Environmental control of adventitious rooting in Eucalyptus and Populus cuttings

Author

• M. R. De Almeida
• M. AumondJr.
• C. T. Da Costa
• J. Schwambach
• C. M. Ruedell
• L. R. Correa
• A. G. Fett-NetoEmail author

1. 1.
2. 2.
3. 3.

Review

First Online: 

21 April 2017

DOI: 10.1007/s00468-017-1550-6

Cite this article as:

De Almeida, M.R., Aumond, M., Da Costa, C.T. et al. Trees (2017). doi:10.1007/s00468-017-1550-6

Abstract

Key message

Concerted control of irradiance, temperature, water availability, mineral nutrition and beneficial root-associated microorganisms significantly improves adventitious rooting in eucalypts and poplars, essentially by modulating auxin and carbohydrate metabolism.

Abstract

Eucalyptus and Populus are among the most economically relevant tree genera. Clonal propagation allows fast genetic gain obtained using elite genotypes. Adventitious rooting (AR), a complex and multifactorial process, is often the main limiting factor for tree cloning. Herein, practical and basic approaches to optimize clonal propagation of eucalypts and poplars, focusing on the main environmental control factors affecting it, are explored. Auxin homeostasis and function are central to AR. Irradiance quality and quantity, as well as temperature, can effectively modulate auxin availability, transport and activity. The interaction of carbohydrates, irradiance and temperature is also at the core of AR. Root architecture may be effectively modified by different N sources. Several macro and micronutrients impact on central factors of rhizogenesis, including energy metabolism, gene expression and enzymatic activities regulating auxin and other phytohormonal steady-states driving AR. Appropriate mineral nutrition is often determinant for successful AR and survival. Microbial associations with the root system and the rhizosphere, both bacterial and fungal, can have a role in auxin availability to cuttings, as well as improve disease resistance, nutrition and water relations. Significant cost reduction in clonal propagation systems of eucalypt and poplar are attainable with an adequate control of environmental factors, particularly for donor plants. Future studies should extend the molecular and physiological findings of basic research to the commercial propagation systems, and these, by their turn, should be explored to provide further advances in the basic understanding of this crucial developmental process for human economy.

Keywords

Adventitious rooting Clonal propagation Environment Eucalyptus Populus 

Communicated by K. Noguchi.

