Skip to main content
SpringerLink
Log in

Influence of plant growth regulators and water stress on ramet induction, rosette engrossment, and fructan accumulation in Agave tequilana Weber var. Azul

  • Original Paper
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

Agave tequilana Weber var. Azul plants reproduce asexually by producing ramets. Continuous production of ramets throughout the vegetative cycle of the parent delays the time of harvesting of heads for tequila production. Little is known about the factors influencing their emergence. Heads are engrossed rosettes where fructans are stored. We show here that, in plantlets grown in vitro, growth regulators such as 2,4-dichlorophenoxyacetic acid (2,4-D), a combination of 1-naphthaleneacetic acid (NAA)/6-benzyladenine (BA), or abscisic acid (ABA) increased the production of ramets, whereas BA, NAA, gibberellic acid (GA3), glycerol, or a combination of glycerol/ABA decreased ramet production. Plantlets that developed ramets did not form heads. Head formation was improved on solid media in the presence of BA, NAA, the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC), or the water stress inducer polyethylene glycol (PEG). Basal Murashige–Skoog (MS) liquid media also enhanced rosette engrossment, which was further increased by addition of ACC or PEG. In contrast, CoCl2, an ethylene biosynthesis inhibitor, reduced rosette engrossment. Furthermore, heads from A. tequilana plantlets grown in tissue culture in MS media, or in MS media supplemented with NAA, ACC or PEG, showed fructan concentrations 10–30 times higher than in leaves from greenhouse-grown plants. Our results indicated that BA, NAA, water stress, and ethylene are critical regulators of rosette engrossment, whereas asexual reproduction in A. tequilana seems to be controlled by a complex hormonal network.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

2-4,D:

2,4-Dichlorophenoxyacetic acid

ABA:

Abscisic acid

ACC:

1-Aminocyclopropane-1-carboxylic acid

BA:

6-Benzyladenine

FAA:

Formalin-acid-alcohol

f.w.:

Fresh weight

GA3 :

Gibberellic acid

MS:

Murashige–Skoog media

NAA:

1-Naphthaleneacetic acid

PEG:

Polyethylene glycol

References

  • Aubert S, Gout E, Bligny R, Douce R (1994) Multiple effects of glycerol on plant metabolism. Phosphorous-31 nuclear magnetic resonance studies. J Biol Chem 269:21420–21427

    CAS  PubMed  Google Scholar 

  • Avila-Fernández A, Olvera-Carranza C, Rudiño-Piñera E, Cassab GI, Nieto-Sotelo J, López-Munguía A (2007) Molecular characterization of sucrose: sucrose 1-fructosyltransferase (1-SST) from Agave tequilana Weber var. Azul Plant Sci 173:478–486

    Article  Google Scholar 

  • Avila-Fernández A, Rendón-Poujol X, Olvera C, González F, Capella S, Peña-Alvarez A, López-Munguía A (2009) Enzymatic hydrolysis of fructans in the tequila production process. J Agric Food Chem 57:5578–5585

    Article  PubMed  Google Scholar 

  • Banerjee S, Sharma AK (1988) Structural differences of chromosomes in diploid Agave. Cytologia 53:415–420

    Google Scholar 

  • Barazesh S, McSteen P (2008) Hormonal control of grass inflorescence development. Trends Plant Sci 13:656–662

    Article  CAS  PubMed  Google Scholar 

  • Binh LT, Muoi LT, Oanh HTK, Thang TD, Phong DT (1990) Rapid propagation of agave by in vitro tissue culture. Plant Cell Tiss Org Cult 23:67–70

    Article  Google Scholar 

  • Blunden G, Carabot C, Jewers K (1980) Steroidal sapogenins from leaves of some species of Agave and Fureraea. Phytochemistry 19:2489–2490

    Article  CAS  Google Scholar 

  • Cedeño GM (1999) Tequila production. Crit Rev Biotechnol 15:1–11

    Article  Google Scholar 

  • Christmann A, Hoffmann T, Teplova I, Grill E, Müller A (2005) Generation of active pools of abscisic acid revealed by in vivo imaging of water-stressed Arabidopsis. Plant Physiol 137:209–219

