Compact shoot architecture of Osteospermum fruticosum transformed with Rhizobium rhizogenes

Adams SR, Pearson S, Hadley P (1998) Inflorescence commitment and subsequent development differ in their responses to temperature and photoperiod in Osteospermum jucundum. Physiol Plant 104:225–231. https://doi.org/10.1034/j.1399-3054.1998.1040210.x Allavena A, Giovannini A, Berio T, et al (2000) Genetic engineering of Osteospermum spp.: a case story. Acta Hortic 129–134. doi: https://doi.org/10.17660/ActaHortic.2000.508.16 Andersen AS, Andersen L (2000) Growth regulation as a necessary prerequisite for introduction of new plants. Acta Hortic 53:183–192. https://doi.org/10.17660/ActaHortic.2000.541.26 Bergstrand KJI (2017) Methods for growth regulation of greenhouse produced ornamental pot- and bedding plants - a current review. Folia Hortic 29:63–74. https://doi.org/10.1515/fhort-2017-0007 Börnke F, Rocksch T (2018) Thigmomorphogenesis – control of plant growth by mechanical stimulation. Sci Hortic (amsterdam) 234:344–353. https://doi.org/10.1016/j.scienta.2018.02.059 Bouchez D, Tourneur J (1991) Organization of the agropine synthesis region of the T-DNA of the Ri plasmid from Agrobacterium rhizogenes. Plasmid 25:27–39. https://doi.org/10.1016/0147-619X(91)90004-G Britton MT, Escobar MA, Dandekar AM (2008) The oncogenes of Agrobacterium tumefaciens and Agrobacterium thizogenes. In: Tzfira T, Citovsky V (eds) Agrobacterium: From Biology to Biotechnology. Springer, New York, New York, pp 523–563 Cameron RWF, Wilkinson S, Davies WJ et al (2004) Regulation of plant growth in container-grown ornamentals through the use of controlled irrigation. Acta Hortic 630:305–312. https://doi.org/10.17660/ActaHortic.2004.630.38 Camilleri C, Jouanin L (1991) The TR-DNA region carrying the auxin synthesis genes of the Agrobacterium rhizogenes agropine-type plasmid pRiA4: nucleotide sequence analysis and introduction into tobacco plants. Mol Plant-Microbe Interact 4:155–162 Casanova E, Zuker A, Trillas MI et al (2003) The rolC gene in carnation exhibits cytokinin- and auxin-like activities. Sci Hortic (amsterdam) 97:321–331. https://doi.org/10.1016/S0304-4238(02)00155-3 Cheng T, Xu C, Lei L et al (2016) Barcoding the kingdom Plantae: new PCR primers for ITS regions of plants with improved universality and specificity. Mol Ecol Resour 16:138–149. https://doi.org/10.1111/1755-0998.12438 Choi PS, Kim YD, Choi KM et al (2004) Plant regeneration from hairy-root cultures transformed by infection with Agrobacterium rhizogenes in Catharanthus roseus. Plant Cell Rep 22:828–831. https://doi.org/10.1007/s00299-004-0765-3 Christensen B, Müller R (2009) The use of Agrobacterium rhizogenes and its rol-genes for quality improvement in ornamentals. Eur J Hortic Sci 74:275–287 Christensen B, Sriskandarajah S, Serek M, Müller R (2008) Transformation of Kalanchoe blossfeldiana with rol-genes is useful in molecular breeding towards compact growth. Plant Cell Rep 27:1485–1495. https://doi.org/10.1007/s00299-008-0575-0 Dadpour MR, Naghiloo S, Gohari G (2011) Inflorescence and floral ontogeny in Osteospermum ecklonis (Asteraceae). Botany 89:605–614. https://doi.org/10.1139/b11-052 Daimon H, Mii M (1995) Plant regeneration and thiophene production in hairy root cultures of Rudbeckia hirta L. used as an antagonistic plant to nematodes. Japanese J Crop Sci 64:650–655. https://doi.org/10.1626/jcs.64.650 Dehio C, Grossmann K, Schell J, Schmülling T (1993) Phenotype and hormonal status of transgenic tobacco plants overexpressing the rolA gene of Agrobacterium rhizogenes T-DNA. Plant Mol Biol 23:1199–1210. https://doi.org/10.1007/BF00042353 Delbarre A, Muller P, Imhoff V et al (1994) The rolB gene of Agrobacterium rhizogenes does not increase the auxin sensitivity of tobacco protoplasts by modifying the intracellular auxin concentration. Plant Physiol 105:563–569. https://doi.org/10.1104/pp.105.2.563 Desmet S, De Keyser