References

1. Abu-Abied M, Szwerdszarf D, Mordehaev I, Yaniv Y, Levinkron S, Rubinstein M, RiovJ Ophir R, Sadot E (2014) Gene expression profiling in juvenile and mature cuttings of Eucalyptus grandis reveals the importance of microtubule remodeling during adventitious root formation. BMC Genom 15:826. doi:10.1186/1471-2164-15-826CrossRefGoogle Scholar
2. Alcântara GB, Ribas LLF, Higa AR, Ribas KCZ, Koehler HS (2007) Efeito da idade da muda e da estação do ano no enraizamento de miniestacas de Pinus taeda L. Rev Árvore 31:399–404. doi:10.1590/S0100-67622007000300005CrossRefGoogle Scholar
3. Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341. doi:10.1093/jexbot/53.372.1331PubMedCrossRefGoogle Scholar
4. Altamura MM (1996) Root histogenesis in herbaceous and woody explants cultured in vitro. A critical review. Agronomie 16:589–602. doi:10.1051/agro:19961001CrossRefGoogle Scholar
5. Antonopoulou C, Dimassi K, Therios I, Chatzissavvidis C (2004) The influence of radiation quality on in vitro rooting and nutrient concentrations of peach rootstock. Biol Plant 48:549–553. doi:10.1023/B:BIOP.0000047151.26284.5fCrossRefGoogle Scholar
6. Argus RE, Colmer TD, Grierson PF (2015) Early physiological flood tolerance is followed by slow post-flooding root recovery in the dryland riparian tree Eucalyptus camaldulensis subsp. refulgens. Plant Cell Environ 38:1189–1199. doi:10.1111/pce.12473PubMedCrossRefGoogle Scholar
7. Assis T (2011) Hybrids and minicutting: a powerful combination that has revolutionized the Eucalyptus clonal forestry. BMC Proc 5(Suppl. 7):I18. doi:10.1186/1753-6561-5-S7-I18PubMedCentralCrossRefGoogle Scholar
8. Assis TF, Fett-Neto AG, Alfenas AC (2004) Current techniques and prospects for the clonal propagation of hardwoods with emphasis on Eucalyptus. In: Walter C, Carson M (eds) Plantation forest biotechnology for the 21th century. Research SignPost, New Delhi, pp 303–333Google Scholar
9. Azevedo GTOS, De Souza AM, De Azevedo GM, De Cerqueira PHA (2015) Minicutting rooting of eucalyptus with different doses of the hydrophilic polymer incorporated into the substrate. Sci For 43:773–780. doi:10.18671/scifor.v43n108.3CrossRefGoogle Scholar
10. Baltierra CX, Montenegro G, De Garcia E (2004) Ontogeny of in vitro rooting processes in Eucalyptus globulus. In Vitro Cell Dev Biol Plant 40:499–503. doi:10.1079/IVP2004559CrossRefGoogle Scholar
11. Batista AF, Santos GA, Silva LD, Quevedo FF, Assis TF (2015) The use of minitunnels and the effects of seasonality in the clonal propagation of Eucalyptus in a subtropical environment. Austral For 78:65–72. doi:10.1080/00049158.2015.1039162CrossRefGoogle Scholar
12. Bellamine J, Penel C, Greppin H, 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. doi:10.1023/A:1006182801823CrossRefGoogle Scholar
13. Bellini C, Pacurar DI, Perrone I (2014) Adventitious roots and lateral roots: similarities and differences. Annu Rev Plant Biol 65:639–666. doi:10.1146/annurev-arplant-050213-035645PubMedCrossRefGoogle Scholar
14. Bennett IJ, McDavidan DAJ, McComb JA (2003) The influence of ammonium nitrate, pH and indole butyric acid on root induction and survival in soil of micropropagated Eucalyptus globulus. Biol Plant 47:355–360. doi:10.1023/B:BIOP.0000023877.21262.a5CrossRefGoogle Scholar
15. Birnbaum KD (2016) How many ways are there to make a root? Curr Opin Plant Biol 34:61–67. doi:10.1016/j.pbi.2016.10.001PubMedCrossRefGoogle Scholar
