-207. Boca Raton, FL: Anamaya Publ. New Delhi and CRC Press
5. Ballester A, San-José MC, Vidal N, Fernández-Lorenzo JL, Vieitez AM. 1999. Anatomical and biochemical events during in vitro rooting of microcuttings from juvenile and mature phases of chestnut. Ann. Bot. 83:619-29
6. Bao F, Shen J, Brady SR, Muday GK, Asami T, Yang Z. 2004. Brassinosteroids interact with auxin to promote lateral root development in Arabidopsis. Plant Physiol. 134:1624-31
7. Baraldi R, Rossi F, Lercari B. 1988. In vitro shoot development of PrunusGF 655-2: interaction between light and benzyladenine. Physiol. Plant. 74:440-43
8. Baurens FC, Nicolleau J, Legavre T, Verdeil JL, Monteuuis O. 2004. Genomic DNA methylation of juvenile and mature Acacia mangium micropropagated in vitro with reference to leaf morphology as a phase change marker. Tree Physiol. 24:401-7
9. Bayuelo-Jiménez JS, Gallardo-Valdéz M, Pérez-Decelis VA, Magdaleno-Armas L, Ochoa I, Lynch JP. 2011. Genotypic variation for root traits of maize (Zea mays L.) from the Purhepecha Plateau under contrasting phosphorus availability. Field Crops Res. 121:350-62
10. Beeckman T, ed. 2009. Root Development. Annu. Plant Rev. Vol. 37. London:Wiley & Sons
11. Boerjan W, Cervera MT, Delarue M, Beeckman T, Dewitte W, et al. 1995. superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. Plant Cell 7:1405-19
12. Brady SM, Sarkar SF, Bonetta D, McCourt P. 2003. The ABSCISIC ACID INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis. Plant J. 34:67-75
13. Busov V, Meilan R, Pearce DW, Rood SB, Ma C, et al. 2006. Transgenic modification of gai or rgl1 causes dwarfing and alters gibberellins, root growth, and metabolite profiles in Populus. Planta 224:288-99
14. Camehl I, Sherameti I, Venus Y, Bethke G, Varma A, et al. 2010. Ethylene signalling and ethylenetargeted transcription factors are required to balance beneficial and nonbeneficial traits in the symbiosis between the endophytic fungus Piriformospora indica and Arabidopsis thaliana. New Phytol. 185:1062-73
15. Casero PJ, Casimiro I, Lloret PG. 1995. Lateral root initiation by asymmetrical transverse divisions of pericycle cells in four plant species: Raphanus sativus, Helianthus annuus, Zea mays, and Daucus carota. Protoplasma 188:49-58
16. Chen CW, Yang YW, Lur HS, Tsai YG, Chang MC. 2006. A novel function of abscisic acid in the regulation of rice (Oryza sativa L.) root growth and development. Plant Cell Physiol. 47:1-13
17. Chiou TJ, Lin SI. 2011. Signaling network in sensing phosphate availability in plants. Annu. Rev. Plant Biol. 62:185-206
18. Contesto C, Milesi S, Mantelin S, Zancarini A, Desbrosses G, et al. 2010. The auxin-signaling pathway is required for the lateral root response of Arabidopsis to the rhizobacterium Phyllobacterium brassicacearum. Planta 232:1455-70
19. Cooper WC. 1935. Hormones in relation to root formation on stem cuttings. Plant Physiol. 10:789-94
20. Correa-Aragunde N, Graziano M, Chevalier C, Lamattina L. 2006. Nitric oxidemodulates the expression of cell cycle regulatory genes during lateral root formation in tomato. J. Exp. Bot. 57:581-88
21. Correa-Aragunde N, Graziano M, Lamattina L. 2004. Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900-5
22. Costigan SE, Warnasooriya SN, Humphries BA, Montgomery BL. 2011. Root-localized phytochrome chromophore synthesis is required for photoregulation of root elongation and impacts root sensitivity to jasmonic acid in Arabidopsis. Plant Physiol. 157:1138-50
23. Coudert Y, Perin C, Courtois B, Khong NG, Gantet P. 2010. Genetic control of root development in rice, the model cereal. Trends Plant Sci. 15:219-26
24. da Costa CT, de Almeida MR, Ruedell CM, Schwambach J, Maraschin FS, Fett-Neto AG. 2013. When stress and development go hand in hand: main hormonal controls of adventitious rooting in cuttings. Front. Plant Sci. 4:133
25. da Rocha Correa L, Troleis J, Mastroberti AA, Mariath JE, Fett-Neto AG. 2012. Distinct modes of adventitious rooting in Arabidopsis thaliana. Plant Biol. 14:100-9
26. Dag A, Erel R, Ben-Gal A, Zipori I, Yermiyahu U. 2012. The effect of olive tree stock plant nutritional status on propagation rates. Hort Science 47:307-10
27. Dai X, Wang Y, Yang A, Zhang WH. 2012. OsMYB2P-1, an R2R3MYB transcription factor, is involved in the regulation of phosphate-starvation responses and root architecture in rice. Plant Physiol. 159:169-83
28. Daud N, Faizal A, Geelen D. 2013. Adventitious rooting of Jatropha curcas L. is stimulated by phloroglucinol and by red LED light. In Vitro Cell. Dev. Biol. Plant 49:183-90
29. De Klerk GJ, Van der Krieken W, De Jong JC. 1999. The formation of adventitious roots: new concepts, new possibilities. In Vitro Cell. Dev. Biol. Plant 35:189-99
