Environmentally Induced Programmed Cell Death in Leaf Protoplasts of Aponogeton Madagascariensis

Overview

Journal Planta

Specialty Biology

Date 2010 Nov 11

PMID 21063887

Citations 13

Authors

Christina E N Lord

Arunika H L A N Gunawardena

Affiliations

Soon will be listed here.

Abstract

Within plant systems, two main forms of programmed cell death (PCD) exist: developmentally regulated and environmentally induced. The lace plant (Aponogeton madagascariensis) naturally undergoes developmentally regulated PCD to form perforations between longitudinal and transverse veins over its leaf surface. Developmental PCD in the lace plant has been well characterized; however, environmental PCD has never before been studied in this plant species. The results presented here portray heat shock (HS) treatment at 55 °C for 20 min as a promising inducer of environmental PCD within lace plant protoplasts originally isolated from non-PCD areas of the plant. HS treatment produces cells displaying many characteristics of developmental PCD, including blebbing of the plasma membrane, increased number of hydrolytic vesicles and transvacuolar strands, nuclear condensation, terminal deoxynucleotidyl transferase-mediated dUTP nick-end labeling positive nuclei, as well as increased Brownian motion within the vacuole. Results presented here for the first time provide evidence of chloroplasts in the vacuole of living protoplasts undergoing environmentally induced PCD. Findings suggest that the mitochondria play a critical role in the cell death process. Changes in mitochondrial dynamics were visualized in HS-treated cells, including loss of mitochondrial mobility, reduction in ΔΨ(m), as well as the proximal association with chloroplasts. The role of the mitochondrial permeability transition pore (PTP) was examined by pre-treatment with the PTP agonist cyclosporine A. Overall, HS is depicted as a reliable method to induce PCD within lace plant protoplasts, and proves to be a reliable technique to enable comparisons between environmentally induced and developmentally regulated PCD within one species of plant.

Citing Articles

The role of Atg16 in autophagy, anthocyanin biosynthesis, and programmed cell death in leaves of the lace plant (Aponogeton madagascariensis).

Rowarth N, Dauphinee A, Lacroix C, Gunawardena A PLoS One. 2023; 18(2):e0281668.

PMID: 36795694 PMC: 9934333. DOI: 10.1371/journal.pone.0281668.

Insights into Plant Programmed Cell Death Induced by Heavy Metals-Discovering a .

Sychta K, Slomka A, Kuta E Cells. 2021; 10(1).

PMID: 33406697 PMC: 7823951. DOI: 10.3390/cells10010065.

EDS1-Dependent Cell Death and the Antioxidant System in Leaves is Deregulated by the Mammalian Bax.

Bernacki M, Czarnocka W, Zaborowska M, Rozanska E, Labudda M, Rusaczonek A Cells. 2020; 9(11).

PMID: 33182774 PMC: 7698216. DOI: 10.3390/cells9112454.

Caspases in plants: metacaspase gene family in plant stress responses.

Fagundes D, Bohn B, Cabreira C, Leipelt F, Dias N, Bodanese-Zanettini M Funct Integr Genomics. 2015; 15(6):639-49.

PMID: 26277721 DOI: 10.1007/s10142-015-0459-7.

A comparison of induced and developmental cell death morphologies in lace plant (Aponogeton madagascariensis) leaves.

Dauphinee A, Warner T, Gunawardena A BMC Plant Biol. 2014; 14:389.

PMID: 25547402 PMC: 4302576. DOI: 10.1186/s12870-014-0389-x.

References

Minamikawa T, Toyooka K, Okamoto T, Hara-Nishimura I, Nishimura M . Degradation of ribulose-bisphosphate carboxylase by vacuolar enzymes of senescing French bean leaves: immunocytochemical and ultrastructural observations. Protoplasma. 2002; 218(3-4):144-53. DOI: 10.1007/BF01306604. View

Ryerson D, Heath M . Cleavage of Nuclear DNA into Oligonucleosomal Fragments during Cell Death Induced by Fungal Infection or by Abiotic Treatments. Plant Cell. 1996; 8(3):393-402. PMC: 161108. DOI: 10.1105/tpc.8.3.393. View