    Article  CAS  PubMed  Google Scholar 

  • Das T (1992) Micropropagation of Agave sisalana. Plant Cell Tiss Org Cult 31:293–295

    Google Scholar 

  • Davies PJ (2004) Plant Hormones. Biosynthesis, signal transduction, action!. Kluwer Academic, Dordrecht, The Netherlands

    Google Scholar 

  • Diaz G, Wolf W, Kostaropoulos AE, Spiess WEL (1993) Diffusion of low-molecular compounds in food model systems. J Food Process Preserv 17:437–454

    Article  CAS  Google Scholar 

  • Dodd IC, Davies WJ (2004) Hormones and the regulation of water balance. In: Davies PJ [ed] Plant hormones. Biosynthesis, signal transduction, action! Kluwer Academic, Dordrecht, The Netherlands, pp 493–512

    Google Scholar 

  • Eapen D, Barroso ML, Campos ME, Ponce G, Corkidi G, Dubrovsky JG, Cassab GI (2003) A no hydrotropic root mutant that responds to gravitropism in Arabidopsis thaliana. Plant Physiol 131:536–546

    Article  CAS  PubMed  Google Scholar 

  • Feng X (1996) Is ABA an inhibitor or promoter of shoot growth in water-stressed plants? MS thesis. University of Missouri, Columbia

  • Finkelstein R (2004) The role of hormones during seed development and germination. In: Davies PJ (ed) Plant Hormones. Biosynthesis, signal transduction, action!. Kluwer Academic, Dordrecht, The Netherlands, pp 513–537

    Google Scholar 

  • García-Mendoza A (1998) Con sabor a maguey. Guía de la Colección Nacional de agaváceas y nolináceas del Jardín Botánico del Instituto de Biología- UNAM. Instituto de Biología, Universidad Nacional Autónoma de México. México, D.F., Mexico

    Google Scholar 

  • García-Mendoza A, Galván VR (1995) Riqueza de las familias Agavaceae y Nolinaceae en México. Bol Soc Bot Mex 56:7–24

    Google Scholar 

  • Gentry HS (2003) Agaves of Continental North America. The University of Arizona Press. Tucson, AZ, USA

    Google Scholar 

  • Groenewald EG, Wessels DCJ, Koeleman A (1977) Callus formation and subsequent plant regeneration from seed tissue of an Agave species (Agavaceae). Z Planzenphysiol 81:369–373

    Google Scholar 

  • Hamant O, Heisler MG, Jönsson H, Krupinski P, Uyttewaal M, Bokov P, Corson F, Sahlin P, Boudaoud A, Meyerowitz EM, Couder Y, Traas J (2008) Developmental patterning by mechanical signals in Arabidopsis. Science 322:1650–1655

    Article  CAS  PubMed  Google Scholar 

  • Ho S, Chao Y, Tong W, Yu S (2001) Sugar coordinately and differentially regulates growth- and stress-related gene expression via a complex signal transduction network and multiple control mechanisms. Plant Physiol 125:877–890

    Article  CAS  PubMed  Google Scholar 

  • Horvath DP, Wun SC, Anderson JV (2002) Molecular analysis of signals controlling dormancy and growth in underground adventitious buds of leafy sponge. Plant Physiol 128:1439–1446

    Article  CAS  PubMed  Google Scholar 

  • Jang J-C, León P, Zhou L, Sheen J (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell 9:5–19

    Article  CAS  PubMed  Google Scholar 

  • Lagerwerff JV, Ogata G, Eagle HE (1961) Control of osmotic pressure of culture solutions with polyethylene glycol. Science 133:1486–1487

    Article  CAS  PubMed  Google Scholar 

  • Lau O-L, Yang SF (1976) Inhibition of ethylene production by cobalt ion. Plant Physiol 58:114–117

    Article  CAS  PubMed  Google Scholar 

  • Le Guen-Le Saos F, Hourmant A, Esnault F, Chauvin JE (2002) In vitro bulb development in shallot (Allium cepa L. Aggregatum Group): effects of anti-gibberellins, sucrose and light. Ann Bot 89:419–425

