Skip to main content
Log in

Axillary bud development in pineapple nodal segments correlates with changes on cell cycle gene expression, hormone level, and sucrose and glutamate contents

  • Developmental Biology
  • Published:
In Vitro Cellular & Developmental Biology - Plant Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

During the process of lateral organ development after plant decapitation, cell division and differentiation occur in a balanced manner initiated by specific signaling, which triggers the reentrance into the cell cycle. Here, we investigated short-term variations in the content of some endogenous signals, such as auxin, cytokinins (Cks), and other mitogenic stimuli (sucrose and glutamate), which are likely correlated with the cell cycle reactivation in the axillary bud primordium of pineapple nodal segments. Transcript levels of cell cycle-associated genes, CycD2;1, and histone H2A were analyzed. Nodal segments containing the quiescent axillary meristem cells were cultivated in vitro during 24 h after the apex removal and de-rooting. From the moment of stem apex and root removal, decapitated nodal segment (DNS) explants showed a lower indol-3-acetic acid (IAA) concentration than control explants, and soon after, an increase of endogenous sucrose and iP-type Cks were detected. The decrease of IAA may be the primary signal for cell cycle control early in G1 phase, leading to the upregulation of CycD2;1 gene in the first h. Later, the iP-type Cks and sucrose could have triggered the progression to S-phase since there was an increase in H2A expression at the eighth h. DNS explants revealed substantial increase in Z-type Cks and glutamate from the 12th h, suggesting that these mitogens could also operate in promoting pineapple cell cycle progression. We emphasize that the use of non-synchronized tissue rather than synchronous cell suspension culture makes it more difficult to interpret the results of a dynamic cell division process. However, pineapple nodal segments cultivated in vitro may serve as an interesting model to shed light on apical dominance release and the reentrance of quiescent axillary meristem cells into the cell cycle.

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.

Figure 1.
Figure 2.
Figure 3.
Figure 4.

Similar content being viewed by others

References

  • Balibrea L. M. E.; Gonzales Garcia M. C.; Fatima T.; Ehness R.; Lee T. K.; Tanner W.; Roitsch T. Extracellular invertase is an essential component of cytokinin-mediated delay of senescence. Plant Cell 16: 1276–1287; 2004.

    Article  Google Scholar 

  • Bredmose N.; Kristiansen K.; Norbaek R.; Christensen L. P.; Hansen-Moller J. Changes in concentrations in root and axillary bud tissue of miniature rose suggest that local Ck biosynthesis and zeatin-type Cks play important roles in axillary bud growth. J. Plant Regul. 24: 238–250; 2005.

    Article  CAS  Google Scholar 

  • TJr C.; Figueira A. Serial analysis of gene expression in sugarcane (Saccharum spp.) leaves revealed alternative C4 metabolism and putative antisense transcripts. Plant Mol. Biol. 63: 745–762; 2007.

    Article  Google Scholar 

  • Cline M. G. Concepts and terminology of apical dominance. Am. J. Bot. 84: 1064–1069; 1997.

    Article  Google Scholar 

  • Coruzzi G. M.; Bush D. R. Nitrogen and carbon: nutrient and metabolite signaling in plants. Plant Physiol. 125: 61–64; 2001.

    Article  CAS  PubMed  Google Scholar 

  • Dubois M.; Gilles A.; Hamilton J. K.; Rebers P. A.; Simith F. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28: 350–355; 1956.

    Article  CAS  Google Scholar 

  • Endres L.; Souza B. M.; Mercier H. In vitro nitrogen nutrition and hormonal pattern in bromeliads. In Vitro Cell. Dev. Biol., Plant 38: 481–486; 2002.

    CAS  Google Scholar 

  • Forde B. G.; Lea P. J. Glutamate in plants: metabolism, regulation, and signaling. J. Exp. Bot. 58: 2339–2358; 2007.

    Article  CAS  PubMed  Google Scholar 

  • Francis D.; Sorrell D. A. The interface between the cell cycle and plant growth regulators: a mini review. Plant Growth Regul. 33: 1–12; 2001.

