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.
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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.
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.
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.
Cline M. G. Concepts and terminology of apical dominance. Am. J. Bot. 84: 1064–1069; 1997.
Coruzzi G. M.; Bush D. R. Nitrogen and carbon: nutrient and metabolite signaling in plants. Plant Physiol. 125: 61–64; 2001.
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.
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.
Forde B. G.; Lea P. J. Glutamate in plants: metabolism, regulation, and signaling. J. Exp. Bot. 58: 2339–2358; 2007.
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.
Gegas V. C.; Doonan J. H. Expression of cell cycle genes in shoot apical meristems. Plant Mol. Biol. 60: 947–961; 2006.
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.
Hartig K.; Beck E. Crosstalk between auxin, cytokinin, and sugars in the plant cell cycle. Plant Biol. 8: 389–396; 2006.
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.
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.
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.
Koch K. E. Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr. Opin. Plant Biol. 7: 235–246; 2004.
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.
Leyser O. Regulation of shoot branching by auxin. Trends Plant Sci. 8: 541–545; 2003.
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.
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.
Meijer M.; Murray J. A. H. Cell cycle controls and the development of plant form. Curr. Opin. Plant Biol. 4: 44–49; 2001.
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.
Meshi T.; Taoka K.; Iwabuchi M. Regulation of histone gene expression during the cell cycle. Plant Mol. Biol. 43: 643–657; 2000.
Murashige T.; Skoog F. A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant. 15: 473–497; 1962.
Ongaro V.; Leyser O. Hormonal control of shoot branching. J. Exp. Bot. 59: 67–74; 2008.
Pfaffl M. W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29: 2002–2007; 2001.
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.
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.
Pollock C. G.; Jones T. Seasonal patterns of fructan metabolism in forage grasses. New Phytol. 83: 8–15; 1979.
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.
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.
Roitsch T.; Ehness R. Regulation of source/sink relations by cytokinins. Plant Growth Regul. 32: 359–367; 2000.
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.
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.
Shen W. H. The plant E2F-Rb pathway and epigenetic control. Trends Plant Sci. 7: 505–511; 2002.
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.
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.
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.
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.
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.
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.
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.
Yemm E. M.; Coking E. C. Estimation of amino acid by ninhydrin. Analyst 80: 209–213; 1955.
Zhang S.; Lemaux P. G. Molecular analysis of in vitro shoot organogenesis. Crit. Rev. Plant Sci. 23: 325–335; 2004.
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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.
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Editor: D. T. Tomes
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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
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DOI: https://doi.org/10.1007/s11627-009-9276-9