E, Van Vaerenbergh J et al (2019) Differential efficiency of wild type rhizogenic strains for rol gene transformation of plants. Appl Microbiol Biotechnol 103:6657–6672. https://doi.org/10.1007/s00253-019-10003-0 Desmet S, Dhooghe E, De Keyser E et al (2020a) Rhizogenic agrobacteria as an innovative tool for plant breeding: current achievements and limitations. Appl Microbiol Biotechnol 104:2435–2451. https://doi.org/10.1007/s00253-020-10403-7 Desmet S, Dhooghe E, De Keyser E et al (2020b) Segregation of rol genes in two generations of Sinningia speciosa engineered through wild type Rhizobium rhizogenes. Front Plant Sci 11:1–18. https://doi.org/10.3389/fpls.2020.00859 Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus (madison) 12:39–40 Faccioli P, Terzi V, Pecchioni N et al (2000) Genetic diversity in cultivated Osteospermum as revealed by random amplified polymorphic DNA analysis. Plant Breed 119:351–355. https://doi.org/10.1046/j.1439-0523.2000.00511.x Fladung M (1990) Transformation of diploid and tetraploid potato clones with the rol C gene of Agrobacterium rhizogenes and characterization of transgenic plants. Plant Breed 104:295–304. https://doi.org/10.1111/j.1439-0523.1990.tb00439.x Folta KM, Childers KS (2008) Light as a growth regulator: controlling plant biology with narrow-bandwidth solid-state lighting systems. HortScience 43:1957–1964. https://doi.org/10.21273/HORTSCI.43.7.1957 Gi F, Reverberi M, Lauri P et al (2000) How Agrobacterium rhizogenes triggers de novo root formation in a recalcitrant woody plant: an integrated histological, ultrastructural and molecular analysis. New Phytol 145:77–93. https://doi.org/10.1046/j.1469-8137.2000.00558.x Gibson JL, Whipker BE (2003) Efficacy of plant growth regulators on the growth of vigorous Osteospermum cultivars. HortTechnology 13:132–135 Giovannini A, Zothni M, Morreale G et al (1999) Ornamental traits modification by rol genes in Osteospermum ecklonis transformed with Agrobacterium tumefaciens. Vitr Cell Dev Biol - Plant 5:70–75. https://doi.org/10.1007/s11627-999-0012-2 Giovannini A, Mascarello C, Pipino L, Nostro A (2008) Agrobacterium rhizogenes - mediated transformation in Mediterranean Helichrysum. Transgenic Plant J 2:54–61 Godo T, Tsujii O, Ishikawa K, Mii M (1997) Fertile transgenic plants of Nierembergia scoparia Sendtner obtained by a mikimopine type strain of Agrobacterium rhizogenes. Sci Hortic (amsterdam) 68:101–111. https://doi.org/10.1016/S0304-4238(96)00964-8 Golds T, Lee J, Husnain T et al (1991) Agrobacterium rhizogenes mediated transformation of the forage legumes Medicago sativa and Onobrychis viciifolia. J Exp Bot 42:1147–1157. https://doi.org/10.1093/jxb/42.9.1147 Haas JH, Moore LW, Ream W, Manulis S (1995) Universal PCR primers for detection of phytopathogenic Agrobacterium strains. Appl Environ Microbiol 61:2879–2884 Hansen CW, Nielsen KL (2001) Reduced phosphorus availability as a method to reduce chemical growth regulation and to improve plant quality. In: Horst W, Schenk M, Bürkert A et al (eds) Plant Nutrition. Springer, Dordrecht, Dordrecht, pp 314–315 Hedden P, Kamiya Y (1997) Gibberellin biosynthesis: enzymes, genes and their regulation. Annu Rev Plant Physiol Plant Mol Biol 48:431–460. https://doi.org/10.1146/annurev.arplant.48.1.431 Heins R, Erwin J (1993) Growth control without chemicals. Minnesota Commer. Flower Grow. Assoc. Bull. 1–6 Hosokawa K, Matsuki R, Oikawa Y, Yamamura S (1997) Genetic transformation of gentian using wild-type Agrobacterium rhizogenes. Plant Cell Tissue Organ Cult 51:137–140. https://doi.org/10.1023/A:1005962913491 Huffman GA, White FF, Gordon MP, Nester EW (1984) Hairy-root-inducing plasmid: physical map and homology to tumor-inducing plasmids. J Bacteriol 157:269–276 Illing HPA (1997) Is working in greenhouses healthy? Evidence concerning the toxic risks that might affect greenhouse workers. Occup Med (chic Ill) 