Skip to main content
Log in

Type II metacaspase protein localization and gene transcription during programmed cell semi-death of sieve elements in developing caryopsis of Tritium aestivum

  • Published:
Biologia Aims and scope Submit manuscript

Abstract

Metacaspases are cysteine-dependent proteases essential in plant PCD. This study focused on PCD features, the metacaspase II protein (TaeMCAII) and its gene expression and dynamic distribution during the developmental process of wheat sieve elements (SEs). Our results showed that the SEs experienced enucleation, inclusion loss, cell wall thickening and decreased cytosol density during their development. The RT-qPCR and in situ hybridization showed that the transcriptional levels of TaeMCAII in the development of SEs increased to high levels 3 days after flowering (DAF), then decreased, but then sharply increased at 7 DAF. Immunohistochemical observations revealed dynamic changes of TaeMCAII at the protein level. TaeMCAII was primarily detected at 3 DAF, 4 DAF and 7 DAF, which indicated that TaeMCAII played an important role during these stages. Immunoelectron microscopy showed that TaeMCAII was first localized in the nucleus, then in the cell cytoplasm, and finally on the cell membranes and cell walls of late-stage SEs. Our study found that TaeMCAII was key in the PCD-like process of the development of SEs.

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.

Similar content being viewed by others

References

  • Bozhkov P.V., Smertenko A.P. & Zhivotovsky B. 2010. Aspasing out metacaspases and caspases: proteases of many trades. Sci. Signal. 3: 48.

    Article  Google Scholar 

  • Bozhkov P.V., Suarez M.F., Filonova L.H., Daniel G., Zamyatnin A.A., Rodriguez-Nieto J.S., Zhivotovsky B. & Smertenko A. 2005. Cysteine protease mcII-Pa executes programmed cell death during plant embryogenesis. Proc. Natl. Acad. Sci. USA 102: 14463–14468.

    Article  CAS  Google Scholar 

  • Cai J.T., Zhang Z.H., Zhou Z.Q., Yang W.L, Liu Y., Mei F.Z., Zhou G.S. & Wang L.K. 2015. Localization of BEN1-LIKE protein and nuclear degradation during development of metaphloem sieve elements in Triticum aestivum L. Acta Biol. Hung. 66: 66–79.

    Article  CAS  Google Scholar 

  • Castillo-Olamendi L., Bravo-García A., Morán J., Rocha-Sosa M. & Porta H. 2007. AtMCP1b, a chloroplast-localised metacaspase, is induced in vascular tissue after wounding or pathogen infection. Funct. Plant Biol. 34: 1061–1071.

    Article  CAS  Google Scholar 

  • Choi C.J. & Berges J.A. 2013. New types of metacaspases in phytoplankton reveal diverse origins of cell death proteases. Cell Death Differ. 4: e490.

    Article  CAS  Google Scholar 

  • Coll N.S., Vercammen D., Smidler A., Clover C., Van Breusegem F., Dangl J.L. & Epple P. 2010. Arabidopsistype I metacaspases control cell death. Science 330: 1393–1397.

    Article  CAS  Google Scholar 

  • Earnshaw W.C., Martins L.M. & Kaufmann S.H. 1999. Mammalian caspases: structure, activation, substrates and functions during apoptosis. Annu. Rev. Biochem. 68: 383–424.

    Article  CAS  Google Scholar 

  • Gan S. & Amasino R.M. 1997. Making sense of senescence. Molecular genetic regulation and manipulation of leaf senescence. Plant Physiol. 113: 313–319.

    Article  CAS  Google Scholar 

  • Guo Y.J. 2013. Influence of Caspase 3-like proteases on programmed cell death of endosperm cells in winter wheat (Triticum aestivum L.) under waterlogging. Dissertation, Huazhong Agricult Univ, China.

    Google Scholar 

  • Hao X., Qian J., Xu S., Song X. & Zhu J. 2008. Location f caspase 3-like protease in the development of sieve element and tracheary element of stem in Cucurbita moschata. J. Integ. Plant Biol. 50: 1499–1507.

    Article  Google Scholar 

  • He R., Drury G.E., Rotari V.I., Gordon A., Willer M., Farzaneh T., Woltering E.J. & Gallois P. 2008. Metacaspase-8 modulates programmed cell death induced by ultraviolet light and H2O2 in Arabidopsis. J. Biol. Chem. 283: 774–783.

    Article  CAS  Google Scholar 

  • Jones A.M. 2001. Programmed cell death in development and defense. Plant Physiol. 125: 94–97.

    Article  CAS  Google Scholar 

  • Jones A.M. & Dangl J.L. 1996. Logiam at the Styx: Programmed cell death in plants. Trends Plant Sci. 1: 114–119.

    Article  Google Scholar 

  • Jones D.P., McConkey D.J., Nieotera P. & Orrenius S. 1989. Caleium-activated DNA fragmentation in rat liver nuclei. J. Biol. Chem. 264: 6398–640.

    CAS  PubMed  Google Scholar 

  • Li J.W. 2009. Locaization of Ca2+ and related enzymes in phloem in the developing caryopsis of Triticum aestivum L. Dissertation, Huazhong Agricult. Univ., China.

    Google Scholar 

  • McLuskey K., Rudolf J., Proto W.R., Isaacs N.W., Coombs G.H., Moss C.X. & Mottram J. C. 2012. Crystal structure of a Trypanosoma brucei metacaspase. Proc. Natl. Acad. Sci. USA 109: 7469–7474.

