Abstract
Acca sellowiana (Myrtaceae) is a multipurpose species with edible fruits and ornamental value, native to Uruguay and southern Brazil. Domestication of the species in Uruguay is incipient although in other countries, it is widely cultivated. It is an evergreen out-crossing shrub, pollinated by birds and bees. For this reason, it is necessary to develop vegetative propagation strategies such as stem cuttings to reproduce outstanding genotypes for conservation or breeding programs. Adventitious root (AR) formation in cuttings is regulated by environmental and endogenous factors. Among phytohormones, indole-butyric acid (IBA) is the most widely exogenous auxin used to improve rooting of cuttings. Most studies on AR formation at the molecular level use model species; however, the conservation of these mechanisms in non-model plants has been little studied, consequently the effects of different factors and their interactions in A. sellowiana are not well understood. The identification and expression analysis of genes known to be involved in the regulation of the process is an important step to elucidate the molecular mechanisms that regulate AR differentiation in A. sellowiana cuttings. In this study, we compared two genotypes with contrasting rooting ability, and we identified and characterized three genes that might regulate the onset of AR development in A. sellowiana: AsPIN1, AsTIR1 and AsSHR. Their expression analysis showed that in the difficult-to-root genotype, AsTIR1 increases strongly in response to exogenous IBA, shortly after induction treatment. Relative expression of AsPIN1 and AsSHR also increases 24 h later. The biological significance of this gene expression pattern is discussed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated and analyzed during the current study are available in the GenBank repository at https://www.ncbi.nlm.nih.gov/genbank/, reference number MZ130946-MZ13095.
References
Abarca D, Pizarro A, Hernández I et al (2014) The GRAS gene family in pine: transcript expression patterns associated with the maturation-related decline of competence to form adventitious roots. BMC Plant Biol. https://doi.org/10.1186/s12870-014-0354-8
Aumond ML, de Araujo AT, de Oliveira Junkes CF et al (2017) Events Associated with Early Age-Related Decline in Adventitious Rooting Competence of Eucalyptus globulus Labill. Front Plant Sci 8:1–10. https://doi.org/10.3389/fpls.2017.01734
Bellini C, Pacurar DI, Perrone I (2014) Adventitious roots and lateral roots: similarities and differences. Annu Rev Plant Biol 65:639–666. https://doi.org/10.1146/annurev-arplant-050213-035645
Benedini FJ, Brondani GE, de Almeida LV et al (2015) Vegetative rescue and cloning of Eucalyptus benthamii selected adult trees. New for. https://doi.org/10.1007/s11056-015-9472-x
Bisognin DA, Lencina KH, Kielse P et al (2017) Cuttings of post fire epicormic shoots of Ilex paraguariensis and Cabralea canjerana adult plants. Ciência Rural. https://doi.org/10.1590/0103-8478cr20151287
Bisognin DA, Lencina KH, da Luz LV et al (2018) Adventitious rooting competence and rescue of adult mate plants by cuttings. Rev Árvore 42:1–10. https://doi.org/10.1590/1806-90882018000300012
Blakesley D (1994) Auxin Metabolism and Adventitious Root Initiation. In: Davis TD, Haissig BE (eds) Biology of Adventitious Root Formation. Plenum Press, New York, pp 143–154
Blilou I, Xu J, Wildwater M et al (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44. https://doi.org/10.1038/nature03184
Bontempo P, Mita L, Miceli M et al (2007) Feijoa sellowiana derived natural Flavone exerts anti-cancer action displaying HDAC inhibitory activities. Int J Biochem Cell Biol 39:1902–1914. https://doi.org/10.1016/j.biocel.2007.05.010