30. De Smet I, Signora L, Beeckman T, Inzé D, Foyer CH, Zhang H. 2003. An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. Plant J. 33:543-55
31. De Smet I, Vanneste S, InzéD, Beeckman T. 2006. Lateral root initiation or the birth of a newmeristem. Plant Mol. Biol. 60:871-87
32. Devaiah BN, Karthikeyan AS, Raghothama KG. 2007. WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol. 143:1789-801
33. Devaiah BN, Nagarajan VK, Raghothama KG. 2007. Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiol. 145:147-59
34. Díaz-Sala C, Garrido G, 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. 114:601-7
35. Ding Z, Galvan-Ampudia CS, Demarsy E, Langowski L, Kleine-Vehn J, et al. 2011. Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nat. Cell Biol. 13:447-52
36. Druart P, Kevers C, Boxus P, Gaspar T. 1982. In vitro promotion of root-formation by apple shoots through darkness effect on endogenous phenols and peroxidases. Z. Pflanzenphysiol. 108:429-36
37. Druege U, Zerche S, Kadner R. 2004. Nitrogen-and storage-affected carbohydrate partitioning in highlight-adapted Pelargonium cuttings in relation to survival and adventitious root formation under low light. Ann. Bot. 94:831-42
38. Esau K. 1977. Anatomy of Seed Plants. New York:Wiley & Sons
39. Fahn A. 1990. Plant Anatomy. Oxford, UK: Pergamon
40. Fattorini L, Falasca G, Kevers C, Rocca LM, Zadra C, Altamura MM. 2009. Adventitious rooting is enhanced by methyl jasmonate in tobacco thin cell layers. Planta 231:155-68
41. Felten J, Kohler A, Morin E, Bhalerao RP, Palme K, et al. 2009. The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. Plant Physiol. 151:1991-2005
42. Fernandez A, Drozdzecki A, Hoogewijs K, Nguyen A, Beeckman T, et al. 2013. Transcriptional and functional classification of the GOLVEN/ROOT GROWTH FACTOR/CLE-like signaling peptides reveals their role in lateral root and hair formation. Plant Physiol. 161:954-70
43. Fett-Neto AG, Fett JP, Veira Goulart LW, Pasquali G, Termignoni RR, Ferreira AG. 2001. Distinct effects of auxin and light on adventitious root development in Eucalyptus saligna and Eucalyptus globulus. Tree Physiol. 21:457-64
44. Fitz Gerald JN, Lehti-Shiu MD, Ingram PA, Deak KI, Biesiada T, Malamy JE. 2006. Identification of quantitative trait loci that regulate Arabidopsis root system size and plasticity. Genetics 172:485-98
45. Fu X, Harberd NP. 2003. Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740-43
46. Fuernkranz HA, Nowak CA, Maynard CA. 1990. Light effects on in vitro adventitious root formation in axillary shoots of mature Prunus serotina. Physiol. Plant. 80:337-41
47. Galen C, Rabenold JJ, Liscum E. 2007. Functional ecology of a blue light photoreceptor: effects of phototropin-1 on root growth enhance drought tolerance in Arabidopsis thaliana. New Phytol. 173:91-99
48. Geiss G, Gutierrez L, Bellini C. 2009. Adventitious root formation: new insights and perspective. See Ref. 10, pp. 127-56
49. Glick BR, Todorovic B, Czarny J, Cheng ZY, Duan J, McConkey B. 2007. Promotion of plant growth by bacterial ACC deaminase. Crit. Rev. Plant Sci. 26:227-42
50. Gonzalez-Rizzo S, Crespi M, Frugier F. 2006. The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18:2680-93
51. Grattapaglia D, Bertolucci FL, Sederoff RR. 1995. Genetic mapping of QTLs controlling vegetative propagation in Eucalyptus grandis and E. urophylla using pseudo-testcross strategy and RAPD markers. Theor. Appl. Genet. 90:933-47
52. Greenwood MS, Cui X, Xu F. 2001. Response to auxin changes during maturation-related loss of adventitious rooting competence in loblolly pine (Pinus taeda) stem cuttings. Physiol. Plant. 111:373-80
53. Guan JC, Koch KE, Suzuki M, Wu S, Latshaw S, et al. 2012. Diverse roles of strigolactone signaling in maize architecture and the uncoupling of a branching-specific subnetwork. Plant Physiol. 160:1303-17
54. Gutierrez L, Bussell JD, Pacurar DI, Schwambach J, Pacurar M, Bellini C. 2009. Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell 21:3119-32
55. Gutierrez L, Mongelard G, Flokova K, Pacurar DI, Novak O, et al. 2012. Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell 24:2515-27
56. Gutjahr C, Casieri L, Paszkowski U. 2009. Glomus intraradices induces changes in root system architecture of rice independently of common symbiosis signaling. New Phytol. 182:829-37
57. Hammerschlag FA, Bauchan GR, Scorza R. 1987. Factors influencing in vitro multiplication and rooting of peach cultivars. Plant Cell Tissue Organ Cult. 8:235-42
58. Hartmann HT, Kester DE, Davies FT. 1990. Plant Propagation: Principles and Practices. Englewood Cliffs, NJ: Prentice Hall. 5th ed.
