Skip to main content
Log in

Adventitious rooting is enhanced by methyl jasmonate in tobacco thin cell layers

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Adventitious roots (ARs) are induced by auxins. Jasmonic acid (JA) and methyl jasmonate (MeJA) are also plant growth regulators with many effects on development, but their role on ARs needs investigation. To this aim, we analyzed AR formation in tobacco thin cell layers (TCLs) cultured with 0.01–10 μM MeJA, either under root-inductive conditions, i.e., on medium containing 10 μM indole-3-butyric acid (IBA) and 0.1 μM kinetin, or without hormones. The explants were excised from the cultivars Samsun, Xanthii and Petite Havana, and from genotypes with altered AR-forming ability in response to auxin, namely the non-rooting rac mutant and the over-rooting Agrobacterium rhizogenes rolB transgenic line. Results show that NtRNR1 (G1/S) and Ntcyc29 (G2/M) gene activity, cell proliferation and meristemoid formation were stimulated in hormone-cultured TCLs by submicromolar MeJA concentrations. The meristemoids developed either into ARs and xylogenic nodules, or into xylogenic nodules only (rac TCLs). MeJA-induced meristemoid over-production characterized rolB TCLs. No rooting or xylogenesis occurred under hormone-free conditions, independently of MeJA and genotype. Endogenous JA progressively (days 1–4) increased in hormone-cultured TCLs in the absence of MeJA. JA levels were enhanced by 0.1 μM MeJA, on both days 1 and 4. Endogenous IBA was the only auxin detected, both in the free form and as IBA-glucose. Free IBA increased up to day 2, remaining constant thereafter (day 4). Its level was enhanced by 0.1 μM MeJA only on day 1, while IBA conjugation was not affected by MeJA. Taken together, these results show that an interplay between jasmonates and auxins regulates AR formation and xylogenesis in tobacco TCLs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

AR:

Adventitious root

HF:

Hormone free

IBA:

Indole-3-butyric acid

JA:

Jasmonic acid

Kin:

Kinetin

LR:

Lateral root

MCC:

Meristematic cell cluster

MeJA:

Methyl jasmonate

PR:

Primary root

SE:

Standard error

TCL:

Thin cell layer

References

  • Altamura MM (2004) Agrobacterium rhizogenes rolB and rolD genes: regulation and involvement in plant development. Plant Cell Tissue Organ Cult 77:89–101

    Article  CAS  Google Scholar 

  • Altamura MM, Falasca G (2009) Adventitious rooting in model plants and in in vitro systems: an integrated molecular and cytohistological approach. In: Niemi K, Scagel C (eds) Adventitious root formation of forest trees and horticultural plants-from genes to applications. Research Signpost, Kerala, India, pp 123–144. ISBN:978-81-308-0342-5

  • Altamura MM, Capitani F, Serafini-Fracassini D, Torrigiani P, Falasca G (1991) Root histogenesis from tobacco thin cell layers. Protoplasma 161:31–42

    Article  Google Scholar 

  • Altamura MM, Capitani F, Gazza L, Caponi I, Costantino P (1994) The plant oncogene rolB stimulates the formation of flower and root meristemoids in tobacco thin cell layers. New Phytol 126:283–293

    Article  CAS  Google Scholar 

  • Altamura MM, Capitani F, Falasca G, Gallelli A, Scaramagli S, Bueno M, Torrigiani P, Bagni N (1995) Morphogenesis in cultured thin layers and pith explants of tobacco. I. Effect of putrescine on cell size, xylogenesis and meristemoid organization. J Plant Physiol 147:101–106

    CAS  Google Scholar 

  • Baraldi R, Bertazza G, Predieri S, Bregoli AM, Cohen JD (1993) Uptake and metabolism of indole-3-butyric acid during the in vitro rooting phase in pear cultivars (Pyrus communis). Acta Hortic 329:289–291

    Google Scholar 

  • Bartel B, LeClere S, Magidin M, Zolman BK (2001) Inputs to the active indole-3-acetic acid pool: de novo synthesis, conjugate hydrolysis, and indole-3-butyric acid β-oxidation. J Plant Growth Regul 20:198–216

    Article  CAS  Google Scholar 

  • Browse J (2005) Jasmonate: an oxylipin signal with many roles in plants. Vitam Horm 72:431–456

    Article  CAS  PubMed  Google Scholar 

  • Canas LA, Busscher M, Angenent GC, Beltran JP, van Tunen AJ (1994) Nuclear localization of the petunia MADS box protein FBP1. Plant J 6:597–604

