Abstract
For perennial woody plants, softwood cutting is an efficient technique for larger scale propagation and adventitious rooting of cuttings is one of the most crucial steps. To evaluate the significance of juvenility on adventitious rooting, rooting rates was compared between softwood cuttings collected from apomictic seedlings (juvenile), in vitro cultured plants (rejuvenated), suckers (juvenile like) and canopy shoots (adult) of reproductively mature trees in Malus xiaojinensis. After pre-treatment with indole-3-butytric acid (IBA) (3,000 mg L−1) + H2O2 (50 mM), rooting rates in cutting from juvenile, juvenile like and rejuvenated donor plants were significantly higher (>90 %) than that from adult trees. The effects of IBA on adventitious rooting were enhanced significantly by exogenous H2O2. After 15 passages of in vitro subculture, the micro-shoots from adult phase explants were rejuvenated successfully, marked by the elevated expression of miR156 in the leaflets of the micro-shoots. But the rooting ability of rejuvenated micro-shoots was recovered delayed at the 18th or 21st passage of subculture. During the process of rejuvenation, the leaf indole-3-acetic acid contents and the expressions of rooting related genes CKI1, ARRO-1, ARF7 and ARF19 increased significantly. In contrary, the leaf abscisic acid contents decreased. A lack of juvenility is the most important limiting factor governing adventitious rooting of softwood cuttings in apple rootstocks.
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References
Al-Salem MM, Karam NS (2001) Auxin, wounding, and propagation medium affect rooting response of stem cuttings of Arbutus andrachne. HortScience 36(5):976–978
Alvarez R, Nissen SJ, Sutter EG (1989) Relationship between indole-3-acetic acid levels in apple (Malus pumila Mill) rootstocks cultured in vitro and adventitious root formation in the presence of indole-3-butyric acid. Plant Physiol 89(2):439–443
Amri E, Lyaruu HVM, Nyomora AS, Kanyeka ZL (2010) Vegetative propagation of African Blackwood (Dalbergia melanoxylon Guill. & Perr.): effects of age of donor plant, IBA treatment and cutting position on rooting ability of stem cuttings. N Forest 39(2):183–194
Anderson DR, Camper ND (1987) Application of the disk method: responses to growth regulators. J Plant Growth Regult 6(1):57–65
Bhardwaj DR, Mishra VK (2005) Vegetative propagation of Ulmus villosa: effects of plant growth regulators, collection time, type of donor and position of shoot on adventitious root formation in stem cuttings. N Forest 29(2):105–116
Bouza L, Jacques M, Sotta B, Miginiac E (1994) Relations between auxin and cytokinin contents and in vitro rooting of tree Peony (Paeonia suffruticosa Andr.). Plant Growth Regul 15(1):69–73
Butler ED, Gallagher TF (2000) Characterization of auxin-induced ARRO-1 expression in the primary root of Malus domestica. J Exp Bot 51(351):1765–1766
Caboni E, Tonelli MG, Lauri P, Iacovacci P, Kevers C, Damiano C, Gaspar T (1997) Biochemical aspects of almond microcuttings related to in vitro rooting ability. Biol Plant 39(1):91–97
Chen SW, Zha XJ, Ma BK, Li ZZ, Yuan XL (1981) A preliminary study on propagation of several fruit trees and rootstocks from hardwood cuttings. J Agric Univ Hebei 4(2):103–116
Chen YH, Chao YY, Hsu YY, Kao CH (2013) Heme oxygenase is involved in H2O2-induced lateral root formation in apocynin-treated rice. Plant Cell Rep 32(2):219–226
Christov C, Koleva A (1995) Stimulation of root initiation in hardwood sweet and sour cherry rootstocks (Prunus mahaleb L.). Bulgar J Plant Physiol 21(1):68–72
Ciccotti AM, Bisognin C, Battocletti I, Salvadori A, Herdemertens M, Jarausch W (2008) Micropropagation of apple proliferation-resistant apomictic Malus sieboldii genotypes. Agron Res 6:445–458
De Klerk GJ, Brugge JT (1992) Factors affecting adventitious root formation in microcuttings of Malus. Agronomie 12:747–755
Delargy JA, Wright CE (1979) Root formation in cuttings of apple in relation to auxin application and to etiolation. N Phytol 82(2):341–347
Dunand C, Crèvecoeur M, Penel C (2007) Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases. N Phytol 174(2):332–341
Ersoy N, Kalyoncu IH, Aydin M, Yilmaz M (2010) Effects of some humidity and IBA hormone dose applications on rooting of M9 apple clonal rootstock softwood top cuttings. Afr J Biotechnol 9(17):2510–2514
Evert DR, Smittle DA (1990) Limb girdling influences rooting, survival, total sugar, and starch of dormant hardwood peach cuttings. HortScience 25(10):1224–1226
Fouret Y, Arnaud Y, Maldiney R, Sotta B, Miginiac E (1986) Relation entre rhizogenese et teneur en auxine et acide abscissique chez trois clones de Sequoia sempervirens (Endl.) issus d’arbres d’age different. C R Aca des Sci Série 3 303(4):135–138