Davies PJ (2010) Plant Hormones: Biosynthesis, Signal, Transduction, Action!, Revised 3r. Springer, New York
de Almeida MR, Ruedell CM, Ricachenevsky FK et al (2010) Reference gene selection for quantitative reverse transcription-polymerase chain reaction normalization during in vitro adventitious rooting in Eucalyptus globulus Labill. BMC Mol Biol 11:73. https://doi.org/10.1186/1471-2199-11-73
de Almeida M, de Almeida CV, Graner EM et al (2012) Pre-procambial cells are niches for pluripotent and totipotent stem-like cells for organogenesis and somatic embryogenesis in the peach palm: A histological study. Plant Cell Rep 31:1495–1515. https://doi.org/10.1007/s00299-012-1264-6
de Almeida MR, de Bastiani D, Gaeta ML et al (2015) Comparative transcriptional analysis provides new insights into the molecular basis of adventitious rooting recalcitrance in Eucalyptus. Plant Sci 239:155–165. https://doi.org/10.1016/j.plantsci.2015.07.022
de Almeida MR, Schwambach J, Silveira V et al (2020) Proteomic profiles during adventitious rooting of Eucalyptus species relevant to the cellulose industry. New for 51:213–241. https://doi.org/10.1007/s11056-019-09728-7
De Lucas M, Brady SM (2013) Gene regulatory networks in the Arabidopsis root. Curr Opin Plant Biol 16:50–55. https://doi.org/10.1016/j.pbi.2012.10.007
Della Rovere F, Fattorini L, D’Angeli S et al (2013) Auxin and cytokinin control formation of the quiescent centre in the adventitious root apex of Arabidopsis. Ann Bot 112:1395–1407. https://doi.org/10.1093/aob/mct215
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19(1):11–15
Druege U, Franken P, Hajirezaei MR (2016) Plant Hormone Homeostasis, Signaling, and Function during Adventitious Root Formation in Cuttings. Front Plant Sci 7:381. https://doi.org/10.3389/fpls.2016.00381
Druege U, Hilo A, Pérez-Pérez JM et al (2019) Molecular and physiological control of adventitious rooting in cuttings: phytohormone action meets resource allocation. Ann Bot 123:929–949. https://doi.org/10.1093/aob/mcy234
Fett-Neto AG, De AM, Ruedell C (2011) Expression of auxin carrier genes during adventitious rooting in Eucalyptus globulus. BMC Proc 5:P64. https://doi.org/10.1186/1753-6561-5-S7-P64
Ford Y, Bonham EC, Cameron RWF et al (2001) Adventitious rooting: examining the role of auxin in an easy- and a difficult-to-root plant. Plant Growth Regul 36:149–159
Franzon RC, Antunes LEC, Raseira M (2004) Efeito do AIB e de diferentes tipos de estaca na propagação vegetativa da Goiabeira-serrana (Acca sellowiana Berg). Rev Bras Agrociência 10:515–518
Gonin B, Nguyen, et al (2019) What Makes Adventitious Roots? Plants 8:240. https://doi.org/10.3390/plants8070240
Guan L, Murphy AS, Peer WA et al (2015) Physiological and Molecular Regulation of Adventitious Root Formation. CRC Crit Rev Plant Sci 34:506–521. https://doi.org/10.1080/07352689.2015.1090831
Guerra MP, Cangahuala-Inocente GC, Vesco LLD, et al (2012) Micropropagation Systems of Feijoa (Acca sellowiana (O. Berg) Burret). In: Lambardi M, Ozudogru E, Jain S (eds) Protocols for Micropropagation of Selected Economically Important Horticultural Plants. Methods in Molecular Biology (Methods and Protocols). Humana Press, Totowa, NJ, pp 45–62
Hall TA (1999) BioEdit_ user friendly biological sequence alignment editor. Nucleic Acids Symp Ser 41:95–98
Han H, Zhang S, Sun X (2009) A review on the molecular mechanism of plants rooting modulated by auxin. African J Biotechnol 8:348–353. https://doi.org/10.5897/AJB2009.000-9062
Kelen M, Ozkan G (2003) Relationships between rooting ability and changes of endogenous IAA and ABA during the rooting of hardwood cuttings of some grapevine rootstocks. Eur J Hortic Sci 68:8–13