16. Blazich FA (1988) Mineral nutrition and adventitious rooting. In: Davis T, Haissig BE, Sankhla N (eds) Adventitious root formation in cuttings, advances in plant sciences series, vol 2. Dioscorides Press, Portland, pp 61–69Google Scholar
17. Brondani GE, Baccarin FJB, Ondas HWW, Stape JL, Gonçalves AN, Almeida M (2012) Low temperature, IBA concentrations and optimal time for AR of Eucalyptus benthamii minicuttings. J For Res Jpn 23:583–592. doi:10.1007/s11676-012-0298-5CrossRefGoogle Scholar
18. Brondani GE, Baccarin FJB, Bergonci T, Gonçalves AN, Almeida M (2014) Miniestaquia de Eucalyptus benthamii: efeito do genótipo, AIB, zinco, boro e coletas de brotações. Cerne 20:147–156. doi:10.1590/S0104-77602014000100018CrossRefGoogle Scholar
19. Buchanan BB, Gruissem W, Jones RL (2015) Biochemistry and molecular biology of plants. Wiley, HobokenGoogle Scholar
20. Castiglione S, Franchin C, Fossati T, Lingua G, Torrigiani P, Biondi S (2007) High zinc concentrations reduce rooting capacity and alter metallothionein gene expression in white poplar (Populus alba L. cv. Villafranca). Chemosphere 67:1117–1126. doi:10.1016/j.chemosphere.2006.11.039PubMedCrossRefGoogle Scholar
21. Correa LR, Fett-Neto AG (2004) Effects of temperature on adventitious root development in microcuttings of Eucalyptus saligna Smith and Eucalyptus globulus Labill. J Therm Biol 29:315–324. doi:10.1016/j.jtherbio.2004.05.006CrossRefGoogle Scholar
22. Correa LR, Paim DC, Schwambach J, Fett-Neto AG (2005) Carbohydrates as regulatory factors on the rooting of Eucalyptus saligna Smith and Eucalyptus globulus Labill. Plant Growth Regul 45:63–73. doi:10.1007/s10725-004-6125-zCrossRefGoogle Scholar
23. Correa LR, Troleis J, Mastroberti AA, Mariath JEA, Fett-Neto AG (2012) Distinct modes of adventitious rooting in Arabidopsis thaliana. Plant Biology 14:100–109. doi:10.1111/j.1438-8677.2011.00468.xGoogle Scholar
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. doi:10.3389/fpls.2013.00133PubMedPubMedCentralCrossRefGoogle Scholar
25. Da Cunha ACMCM, Paiva HN, Leite HG, Barros NF, Leite FP (2009a) Relações entre variáveis climáticas com produção e enraizamento de miniestacas de eucalipto. Revista Árvore 33:195–203. doi:10.1590/S0100-67622009000200001CrossRefGoogle Scholar
26. Da Cunha ACMCM, de Paiva HN, Xavier A, Otoni WC (2009b) Papel da nutrição mineral na formação de raízes adventícias em plantas lenhosas. Pesq Flor Bras 58:35–47. doi:10.4336/2009.pfb.58.35Google Scholar
27. Da Cunha ACMCM, de Paiva HN, de Barros NF, Leite HG, Palha Leite FP (2009c) Influência do estado nutricional de mini cepas no enraizamento de mini estacas de eucalipto. Rev Árvore 33:607–615. doi:10.1590/S0100-67622009000400003CrossRefGoogle Scholar
28. Da Cunha ACMCM, de Paiva HN, de Barros NF, Leite HG, Palha Leite FP (2009d) Relação do estado nutricional de mini cepas com o enraizamento de mini estacas de eucalipto. Rev Bras Ci Solo 33:591–599. doi:10.1590/S0100-06832009000300012Google Scholar
29. De Almeida MR, Bastiani D, Gaeta ML, Mariath JEA, De Costa F, Retallick J, Nolan L, Tai HH, Stromvik MV, Fett-Neto AG (2015) Comparative transcriptional analysis provides new insights into the molecular basis of adventitious rooting recalcitrance in Eucalyptus. Plant Sci 239:155–165. doi:10.1016/j.plantsci.2015.07.022PubMedCrossRefGoogle Scholar
30. Delker C, Van Zanten M, Quint M (2017) Thermosensing enlightened. Trends Plant Sci 22:185–187. doi:10.1016/j.tplants.2017.01.007PubMedCrossRefGoogle Scholar
31. Desrochers A, Thomas BR (2003) A comparison of pre-planting treatments on hardwood cuttings of four hybrid poplar clones. New For 26:17–32. doi:10.1023/A:1024492103150CrossRefGoogle Scholar