59. Hasbún R, Valledor L, Santamariá E, Cañal MJ, Rodríguez R. 2007. Dynamics of DNA methylation in chestnut trees development. Acta Hortic. 760:563-66
60. Hetz W, Hochholdinger F, Schwall M, Feix G. 1996. Isolation and characterisation of rtcs, a maize mutant deficient in the formation of nodal roots. Plant J. 10:845-57
61. Hochholdinger F, Park WJ, Sauer M, Woll K. 2004. From weeds to crops: genetic analysis of root development in cereals. Trends Plant Sci. 9:42-48
62. Hochholdinger F, Woll K, Sauer M, Dembinsky D. 2004. Genetic dissection of root formation in maize (Zea mays) reveals root-type specific developmental programmes. Ann. Bot. 93:359-68
63. Hochholdinger F, Zimmermann R. 2008. Conserved and diverse mechanisms in root development. Curr. Opin. Plant Biol. 11:70-74
64. Hochholdinger F, Zimmermann R. 2009. Molecular and genetic dissection of cereal root system development. See Ref. 10, pp. 175-91
65. Hu B, Zhu CG, Li F, Tang JY, Wang YQ, et al. 2011. LEAF TIP NECROSIS1 plays a pivotal role in the regulation of multiple phosphate starvation responses in rice. Plant Physiol. 156:1101-15
66. Huang LC, Hsiao LJ, Pu SY, Kuo CI, Huang BL, et al. 2012. DNA methylation and genome rearrangement characteristics of phase change in cultured shoots of Sequoia sempervirens. Physiol. Plant. 145:360-68
67. Huang LC, Lius S, Huang BL, Murashige T, Mahdi EFM, Van Gundy R. 1992. Rejuvenation of Sequoia sempervirens by repeated grafting of shoot tips onto juvenile rootstocks in vitro: model for phase reversal of trees. Plant Physiol. 98:166-73
68. Ikeda H, Kamoshita A, Manabe T. 2007. Genetic analysis of rooting ability of transplanted rice (Oryza sativa L.) under different water conditions. J. Exp. Bot. 58:309-18
69. Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Shibata Y, Gomi K, et al. 2005. Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling. Plant Cell 17:1387-96
70. Jansen L, Hollunder J, Roberts I, Forestan C, Fonteyne P, et al. 2013. Comparative transcriptomics as a tool for the identification of root branching genes in maize. Plant Biotechnol. J. 11:1092-1102
71. Jarvis BC, Shaheed AI. 1987. Adventitious root formation in relation to irradiance and auxin supply. Biol. Plant. 29:321-33
72. Jásik J, De Klerk GJ. 1997. Anatomical and ultrastructural examination of adventitious root formation in stem slices of apple. Biol. Plant. 39:79-90
73. Jung JK, McCouch S. 2013. Getting to the roots of it: genetic and hormonal control of root architecture. Front. Plant Sci. 4:186
74. Kaneko M, Itoh H, Inukai Y, Sakamoto T, Ueguchi-Tanaka M, et al. 2003. Where do gibberellin biosynthesis and gibberellin signaling occur in rice plants? Plant J. 35:104-15
75. King JJ, Stimart DP. 1998. Genetic analysis of variation for auxin-induced adventitious root formation among eighteen ecotypes of Arabidopsis thaliana L. Heynh. J. Hered. 89:481-87
76. Klopotek Y, Haensch KT, Hause B, Hajirezaei MR, Druege U. 2010. Dark exposure of petunia cuttings strongly improves adventitious root formation and enhances carbohydrate availability during rooting in the light. J. Plant Physiol. 167:547-54
77. Kohlen W, Charnikhova T, Lammers M, Pollina T, Toth P, et al. 2012. The tomato CAROTENOID CLEAVAGE DIOXYGENASE8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytol. 196:535-47
78. Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K, et al. 2010. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell 18:927-37
79. Kurepin L, Haslam T, Lopez-Villalobos A, Oinam G, Yeung E. 2011. Adventitious root formation in ornamental plants: II. The role of plant growth regulators. Propag. Ornam. Plants 11:161-71
80. Kuroha T, Sakakibara H. 2007. Involvement of cytokinins in adventitious and lateral root formation. Plant Root 1:27-33
81. 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. J. Exp. Bot. 57:1341-51
82. Laplaze L, Benkova E, Casimiro I, Maes L, Vanneste S, et al. 2007. Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell 19:3889-900