    Article  CAS  Google Scholar 

  • Gegas V. C.; Doonan J. H. Expression of cell cycle genes in shoot apical meristems. Plant Mol. Biol. 60: 947–961; 2006.

    Article  CAS  PubMed  Google Scholar 

  • Gould A. R.; Everett N. P.; Wang T. L.; Street H. E. Studies on the control of the cell cycle in cultured plants. I. Effects on nutrient limitation and nutrient starvation. Protoplasma 106: 1–13; 1981.

    Article  CAS  Google Scholar 

  • Hartig K.; Beck E. Crosstalk between auxin, cytokinin, and sugars in the plant cell cycle. Plant Biol. 8: 389–396; 2006.

    Article  CAS  PubMed  Google Scholar 

  • Horta A. C.; Sodek L. Free amino acids and storage protein composition of soybean fruit explants and isolated cotyledons cultured with and without methionine. Ann. Bot. 79: 547–552; 1997.

    Article  CAS  Google Scholar 

  • Horvath D. P.; Anderson J. V.; Chao W. S.; Foley M. E. Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci. 8: 534–540; 2003.

    Article  CAS  PubMed  Google Scholar 

  • Joyce S. M.; Cassells A. C.; Jain S. M. Stress and aberrant phenotypes in in vitro culture. Plant Cell Tissue Organ Cult. 74: 103–121; 2003.

    Article  CAS  Google Scholar 

  • Koch K. E. Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr. Opin. Plant Biol. 7: 235–246; 2004.

    Article  CAS  PubMed  Google Scholar 

  • Lam H.-M.; Chiu J.; Hsieh M.-H.; Meiesel L.; Oliveira I. C.; Shin M.; Coruzzi G. Glutamate-receptor genes in plants. Nature 396: 125–126; 1998.

    Article  CAS  PubMed  Google Scholar 

  • Leyser O. Regulation of shoot branching by auxin. Trends Plant Sci. 8: 541–545; 2003.

    Article  CAS  PubMed  Google Scholar 

  • Li C.-J.; Guevara E.; Herrera J.; Bangerth F. Effect of apex excision and replacement by 1-naphthylacetic acid on cytokinin concentration and apical dominance in pea plants. Physiol Plant 94: 465–469; 1995.

    Article  CAS  Google Scholar 

  • McCready R. M.; Guggolzs J.; Silveira V.; Owens H. S. Determination of starch and amylose in vegetables -application to peas. Anal. Chem. 22: 1156–1158; 1950.

    Article  CAS  Google Scholar 

  • Meijer M.; Murray J. A. H. Cell cycle controls and the development of plant form. Curr. Opin. Plant Biol. 4: 44–49; 2001.

    Article  CAS  PubMed  Google Scholar 

  • Mercier H.; Endres L. Alteration of hormonal levels in a rootless epiphytic bromeliad in different phenological phases. J. Plant Growth Regul. 18: 121–125; 1999.

    Article  CAS  PubMed  Google Scholar 

  • Meshi T.; Taoka K.; Iwabuchi M. Regulation of histone gene expression during the cell cycle. Plant Mol. Biol. 43: 643–657; 2000.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ongaro V.; Leyser O. Hormonal control of shoot branching. J. Exp. Bot. 59: 67–74; 2008.

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl M. W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29: 2002–2007; 2001.

    Article  Google Scholar 

  • Pfaffl M. W.; Tichopád A.; Prgomet C.; Neuvians T. P. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper—Excel-based tool using pair-wise correlations. Biotechnol. Lett. 26: 509–515; 2004.

    Article  CAS  PubMed  Google Scholar 

  • Pischke M. S.; Huttlin E. L.; Hegeman A. D.; Sussman M. R. A transcriptome-based characterization of habituation in plant tissue culture. Plant Physiol. 140: 1255–1278; 2006.

    Article  CAS  PubMed  Google Scholar 

  • Pollock C. G.; Jones T. Seasonal patterns of fructan metabolism in forage grasses. New Phytol. 83: 8–15; 1979.

    Article  Google Scholar 

  • Richard C.; Lescot M.; Inzé D.; De Veylder L. Effects of auxin, cytokinin, and sucrose on cell cycle gene expression in Arabidopsis thaliana cell suspension cultures. Plant Cell Tissue Organ Cult. 69: 167–176; 2002.