    Article  CAS  Google Scholar 

  • Møller S.G. & McPherson M.J. 1998. Developmental expression and biochemical analysis of the Arabidopsis atao1 gene encoding an H2O2-generating diamine oxidase. Plant J. 13: 781–791.

    Article  Google Scholar 

  • Pennell R.I. & Lamb C. 1997. Programmed cell death in plants. Plant Cell 9: 1157–1168.

    Article  CAS  Google Scholar 

  • Piszczek E., Dudkiewicz M. & Mielecki M. 2012. Biochemical and bioinformatic characterization of type II metacaspase protein (TaeMCAII) from wheat. Plant Mol. Biol. Rep. 30: 1338–1347.

    Article  CAS  Google Scholar 

  • Piszczek E., Dudkiewicz M. & Sobczak M. 2011. Molecular cloning and phylogenetic analysis of cereal type II metacas-pase cDNA from wheat. Biol. Plantarum 55: 614–624.

    Article  CAS  Google Scholar 

  • Piszczek E. & Gutman W. 2007. Caspase-like proteases and their role in programmed cell death in plants. Acta Physiol. Plant. 29: 391–398.

    Article  CAS  Google Scholar 

  • Richard D.S. 1997. The phloem sieve element: a river runs through it. Plant Cell 9: 1137–1146.

    Google Scholar 

  • Sanmartin M., Jaroszewski L., Raikhel N.V. & Rojo E. 2005. Caspases. Regulating death since the origin of life. Plant Physiol. 137: 841–847.

    Article  CAS  Google Scholar 

  • Suarez M.F., Filonova L.H., Smertenko A., Savenkov E.I., Clapham D.H., Von Arnold S., Zhivotovsky B. & Bozhkov P.V. 2004. Metacaspase dependent programmed cell death is essential for plant embryogenesis. Curr. Biol. 14: 339–340.

    Article  Google Scholar 

  • Sun Y. 1998. Progress in calcium signaling of the cell nuclei. Plant Biol. 20: 133–137.

    Google Scholar 

  • Tsiatsiani L., Van Breusegem F., Gallois P., Zavialov A., Lam E. & Bozhkov P.V. 2011. Metacaspases. Cell Death Differ. 18: 1279–1288.

    Article  CAS  Google Scholar 

  • Uren A.G.O., Rourke K. & Aravind L.A. et al. 2000. Identification of Paracaspases and Metacaspase: two ancient families of Caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol. Cell. 6: 961–967.

    CAS  PubMed  Google Scholar 

  • Van Bel A.J.E. 2003. The phloem, a miracle of ingenuity. Plant Cell Environ. 26: 125–149.

    Article  Google Scholar 

  • Wang L.K., Zhou Z.Q., Song X.F., Li J.W., Deng X.X. & Mei F. Z. 2008. Evidence of ceased programmed cell death in metaphloem sieve elements in the developing caryopsis of Triticum aestivum L. Protoplasma 234: 87–96.

    Article  Google Scholar 

  • Wang M., Oppedijk B.J., Lu X., Van Duijn B. & Schilperoort R.A. 1996b. Apoptosis in barley aleurone during germination and its inhibition by abscisic acid. Plant Mol. Biol. 32: 1125–1134.

    Article  CAS  Google Scholar 

  • Watanabe N. & Lam E. 2011a. Arabidopsis metacaspase 2d is a positive mediator of cell death induced during biotic and abiotic stresses. Plant J. 66: 969–982.

    Article  CAS  Google Scholar 

  • Watanabe N. & Lam E. 2011b. Calcium-dependent activation and autolysis of Arabidopsis metacaspase 2d. J Bio. Chem. 286: 10027–10040.

    CAS  Google Scholar 

  • Wong A.H.H., Yan C. & Shi Y. 2012. Crystal structure of the yeast metacaspase Yca1. J. Biol. Chem. 287: 29251–29259.

    Article  CAS  Google Scholar 

  • Xu Q.T., Yang L., Zhou Z.Q., Mei F.Z., Qu L.H. & Zhou G.S. 2013. Process of aerenchyma formation and reactive oxygen species induced by waterlogging in wheat seminal roots. Planta 238: 969–982.

    Article  CAS  Google Scholar 

  • Yang W.L. 2013. Study on Programmed Cell Semi-Death of Sieve Elements in Root and Developing Caryopsis of Triticum aestivum L. Dissertation, Huazhong Agricult. Univ., China.

    Google Scholar 

  • Zhang X., Coté G. & Crain R. 2002. Involvement of phosphoinositide turnover in tracheary element differentiation in Zinnia elegans L. cells. Planta 215: 312–318.

    Article  CAS  Google Scholar 

  • Zhang Y. & Lam E. 2011. Sheathing the swords of death. Post-translational modulation of plant metacaspases. Plant Signal Behav. 6: 2051–2056.

    Article  CAS  Google Scholar 

  • Zhou Z.Q., Lan S.Y., Zhu X.T., Wang W.J. & Xu Z.X. 2004. Utrastructure and its function of phloem cell in abdominal vascular bundle of wheat caryopsis. Acta Agron. Sin. 30: 163–168.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhuqing Zhou.

Supplementary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Z., Lv, Y., Zhou, Z. et al. Type II metacaspase protein localization and gene transcription during programmed cell semi-death of sieve elements in developing caryopsis of Tritium aestivum. Biologia 72, 398–406 (2017). https://doi.org/10.1515/biolog-2017-0041

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1515/biolog-2017-0041

Key words

Navigation