Skip to main content

Active telomerase during leaf growth and increase of age in plants from Agave tequilana var. Azul

Abstract

In plants, previous studies show that telomerase activity contributes to the maintenance of telomeric length for the proper development of organs and tissues. In this work, we investigated telomerase activity in A. tequilana during several years of cultivation. We found that during growth of the leaf there are two crucial phases: (1) the onset of cell elongation in 3 years and (2) differentiation of vascular bundles in 6 years. This coincides with the ages where the highest telomerase activity is seen. Therefore indicates that telomerase is associated with cellular activities such as; elongation, division, and cell differentiation. Likewise, we detected high activity during the period of vegetative growth, indicating that telomerase also contributes to telomeric maintenance on the leaf in A. tequilana.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Abbreviations

TRAP assay:

Telomerase repeated amplification protocol

qTRAP assay:

Quantitative telomerase repeated amplification protocol

A. tequilana :

Agave tequilana var. Azul

IA:

Internal apical region

References

  1. Campanoni P, Nick P (2005) Auxin-dependent cell division and cell elongation. 1-naphthaleneacetic acid and 2,4-dichlorophenoxyacetic acid activate different pathways. Plant Physiol 137:939–948. https://doi.org/10.1104/pp.104.053843.involvement

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. Cho KH, Jun SE, Jeong SJ et al (2007) Developmental processes of leaf morphogenesis in Arabidopsis. J Plant Biol 50:282–290. https://doi.org/10.1007/bf03030656

    CAS  Article  Google Scholar 

  3. Dodd AN, Borland AM, Haslam RP et al (2002) Crassulacean acid metabolism: plastic, fantastic. J Exp Bot 53:569–580

    CAS  Article  Google Scholar 

  4. Fajkus J, Kovarík A, Královics R (1996) Telomerase activity in plant cells. FEBS Lett 391:307–309. https://doi.org/10.1016/0014-5793(96)00757-0

    CAS  Article  PubMed  Google Scholar 

  5. Fajkus J, Fulnečková J, Hulánová M et al (1998) Plant cells express telomerase activity upon transfer to callus culture, without extensively changing telomere lengths. Mol Gen Genet 260:470–474. https://doi.org/10.1007/s004380050918

    CAS  Article  PubMed  Google Scholar 

  6. Fitzgerald MS, McKnight TD, Shippen DE (1996) Characterization and developmental patterns of telomerase expression in plants. Proc Natl Acad Sci USA 93:14422–14427. https://doi.org/10.1073/pnas.93.25.14422

    CAS  Article  PubMed  Google Scholar 

  7. Flanary BE, Kletetschka G (2005) Analysis of telomere length and telomerase activity in tree species of various life-spans, and with age in the bristlecone pine Pinus longaeva. Biogerontology 6:101–111. https://doi.org/10.1007/s10522-005-3484-4

    CAS  Article  PubMed  Google Scholar 

  8. Flores I, Cayuela ML, Blasco MA (2005) Molecular biology: effects of telomerase and telomere length on epidermal stem cell behavior. Science 309(80):1253–1256. https://doi.org/10.1126/science.1115025

    Article  PubMed  Google Scholar 

  9. Gomes NMV, Ryder OA, Houck ML et al (2011) Comparative biology of mammalian telomeres: hypotheses on ancestral states and the roles of telomeres in longevity determination. Aging Cell 10:761–768. https://doi.org/10.1111/j.1474-9726.2011.00718.x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Gonzalez N, De Bodt S, Sulpice R et al (2010) Increased leaf size: different means to an end. Plant Physiol 153:1261–1279. https://doi.org/10.1104/pp.110.156018

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. González-García MP, Pavelescu I, Canela A et al (2015) Single-cell telomere-length quantification couples telomere length to meristem activity and stem cell development in Arabidopsis. Cell Rep. https://doi.org/10.1016/j.celrep.2015.04.013

    Article  PubMed  PubMed Central  Google Scholar 

  12. Greider CW (1991) Telomeres. Curr Opin Cell Biol 3:444–451. https://doi.org/10.1016/0955-0674(91)90072-7

    CAS  Article  PubMed  Google Scholar 

  13. Greider CW (2010) Telomerase discovery: the excitement of putting together pieces of the puzzle (Nobel lecture). Angew Chem Int Ed 49:7422–7439. https://doi.org/10.1002/anie.201002408