Graves WR (2002) IBA, juvenility, and position on ortets influence propagation of carolina buckthorn from softwood cuttings. J Environ Hortic 20(1):57–61
Greenwood MS (1987) 1. Rejuvenation of forest trees. Plant Growth Regul 6(1–2):1–12
Hartmann HT, Kester DE (1975) Plant propagation: principles and practices. Prentice-Hall, Upper Saddle River
Huang LC, Lius S, Huang BL, Murashige T, Ei Fatih MM, 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(1):166–173
Huang AX, She XP, Cao BH, Ren Y (2011) Distribution of hydrogen peroxide during adventitious roots initiation and development in mung bean hypocotyls cuttings. Plant Growth Regul 64(2):109–118
Huang H, Han SS, Wang Y, Zhang XZ, Han ZH (2012) Variations in leaf morphology and DNA methylation following in vitro culture of Malus xiaojinensis. Plant Cell Tiss Organ Cult 111:153–161
Huijser P, Schmid M (2011) The control of developmental phase transitions in plants. Development 138:4117–4129
Hung KT, Hsu YT, Kao CH (2006) Hydrogen peroxide is involved in methyl jasmonate-induced senescence of rice leaves. Physiol Plant 127(2):293–303
Husen A (2004) Clonal propagation of Dalbergia sissoo Roxb. by softwood nodal cuttings: effects of genotypes, application of IBA and position of cuttings on shoots. Silvae Genet 53(2):50–54
Husen A (2008a) Clonal propagation of Dalbergia sissoo Roxb. and associated metabolic changes during adventitious root primordium development. New Forest 36:13–27
Husen A (2008b) 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
Husen A, Pal M (2003) Effect of serial bud grafting and etiolation on rejuvenation and rooting of mature trees of Tectona grandis Linn. f. Silvae Genet 52:84–88
Husen A, Pal M (2007a) Effect of branch position and auxin treatment on clonal propagation of Tectona grandis Linn. f. N Forest 34:223–233
Husen A, Pal M (2007b) 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. N Forest 33(3):309–323
Karakurt H, Aslantas R, Ozkan G, Guleryuz M (2009) Effects of indol-3-butyric acid (IBA), plant growth promoting rhizobacteria (PGPR) and carbohydrates on rooting of hardwood cutting of MM106 Apple rootstock. Afr J Agric Res 4:60–64
Kataeva NV, Popowich EA (1993) Maturation and rejuvenation of Coriandrum sativum shoot clones during micropropagation. Plant Cell Tiss Organ Cult 34(2):141–148
Kaul K (2008) Variation in rooting behavior of stem cuttings in relation to their origin in Taxus wallichiana Zucc. N Forest 36(3):217–224
Kürkcüoglu S, Degenhardt J, Lensing J, Al-Masri AN, Gau AE (2007) Identification of differentially expressed genes in Malus domestica after application of the non-pathogenic bacterium Pseudomonas fluorescens Bk3 to the phyllosphere. J Exp Bot 58(3):733–741
Label PH, Sotta B, Miginiac E (1989) Endogenous levels of abscisic acid and indole-3-acetic acid during in vitro rooting of wild cherry explants produced by micropropagation. Plant Growth Regul 8(4):325–333
Li SW, Xue LG, Xu SJ, Feng HY, An LZ (2007) Hydrogen peroxide involvement in formation and development of adventitious roots in cucumber. Plant Growth Regul 52(2):173–180
Li SW, Xue LG, Xu SJ, Feng HY, An LZ (2009a) Hydrogen peroxide acts as a signal molecule in the adventitious root formation of mung bean seedlings. Environ Exp Bot 65(1):63–71
Li SW, Xue LG, Xu SJ, Feng HY, An LZ (2009b) IBA-induced changes in antioxidant enzymes during adventitious rooting in mung bean seedlings: the role of H2O2. Environ Exp Bot 66(3):442–450
Li TY, Wang Y, Zhang XZ, Han ZH (2012) Isolation and characterization of ARRO-1 genes from apple rootstocks in response to auxin treatment. Plant Mol Biol Rep 30(6):1408–1414
Liu W, Xu ZH, Luo D, Xue HW (2003) Roles of OsCKI1, a rice casein kinase I, in root development and plant hormone sensitivity. Plant J 36(2):189–202
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15(3):473–497
Noiton D, Vine JH, Mullins MG (1992a) Endogenous indole-3-acetic acid and abscisic acid in apple microcuttings in relation to adventitious root formation. Plant Growth Regul 11(1):63–67
Noiton D, Vine JH, Mullins MG (1992b) Effects of serial subculture in vitro on the endogenous levels of indole-3-acetic acid and abscisic acid and root ability in microcuttings of ‘Jonathan’apple. Plant Growth Regul 11(4):377–383
Nordström AC, Jacobs FA, 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(3):856–886
Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19(1):118–130
Opuni-Frimpong E, Karnosky DF, Storer AJ, Cobbinah JR (2008) Key roles of leaves, stockplant age, and auxin concentration in vegetative propagation of two African mahoganies: khaya anthotheca Welw. and Khaya ivorensis A. Chev N Forest 36(2):115–123