32. Díaz K, Valiente C, Martínez M, Castillo M, Sanfuentes E (2009) Root-promoting rhizobacteria in Eucalyptus globulus cuttings. World J Microb Biotechnol 25(5):867–873. doi:10.1007/s11274-009-9961-1CrossRefGoogle Scholar
33. Douglas GB, McIvor IR, Lloyd-West CM (2016) Early root development of field-grown poplar: effects of planting material and genotype. New Zeal J For Sci 46:1. doi:10.1186/s40490-015-0057-4CrossRefGoogle Scholar
34. Druart P (1997) Optimization of culture media for in vitro rooting of Malus domestica Borkh. Cv Compact Spartan. Biologia Plant 39:67–77. doi:10.1023/A:1000309023415CrossRefGoogle Scholar
35. Druege U, Kadner R (2008) Response of post-storage carbohydrate levels in pelargonium cuttings to reduced air temperature during rooting and the relationship with leaf senescence and adventitious root formation. Postharvest Biol Technol 47:126–135. doi:10.1016/j.postharvbio.2007.06.008CrossRefGoogle Scholar
36. FAO (2014) The state of the world’s forest genetic resources. FAO, RomeGoogle Scholar
37. Fege AS, Brown GN (1984) Carbohydrate distribution in dormant Populus shoots and hardwood cuttings. For Sci 30:999–1010Google Scholar
38. Ferreira EVO, Novais RF, Pereira GL, de Barros NF, da Silva IR (2015) Differential behavior of young Eucalyptus clones in response to nitrogen supply. Rev Bras Ci Solo 39:809–820. doi:10.1590/01000683rbcs20140560CrossRefGoogle Scholar
39. Fett-Neto AG, Fett JP, Goulart LW, Pasquali G, Termignoni RR, Ferreira AG (2001) Distinct effects of auxin and light on adventitious root development in Eucalyptus saligna Smith and Eucalyptus globulus Labill. Tree Physiol 21:457–464. doi:10.1093/treephys/21.7.457PubMedCrossRefGoogle Scholar
40. Fleck J, Schwambach J, Almeida ME, Yendo ACA, De Costa F, Gosmann G, Fett-Neto AG (2009) Immunoadjuvant saponin production in seedlings and micropropagated plants of Quillaja brasiliensis. In Vitro Cel Dev Biol Pl 45:715–720. doi:10.1007/s11627-009-9222-xCrossRefGoogle Scholar
41. Fogaça CM, Fett-Neto AG (2005) Role of auxin and its modulators in the adventitious rooting of Eucalyptus species differing in recalcitrance. Plant Growth Regul 45:1–10. doi:10.1007/s10725-004-6547-7CrossRefGoogle Scholar
42. Franco JA, Banõn S, Vicente MJ, Miralles J, Martiínez-Sanchez JJ (2011) Root development in horticultural plants grown under abiotic stress conditions—a review. J Hortic Sci Biotechnol 86:543–556. doi:10.1080/14620316.2011.11512802CrossRefGoogle Scholar
43. Gandini AMM, Grazziotti PH, Rossi MJ, Grazziotti DCFS, Gandini EMM, Silva EB, Ragonezi C (2015) Growth and nutrition of eucalypt rooted cuttings promoted by ectomycorrhizal fungi in commercial nurseries. R Bras Ci Solo 39:1554–1565. doi:10.1590/01000683rbcs20150075CrossRefGoogle Scholar
44. Garssen AG, Verhoeven JTA, Soons MB (2014) Effects of climate-induced increases in summer drought on riparian plant species: a meta-analysis. Freshw Biol 59:1052–1063. doi:10.1111/fwb.12328PubMedPubMedCentralCrossRefGoogle Scholar
45. Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12:259–266. doi:10.1016/j.pbi.2009.05.006PubMedCrossRefGoogle Scholar
46. Hartmann HT, Kester DE, Davies FT, Geneve RL (2002) Plant propagation: principles and practices, 7th edn. Prentice Hall, Englewood CliffsGoogle Scholar
47. Hoad SP, Leakey RRB (1996) Effects of pre-severance light quality on the vegetative propagation of Eucalyptus grandis W. Hill ex Maiden—cutting morphology, gas exchange and carbohydrate status during rooting. Trees Struct Funct 10:317–324. doi:10.1007/BF02340778Google Scholar