83. Lavenus J, Goh T, Roberts I, Guyomarc'h S, Lucas M, et al. 2013. Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci. 18:450-58
84. Li ZX, Xu CZ, Li KP, Yan S, Qu X, Zhang JR. 2012. Phosphate starvation of maize inhibits lateral root formation and alters gene expression in the lateral root primordium zone. BMC Plant Biol. 12:89
85. Lo SF, Yang SY, Chen KT, Hsing YI, Zeevaart JA, et al. 2008. A novel class of gibberellin 2-oxidases control semidwarfism, tillering, and root development in rice. Plant Cell 20:2603-18
86. Lombardi-Crestana S, da Silva Azevedo M, e Silva GFF, Pino LE, Appezzato-da-Glória B, et al. 2012. The tomato (Solanum lycopersicum cv. Micro-Tom) natural genetic variation Rg1 and the DELLA mutant procera control the competence necessary to form adventitious roots and shoots. J. Exp. Bot. 63:5689-703
87. Long HH, Schmidt DD, Baldwin IT. 2008. Native bacterial endophytes promote host growth in a species-specificmanner; phytohormone manipulations do not result in common growth responses. PLoS ONE 3:e2702
88. López-Bucio J, Campos-Cuevas JC, Hernández-Calder ón E, Velásquez-Becerra C, Farías-Rodríguez R, et al. 2007. 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. 20:207-17
89. López-Bucio J, Hernández-Abreu E, Sánchez-Calder ón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L. 2002. Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol. 129:244-56
90. Lorbiecke R, Sauter M. 1999. Adventitious root growth and cell-cycle induction in deepwater rice. Plant Physiol. 119:21-30
91. Maillet F, Poinsot V, Andre O, Puech-Pages V, Haouy A, et al. 2011. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58-63
92. Malamy JE. 2005. Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ. 28:67-77
93. Malamy JE, Benfey PN. 1997. Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124:33-44
94. Malamy JE, Ryan KS. 2001. Environmental regulation of lateral root initiation in Arabidopsis. Plant Physiol. 127:899-909
95. Mano Y, Omori F, Muraki M, Takamizo T. 2005. QTL mapping of adventitious root formation under flooding conditions in tropical maize (Zea mays L.) seedlings. Breed. Sci. 55:343-47
96. Mantelin S, Desbrosses G, Larcher M, Tranbarger TJ, Cleyet-Marel JC, Touraine B. 2006. Nitratedependent control of root architecture and N nutrition are altered by a plant growth-promoting Phyllobacterium sp. Planta 223:591-603
97. Marques C, Vasquez-Kool J, Carocha V, Ferreira J, O'Malley D, et al. 1999. Genetic dissection of vegetative propagation traits in Eucalyptus tereticornis and E. globulus. Theor. Appl. Genet. 99:936-46
98. McCully M. 1995. How do real roots work? Some new views of root structure. Plant Physiol. 109:1-6
99. Miller CR, Ochoa I, Nielsen KL, Beck D, Lynch JP. 2003. Genetic variation for adventitious rooting in response to low phosphorus availability: potential utility for phosphorus acquisition from stratified soils. Funct. Plant Biol. 30:973-85
100. Monteuuis O, Doulbeau S, Verdeil JL. 2008. DNA methylation in different origin clonal offspring from a mature Sequoiadendron giganteum genotype. Trees 22:779-84
101. Moreno-Risueno MA, Busch W, Benfey PN. 2010. Omics meet networks: using systems approaches to infer regulatory networks in plants. Curr. Opin. Plant Biol. 13:126-31
102. Mori M, Nomura T, Ooka H, Ishizaka M, Yokota T, et al. 2002. Isolation and characterization of a rice dwarf mutant with a defect in brassinosteroid biosynthesis. Plant Physiol. 130:1152-61
103. Mouchel CF, Briggs GC, Hardtke CS. 2004. Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root. Genes Dev. 18:700-14
104. Muday GK, Rahman A, Binder BM. 2012. Auxin and ethylene: collaborators or competitors? Trends Plant Sci. 17:181-95
105. Muños S, Cazettes C, Fizames C, Gaymard F, Tillard P, et al. 2004. Transcript profiling in the chl1-5 mutant of Arabidopsis reveals a role of the nitrate transporter NRT1.1 in the regulation of another nitrate transporter, NRT2.1. Plant Cell 16:2433-47
106. Murphy E, Smith S, De Smet I. 2012. Small signaling peptides in Arabidopsis development: how cells communicate over a short distance. Plant Cell 24:3198-217