47:281–293. https://doi.org/10.1093/occmed/47.5.281 Kim YS, Kim YK, Xu H et al (2012) Improvement of ornamental characteristics in Rehmannia elata through Agrobacterium rhizogenes-mediated transformation. Plant Omics 5:376–380 Klougart A (1987) Exploration, adaptation, evaluation, amelioration. Acta Hortic. https://doi.org/10.17660/ActaHortic.1987.205.2 Laura M, Consonni R, Locatelli F et al (2010) Metabolic response to cold and freezing of Osteospermum ecklonis overexpressing Osmyb4. Plant Physiol Biochem 48:764–771. https://doi.org/10.1016/j.plaphy.2010.06.003 Lütken H, Clarke JL, Müller R (2012a) Genetic engineering and sustainable production of ornamentals: current status and future directions. Plant Cell Rep 31:1141–1157. https://doi.org/10.1007/s00299-012-1265-5 Lütken H, Jensen EB, Wallström SV et al (2012b) Development and evaluation of a non-gmo breeding technique exemplified by Kalanchoë. Acta Hortic 961:51–58. https://doi.org/10.17660/ActaHortic.2012.961.3 Lütken H, Wallström SV, Jensen EB et al (2012c) Inheritance of rol-genes from Agrobacterium rhizogenes through two generations in Kalanchoë. Euphytica 188:397–407. https://doi.org/10.1007/s10681-012-0701-5 Maurel C, Leblanc N, Barbier-Brygoo H et al (1994) Alterations of auxin perception in rolB-transformed tobacco protoplasts (time course of rolB mRNA expression and increase in auxin sensitivity reveal multiple control by auxin). Plant Physiol 105:1209–1215. https://doi.org/10.1104/pp.105.4.1209 Mishiba KI, Nishihara M, Abe Y et al (2006) Production of dwarf potted gentian using wild-type Agrobacterium rhizogenes. Plant Biotechnol 23:33–38. https://doi.org/10.5511/plantbiotechnology.23.33 Moore L, Warren G, Strobel G (1979) Involvement of a plasmid in the hairy root disease of plants caused by Agrobacterium rhizogenes. Plasmid 2:617–626. https://doi.org/10.1016/0147-619X(79)90059-3 Moritz T, Schmulling T (1998) The gibberellin content of rolA transgenic tobacco plants is specifically altered. J Plant Physiol 153:774–776. https://doi.org/10.1016/S0176-1617(98)80234-4 Mugnier J (1988) Establishment of new axenic hairy root lines by inoculation with Agrobacterium rhizogenes. Plant Cell Rep 7:9–12. https://doi.org/10.1007/BF00272966 Nilsson O, Moritz T, Imbault N et al (1993) Hormonal characterization of transgenic tobacco plants expressing the rolC gene of Agrobacterium rhizogenes TL-DNA. Plant Physiol 102:363–371. https://doi.org/10.1104/pp.102.2.363 Norlindh T (1943) Studies in the Calendulaea I. Monograph of the Genera Dimorphotheca, Castalis, Osteospermum, Gibbaria and Chrysanthemoides. CWK Gleerup, Lund Norlindh T (1978) The Compositae of the flora Zambesiaca, area 10 - Calendulae. Kirkia 11:143–168 Olsen WW, Andersen AS (1995) Growth retardation of Osteospermum ecklonis. Acta Hortic. https://doi.org/10.17660/ActaHortic.1995.397.12 Panda BM, Mehta UJ, Hazra S (2017) Optimizing culture conditions for establishment of hairy root culture of Semecarpus anacardium L. 3 Biotech 7:21. doi: https://doi.org/10.1007/s13205-017-0608-x Pavlova OA, Matveyeva TV, Lutova LA (2014) rol-Genes of Agrobacterium rhizogenes. Russ J Genet Appl Res 4:137–145. https://doi.org/10.1134/S2079059714020063 Pearson S, Parker A, Hadley P, Kitchener HM (1995) The effect of photoperiod and temperature on reproductive development of Cape Daisy (Osteospermum jucundum cv. “Pink Whirls”). Sci Hortic (amsterdam) 62:225–235. https://doi.org/10.1016/0304-4238(95)00792-R Pérez de la Torre MC, Fernández P, Greppi JA et al (2018) Transformation of Mecardonia (Plantaginaceae) with wild-type Agrobacterium rhizogenes efficiently improves compact growth, branching and flower related ornamental traits. Sci Hortic (amsterdam) 234:300–311. https://doi.org/10.1016/j.scienta.2018.02.047 Petersen SG, Stummann BM, Olesen P, Henningsen KW (1989) Structure and function of root-inducing (Ri) plasmids and their relation to tumor-inducing (Ti) plasmids. Physiol Plant 