    Article  CAS  Google Scholar 

  • Capitani F, Biondi S, Falasca G, Ziosi V, Balestrazzi A, Carbonera D, Torrigiani P, Altamura MM (2005) Methyl jasmonate disrupts shoot formation in tobacco thin cell layers by over-inducing mitotic activity and cell expansion. Planta 220:507–519

    Article  CAS  PubMed  Google Scholar 

  • Cardarelli M, Mariotti D, Pomponi M, Spanò L, Capone I, Costantino P (1987) Agrobacterium rhizogenes T-DNA genes capable of inducing hairy root phenotype. Mol Gen Genet 209:475–480

    Article  CAS  PubMed  Google Scholar 

  • Cenzano A, Vigliocco A, Kraus T, Abdala G (2003) Exogenously applied jasmonic acid induces changes in apical meristem morphology of potato stolons. Ann Bot (Lond) 91:915–919

    Article  CAS  Google Scholar 

  • Chabouté ME, Combettes B, Clement B, Gigot C, Philipps G (1998) Molecular characterization of tobacco ribonucleotide reductase RNR1 and RNR2 cDNAs and cell cycle-regulated expression in synchronized plant cells. Plant Mol Biol 38:797–806

    Article  PubMed  Google Scholar 

  • Clutter ME (1960) Hormonal induction of vascular tissue in tobacco pith in vitro. Science 132:548–549

    Article  CAS  PubMed  Google Scholar 

  • Delbarre A, Muller P, Imhoff V, Barbier-Brygoo H, Maurel C, Guern J (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

    CAS  PubMed  Google Scholar 

  • Delker C, Raschke A, Quint M (2008) Auxin dynamics: the dazzling complexity of a small molecule’s message. Planta 227:929–941

    Article  CAS  PubMed  Google Scholar 

  • Devoto A, Ellis C, Magusin A, Chang HS, Chilcott C, Zhu T, Turner JG (2005) Expression profiling reveals COI1 to be a key regulator of genes involved in wound- and methyl jasmonate-induced secondary metabolism, defence, and hormone interactions. Plant Mol Biol 58:497–513

    Article  CAS  PubMed  Google Scholar 

  • Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, Fitt GP, Sewelam N, Schenk PM, Manners JM, Kazan K (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225–2245

    Article  CAS  PubMed  Google Scholar 

  • Epstein E, Ludwig-Müller J (1993) Indole-3-butyric acid in plants: occurrence, synthesis, metabolism and transport. Physiol Plant 88:382–389

    Article  CAS  Google Scholar 

  • Faivre-Rampant O, D’Angeli S, Falasca G, Dommes J, Gaspar T, Altamura MM (2003) Rooting blockage in the tobacco rac mutant occurs at the initiation phase, and induces diversion to xylem. Plant Biosyst 137:163–174

    Google Scholar 

  • Falasca G, Altamura MM (2003) Histological analysis of adventitious rooting in Arabidopsis thaliana (L.) Heynh seedlings. Plant Biosyst 137:265–274

    Google Scholar 

  • Falasca G, Zaghi D, Possenti M, Altamura MM (2004) Adventitious root formation in Arabidopsis thaliana thin cell layers. Plant Cell Rep 23:17–25

    Article  CAS  PubMed  Google Scholar 

  • Grossman K, Rosenthal C, Kwiatkowsski J (2004) Increases in jasmonic acid caused by indole-3-acetic and auxin herbicides in cleavers (Galium aparine). J Plant Physiol 161:809–814

    Article  Google Scholar 

  • Kim YS, Yeung EC, Hahn EJ, Paek KY (2007) Combined effects of phytohormone indole-3-butyric acid, and methyl jasmonate on root growth and ginsenoside production in adventitious root cultures of Panax ginseng CA Meyer. Biotechnol Lett 29:1789–1792

    Article  CAS  PubMed  Google Scholar 

  • 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 89:481–487

    Article  CAS  PubMed  Google Scholar 

  • Kondo S, Motoyama M, Michiyama H, Kim M (2002) Roles of jasmonic acid in the development of sweet cherries as measured from fruit or disc samples. Plant Growth Regul 37:37–44

    Article  CAS  Google Scholar 

  • Kuroha T, Sato S (2007) Involvement of cytokinins in adventitious and lateral root formation. Plant Root 1:27–33

    Article  CAS  Google Scholar 

  • Ludwig-Müller J (2000) Indole-3-butyric acid in plant growth and development. Plant Growth Regul 32:219–230

    Article  Google Scholar 

  • Ludwig-Müller J, Vertocnik A, Town CD (2005) Analysis of indole-3-butyric acid-induced adventitious root formation on Arabidopsis stem segments. J Exp Bot 56:2095–2105