    CAS  Article  Google Scholar 

  14. Greider CW, Blackburn EH (1985) Identification of a specific telomere terminal transferase activity in tetrahymena extracts. Cell 43:405–413. https://doi.org/10.1016/0092-8674(85)90170-9

    CAS  Article  PubMed  Google Scholar 

  15. Heacock ML, Idol RA, Friesner JD et al (2007) Telomere dynamics and fusion of critically shortened telomeres in plants lacking DNA ligase IV. Nucleic Acids Res 35:6490–6500. https://doi.org/10.1093/nar/gkm472

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Heller K, Kilian A, Piatyszek MA, Kleinhofs A (1996) Telomerase activity in plant extracts. Mol Gen Genet 252:342–345

    CAS  Article  Google Scholar 

  17. Horiguchi G, Tsukaya H (2011) Organ size regulation in plants: insights from compensation. Front Plant Sci 2:1–6. https://doi.org/10.3389/fpls.2011.00024

    Article  Google Scholar 

  18. Horiguchi G, Kim GT, Tsukaya H (2005) The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J 43:68–78. https://doi.org/10.1111/j.1365-313X.2005.02429.x

    CAS  Article  PubMed  Google Scholar 

  19. Horiguchi G, Ferjani A, Fujikura U, Tsukaya H (2006) Coordination of cell proliferation and cell expansion in the control of leaf size in Arabidopsis thaliana. J Plant Res 119:37–42. https://doi.org/10.1007/s10265-005-0232-4

    Article  PubMed  Google Scholar 

  20. Ismail AM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3

    Article  Google Scholar 

  21. Killan A, Heller K, Kleinhofs A (1998) Development patterns of telomerase activity in barley and maize. Plant Mol Biol 37:621–628. https://doi.org/10.1023/A:1005994629814

    CAS  Article  PubMed  Google Scholar 

  22. Kuchař M, Fajkus J (2004) Interactions of putative telomere-binding proteins in Arabidopsis thaliana: Identification of functional TRF2 homolog in plants. FEBS Lett 578:311–315. https://doi.org/10.1016/j.febslet.2004.11.021

    CAS  Article  PubMed  Google Scholar 

  23. Little EL, Gentry HS (2006) Agaves of continental North America. Bull Torrey Bot Club. https://doi.org/10.2307/2996199

    Article  Google Scholar 

  24. Mencuccini M (2003) The ecological significance of long-distance water transport: short-term regulation, long-term acclimation and the hydraulic costs of stature across plant life forms. Plant Cell Environ 26:163–182. https://doi.org/10.1046/j.1365-3040.2003.00991.x

    Article  Google Scholar 

  25. Mencuccini M, Martínez-Vilalta J, Vanderklein D et al (2005) Size-mediated ageing reduces vigour in trees. Ecol Lett 8:1183–1190. https://doi.org/10.1111/j.1461-0248.2005.00819.x

    CAS  Article  PubMed  Google Scholar 

  26. Mu Y, Ren L, Hu X et al (2015) Season-specific changes in telomere length and telomerase activity in Chinese Pine (Pinus tabulaeformis Carr.). Физиoлoгия pacтeний. https://doi.org/10.7868/s0015330315040144

  27. Nelson EA, Sage TL, Sage RF (2005) Functional leaf anatomy of plants with crassulacean acid metabolism. Funct Plant Biol 2:409–419. https://doi.org/10.1071/FP04195

    Article  Google Scholar 

  28. Nicholls C, Li H, Wang JQ, Liu JP (2011) Molecular regulation of telomerase activity in aging. Protein Cell 2:726–738. https://doi.org/10.1007/s13238-011-1093-3

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. Palomino G, Dolezel J, Mèndez I, Rubluo A (2012) Nuclear genome size analysis of Agave tequilana Weber. Caryologia. https://doi.org/10.1080/00087114.2003.10589305

    Article  Google Scholar 

  30. Pérez-Núñez MT, Chan JL, Sáenz L et al (2006) Improved somatic embryogenesis from Cocos nucifera (L.) plumule explants. Vitr Cell Dev Biol Plant 42:37–43. https://doi.org/10.1079/IVP200572

    Article  Google Scholar 

  31. Procházková Schrumpfová P, Fojtová M, Fajkus J (2019) Telomeres in plants and humans: not so different, not so similar. Cells 8:58. https://doi.org/10.3390/cells8010058