Osterc G, Štampar F (2011) Differences in endo/exogenous auxin profile in cuttings of different physiological ages. J Plant Physiol 168(17):2088–2092
Perrin Y, Doumas P, Lardet L, Carron MP (1997) Endogenous cytokinins as biochemical markers of rubber-tree (Hevea brasiliensis) clone rejuvenation. Plant Cell Tiss Organ Cult 47(3):239–245
Poethig RS (2009) Small RNAs and developmental timing in plants. Curr Opin Genet Dev 19:374–378
Schopfer P, Plachy C, Frahry G (2001) Release of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberellin, and abscisic acid. Plant Physiol 125(4):1591–1602
Sebastiani L, Tognetti R (2004) Growing season and hydrogen peroxide effects on root induction and development in Olea europaea L. (cvs ‘Frantoio’ and ‘Gentile di Larino’) cuttings. Sci Hortic 100(1):75–82
Smolka A, Welander M, Olsson P, Holefors A, Zhu LH (2009) Involvement of the ARRO-1 gene in adventitious root formation in apple. Plant Sci 177(6):710–715
Su GX, Zhang WH, Liu YL (2006) Involvement of hydrogen peroxide generated by polyamine oxidative degradation in the development of lateral roots in soybean. J Integr Plant Biol 48(4):426–432
Swamy SL, Puri S, Singh AK (2002) Effect of auxins (IBA and NAA) and season on rooting of juvenile and mature hardwood cuttings of Robinia pseudoacacia and Grewia optiva. N Forest 23(2):143–157
Takayama S, Misawa M (1980) Differentiation in Lilium bulbscales grown in vitro. Effects of activated charcoal, physiological age of bulbs and sucrose concentration on differentiation and scale leaf formation in vitro. Physiol Plant 48(1):121–125
Tchoundjeu Z, Avana ML, Leakey RRB, Simons AJ, Assah E, Duguma B, Bell JM (2002) Vegetative propagation of Prunus africana: effects of rooting medium, auxin concentrations and leaf area. Agroforest Syst 54(3):183–192
Tworkoski T, Takeda F (2007) Rooting response of shoot cuttings from three peach growth habits. Sci Hortic 115(1):98–100
Üçler AÖ, Parlak S, Yücesan Z (2009) Effects of IBA and cutting dates on the rooting ability of semi-hardwood kiwifruit (Actinidia deliciosa A. Chev.) cuttings. Turk J Agric For 28(3):195–201
Wang JX, Yan XL, Pan RC (2005) Relationship between adventitious root formation and plant hormones. Plant Physiol Comm 41(2):133–142
Wang JW, Park MY, Wang LJ, Koo Y, Chen XY, Weigel D, Poethig RS (2011) MiRNA control of vegetative phase change in trees. Plos Genet 7:e1002012
Wang L, Han DG, Gao C, Wang Y, Zhang XZ, Xu XF, Han ZH (2012) Paternity and ploidy segregation of progenies derived from tetraploid Malus xiaojinensis. Tree Genet Genomes 8:1469–1476
Wilmoth JC, Wang SC, Tiwari SB, Joshi AD, Hagen G, Guilfoyle TJ, Alonso JM, Ecker JR, Reed JW (2005) NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J 43(1):118–130
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 138:750–759
Zha Q, Wang Y, Zhang XZ, Han ZH (2014) Both immanently high active iron contents and increased root ferrous uptake in response to low iron stress contribute to the iron deficiency tolerance in Malus xiaojinensis. Plant Sci 214:47–56
Zhang YG, Chen JH, Han ZH, Xu XF, Li TZ (2005) Comparison of methods for total RNA isolation from Malus Xiaojinensis and cDNA LD-PCR amplification. Biotech Inform 4:50–53
Zhang XZ, Zhao YB, Wang GP, Chang RF, Li CM, Shu HR (2008) Dynamics of endogenous cytokinins during phase change in Malus domestica Borkh. Acta Hort 774:29–33
Zhang XM, Li BJ, Yang F, Yi K (2009) The Research of greenwood cutting propagation of apple rootstock. China Fruits 1:22–25
Zhu LH, Holefors A, Ahlman A, Xue ZT, Welander M (2001) Transformation of the apple rootstock M9/29 with the rolB gene and its influence on rooting and growth. Plant Sci 160:433–439
Acknowledgments
This project was funded by the National Special Funds for Scientific Research on Public Causes (Agriculture) (201203075), the National Natural Science Foundation of China (NSFC) (Grant 31372020), the Modern Agricultural Industry Technology System (Apple) (CARS-28) and the Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Nutrition and Physiology) Ministry of Agriculture, P.R. China.
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Zufei Xiao and Na Ji have contributed equally to this work.
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Xiao, Z., Ji, N., Zhang, X. et al. The lose of juvenility elicits adventitious rooting recalcitrance in apple rootstocks. Plant Cell Tiss Organ Cult 119, 51–63 (2014). https://doi.org/10.1007/s11240-014-0513-5
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DOI: https://doi.org/10.1007/s11240-014-0513-5