48. Hoffman AP, Adams JP, Nelson A (2016) Effects of light regime and IBA concentration on AR of an eastern cottonwood (Populus deltoides) clone. In: Schweitzer CJ, Clatterbuck WK, Oswalt CM (eds) Proceedings of the 18th biennial southern silvicultural research conference, e–Gen. Tech. Rep. SRS–212. US Department of Agriculture, Forest Service, Southern Research Station, Asheville, pp 478–485
49. Kim J-M, Sasaki T, Ueda M, Sako K, Seki M (2015) Chromatin changes in response to drought, salinity, heat and cold stresses in plants. Front Plant Sci 6:114. doi:10.3389/fpls.2015.00114PubMedPubMedCentralGoogle Scholar
50. Kristiansen K, Bredmose N, Nielsen B (2005) Influence of propagation temperature, photosynthetic photon flux density, auxin treatment and cutting position on root formation, axillary bud growth and shoot development in Schlumbergera ‘Russian Dancer’. J Hortic Sci Biotechnol 80:297–302. doi:10.1080/14620316.2005.11511933CrossRefGoogle Scholar
51. Lee H-J, Ha J-H, Kim S-G, Choi HK, Kim Z-H, Han Y-J, Kim J-II, Oh Y, Fragoso V, Shin K, Hyeon T, Choi H-G, Oh K-H, Baldwin IT, Park C-M (2016) Stem-piped light activates phytochrome B to trigger light responses in Arabidopsis thaliana roots. Sci Signal 9:106. doi:10.1126/scisignal.aaf6530CrossRefGoogle Scholar
52. Li J, Yu B, Zhao C, Nowak RS, Zhao Z, Sheng Y, Li J (2012) Physiological and morphological responses of Tamarix ramosissima and Populus euphratica to altered groundwater availability. Tree Physiol 33:57–68. doi:10.1093/treephys/tps120PubMedCrossRefGoogle Scholar
53. Ma X, Zhang C, Zhang B, Yang C, Li S (2016) Identification of genes regulated by histone acetylation during root development in Populus trichocarpa. BMC Genom 17:96. doi:10.1186/s12864-016-2407-xCrossRefGoogle Scholar
54. Maathuis FJM (2009) Physiological functions of mineral macronutrients. Curr Opin Plant Biol 12:250–258. doi:10.1016/j.pbi.2009.04.003PubMedCrossRefGoogle Scholar
55. Mafia RG, Alfenas AC, Ferreira EM, Binoti DH, Mafia GM, Mounteer AH (2009) Root colonization and interaction among growth promoting rhizobacteria isolates and eucalypts species. Rev Árvore 33(1):1–9. doi:10.1590/S0100-67622009000100001CrossRefGoogle Scholar
56. Mateja S, Dominik V, Franci S, Gregor O (2007) The effects of a fogging system on the physiological status and rooting capacity of leafy cuttings of woody species. Trees Struct Funct 21:491–496. doi:10.1007/s00468-006-0121-zCrossRefGoogle Scholar
57. Mauriat M, Petterle A, Bellini C, Moritz T (2014) Gibberellins inhibit AR in hybrid aspen and Arabidopsis by affecting auxin transport. Plant J 78:372–384. doi:10.1111/tpj.12478PubMedCrossRefGoogle Scholar
58. Melo LA, Xavier A, Takahashi EK, Rosado AM, Paiva HN (2011) Effectiveness of ascorbic acid and PVP in the rooting of clonal mini-cuttings of Eucalyptus urophylla × Eucalyptus grandis. Cerne 17:499–507. doi:10.1590/S0104-77602011000400008CrossRefGoogle Scholar
59. Mengel K, Kirkby EA (2001) Principles of plant nutrition, 5th edn. Kluwer Academic Publishers, DordrechtCrossRefGoogle Scholar
60. Miller AJ, Cramer MD (2004) Root nitrogen acquisition and assimilation. Plant Soil 274:1–36. doi:10.1007/s11104-004-0965-1CrossRefGoogle Scholar
61. Morelli G, Ruberti I (2002) Light and shade in the photocontrol of Arabidopsis growth. Trends Plant Sci 7:399–404. doi:10.1016/S1360-1385(02)02314-2PubMedCrossRefGoogle Scholar