    CAS  Article  PubMed Central  Google Scholar 

  32. Rescalvo-Morales A, Monja-Mio KM, Herrera-Herrera G et al (2016) Analysis of telomere length during the organogenesis induction of Agave fourcroydes Lem and Agave tequilana Weber. Plant Cell Tissue Organ Cult 127:135–143. https://doi.org/10.1007/s11240-016-1037-y

    CAS  Article  Google Scholar 

  33. Rescalvo-Morales A, Monja-Mio KM, Robert ML, Sánchez-Teyer LF (2019) Telomere length in Agave tequilana Weber plants during the in vitro to ex vitro transition. Plant Cell Tissue Organ Cult. https://doi.org/10.1007/s11240-018-1499-1

    Article  Google Scholar 

  34. Richards EJ, Ausubel FM (1988) Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell. https://doi.org/10.1016/0092-8674(88)90494-1

    Article  PubMed  Google Scholar 

  35. Riha K, Fajkus J, Siroky J, Vyskot B (1998) Developmental control of telomere lengths and telomerase activity in plants. Plant Cell 10:1691–1698. https://doi.org/10.1105/tpc.10.10.1691

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Riha K, Fajkus J, Siroky J, Vyskot B (2007) Developmental control of telomere lengths and telomerase activity in plants. Plant Cell. https://doi.org/10.2307/3870766

    Article  Google Scholar 

  37. Song H, Liu D, Chen X et al (2010) Change of season-specific telomere lengths in Ginkgo biloba L. Mol Biol Rep 37:819–824. https://doi.org/10.1007/s11033-009-9627-y

    CAS  Article  PubMed  Google Scholar 

  38. Song H, Liu D, Li F, Lu H (2011) Season- and age-associated telomerase activity in Ginkgo biloba L. Mol Biol Rep 38:1799–1805. https://doi.org/10.1007/s11033-010-0295-8

    CAS  Article  PubMed  Google Scholar 

  39. Sýkorová E, Leitch AR, Fajkus J (2006) Asparagales telomerases which synthesize the human type of telomeres. Plant Mol Biol 60:633–646. https://doi.org/10.1007/s11103-005-5091-9

    CAS  Article  PubMed  Google Scholar 

  40. Tamura K, Liu H, Takahashi H (1999) Auxin induction of cell cycle regulated activity of tobacco telomerase. J Biol Chem 274:20997–21002. https://doi.org/10.1074/jbc.274.30.20997

    CAS  Article  PubMed  Google Scholar 

  41. Valenzuela A (2011) A new agenda for blue agave landraces: food, energy and tequila. GCB Bioenergy 3:15–24. https://doi.org/10.1111/j.1757-1707.2010.01082.x

    Article  Google Scholar 

  42. Winter K, Holtum JAM, Smith JAC (2015) Tansley insight Crassulacean acid metabolism: a continuous or discrete trait? Evolution (N Y). https://doi.org/10.1038/nature12511

    Article  Google Scholar 

  43. Yang SW, Jin E, Chung IK, Kim WT (2002) Cell cycle-dependent regulation of telomerase activity by auxin, abscisic acid and protein phosphorylation in tobacco BY-2 suspension culture cells. Plant J 29:617–626. https://doi.org/10.1046/j.0960-7412.2001.01244.x

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

Dr. Antonio Rescalvo Morales and Dr. Laura Espinosa Barrera, for the technical guidance, Eva Sykorova PhD, Miloslava Fojtova PhD, Peter Fijkus PhD for academic feedback during the internship in qTRAP. This project was funded by CONACyT project CB-2012-180757-Z and by the grant awarded. We like to thank Goty Bautelpacher, owner of the hacienda “MAYAPAN” farm for the plant material.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Lorenzo Felipe Sánchez-Teyer.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 2761 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

De la Torre-Espinosa, Z.Y., Barredo-Pool, F., Castaño de la Serna, E. et al. Active telomerase during leaf growth and increase of age in plants from Agave tequilana var. Azul. Physiol Mol Biol Plants 26, 639–647 (2020). https://doi.org/10.1007/s12298-020-00781-7

Download citation

Keywords

  • Agave tequilana
  • Telomerase activity
  • Development
  • Growth
  • Leaf
  • Cell proliferation