77:427–435. https://doi.org/10.1111/j.1399-3054.1989.tb05664.x Pitzschke A (2013) Agrobacterium infection and plant defense—transformation success hangs by a thread. Front Plant Sci 4:1–12. https://doi.org/10.3389/fpls.2013.00519 Porter JR, Flores H (1991) Host range and implications of plant infection by Agrobacterium rhizogenes. Crit Rev Plant Sci 10:387–421. https://doi.org/10.1080/07352689109382318 Rademacher W (2000) Growth retardants: effects on gibberellin biosynthesis and other metabolic pathways. Annu Rev Plant Physiol Plant Mol Biol 51:501–531. https://doi.org/10.1146/annurev.arplant.51.1.501 Rademacher W (2015) Plant growth regulators: backgrounds and uses in plant production. J Plant Growth Regul 34:845–872. https://doi.org/10.1007/s00344-015-9541-6 Rajapakse NC, Young RE, McMahon MJ, Oi R (1999) Plant height control by photoselective filters: current status and future prospects. HortTechnology 9:618–624. https://doi.org/10.21273/horttech.9.4.618 Saxena G, Banerjee S, Laiq-Ur-Rahman, et al (2007) Rose-scented geranium (Pelargonium sp.) generated by Agrobacterium rhizogenes mediated Ri-insertion for improved essential oil quality. Plant Cell Tissue Organ Cult 90:215–223. https://doi.org/10.1007/s11240-007-9261-0 Schmülling T, Schell J, Spena A (1988) Single genes from Agrobacterium rhizogenes influence plant development. EMBO J 7:2621–2629 Schmülling T, Fladung M, Grossmann K, Schell J (1993) Hormonal content and sensitivity of transgenic tobacco and potato plants expressing single rol genes of Agrobacterium rhizogenes T-DNA. Plant J 3:371–382. https://doi.org/10.1046/j.1365-313X.1993.t01-20-00999.x Sinkar VP, White FF, Gordon MP (1987) Molecular biology of Ri-plasmid—A review. J Biosci 11:47–57. https://doi.org/10.1007/BF02704657 Skała E, Kicel A, Olszewska MA et al (2015) Establishment of hairy root cultures of Rhaponticum carthamoides (Willd.) Iljin for the production of biomass and caffeic acid derivatives. Biomed Res Int 2015:1–11. https://doi.org/10.1155/2015/181098 Suzuki A, Metzger JD (2001) Vernalization in a greenhouse promotes and synchronizes flowering of Osteospermum ecklonis Norl. HortScience 36:658–660. https://doi.org/10.21273/hortsci.36.4.658 Tao R, Handa T, Tamura M, Sugiura A (1994) Genetic transformation of Japanese persimmon (Diospyros kaki L.) by Agrobacterium rhizogenes wild type strain A4. J Japanese Soc Hortic Sci 63:283–289 Taylor BH, Amasino RM, White FF et al (1985) T-DNA analysis of plants regenerated from hairy root tumors. Mol Gen Genet 201:554–557. https://doi.org/10.1007/BF00331355 Tepfer D (1984) Transformation of several species of higher plants by Agrobacterium rhizogenes: sexual transmission of the transformed genotype and phenotype. Cell 37:959–967. https://doi.org/10.1016/0092-8674(84)90430-6 Tsuro M, Ikedo H (2011) Changes in morphological phenotypes and essential oil components in lavandin (Lavandula×intermedia Emeric ex Loisel.) transformed with wild-type strains of Agrobacterium rhizogenes. Sci Hortic (amsterdam) 130:647–652. https://doi.org/10.1016/j.scienta.2011.08.011 Van Huylenbroeck J, Desmet S, Dhooghe E et al (2019) Breeding for compact growing ornamentals. Acta Hortic 1237:1–6. https://doi.org/10.17660/ActaHortic.2019.1237.1 Veena V, Taylor CG (2007) Agrobacterium rhizogenes: recent developments and promising applications. Vitr Cell Dev Biol - Plant 43:383–403. https://doi.org/10.1007/s11627-007-9096-8 Verma P, Khan SA, Masood N et al (2017) Differential rubisco content and photosynthetic efficiency of rol gene integrated Vinca minor transgenic plant: correlating factors associated with morpho-anatomical changes, gene expression and alkaloid productivity. J Plant Physiol 219:12–21. https://doi.org/10.1016/j.jplph.2017.09.004 White FF, Taylor BH, Huffman GA et al (1985) Molecular and genetic analysis of the transferred DNA regions of the root-inducing plasmid of Agrobacterium rhizogenes. J Bacteriol 164:33–44