62. Müller A, Volmer K, Mishra-Knyrim M, Polle A (2013) Growing poplars for research with and without mycorrhizas. Front Plant Sci 4:332. doi:10.3389/fpls.2013.00332PubMedPubMedCentralGoogle Scholar
63. Nick P (2013) Control of plant height. In: Nick P (ed) Plant microtubules: potential for biotechnology, plant cell monographs, vol 11. Springer, Berlin, pp 1–23CrossRefGoogle Scholar
64. O’Brien JA, Vega A, Bouguyon E, Krouk G, Gojon A, Coruzzi G, Gutierrez RA (2016) Nitrate transport, sensing, and responses in plants. Mol Plant 9:837–856. doi:10.1016/j.molp.2016.05.004PubMedCrossRefGoogle Scholar
65. Oberschelp GPJ, Gonçalves AN (2016) Assessing the effects of basal media on the in vitro propagation and nutritional status of Eucalyptus dunnii Maiden. In Vitro Cell Dev Biol Plant 52:28–37. doi:10.1007/s11627-015-9740-7CrossRefGoogle Scholar
66. Osmond KS, Sibout R, Hardtke CS (2007) Hidden branches: developments in root system architecture. Ann Rev Plant Biol 58:93–113. doi:10.1146/annurev.arplant.58.032806.104006CrossRefGoogle Scholar
67. Park Y-S, Bonga JM, Moon H-K (2016) Vegetative propagation of forest trees, National Institute of Forest Science. http://www.iufro.org/science/divisions/division-2/20000/20900/20902/publications/. Accessed 5 Jan 2017
68. Pastur GM, Arena M, Hernandez L, Curvetto N, Eliasco E (2010) Histological events during in vitro rooting of Nothofagus nervosa (Fagaceae). N Z J Bot 43:61–70. doi:10.1080/0028825X.2005.9512944CrossRefGoogle Scholar
69. Paz IC, Santin RC, Guimarães AM, Rosa OP, Dias AC, Quecine MC, Azevedo JL, Matsumura AT (2012) Eucalyptus growth promotion by endophytic Bacillus spp. Genet Mol Res 11(4):3711–3720. doi:10.4238/2012.August.17.9PubMedCrossRefGoogle Scholar
70. Peer WA, Blakeslee JJ, Yang H, Murphy AS (2011) Seven things we think we know about auxin transport. Mol Plant 4:487–504. doi:10.1093/mp/ssr034PubMedCrossRefGoogle Scholar
71. Peralta KD, Araya T, Valenzuela S, Sossa K, Martínez M, Peña-Cortés H, Sanfuentes E (2012) Production of phytohormones, siderophores and population fluctuation of two root-promoting rhizobacteria in Eucalyptus globulus cuttings. World J Microb Biot 28(5):2003–2014. doi:10.1007/s11274-012-1003-8CrossRefGoogle Scholar
72. Prado DZ, Dionizio RC, Vianello F, Baratella D, Costal SM, Lima GPP (2015) Quercetin and indole 3-butyric acid (IBA) as rooting inducers in Eucalyptus grandis × E. urophylla. Aust J Crop Sci 9:1057–1063Google Scholar
73. Proveniers MCG, Zanten MV (2013) High temperature acclimation through PIF4 signaling. Trends Plant Sci 18:59–64. doi:10.1016/j.tplants.2012.09.002PubMedCrossRefGoogle Scholar
74. Qu CP, Xu ZR, Hu YB, Lu Y, Yang CJ, Sun GY, Liu GJ (2016) RNA-Seq reveals transcriptional level changes of poplar roots in different forms of nitrogen treatments. Front Plant Sci. doi:10.3389/fpls.2016.00051Google Scholar
75. Puri S, Thompson FB (2003) Relationship of water to adventitious rooting in stem cuttings of Populus species. Agrofor Syst 58:1–9. doi:10.1023/A:1025494221846CrossRefGoogle Scholar
76. Ragonezzi C, Klimaszewska K, Castro MR, Lima M, De Oliveira P, Zavattieri MA (2010) Adventitious rooting of conifers: influence of physical and chemical factors. Trees Struct Funct 24:975–992. doi:10.1007/s00468-010-0488-8CrossRefGoogle Scholar
77. Requesens DV, Malone RP, Dix PJ (2014) Expression of a barley peroxidase in transgenic apple (Malus domestica L.) results in altered growth, xylem formation, and tolerance to heat stress. J Plant Sci 9:58–66. doi:10.3923/jps.2014.58.66CrossRefGoogle Scholar