    Article  CAS  PubMed  Google Scholar 

  • Lian H-L, Yu X, Lane D, Sun W-N, Tang Z-C, Su W-A (2006) Upland rice and lowland rice exhibited different PIP expression under water deficit and ABA treatment. Cell Res 16:651–660

    Article  CAS  PubMed  Google Scholar 

  • Luján R, Lledías F, Martínez LM, Barreto R, Cassab GI, Nieto-Sotelo J (2009) Small heat-shock proteins and leaf cooling capacity account for the unusual heat tolerance of the central spike leaves in Agave tequilana var. Weber. Plant Cell Environ 32:1791–1803

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nelson C, Jean RP, Tan JL, Liu WF, Sniadecki NJ, Spector AA, Chen CS (2005) Emergent patterns of growth controlled by multicellular form and mechanics. Proc Natl Acad Sci U S A 102:11594–11599

    Article  CAS  PubMed  Google Scholar 

  • Nikam TD (1997) High frequency shoot regeneration in Agave sisalana. Plant Cell Tiss Org Cult 51:225–228

    Article  CAS  Google Scholar 

  • Perata P, Matsukura C, Vernieri P, Yamaguchi J (1997) Sugar repression of a gibberelin-dependant signaling pathway in barley embryos. Plant Cell 9:2197–2208

    Article  CAS  PubMed  Google Scholar 

  • Pitelka LF, Asmun JW (1985) Physiology and integration of ramets in clonal plants. In: Jackson JBG, Buss LW, Cook RE (eds) The population biology and evolution of clonal organisms. Yale University Press, New Haven, Connecticut, USA, pp 399–435

    Google Scholar 

  • Ponce G, Barlow PW, Feldman LJ, Cassab GI (2005) Auxin and ethylene interactions control mitotic activity of the quiescent center, root cap size and pattern of cap cell differentiation in maize. Plant Cell Environ 28:719–732

    Article  CAS  PubMed  Google Scholar 

  • Portillo L, Santacruz-Ruvalcaba F, Gutiérrez-Mora A, Rodríguez-Garay B (2007) Somatic embryogenesis in Agave tequilana Weber cultivar azul. In Vitro Cell Dev Biol Plant 43:569–575

    Article  CAS  Google Scholar 

  • Raphael DO, Nobel PS (1986) Growth and survivorship of ramets and seedlings of Agave deserti: influences of parent-ramet connections. Bot Gaz 147:78–83

    Article  Google Scholar 

  • Robert ML, Herrera JL, Contreras F, Scorer KN (1987) In vitro propagation of Agave fourcroydes Lem.(Henequen). Plant Cell Tiss Org Cult 8:37–48

    Article  CAS  Google Scholar 

  • Salisbury FB, Ross CW (1992) Plant physiology. 4th edition, Wadsworth, Belmont, USA

    Google Scholar 

  • Sánchez-Marroquín A, Hope PH (1953) Agave juice: Fermentation and chemical composition studies of some species. J Agric Food Chem 1:246–249

    Article  Google Scholar 

  • Santacruz-Ruvalcaba F, Gutiérrez-Pulido H, Rodríguez-Garay B (1999) Efficient in vitro propagation of Agave parrasana Berger. Plant Cell Tiss Org Cult 56:163–167

    Article  Google Scholar 

  • Shraiman BI (2005) Mechanical feedback as a possible regulator of tissue growth. Proc Natl Acad Sci U S A 102:3318–3323

    Article  CAS  PubMed  Google Scholar 

  • Spollen WG, LeNoble ME, Samuels TD, Bernstein N, Sharp RE (2000) Abscisic acid accumulation maintains maize primary root elongation at low water potentials by restricting ethylene production. Plant Physiol 122:967–976

    Article  CAS  PubMed  Google Scholar 

  • Stecchini ML, Del Torre M, Sarais I, Saro O, Messina M, Maltini E (1998) Influence of structural properties and kinetic constraints on Bacillus cereus growth. Appl Environ Microbiol 64:1075–1078