107. Mussig C, Shin GH, Altmann T. 2003. Brassinosteroids promote root growth in Arabidopsis. Plant Physiol. 133:1261-71
108. Myburg AA, Grattapaglia D, Tuskan GA, Schmutz J, Mizrachi E, et al. 2011. The Eucalyptus grandis Genome Project: genome and transcriptome resources for comparative analysis of woody plant biology. BMC Proc. 5:I20
109. Naija S, Elloumi N, Ammar S, Kevers C, Dommes J. 2008. Involvement of polyamines in the adventitious rooting ofmicropropagated shoots of the apple rootstock MM106. In Vitro Cell. Dev. Biol. Plant 45:83-91
110. Naija S, Elloumi N, Jbir N, Ammar S, Kevers C. 2008. Anatomical and biochemical changes during adventitious rooting of apple rootstocks MM 106 cultured in vitro. C. R. Biol. 331:518-25
111. Narise T, Kobayashi K, Baba S, Shimojima M, Masuda S, et al. 2010. Involvement of auxin signaling mediated by IAA14 and ARF7/19 inmembrane lipid remodeling during phosphate starvation. Plant Mol. Biol. 72:533-44
112. Negi S, Sukumar P, Liu X, Cohen JD, Muday GK. 2010. Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. Plant J. 61:3-15
113. Nemhauser JL, Mockler TC, Chory J. 2004. Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol. 2:E258
114. Niemi K, Haggman H, Sarjala T. 2002. Effects of exogenous diamines on the interaction between ectomycorrhizal fungi and adventitious root formation in Scots pine in vitro. Tree Physiol. 22:373-81
115. Niemi K, Scagel C, Haggman H. 2004. Application of ectomycorrhizal fungi in vegetative propagation of conifers. Plant Cell Tissue Organ Cult. 78:83-91
116. Niemi K, Vuorinen T, Ernstsen A, Haggman H. 2002. Ectomycorrhizal fungi and exogenous auxins influence root and mycorrhiza formation of Scots pine hypocotyl cuttings in vitro. Tree Physiol. 22:1231-39
117. Niu YF, Chai RS, Jin GL, Wang H, Tang CX, Zhang YS. 2013. Responses of root architecture development to low phosphorus availability: a review. Ann. Bot. 112:391-408
118. Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin YC, et al. 2013. The Norway spruce genome sequence and conifer genome evolution. Nature 497:579-84
119. Ochoa IE, Blair MW, Lynch JP. 2006. QTL analysis of adventitious root formation in common bean under contrasting phosphorus availability. Crop Sci. 46:1609-21
120. Olah B, Briere C, Becard G, Denarie J, Gough C. 2005. Nodfactors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant J. 44:195-207
121. Oldacres AM, Newbury HJ, Puddephat IJ. 2005. QTLs controlling the production of transgenic and adventitious roots in Brassica oleracea following treatment with Agrobacterium rhizogenes. Theor. Appl. Genet. 111:479-88
122. Orfanoudakis M, Wheeler CT, Hooker JE. 2010. Both the arbuscular mycorrhizal fungus Gigaspora rosea and Frankia increase root system branching and reduce root hair frequency in Alnus glutinosa. Mycorrhiza 20:117-26
123. Orman-Ligeza B, Parizot B, Gantet PP, Beeckman T, Bennett MJ, Draye X. 2013. Post-embryonic root organogenesis in cereals: branching out from model plants. Trends Plant Sci. 18:459-67
124. Osmont KS, Sibout R, Hardtke CS. 2007. Hidden branches: developments in root system architecture. Annu. Rev. Plant Biol. 58:93-113
125. Osterc G. 2009. A change in perspective: stock plant qualities that influence adventitious root formation in woody species. In Adventitious Root Formation of Forest Trees and Horticultural Plants-from Genes to Applications, ed. K Niemi, C Scagel, pp. 175-85. Kerala, India: Res. Signpost
126. Pagnussat GC, Lanteri ML, Lamattina L. 2003. Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol. 132:1241-48
127. Pagnussat GC, Lanteri ML, Lombardo MC, 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 Physiol. 135:279-86
128. Paz IC, Santin RC, Guimaraes AM, Rosa OP, Dias AC, et al. 2012. Eucalyptus growth promotion by endophytic Bacillus spp. Genet. Mol. Res. 11:3711-20
129. Peret B, De Rybel B, Casimiro I, Benkova E, Swarup R, et al. 2009. Arabidopsis lateral root development: an emerging story. Trends Plant Sci. 14:399-408
