Abstract
Transmission electron microscopy (TEM) and fluorescence microscopy studies revealed that the metaphloem sieve elements (MSEs) in the ventral vascular bundle of the caryopses of developing wheat (Triticum aestivum L.) undergo a unique type of programmed cell death (PCD). Terminal deoxynucleotidyl transferase-mediated dUTP nick-end labeling (TUNEL)-positive nuclei were observed at 3 and 4 days after flowering (DAF). Transmission electron microscopy studies of differentiating MSEs revealed increased vacuolation, nuclear degeneration, chromatin condensation and localization to the periphery of the nucleus, and partly dilated perinuclear spaces, all typical characteristics of PCD in plant cells. In addition, vacuoles were disrupted at the last stages of differentiation. These results demonstrate that MSE differentiation is a unique type of PCD with highly selective autophagic processes, in which PCD ceases just prior to death. During this cessation of PCD, vacuoles and the endoplasmic reticulum appear to be associated with selective organelle digestion.
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Abbreviations
- DAF:
-
days after flowering
- MSEs:
-
metaphloem sieve elements
- PCD:
-
programmed cell death
- PSEs:
-
protophloem sieve elements
- SEs:
-
sieve elements
- TEs:
-
tracheary elements
- TUNEL:
-
terminal deoxynucleotidyl transferase-mediated dUTP nick-end labeling
References
Ameisen J-C (2002) On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death Differ 9:367–393
Bassham D-C (2007) Plant autophagy—more than a starvation response. Curr Opin Plant Biol 10:587–593
Eleftheriou E-P (1982) Development of protophloem in roots of Aegilops comosa var.thessalica. II. Sieve-element differentiation. Protoplasma 11:3221–3233
Eleftheriou E-P (1984) Sieve-element plastids of Triticum and Aegilops (Poaceae). PIant Syst Evol 14:5119–5133
Eleftheriou E-P (1986) Ultrastructural studies on protophloem sieve elements in Triticum aestivum L. nuclear degeneration. J Ultra Mol Struct Res 9:547–560
Eleftheriou E-P (1996) Developmental features of protophloem sieve elements in roots of wheat (Triticum aestivum L.). Protoplasma 193:204–212
Esau K (1972) Changes in the nucleus and the endoplasmic reticulum during differentiation of a sieve element in Mimosa pudica L. Ann Bot (London) 36:703–710
Evert R-F (1977) Phloem structure and histochemistry. Annu Rev Plant Physiol 28:199–222
Fukuda H (2000) Programmed cell death of tracheary elements as a paradigm in plants. Plant Mol Biol 44:245–253
Gaffal K-P, Friedrichs G-J, El-Gammal S (2007)Ultrastructural evidence for a dual function of the phloem and programmed cell death in the floral nectary of Digitalis purpurea. Ann Bot (London) 99:593–607
Groover A, Jones A-M (1999) Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis. Plant Physiol 119:375–384
Groover A, DeWitt N, Heidel A, Jones A (1997) Programmed cell death of plant tracheary elements differentiating in vitro. Protoplasma196:197–211
Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Tsuda S, Kondo M, Nishimura M, Hara-Nishimura I (2004) A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science305:855–858
Hatsugai N, Kuroyanagi M, Nishimura M, Hara-Nishimura I (2006) A cellular suicide strategy of plants: vacuole-mediated cell death. Apoptosis11:905–911
Ishida-Yamamoto A, Yamauchi T, Tanaka H, Nakane H, Takahashi H, Iizuka H (1999) Electron microscopic in situ DNA nick end-labeling in combination with immunoelectron microscopy. J Histochem Cytochem 47:711–717
Jones A-M (2001) Programmed cell death in development and defense. Plant Physiol 125:94–97
Kladnik A, Chamusco K, Dermastia M, Chourey P (2004) Evidence of programmed cell death in post-phloem transport cells of the maternal pedicel tissue in developing caryopsis of maize. Plant Physiol 136:3572–3581
Lam E (2005) Vacuolar proteases livening up programmed cell death. Trends Cell Biol 15:124–127
Mea M-D, Serafini-Fracassini D, Duca S-D (2007)Programmed cell death: similarities and differences in animals and plants: a flower paradigm. Amino Acids 33:395–404
Obara K, Kuriyama H, Fukuda H (2001) Direct evidence of active and rapid nuclear degradation triggered by vacuole rupture during programmed cell death in Zinnia. Plant Physiol 125:615–626
Otsuki Y, Li Z-L, Shibata M-A (2003) Apoptotic detection methods: from morphology to gene. Prog Histochem Cytochem 38:275–339
Pennell R-I, Lamb C (1997) Programmed cell death in plants. Plant Cell 9:1157–1168
Prochazkova D, Wilhelmova N (2007) Leaf senescence and activities of the antioxidant enzymes. Biol Plant 51:401–406
Ryerson D-E, Heath M-C (1996) Cleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by funga1 infection or by abiotic treatments. Plant Cell 8:393–402
Schulz A, Thompson G-A (2001) Phloem structure and function. Encyclopedia of Life Sci, vols 1–10. Macmillan, London
Tolkovsky A-M, Xue L-Z, Fletcher G-C, Borutaite V (2002) Mitochondrial disappearance from cells: a clue to the role of autophagy in programmed cell death and disease? Biochimie 84:233–240
Toyooka K, Moriyasu Y, Goto Y, Takeuchi M, Fukuda H, Matsuoka K (2006) Protein aggregates are transported to vacuoles by a macroautophagic mechanism in nutrient-starved plant cells. Autophagy 2:96–106
van Bel A-J-E (2003)The phloem, a miracle of ingenuity. Plant Cell Environ 26:125–149
van Doorn W-G (2005) Plant programmed cell death and the point of no return. Trends Plant Sci 10:478–483
Wang Y-Q, Cui K-M (1998) Programmed cell death during the vessel element differentiation of the secondary xylem in Eucommia ulmoides shoots. Acta Bot Sin 40:1102–1107
Wu H, Zheng XF (2003) Ultrastructural studies on the sieve elements in root protophleom of Arabidopsis thaliana. Acta Bot Sin 45:322–330
Zavaleta-Mancera H, Thomas H, Scott I (1999) Regreening of senescent Nicotiana leaves. II. Redifferentiation of plastids. J Exp Bot 50:1683–1689
Zhou Z-Q, Lan S-Y, Wang W-J, Zhu X-T, Xu Z-X, Yang Z-M (2003) Observation on the structure change of phloem cells in the developing wheat caryopsis. J Chin Electron Microsc Soc 22:292–297
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
Acknowledgements
This paper has cost the time and energy of many people. Our deepest gratitude goes first and foremost to the National Nature Science Foundation of China (30571101), for their financial support. Moreover, our sincere thanks go to Cao Jian-Bo and Qin Li-Hong who helped us a lot by providing the transmission electron microscope technology. We also owe our sincere thanks to our colleagues and family members, who provided us with encouragement when we encountered difficulties in writing this paper. Without their care and consideration, this study would likely not have been completed.
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Wang, L., Zhou, Z., Song, X. et al. Evidence of ceased programmed cell death in metaphloem sieve elements in the developing caryopsis of Triticum aestivum L.. Protoplasma 234, 87–96 (2008). https://doi.org/10.1007/s00709-008-0023-6
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DOI: https://doi.org/10.1007/s00709-008-0023-6