    CAS  PubMed  Google Scholar 

  • Tissue D, Nobel P (1988) Parent-ramet connections in Agave deserti: influences of carbohydrates on growth. Oecologia (Berlin) 75:266–271

    Article  Google Scholar 

  • Valenzuela-Sánchez KK, Juárez-Hernández RE, Cruz-Hernández A, Olalde-Portugal V, Valverde ME, Paredes-López O (2006) Plant regeneration of Agave tequilana by indirect organogenesis. In Vitro Cell Dev Biol Plant 42:336–340

    Article  Google Scholar 

  • van der Weele C, Spollen WG, Sharp RE, Baskin TI (2000) Growth of Arabidopsis thaliana seedlings under water deficit studied by control of water potential in nutrient-agar media. J Exp Bot 51:1555–1562

    Article  PubMed  Google Scholar 

  • Wang T-W, Arteca RN (1992) Effects of low O2 root stress on ethylene biosynthesis in tomato plants (Lycopersicon esculentum Mill cv Heinz 1350). Plant Physiol 98:97–100

    Article  CAS  PubMed  Google Scholar 

  • Wang N, Nobel P (1998) Phloem transport of fructans in the crassulacean acid metabolism species Agave deserti. Plant Physiol 116:709–714

    Article  CAS  PubMed  Google Scholar 

  • Whalen MC, Feldman LJ (1988) The effect of ethylene on root growth of Zea mays seedlings. Can J Bot 66:719–723

    Article  CAS  PubMed  Google Scholar 

  • Young IM, Montagu K, Conroy J, Bengough AG (1997) Mechanical impedance of root growth directly reduces leaf elongation rates of cereals. New Phytol 135:613–619

    Article  Google Scholar 

Download references

Acknowledgments

We thank Dr. I. del Real and M.C.R. Ayala (Sauza-Pedro Domecq) for providing A. tequilana Azul var. Weber plants and their committed support to the project. We appreciate the generous help of F. González and Dr. A. López-Munguía in the determination of fructose levels in A. tequilana samples and Dr. M.A. Rosales for statistical analysis of the data. We also warmly thank all the members of the laboratory for their continuous support and discussion of the data. The technical expertise of M. Saucedo Ramírez, computer support of R. Bahena, A. Martínez Valle, and J.M. Hurtado, and library support of Shirley Ainsworth are fully appreciated. This work was supported by a grant from Pedro Domecq (P-150) to J.N.-S. and G.I.C.

Author information

Author notes

  1. Rita Barreto

    Present address: Facultad de Ciencias, Universidad Autónoma del Estado de Morelos, Cuernavaca, Mor, Mexico

Authors and Affiliations

  1. Departamento de Biología Molecular de Plantas, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Apdo, Postal 510-3, Cuernavaca, Mor, 62250, Mexico

    Rita Barreto, Jorge Nieto-Sotelo & Gladys I. Cassab

Authors
  1. Rita Barreto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jorge Nieto-Sotelo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gladys I. Cassab
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jorge Nieto-Sotelo or Gladys I. Cassab.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplemental Fig. 1

.Effect of ACC and PEG on rosette development in plantlets of A. tequilana grown for 90 days in solid media. Rosette engrossment is described as the percentage of plants that showed this response. Concentrations of chemicals were: ACC-1 (1 μM), ACC-10 (10 μM), PEG-5 (5% PEG [v/v]), PEG-8 (8% PEG), and PEG-10 (10% PEG). MS, ACC-10, and PEG-5 data were obtained from six, three, and two separate experiments, respectively. Data for ACC-1, PEG-8, and PEG-10 were obtained from one single experiment. Data represent average ± SD values. Bars with different letters differ significantly. (PDF 35 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barreto, R., Nieto-Sotelo, J. & Cassab, G.I. Influence of plant growth regulators and water stress on ramet induction, rosette engrossment, and fructan accumulation in Agave tequilana Weber var. Azul. Plant Cell Tiss Organ Cult 103, 93–101 (2010). https://doi.org/10.1007/s11240-010-9758-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-010-9758-9

Keywords

Search

Navigation