130. Peret B, Svistoonoff S, Laplaze L. 2009. When plants socialize: symbioses and root development. See Ref. 10, pp. 209-38
131. Pérez-Torres CA, López-Bucio J, Cruz-Ramírez A, Ibarra-Laclette E, Dharmasiri S, et al. 2008. Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20:3258-72
132. Petricka JJ, Winter CM, Benfey PN. 2012. Control of Arabidopsis root development. Annu. Rev. Plant Biol. 63:563-90
133. Poethig RS. 1990. Phase change and the regulation of shoot morphogenesis in plants. Science 250:923-30
134. Przemeck GK, Mattsson J, Hardtke CS, Sung ZR, Berleth T. 1996. Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization. Planta 200:229-37
135. Ramírez-Carvajal GA, Morse AM, Dervinis C, Davis JM. 2009. The cytokinin type-B response regulator PtRR13 is a negative regulator of adventitious root development in Populus. Plant Physiol. 150:759-71
136. Rani Debi B, Taketa S, Ichii M. 2005. Cytokinin inhibits lateral root initiation but stimulates lateral root elongation in rice (Oryza sativa). J. Plant Physiol. 162:507-15
137. Rasmussen A, Beveridge CA, Geelen D. 2012. Inhibition of strigolactones promotes adventitious root formation. Plant Signal. Behav. 7:694-97
138. Rasmussen A, Depuydt S, Goormachtig S, Geelen D. 2013. Strigolactones fine-tune the root system. Planta 238:615-26
139. Rasmussen A, Mason MG, De Cuyper C, Brewer PB, Herold S, et al. 2012. Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol. 158:1976-87
140. Ravnikar M, Vilhar B, Gogala N. 1992. Stimulatory effects of jasmonic acid on potato stem node and protoplast culture. J. Plant Growth Regul. 11:29-33
141. Rebouillat J, Dievart A, Verdeil JL, Escoute J, Giese G, et al. 2009. Molecular genetics of rice root development. Rice 2:15-34
142. Remans T, Nacry P, Pervent M, Girin T, Tillard P, et al. 2006. A central role for the nitrate transporter NRT2.1 in the integrated morphological and physiological responses of the root system to nitrogen limitation in Arabidopsis. Plant Physiol. 140:909-21
143. Reymond M, Svistoonoff S, Loudet O, Nussaume L, Desnos T. 2006. Identification of QTL controlling root growth response to phosphate starvation in Arabidopsis thaliana. Plant Cell Environ. 29:115-25
144. Ricci A, Carra A, Torelli A, Maggiali CA, Morini G, Branca C. 2001. Cytokininlike activity of N, N′-diphenylureas. N, N′-bis-(2,3- methylenedioxyphenyl)urea and N, N′-bis-(3,4-methylenedioxyphenyl)urea enhance adventitious root formation in apple rootstock M26 (Malus pumila Mill.). Plant Sci. 160:1055-65
145. Ricci A, Rolli E, Dramis L, Díaz-Sala C. 2008. N, N′-bis-(2,3-methylenedioxyphenyl)urea and N, N′-bis-(3,4- methylenedioxyphenyl)urea enhance adventitious rooting in Pinus radiata and affect expression of genes induced during adventitious rooting in the presence of exogenous auxin. Plant Sci. 175:356-63
146. Riefler M, Novak O, Strnad M, Schmulling T. 2006. Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18:40-54
147. Rigal A, Yordanov Y, Perrone I, Karlberg A, Tisserant E, et al. 2012. The AINTEGUMENTA LIKE 1 homeotic transcription factor PtAIL1 controls the formation of adventitious root primordia. Plant Physiol. 160:1996-2006
148. Ronsch H, Adam G, Matschke J, Schachler G. 1993. Influence of (22S,23S)-homobrassinolide on rooting capacity and survival of adult Norway spruce cuttings. Tree Physiol. 12:71-80
149. Rouached H, Arpat AB, Poirier Y. 2010. Regulation of phosphate starvation responses in plants: signaling players and cross-talks. Mol. Plant 3:288-99
150. Sassi M, Lu Y, Zhang Y, Wang J, Dhonukshe P, et al. 2012. COP1 mediates the coordination of root and shoot growth by light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis. Development 139:3402-12
151. Schlicht M, Ludwig-Müller J, Burbach C, Volkmann D, Baluska F. 2013. Indole-3-butyric acid induces lateral root formation via peroxisome-derived indole-3-acetic acid and nitric oxide. New Phytol. 200:473-82
152. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, et al. 2005. A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37:501-6