    Article  PubMed  Google Scholar 

  • Maliga PA, Sz-Breznovits A, Marton L (1973) Streptomycin-resistant plants from callus culture of haploid tobacco. Nat New Biol 244:29–30

    CAS  PubMed  Google Scholar 

  • Maurel C, Leblanc N, Barbier-Brygoo H, Perrot-Rechenmann C, Bouvier-Durand M, Guern J (1994) Alterations of auxin perception in rolB-transformed tobacco protoplast: time course of rolB mRNA expression and increase in auxin sensitivity reveal multiple control by auxin. Plant Physiol 105:1209–1215

    Article  CAS  PubMed  Google Scholar 

  • Meyer R, Rautenbach GF, Dubery IA (2003) Identification and quantification of methyl jasmonate in leaf volatiles of Arabidopsis thaliana using solid-phase microextraction in combination with gas chromatography and mass spectrometry. Phytochem Anal 14:155–159

    Article  CAS  PubMed  Google Scholar 

  • Moons A, Prinsen E, Bauw G, Van Montagu M (1997) Antagonistic effects of abscisic acid and jasmonates on salt stress-inducible in rice roots. Plant Cell 9:2243–2259

    Article  CAS  PubMed  Google Scholar 

  • Mourelatou M, Doonan JH, McCann MC (2004) Transition of G1 to early S phase may be required for zinnia mesophyll cells to trans-differentiate to tracheary elements. Planta 220:172–176

    Article  CAS  PubMed  Google Scholar 

  • Müller JF, Goujaud J, Caboche M (1985) Isolation in vitro of naphthalene acetic acid-tolerant mutants of Nicotiana tabacum, which are impaired in root morphogenesis. Mol Gen Genet 199:194–200

    Article  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissues cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nilsson O, Crozier A, Schmulling T, Sandberg G, Olsson O (1993) Indole-3-acetic acid homeostasis in transgenic tobacco plants expressing the Agrobacterium rhizogenes rolB gene. Plant J 3:681–689

    Article  CAS  Google Scholar 

  • Paponov IA, Paponov M, Teale W, Menges M, Chakrabortee S, Murray JAH, Palme K (2008) Comprehensive transcriptome analysis of auxin responses in Arabidopsis. Mol Plant 1:321–337

    Article  CAS  PubMed  Google Scholar 

  • Park JE, Park JY, Kim YS, Staswick PE, Jeon J, Yun J, Kim SY, Kim J, Lee YH, Park CM (2007) GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J Biol Chem 282:10036–10046

    Article  CAS  PubMed  Google Scholar 

  • Pauwels L, Moreel K, De Witte E, Lammertyn F, Montagu MV, Boerjan W, Inzé D, Goossens A (2008) Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells. Proc Natl Acad Sci USA 105:1380–1385

    Article  CAS  PubMed  Google Scholar 

  • Phillips R, Press MC, Bingham L, Grimmer C (1988) Polyamines in cultured artichoke explants: effects are primarily on xylogenesis rather than cell division. J Exp Bot 201:473–480

    Article  Google Scholar 

  • Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MAK (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12:98–105

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sasaki Y, Asamizu E, Shibata D, Nakamura Y, Kaneko T, Awai K, Amagai M, Kuwata C, Tsugane T, Masuda T, Shimada H, Takamiya K, Ohta H, Tabata S (2001) Monitoring of methyl jasmonate-responsive genes in Arabidopsis by cDNA macroarray: self-activation of jasmonic acid biosynthesis and crosstalk with other phytohormone signalling pathways. DNA Res 8:153–161

    Article  CAS  PubMed  Google Scholar 

  • Setiady YY, Sekine M, Yamamoto T, Kouchi H (1997) Expression pattern of tobacco cyclin genes. Plant Cell Rep 16:368–372

    CAS  Google Scholar 

  • Stoynova-Bakalova E, Petrov PI, Gigova L, Baskin TI (2008) Differential effects of methyl jasmonate on growth and division of etiolated zucchini cotyledons. Plant Biol 10:476–484

    Article  CAS  PubMed  Google Scholar 

  • Sun J, Xu Y, Ye S, Jiang H, Chen Q, Liu F, Zhou W, Chen R, Li X, Tietz O, Wu X, Cohen JD, Palme K, Li C (2009) Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation. Plant Cell. doi:10.1105/tpc.108.064303

  • Swiatek A, Lenjou M, Van Bockstaele D, Inzé D, Van Onckelen H (2002) Differential effect of jasmonic acid and abscisic acid on cell cycle progression in tobacco BY-2 cells. Plant Physiol 128:201–211