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2^(-ΔΔCT) method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Lloyd G, McCown B (1980) Commercially feasible micropropagation of Mountain Laurel, Kalmia latifolia, by use of shoot-tip culture. In: Proc. Int. Plant Propagator’s Soc. http://www.pubhort.org/ipps/30/99.htm. Accessed 28 Dec 2015
Ludwig-Müller J (2000) Indole-3-butyric acid in plant growth and development. Plant Growth Regul 32:219–230
Mosbah H, Louati H, Boujbiha MA et al (2018) Phytochemical characterization, antioxidant, antimicrobial and pharmacological activities of Feijoa sellowiana leaves growing in Tunisia. Ind Crops Prod 112:521–531. https://doi.org/10.1016/j.indcrop.2017.12.051
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Negishi N, Oishi M, Kawaoka A (2011) Chemical screening for promotion of adventitious root formation in Eucalyptus globulus. BMC Proc 5:P139. https://doi.org/10.1186/1753-6561-5-S7-P139
Negishi N, Nakahama K, Urata N et al (2014) Hormone level analysis on adventitious root formation in Eucalyptus globulus. New for 45:577–587. https://doi.org/10.1007/s11056-014-9420-1
Niella F, Rocha P, Thalmayr P, Duarte E (2018) Propagación vegetativa de dos frutales nativos de interés para productores de Misiones Argentina. In: III Congresso Paranaense de Agroecologia. Foz do Iguaçu, Brazil
Pacurar DI, Perrone I, Bellini C (2014) Auxin is a central player in the hormone cross-talks that control adventitious rooting. Physiol Plant 151:83–96. https://doi.org/10.1111/ppl.12171
Pierre-Jerome E, Moss BL, Nemhauser JL (2013) Tuning the auxin transcriptional response. J Exp Bot 64:2557–2563. https://doi.org/10.1093/jxb/ert100
Pizarro A, Díaz-Sala C (2019) Cellular dynamics during maturation-related decline of adventitious root formation in forest tree species. Physiol Plant 165:73–80. https://doi.org/10.1111/ppl.12768
Rasmussen A, Hosseini SA, Hajirezaei MR et al (2014) Adventitious rooting declines with the vegetative to reproductive switch and involves a changed auxin homeostasis. J Exp Bot 66:1437–1452. https://doi.org/10.1093/jxb/eru499
Ricci A, Rolli E, Brunoni F et al (2016) 1,3-Di(Benzo[D]Oxazol-5-Yl)Urea Acts As Either Adventitious Rooting Adjuvant or Xylogenesis Enhancer in Carob and Pine Microcuttings Depending on the Presence/Absence of Exogenous Indole-3-Butyric Acid. Plant Cell Tissue Organ Cult 126:411–427. https://doi.org/10.1007/s11240-016-1010-9
Ross S, Speroni G, Souza-Pérez M et al (2021) Stem - cutting anatomy and biochemical responses associated with competence for adventitious root differentiation in Acca sellowiana ( Myrtaceae ). Trees 35:1221–1232. https://doi.org/10.1007/s00468-021-02110-1
Ross S, Pechi E, Speroni G, et al (2017) In vitro rooting of Acca sellowiana microshoots. Acta Hortic https://doi.org/10.17660/ActaHortic.2017.1155.79
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 Biochem 97:11–19. https://doi.org/10.1016/j.plaphy.2015.09.005
Schmittgen TD, Zakrajsek BA (2000) Effect of experimental treatment on housekeeping gene expression: Validation by real-time, quantitative RT-PCR. J Biochem Biophys Methods 46:69–81. https://doi.org/10.1016/S0165-022X(00)00129-9
Shu W, Zhou H, Jiang C et al (2019) The auxin receptor TIR1 homolog (PagFBL 1) regulates adventitious rooting through interactions with Aux/IAA28 in Populus. Plant Biotechnol J 17:338–349. https://doi.org/10.1111/pbi.12980
Stevens ME, Woeste KE, Pijut PM (2018) Localized gene expression changes during adventitious root formation in black walnut (Juglans nigra L.). Tree Physiol. https://doi.org/10.1093/treephys/tpx175
Stuepp CA, de Bitencourt J, Wendling I et al (2016) Indução de brotações epicórmicas por meio de anelamento e decepa em erva-mate. Cienc Florest 26:1009–1022