153. Schulze J, Temple G, Temple SJ, Beschow H, Vance CP. 2006. Nitrogen fixation by white lupin under phosphorus deficiency. Ann. Bot. 98:731-40
154. Schwambach J, Fadanelli C, Fett-Neto AG. 2005. Mineral nutrition and adventitious rooting in microcuttings of Eucalyptus globulus. Tree Physiol. 25:487-94
155. Scotti-Saintagne C, Bertocchi E, Barreneche T, Kremer A, Plomion C. 2005. Quantitative trait loci mapping for vegetative propagation in pedunculate oak. Ann. For. Sci. 62:369-74
156. Sergeeva LI, Keurentjes JJ, Bentsink L, Vonk J, van der Plas LH, et al. 2006. Vacuolar invertase regulates elongation of Arabidopsis thaliana roots as revealed by QTL and mutant analysis. Proc. Natl. Acad. Sci. USA 103:2994-99
157. Shkolnik-Inbar D, Bar-Zvi D. 2010. ABI4 mediates abscisic acid and cytokinin inhibition of lateral root formation by reducing polar auxin transport in Arabidopsis. Plant Cell 22:3560-73
158. Sibout R, Sukumar P, Hettiarachchi C, Holm M, Muday GK, Hardtke CS. 2006. Opposite root growth phenotypes of hy5 versus hy5 hyh mutants correlate with increased constitutive auxin signaling. PLoS Genet. 2:e202
159. Sorin C, Bussell JD, Camus I, Ljung K, Kowalczyk M, et al. 2005. Auxin and light control of adventitious rooting in Arabidopsis require ARGONAUTE1. Plant Cell 17:1343-59
160. Sozzani R, Cui H, Moreno-Risueno MA, Busch W, Van Norman JM, et al. 2010. Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth. Nature 466:128-32
161. Spaepen S, Vanderleyden J. 2011. Auxin and plant-microbe interactions. Cold Spring Harb. Perspect. Biol. 3:a001438
162. Splivallo R, Fischer U, Gobel C, Feussner I, Karlovsky P. 2009. Truffles regulate plant root morphogenesis via the production of auxin and ethylene. Plant Physiol. 150:2018-29
163. Staswick PE. 2009. The tryptophan conjugates of jasmonic and indole-3-acetic acids are endogenous auxin inhibitors. Plant Physiol. 150:1310-21
164. Steffens B, Wang J, Sauter M. 2006. Interactions between ethylene, gibberellin and abscisic acid regulate emergence and growth rate of adventitious roots in deepwater rice. Planta 223:604-12
165. Stenzel I, Otto M, Delker C, Kirmse N, Schmidt D, et al. 2012. ALLENE OXIDE CYCLASE (AOC) gene family members of Arabidopsis thaliana: tissue-and organ-specific promoter activities and in vivo heteromerization. J. Exp. Bot. 63:6125-38
166. Stepanova AN, Alonso JM. 2009. Ethylene signaling and response: where different regulatory modules meet. Curr. Opin. Plant Biol. 12:548-55
167. Strader LC, Bartel B. 2009. The Arabidopsis PLEIOTROPIC DRUG RESISTANCE8/ABCG36 ATP binding cassette transporter modulates sensitivity to the auxin precursor indole-3-butyric acid. Plant Cell 21:1992-2007
168. Strader LC, Bartel B. 2011. Transport and metabolism of the endogenous auxin precursor indole-3-butyric acid. Mol. Plant 4:477-86
169. Sukumar P, Maloney GS, Muday GK. 2013. Localized induction of the ATP-binding cassette B19 auxin transporter enhances adventitious root formation in Arabidopsis. Plant Physiol. 162:1392-405
170. Sun JH, Cardoza V, Mitchell DM, Bright L, Oldroyd G, Harris JM. 2006. Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation. Plant J. 46:961-70
171. Tang W, Newton RJ. 2005. Polyamines promote root elongation and growth by increasing root cell division in regenerated Virginia pine (Pinus virginiana Mill.) plantlets. Plant Cell Rep. 24:581-89
172. Thibaud MC, Arrighi JF, Bayle V, Chiarenza S, Creff A, et al. 2010. Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. Plant J. 64:775-89
173. Thompson AJ, Thorne ET, Burbridge A, Jackson AC, Sharp RE, Taylor IB. 2004. Complementation of notabilis, an abscisic acid-deficient mutant of tomato: importance of sequence context and utility of partial complementation. Plant Cell Environ. 27:459-71
174. Tian Q, Chen F, Liu J, Zhang F, Mi G. 2008. Inhibition of maize root growth by high nitrate supply is correlated with reduced IAA levels in roots. J. Plant Physiol. 165:942-51