    Article  CAS  Google Scholar 

  • Riou-Khamlichi C.; Huntley R.; Jacqmard A.; Murray J. A. H. Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283: 1541–1544; 1999.

    Article  CAS  PubMed  Google Scholar 

  • Roitsch T.; Ehness R. Regulation of source/sink relations by cytokinins. Plant Growth Regul. 32: 359–367; 2000.

    Article  CAS  Google Scholar 

  • Rolland F.; Baena-Gonzalez E.; Sheen J. Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu. Rev. Plant Biol. 57: 675–709; 2006.

    Article  CAS  PubMed  Google Scholar 

  • Santos H. P.; Purgato E.; Mercier H.; Buckeridge M. S. The control of storage xyloglucan mobilization in cotyledons of Hymenaea courbaril L. Plant Physiol. 135: 287–299; 2004.

    Article  PubMed  Google Scholar 

  • Shen W. H. The plant E2F-Rb pathway and epigenetic control. Trends Plant Sci. 7: 505–511; 2002.

    Article  CAS  PubMed  Google Scholar 

  • Soni R.; Carmichael J. P.; Shah Z. H.; Murray J. A. A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell 7: 85–103; 1995.

    Article  CAS  PubMed  Google Scholar 

  • Souza B. M.; Kraus J. E.; Endres L.; Mercier H. Relantionships between endogenoous hormonal and axillary bud development of Ananas comosus nodal segments. Plant Physiol. Biochem. 41(7): 33–739; 2003.

    Google Scholar 

  • Stancato G. C.; Mazzafera P.; Buckeridge M. S. Effect of drought period on the mobilization of non-structural carbohydrates photosynthetic efficiency and water status in epiphytic orchid. Plant Physiol. Biochem. 39: 1009–1016; 2001.

    Article  CAS  Google Scholar 

  • Tanaka M.; Takei K.; Kojima M.; Sakakibara H.; Mori H. Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. Plant J. 45: 1028–1036; 2006.

    Article  CAS  PubMed  Google Scholar 

  • Turano F. J.; Muhitch M. J.; Felker F. C.; McMahon M. B. The putative glutamate receptor from Arabidopsis thaliana (AtGLR3 2) is an integral membrane peptide that accumulates in rapidly growing tissues and persists in vascular-associated tissues. Plant Sci. 163: 43–51; 2002.

    Article  CAS  Google Scholar 

  • Uemukai K.; Iwakawa H.; Kosugi S.; de Jager S.; Kato K.; Kondorosi E.; Murray J. A. H.; Ito M.; Shinmyo A.; Sekine M. Transcriptional activation of tobacco E2F is repressed by co-transfection with the retinoblastoma-related protein: cyclin D expression overcomes this repressor activity. Plant Mol. Biol. 57: 83–100; 2005.

    Article  CAS  PubMed  Google Scholar 

  • Watson J. D.; Baker T. A.; Bell S. P.; Gann A.; Levine M.; Losick R. Molecular biology of the gene. Pearson-Benjamin Cummings, CA; 2008.

    Google Scholar 

  • Yemm E. M.; Coking E. C. Estimation of amino acid by ninhydrin. Analyst 80: 209–213; 1955.

    Article  CAS  Google Scholar 

  • Zhang S.; Lemaux P. G. Molecular analysis of in vitro shoot organogenesis. Crit. Rev. Plant Sci. 23: 325–335; 2004.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank FAPESP (02/2669-2) for the financial support awarded to Beatriz Maia Souza and CNPq (303715/2004-9) for the grant to Helenice Mercier.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Helenice Mercier.

Additional information

Editor: D. T. Tomes

Rights and permissions

Reprints and permissions

About this article

Cite this article

Souza, B.M., Molfetta-Machado, J.B., Freschi, L. et al. Axillary bud development in pineapple nodal segments correlates with changes on cell cycle gene expression, hormone level, and sucrose and glutamate contents. In Vitro Cell.Dev.Biol.-Plant 46, 281–288 (2010). https://doi.org/10.1007/s11627-009-9276-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11627-009-9276-9

Keywords

Navigation