    Article  CAS  PubMed  Google Scholar 

  • Swiatek A, Van Dongen W, Esmans EL, Van Onckelen H (2004) Metabolic fate of jasmonates in tobacco bright yellow-2 cells. Plant Physiol 135:161–172

    Article  CAS  PubMed  Google Scholar 

  • Swiatek A, Azmi A, Van Onckelen H (2005) Jasmonic acid positively regulates auxin-dependent lateral root initiation in Arabidopsis thaliana. Biol Plant 49:S30

    Google Scholar 

  • Tiryaki I, Staswick PE (2002) An Arabidopsis mutant defective in jasmonates response is allelic to the auxin-signaling mutant axr1. Plant Physiol 130:887–894

    Article  CAS  PubMed  Google Scholar 

  • Toro FJ, Martin C, Pelacho AM (2003) Jasmonate promote cabbage (Brassica oleracea L. var Capitata L.) root and shoot development. Plant Soil 255:77–83

    Article  CAS  Google Scholar 

  • Torrigiani P, Altamura MM, Capitani F, Falasca G, Bagni N, Serafini-Fracassini D (1989) De novo root formation in thin cell layers of tobacco: changes in free and bound polyamines. Physiol Plant 77:294–301

    Article  CAS  Google Scholar 

  • Tran Thanh Van M, Dien NT, Chlyah A (1974) Regulation of organogenesis in small explants of superficial tissue of Nicotiana tabacum L. Planta 119:149–159

    Article  CAS  Google Scholar 

  • Van der Krieken WM, Breteler H, Visser MHM, Mavridou D (1993) The role of the conversion of IBA into IAA on root regeneration in apple: introduction of a test system. Plant Cell Rep 12:203–206

    Article  Google Scholar 

  • Wang S, Ichii M, Taketa S, Xu L, Xia K, Zhou X (2002) Lateral root formation in rice (Oryza sativa): promotion effect of jasmonic acid. J Plant Physiol 159:827–832

    Article  CAS  Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot (Lond) 100:681–697

    Article  CAS  Google Scholar 

  • Watanabe T, Shigemi S, Sakai S (2001) Wound-induced expression of a gene for 1-aminocyclopropane-1-carboxylate synthase and ethylene production are regulated by both reactive oxygen species and jasmonic acid in Cucurbita maxima. Plant Physiol 39:121–127

    CAS  Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot (Lond) 95:707–735

    Article  CAS  Google Scholar 

  • Wu J, Wang L, Baldwin IT (2008) Methyl jasmonate-elicited herbivore resistance: does MeJA function as a signal without being hydrolyzed to JA? Planta 227:1161–1168

    Article  CAS  PubMed  Google Scholar 

  • Zadra C, Borgogni A, Marucchini C (2006) Quantification of jasmonic acid by SPME in tomato plants stressed by ozone. J Agric Food Chem 54:9317–9321

    Article  CAS  PubMed  Google Scholar 

  • Zolman BK, Martinez N, Millius A, Adham AR, Bartel B (2008) Identification and characterization of Arabidopsis indole-3-butyric acid response mutants defective in novel peroxisomal enzymes. Genetics 180:237–251

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Prof. Alessandra Gentili (Dipartimento di Chimica, Sapienza Università di Roma, Italy) for helpful suggestions in auxin detection, Prof. Stefania Biondi (Dipartimento di Biologia Evol. Sper., Università di Bologna, Italy) for helpful discussion on jasmonates, Dr. Marie-Edith Chabouté (Institut de Biologie Moléculaire des Plantes du CNRS, Universitè Louis Pasteur, Strasbourg, France) and Dr. Masami Sekine (Department of Bioproduction Science, Ishikawa Prefectural University, Ishikawa, Japan) for the generous gift of NtRNR1 and Ntcyc29 cDNA, respectively. We also thank Dr. Maura Cardarelli (Dipartimento di Genetica e Biologia Molecolare, Sapienza Università di Roma, Italy) for the generous gift of rolB seeds and for the preparation of the Ntcyc29 probe for in situ hybridizations. This work was supported by Progetto d’Ateneo, Sapienza Università di Roma (to MMA), and by Progetto di Ateneo Federato 2007–2008, Sapienza Università di Roma (to GF).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maria Maddalena Altamura.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fattorini, L., Falasca, G., Kevers, C. et al. Adventitious rooting is enhanced by methyl jasmonate in tobacco thin cell layers. Planta 231, 155–168 (2009). https://doi.org/10.1007/s00425-009-1035-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-009-1035-y

Keywords

Navigation