175. Topp CN, Iyer-Pascuzzi AS, Anderson JT, Lee CR, Zurek PR, et al. 2013. 3D phenotyping and quantitative trait locus mapping identify core regions of the rice genome controlling root architecture. Proc. Natl. Acad. Sci. USA 110:E1695-704
176. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, et al. 2006. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596-604
177. Ubeda-Tomas S, Beemster GT, Bennett MJ. 2012. Hormonal regulation of root growth: integrating local activities into global behaviour. Trends Plant Sci. 17:326-31
178. Verstraeten I, Beeckman T, Geelen D. 2013. Adventitious root induction in Arabidopsis thaliana as a model for in vitro root organogenesis. In Plant Organogenesis: Methods and Protocols, ed. I De Smet, pp. 159-75. New York: Springer
179. Vidal N, Arellano G, San-José MC, Vieitez AM, Ballester A. 2003. Developmental stages during the rooting of in-vitro-cultured Quercus robur shoots frommaterial of juvenile andmature origin. Tree Physiol. 23:1247-54
180. Vidoz ML, Loreti E, Mensuali A, Alpi A, Perata P. 2010. Hormonal interplay during adventitious root formation in flooded tomato plants. Plant J. 63:551-62
181. Visser E, Cohen JD, Barendse G, Blom C, Voesenek L. 1996. An ethylene-mediated increase in sensitivity to auxin induces adventitious root formation in flooded Rumex palustris Sm. Plant Physiol. 112:1687-92
182. von Behrens I, Komatsu M, Zhang Y, Berendzen KW, Niu X, et al. 2011. Rootless with undetectablemeristem 1 encodes a monocot-specific AUX/IAA protein that controls embryonic seminal and post-embryonic lateral root initiation in maize. Plant J. 66:341-53
183. Wasternack C, Hause B. 2013. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann. Bot. 111:1021-58
184. Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmulling T. 2003. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15:2532-50
185. Wilcox JR, Farmer RE. 1968. Heritability and C effects in early growth of eastern cottonwood cuttings. Heredity 23:239-45
186. Willmann MR, Poethig RS. 2005. Time to grow up: the temporal role of small RNAs in plants. Curr. Opin. Plant Biol. 8:548-52
187. Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS. 2009. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138:750-59
188. Wu G, Poethig RS. 2006. Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539-47
189. Wynne J, McDonald M. 2002. Adventitious root formation in woody plant tissue: influence of light and indole-3-butyric acid (IBA) on adventitious root induction in Betula pendula. In Vitro Cell. Dev. Biol. Plant 38:210-12
190. Xie X, Yoneyama K, Yoneyama K. 2010. The strigolactone story. Annu. Rev. Phytopathol. 48:93-117
191. COI1ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14:1919-35
192. Yamada M, Sawa S. 2013. The roles of peptide hormones during plant root development. Curr. Opin. Plant Biol. 16:56-61
193. Zerche S, Druege U. 2009. Nitrogen content determines adventitious rooting in Euphorbia pulcherrima under adequate light independently of pre-rooting carbohydrate depletion of cuttings. Sci. Hortic. 121:340-47
194. Zhang B, Tong CF, Yin TM, Zhang XY, Zhuge QQ, et al. 2009. Detection of quantitative trait loci influencing growth trajectories of adventitious roots in Populus using functional mapping. Tree Genet. Genomes 5:539-52
195. Zhang H, Forde BG. 1998. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407-9
196. Zhang H, Jennings A, Barlow PW, Forde BG. 1999. Dual pathways for regulation of root branching by nitrate. Proc. Natl. Acad. Sci. USA 96:6529-34
197. Zhao DY, Tian QY, Li LH, Zhang WH. 2007. Nitric oxide is involved in nitrate-induced inhibition of root elongation in Zea mays. Ann. Bot. 100:497-503
198. Zheng BS, Yang L, Zhang WP, Mao CZ, Wu YR, et al. 2003. Mapping QTLs and candidate genes for rice root traits under differentwater-supply conditions and comparative analysis across three populations. Theor. Appl. Genet. 107:1505-15
199. Zhou J, Jiao F, Wu Z, Li Y, Wang X, et al. 2008. OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiol. 146:1673-86