Teale WD, Paponov I, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859. https://doi.org/10.1038/nrm2020
Tortora F, Notariale R, Maresca V et al (2019) Phenol-Rich Feijoa sellowiana (Pineapple Guava) Extracts Protect Human Red Blood Cells from Mercury-Induced Cellular Toxicity. Antioxidants 8:220. https://doi.org/10.3390/antiox8070220
Vandesompele J, De Preter K, Pattyn I et al (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:34–41. https://doi.org/10.1186/gb-2002-3-7-research0034
Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016. https://doi.org/10.1016/j.cell.2009.03.001
Vielba JM, Varas E, Rico S et al (2016) Auxin-mediated expression of a GH3 gene in relation to ontogenic state in Chestnut. Trees Struct Funct 30:2237–2252. https://doi.org/10.1007/s00468-016-1449-7
Vilasboa J, Da Costa CT, Fett-Neto AG (2018) Rooting of eucalypt cuttings as a problem-solving oriented model in plant biology. Prog Biophys Mol Biol. https://doi.org/10.1016/j.pbiomolbio.2018.12.007
Vuotto ML, Basile A, Moscatiello V et al (2000) Antimicrobial and antioxidant activities of Feijoa sellowiana fruit. Int J Antimicrob Agents 13:197–201. https://doi.org/10.1016/S0924-8579(99)00122-3
Wachsman G, Sparks EE, Benfey PN (2015) Genes and networks regulating root anatomy and architecture. New Phytol 208:26–38. https://doi.org/10.1111/nph.13469
Wendling I, Trueman SJ, Xavier A (2014a) Maturation and related aspects in clonal forestry-Part I: Concepts, regulation and consequences of phase change. New for 45:449–471. https://doi.org/10.1007/s11056-014-9421-0
Wendling I, Trueman SJ, Xavier A (2014b) Maturation and related aspects in clonal forestry-part II: Reinvigoration, rejuvenation and juvenility maintenance. New for 45:473–486. https://doi.org/10.1007/s11056-014-9415-y
Wendling I, Brooks PR, Trueman SJ (2015) Topophysis in Corymbia torelliana x C. citriodora seedlings: adventitious rooting capacity, stem anatomy and auxin and abscisic acid concentrations. New Forests 46:107–120. https://doi.org/10.1007/s11056-014-9451-7
Xuan L, Xu M, Chen C et al (2014) Identification and characterization of three PeSHRs and one PeSCR involved in adventitious root development of Populus. Plant Cell Tissue Organ Cult. https://doi.org/10.1007/s11240-014-0437-0
Acknowledgements
This research was funded by AGENCIA NACIONAL DE INVESTIGACIÓN E INNOVACIÓN; grant number FMV-2-2011-1-6320. Mother plants from the breeding program of Acca sellowiana used in this study were kindly provided by Ing. Agr. (M.Sc.) Danilo Cabrera (Instituto Nacional de Investigación Agropecuaria, Canelones, Uruguay) and Ing. Agr. Beatriz Vignale (Facultad de Agronomía, Salto, Uruguay).
Funding
The research leading to these results received funding from AGENCIA NACIONAL DE INVESTIGACIÓN E INNOVACIÓN under Grand Agreement FMV-2–2011-1–6320.
Author information
Authors and Affiliations
Contributions
Conceptualization: SR and PS; Methodology: SR, SR-D; JPS and GP; Formal analysis and investigation: SR; Writing—original draft preparation: SR; Writing—review and editing: SR, PS and OB; Funding acquisition: SR and PS; Project administration: SR; Supervision: PS.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare they have no financial interests. The authors have no competing interests to declare that are relevant to the content of this article.
Additional information
Communicated by V. P. Singh.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ross, S., Rodríguez-Decuadro, S., Pérez, G. et al. Validation and expression analysis of candidate genes for adventitious rooting, in micro-cuttings of Acca sellowiana (Myrtaceae). Acta Physiol Plant 46, 53 (2024). https://doi.org/10.1007/s11738-024-03682-4
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-024-03682-4