Gunawardena A, Pearce D, Jackson M, Hawes C, Evans D . Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta. 2001; 212(2):205-14. DOI: 10.1007/s004250000381. View

Mittler R, Lam E . Characterization of nuclease activities and DNA fragmentation induced upon hypersensitive response cell death and mechanical stress. Plant Mol Biol. 1997; 34(2):209-21. DOI: 10.1023/a:1005868402827. View

Joza N, Susin S, Daugas E, Stanford W, Cho S, Li C . Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature. 2001; 410(6828):549-54. DOI: 10.1038/35069004. View

Wittenbach V, Lin W, Hebert R . Vacuolar localization of proteases and degradation of chloroplasts in mesophyll protoplasts from senescing primary wheat leaves. Plant Physiol. 1982; 69(1):98-102. PMC: 426153. DOI: 10.1104/pp.69.1.98. View

Gunawardena A . Programmed cell death and tissue remodelling in plants. J Exp Bot. 2007; 59(3):445-51. DOI: 10.1093/jxb/erm189. View

Fukuda H . Programmed cell death of tracheary elements as a paradigm in plants. Plant Mol Biol. 2001; 44(3):245-53. DOI: 10.1023/a:1026532223173. View

Zamzami N, Marchetti P, Castedo M, Zanin C, Vayssiere J, Petit P . Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J Exp Med. 1995; 181(5):1661-72. PMC: 2192017. DOI: 10.1084/jem.181.5.1661. View

10.

Iakimova E, Woltering E, Kapchina-Toteva V, Harren F, Cristescu S . Cadmium toxicity in cultured tomato cells--role of ethylene, proteases and oxidative stress in cell death signaling. Cell Biol Int. 2008; 32(12):1521-9. DOI: 10.1016/j.cellbi.2008.08.021. View

11.

Reape T, McCabe P . Apoptotic-like programmed cell death in plants. New Phytol. 2008; 180(1):13-26. DOI: 10.1111/j.1469-8137.2008.02549.x. View

12.

Danon A, Gallois P . UV-C radiation induces apoptotic-like changes in Arabidopsis thaliana. FEBS Lett. 1998; 437(1-2):131-6. DOI: 10.1016/s0014-5793(98)01208-3. View

13.

Vacca R, Valenti D, Bobba A, Merafina R, Passarella S, Marra E . Cytochrome c is released in a reactive oxygen species-dependent manner and is degraded via caspase-like proteases in tobacco Bright-Yellow 2 cells en route to heat shock-induced cell death. Plant Physiol. 2006; 141(1):208-19. PMC: 1459318. DOI: 10.1104/pp.106.078683. View

14.

Green D, Reed J . Mitochondria and apoptosis. Science. 1998; 281(5381):1309-12. DOI: 10.1126/science.281.5381.1309. View

15.

Helmersson A, VON Arnold S, Bozhkov P . The level of free intracellular zinc mediates programmed cell death/cell survival decisions in plant embryos. Plant Physiol. 2008; 147(3):1158-67. PMC: 2442516. DOI: 10.1104/pp.108.122598. View

16.

Filonova L, Suarez M, Bozhkov P . Detection of programmed cell death in plant embryos. Methods Mol Biol. 2008; 427:173-9. DOI: 10.1007/978-1-59745-273-1_14. View

17.

Lam E, del Pozo O . Caspase-like protease involvement in the control of plant cell death. Plant Mol Biol. 2001; 44(3):417-28. DOI: 10.1023/a:1026509012695. View

18.

Lin J, Wang Y, Wang G . Salt stress-induced programmed cell death in tobacco protoplasts is mediated by reactive oxygen species and mitochondrial permeability transition pore status. J Plant Physiol. 2006; 163(7):731-9. DOI: 10.1016/j.jplph.2005.06.016. View

19.

Kroemer G, Zamzami N, Susin S . Mitochondrial control of apoptosis. Immunol Today. 1997; 18(1):44-51. DOI: 10.1016/s0167-5699(97)80014-x. View

20.

Balk J, Leaver C . The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell. 2001; 13(8):1803-18. PMC: 139137. DOI: 10.1105/tpc.010116. View