78. Ruedell CM, De Almeida MR, Schwambach J, Posenato C, Fett-Neto AG (2013) Pre and post-severance effects of light quality on carbohydrate dynamics and microcutting AR of two Eucalyptus species of contrasting recalcitrance. Plant Growth Regul 69:235–245. doi:10.1007/s10725-012-9766-3CrossRefGoogle Scholar
79. Ruedell CM, De Almeida MR, Fett-Neto AG (2015) Concerted transcription of auxin and carbohydrate homeostasis-related genes underlies improved adventitious rooting of microcuttings derived from far-red treated Eucalyptus globulus Labill mother plants. Plant Physiol Bioch 97:11–19. doi:10.1016/j.plaphy.2015.09.005CrossRefGoogle Scholar
80. Sauter M (2013) Root responses to flooding. Curr Opin Plant Biol 16:282–286. doi:10.1016/j.pbi.2013.03.013PubMedCrossRefGoogle Scholar
81. Schwambach J, Fadanelli C, Fett-Neto AG (2005) Mineral nutrition and adventitious rooting in microcuttings of Eucalyptus globulus. Tree Physiol 25:487–494. doi:10.1093/treephys/25.4.487PubMedCrossRefGoogle Scholar
82. Schwambach J, Ruedell CM, Almeida MR, Penchel RP, Araújo EF, Fett-Neto AG (2008) AR of Eucalyptus globulus × maidenii mini-cuttings derived from mini-stumps grown in sand bed and intermittent flooding trays: a comparative study. New For 36:261–271. doi:10.1007/s11056-008-9099-2CrossRefGoogle Scholar
83. Schwambach J, Ruedell CM, de Almeida MR, Fett-Neto AG (2015) Nitrogen sources and adventitious root development in Eucalyptus globulus micro cuttings. J Plant Nutr 38:1628–1638. doi:10.1080/01904167.2014.983125CrossRefGoogle Scholar
84. Shibuya T, Tsukuda S, Tokuda A, Shiozaki S, Endo R, Kitaya Y (2013) Effects of warming basal ends of Carolina poplar (Populus × canadensis Moench.) softwood cuttings at controlled low-air-temperature on their root growth and leaf damage after planting. J For Res 18:279–284. doi:10.1007/s10310-012-0343-4CrossRefGoogle Scholar
85. Smith NG, Wareing PF (1972) Rooting of hardwood cuttings in relation to bud dormancy and the auxin content of the excised stems. New Phytol 71:63–80. doi:10.1111/j.1469-8137.1972.tb04811.xCrossRefGoogle Scholar
86. Stape JL, Gonçalves JLM, Gonçalves AN (2001) Relationships between nursery practices and field performance for Eucalyptus plantations in Brazil. New For 22:19–41. doi:10.1023/A:1012271616115CrossRefGoogle Scholar
87. Steffens B, Rasmussen A (2016) The physiology of adventitious roots. Plant Physiol 170:603–617. doi:10.1104/pp.15.01360PubMedCrossRefGoogle Scholar
88. Stenvall N, Haapala T, Aarlahti S, Pulkkinen P (2005) The effect of soil temperature and light on sprouting and rooting of root cuttings of hybrid aspen clones. Can J For Res 35:2671–2678. doi:10.1139/x05-183CrossRefGoogle Scholar
89. Sukumar P, Legue V, Vayssieres A, Martin F, Tuskan GA, Kalluri UC (2013) Involvement of auxin pathways in modulating root architecture during beneficial plant–microorganism interactions. Plant Cell Environ 36(5):909–919. doi:10.1111/pce.12036PubMedCrossRefGoogle Scholar
90. Sung D-Y, Kaplan F, Lee K-J, Guy CL (2003) Acquired tolerance to temperature extremes. Trends Plant Sci 8(4):179–187. doi:10.1016/S1360-1385(03)00047-5PubMedCrossRefGoogle Scholar
91. Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens N, Barac T, Vangronsveld J, van der Lelie D (2009) Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl Environ Microb 75(3):748–757. doi:10.1128/AEM.02239-08CrossRefGoogle Scholar
92. Teixeira DA, Alfenas AC, Mafia RG, Ferreira EM, Siqueira LD, Maffia LA, Mounteer AH (2007) Rhizobacterial promotion of eucalypt rooting and growth. Braz J Microbiol 38(1):118–123. doi:10.1590/S1517-83822007000100025CrossRefGoogle Scholar
