Advertisement

Plant Cell, Tissue and Organ Culture (PCTOC)

, Volume 103, Issue 1, pp 93–101 | Cite as

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

  • Rita Barreto
  • Jorge Nieto-Sotelo
  • Gladys I. Cassab
Original Paper

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.

Keywords

ABA Asexual reproduction Auxin Cytokinin Ethylene Gibberellin Reserve carbohydrates 

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

Notes

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.

Supplementary material

11240_2010_9758_MOESM1_ESM.pdf (36 kb)
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)

References

  1. 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 269:21420–21427PubMedGoogle Scholar
  2. 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 173:478–486CrossRefGoogle Scholar
  3. 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 57:5578–5585CrossRefPubMedGoogle Scholar
  4. Banerjee S, Sharma AK (1988) Structural differences of chromosomes in diploid Agave. Cytologia 53:415–420Google Scholar
  5. Barazesh S, McSteen P (2008) Hormonal control of grass inflorescence development. Trends Plant Sci 13:656–662CrossRefPubMedGoogle Scholar
  6. 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 23:67–70CrossRefGoogle Scholar
  7. Blunden G, Carabot C, Jewers K (1980) Steroidal sapogenins from leaves of some species of Agave and Fureraea. Phytochemistry 19:2489–2490CrossRefGoogle Scholar
  8. Cedeño GM (1999) Tequila production. Crit Rev Biotechnol 15:1–11CrossRefGoogle Scholar
  9. 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 137:209–219CrossRefPubMedGoogle Scholar
  10. Das T (1992) Micropropagation of Agave sisalana. Plant Cell Tiss Org Cult 31:293–295Google Scholar
  11. Davies PJ (2004) Plant Hormones. Biosynthesis, signal transduction, action!. Kluwer Academic, Dordrecht, The NetherlandsGoogle Scholar
  12. Diaz G, Wolf W, Kostaropoulos AE, Spiess WEL (1993) Diffusion of low-molecular compounds in food model systems. J Food Process Preserv 17:437–454CrossRefGoogle Scholar
  13. 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 493–512Google Scholar
  14. 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 131:536–546CrossRefPubMedGoogle Scholar
  15. Feng X (1996) Is ABA an inhibitor or promoter of shoot growth in water-stressed plants? MS thesis. University of Missouri, ColumbiaGoogle Scholar
  16. 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 513–537Google Scholar
  17. 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., MexicoGoogle Scholar
  18. García-Mendoza A, Galván VR (1995) Riqueza de las familias Agavaceae y Nolinaceae en México. Bol Soc Bot Mex 56:7–24Google Scholar
  19. Gentry HS (2003) Agaves of Continental North America. The University of Arizona Press. Tucson, AZ, USAGoogle Scholar
  20. Groenewald EG, Wessels DCJ, Koeleman A (1977) Callus formation and subsequent plant regeneration from seed tissue of an Agave species (Agavaceae). Z Planzenphysiol 81:369–373Google Scholar
  21. 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 322:1650–1655CrossRefPubMedGoogle Scholar
  22. 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 125:877–890CrossRefPubMedGoogle Scholar
  23. Horvath DP, Wun SC, Anderson JV (2002) Molecular analysis of signals controlling dormancy and growth in underground adventitious buds of leafy sponge. Plant Physiol 128:1439–1446CrossRefPubMedGoogle Scholar
  24. Jang J-C, León P, Zhou L, Sheen J (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell 9:5–19CrossRefPubMedGoogle Scholar
  25. Lagerwerff JV, Ogata G, Eagle HE (1961) Control of osmotic pressure of culture solutions with polyethylene glycol. Science 133:1486–1487CrossRefPubMedGoogle Scholar
  26. Lau O-L, Yang SF (1976) Inhibition of ethylene production by cobalt ion. Plant Physiol 58:114–117CrossRefPubMedGoogle Scholar
  27. 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 89:419–425CrossRefPubMedGoogle Scholar
  28. 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 16:651–660CrossRefPubMedGoogle Scholar
  29. 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 32:1791–1803CrossRefPubMedGoogle Scholar
  30. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  31. 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 102:11594–11599CrossRefPubMedGoogle Scholar
  32. Nikam TD (1997) High frequency shoot regeneration in Agave sisalana. Plant Cell Tiss Org Cult 51:225–228CrossRefGoogle Scholar
  33. Perata P, Matsukura C, Vernieri P, Yamaguchi J (1997) Sugar repression of a gibberelin-dependant signaling pathway in barley embryos. Plant Cell 9:2197–2208CrossRefPubMedGoogle Scholar
  34. 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 399–435Google Scholar
  35. 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 28:719–732CrossRefPubMedGoogle Scholar
  36. 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 43:569–575CrossRefGoogle Scholar
  37. Raphael DO, Nobel PS (1986) Growth and survivorship of ramets and seedlings of Agave deserti: influences of parent-ramet connections. Bot Gaz 147:78–83CrossRefGoogle Scholar
  38. Robert ML, Herrera JL, Contreras F, Scorer KN (1987) In vitro propagation of Agave fourcroydes Lem.(Henequen). Plant Cell Tiss Org Cult 8:37–48CrossRefGoogle Scholar
  39. Salisbury FB, Ross CW (1992) Plant physiology. 4th edition, Wadsworth, Belmont, USAGoogle Scholar
  40. Sánchez-Marroquín A, Hope PH (1953) Agave juice: Fermentation and chemical composition studies of some species. J Agric Food Chem 1:246–249CrossRefGoogle Scholar
  41. Santacruz-Ruvalcaba F, Gutiérrez-Pulido H, Rodríguez-Garay B (1999) Efficient in vitro propagation of Agave parrasana Berger. Plant Cell Tiss Org Cult 56:163–167CrossRefGoogle Scholar
  42. Shraiman BI (2005) Mechanical feedback as a possible regulator of tissue growth. Proc Natl Acad Sci U S A 102:3318–3323CrossRefPubMedGoogle Scholar
  43. 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 122:967–976CrossRefPubMedGoogle Scholar
  44. 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 64:1075–1078PubMedGoogle Scholar
  45. Tissue D, Nobel P (1988) Parent-ramet connections in Agave deserti: influences of carbohydrates on growth. Oecologia (Berlin) 75:266–271CrossRefGoogle Scholar
  46. 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 42:336–340CrossRefGoogle Scholar
  47. 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 51:1555–1562CrossRefPubMedGoogle Scholar
  48. 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 98:97–100CrossRefPubMedGoogle Scholar
  49. Wang N, Nobel P (1998) Phloem transport of fructans in the crassulacean acid metabolism species Agave deserti. Plant Physiol 116:709–714CrossRefPubMedGoogle Scholar
  50. Whalen MC, Feldman LJ (1988) The effect of ethylene on root growth of Zea mays seedlings. Can J Bot 66:719–723CrossRefPubMedGoogle Scholar
  51. Young IM, Montagu K, Conroy J, Bengough AG (1997) Mechanical impedance of root growth directly reduces leaf elongation rates of cereals. New Phytol 135:613–619CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Departamento de Biología Molecular de Plantas, Instituto de BiotecnologíaUniversidad Nacional Autónoma de MéxicoCuernavacaMexico
  2. 2.Facultad de CienciasUniversidad Autónoma del Estado de MorelosCuernavacaMexico

Personalised recommendations