93. Trevizam R, Brondani GE, Nery FU, Gonçalves NA, De Almeida M (2011) Caracterização morfológica de calos de Eucalyptus urophylla S. T. Blake sob concentrações de boro e cálcio. Cerne 17:215–222. doi:10.1590/S0104-77602011000200009CrossRefGoogle Scholar
94. Trindade H, Pais MS (1997) In vitro studies on Eucalyptus globulus rooting ability. In Vitro Cell Dev Biol Plant 33:1–5. doi:10.1007/s11627-997-0032-8CrossRefGoogle Scholar
95. Truax B, Gagnon D, Fortier J, Lambert F (2014) Biomass and volume yield in mature hybrid poplar plantations on temperate abandoned farmland. Forests 5:3107–3130. doi:10.3390/f5123107CrossRefGoogle Scholar
96. Trueman SJ, Mcmahon TV, Bristow M (2013a) Production of cuttings in response to stock plant temperature in the subtropical eucalypts, Corymbia citriodora and Eucalyptus dunnii. New For 44:265–279. doi:10.1007/s11056-012-9315-yCrossRefGoogle Scholar
97. Trueman SJ, McMahon TV, Bristow M (2013b) Production of Eucalyptus cloeziana cuttings in response to stock plant temperature. J Trop For Sci 25:60–69. https://www.frim.gov.my/v1/jtfsonline/jtfs/v25n1/60-69.pdf. Accessed 5 Jan 2017
98. Vance ED, Loehle C, Wigley TB, Weatherford P (2014) Scientific basis for sustainable management of Eucalyptus and Populus as short-rotation woody crops in the US. Forests 5:901–918. doi:10.3390/f5050901CrossRefGoogle Scholar
99. Vasconcelos E, Ribeiro HM, Ramos A, Coutinho J (2007) Influence of nitrogen and potassium on Eucalyptus globulus Labill. mother plants. Rev de Ciências Agrárias 30:87–97Google Scholar
100. Wang L, Zhao C, Li Z, Liu Z, Wang J (2015) Root plasticity of Populus euphratica seedlings in response to different water table depths and contrasting sediment types. PLoS One. doi:10.1371/journal.pone.0118691Google Scholar
101. Weaver LM, Herrmann KM (1997) Dynamics of the shikimate pathway in plants. Trends Plant Sci 2:346–351. doi:10.1016/S1360-1385(97)84622-5CrossRefGoogle Scholar
102. Wendling I, Brondani GE, Dutra LF, Hansel FA (2010) Minicutting technique: a new ex vitro method for clonal propagation of sweetgum. New For 39:343–353. doi:10.1007/s11056-009-9175-2CrossRefGoogle Scholar
103. Woodward AJ, Bennett IJ, Pusswonge S (2006) The effect of nitrogen source and concentration, medium pH and buffering on in vitro shoot growth and rooting in Eucalyptus marginata. Sci Hortic Amst 110:208–213. doi:10.1016/j.scienta.2006.07.005CrossRefGoogle Scholar
104. Zalesny RS, Bauer EO, Riemenschneider DE (2004) Use of belowground growing degree days to predict rooting of dormant hardwood cuttings of Populus. Silvae Genet 53:154–160Google Scholar
105. Zalesny RS, Hall RB, Bauer EO, Rienenschneider DE (2005) Soil temperature and precipitation affect the rooting ability of dormant hardwood cuttings of Populus. Silvae Genet 54:47–58Google Scholar
106. Zavattieri MA, Ragonezi C, Klimaszewska K (2016) Adventitious rooting of conifers: influence of biological factors. Trees Struct Funct 4:1–12. doi:10.1007/s00468-010-0488-8Google Scholar
107. Zhao X, Zheng H, Li S, Yang C, Jiang J, Liu G (2014) The rooting of poplar cuttings: a review. New For 45:21–34. doi:10.1007/s11056-013-9389-1CrossRefGoogle Scholar
108. Zhen S, Van Iersel MW (2017) Far-red light is needed for efficient photochemistry and photosynthesis. J Plant Physiol 209:115–122. doi:10.1016/j.jplph.2016.12.004PubMedCrossRefGoogle Scholar

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