Scientia Agricultura Sinica ›› 2013, Vol. 46 ›› Issue (5): 871-880.doi: 10.3864/j.issn.0578-1752.2013.05.001

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS •     Next Articles

Cytological Mechanism of Autophagosome Biogenesis During Cell Autophagic Apoptosis in Rice and Insect Cell

 CHENG  Xing-An, QIN  Xiang-Jing, JIANG  Xu-Hong, Sammy  ZHENG, LIU  Zhan-Mei, LIU  Xiang-Dong   

  1. 1.Institute of Natural Product Chemistry, Zhongkai University of Agriculture and Engineering, Guangzhou 510225, China; 2.College of Agriculture, South China Agricultural University, Guangzhou 510642, China
    3.School of Life Sciences, Sun Yat-Sen University, Guangzhou 510275, China
    4.Peralta Community City College, California CA 95101, USA
  • Received:2012-12-13 Online:2013-03-01 Published:2013-01-28

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Abstract: 【Objective】An experiment was carried out to study the change of membrane organelles during cell autophagy and the relationship of membrane organelles and autophagosome biogenesis at cellular level. 【Method】 Recent studies have shown that cell apoptosis in the Japonica/Javanica hybrid rice F1 is caused by gene interactions and apoptotic Sf9 cell can be induced by natural chemicals such as azadirachtin, camptothecin, and matrine. In this study, autophagosome biogenesis were observed in the cells of hybrid rice F1 and Sf6 cells treated by chemicals using transmission electron microscope and fluorescence microscopy. 【Result】 The results showed that pollen mother cells of hybrid rice F1 degenerated partly at different stages during microsporogenesis. The morphology of mitochondria in some cells expanded into dumbbell or pipe-like line shape which eventually developed into a double-membrane organelle. Whereas, in tapetal cells the endoplasmic reticulum swelled and expanded into a double-membrane autophagosomes, enwrapping a portion of cytoplasm and other organelles such as mitochondrias and peroxisomes, suggesting the occurrence of autophagic apoptosis. The mitochondrias in apoptotic cells treated by camptothecin and matrine elongated and curved into dumbbell or pipe-like line shape which eventually developed into double-membrane autophagosomes, enwrapping other organelles. Nuclei in apoptotic cells treated by azadirachtin or camptothecin formed the double-membrane autophagosomes by the ways of pagination and sprouting. 【Conclusion】In conclusion, the membrane organelles including endoplasmic reticulum, mitochondrias and nuclei were all the direct origin of autophagosome membrane during the autophagic apoptosis in plant and animal cells. However, the degree and manner contributed by the three membrane organelles during the formation of autophagosome were dependent on the species, cell categories and the factors inducing apoptosis.

Key words: autophagy , apoptosis , autophagosome , rice (Oryza sativa L.) , Sf9 cell

[1]Klionsky D J. Autophagy: From phenomenology to molecular understanding in less than a decade. Molecular Cell Biology, 2007, 8: 931-937.

[2]Axe E L, Walker S A, Manifava M, Chandra P, Roderick H L, Habermann A. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. Journal of Cell Biology, 2008, 182: 685-701.

[3]Crotzer V L, Blum J S. Autophagy and intracellular surveillance: Modulating MHC class II antigen presentation with stress. Proceedings of the National Academy of Sciences of the USA, 2005, 102: 7779-7780.

[4]Doelling J H, Walker J M, Friedman E M, Thompsonand A R, Vierstra R. The APG8/12-activating emzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. Journal of Biology Chemistry, 2002, 277: 33105-33114.

[5]Hanaoka H, Noda T, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Ohsumi Y. Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiology, 2002, 129: 1181-1193.

[6]Juhasz G, Csikos G, Sinka R, Erdelyi M, Sass M. The Drosophila homolog of Aut1 is essential for autophagy and development. FEBS Letters, 2003, 543: 154-158.

[7]Otto G P, Wu M Y, Kazgan N, Anderson O R, Kessin R H. Macroautophagy is required for multicellular development of the social amoeba Dictyostelium discoideum. The Journal of Biological Chemistry, 2003, 278: 17636-17645.

[8]Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K, Tokuhisa T, Ohsumi Y, Yoshimori T. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. Journal of Cell Biology, 2001, 152: 657-667.

[9]Geng J F, Klionsky D J. The golgi as a potential membrane source for autophagy. Autophagy, 2010, 6: 950-951.

[10]Moreau K, Rubinsztein D C. The plasma membrane as a control center for autophagy. Autophagy, 2012, 8: 861-863.

[11]Klionsky D J. The molecular machinery of autophagy: Unanswered questions. Cell Science, 2005, 118: 7-18.

[12]Dunn W A, Cregg J M , Kiel J A K W, Oku M, Sakai Y, Sibirny A, Stasyk O V, Veenbuis M. Pexophagy: The selective autophagy of peroxisomes. Autophagy, 2005, 1: 75-83.

[13]Reggiori F, Shintani T, Nair U, Klionsky D J. Atg9 cycles between mitochondria and the pre-autophagosomal structure in yeasts. Autophagy, 2005, 1: 101-109.

[14]Chang T, Schroder L A, Thomson J M, Klocman A S, Tomasini A J, Strømhaug P E, Dunn W A. PpATG9 encodes a novel membrane protein that traffics to vacuolar membranes, which sequester peroxisomes during pexophagy in Pichia pastoris. Molecular Biology of the Cell, 2005, 16: 4941-4953.

[15]Kirisako T, Ichimura Y, Okada H, Kabeya Y, Mizushima N, Yoshimori T, Ohsumi M, Takao T, Noda T, Ohsumi Y. The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. Journal of Cell Biology, 2000, 151: 263-275.

[16]Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, Mizushima N, Tanida I, Kominami E, Ohsumi M, Noda T, Ohsumi Y. A ubiquitin-like system mediates protein lipidation. Nature, 2000, 408: 488-492.

[17]程杏安, 何金华, 刘向东, 李亚娟. 不同倍性水稻亚种间杂种小孢子发生的细胞学观察. 西北植物学报, 2009, 29(7): 1320-1327

Cheng X A, He J H, Liu X D, Li Y J. Cytological observation on microsporogenesis in inter-subspecific hybrids of rice with different ploidy level. Acta Botanica Boreali-Occidentalia Sinica, 2009, 29(7): 1320-1327. (in Chinese)

[18]冯九焕, 卢永根, 刘向东, 徐雪宾. 水稻花粉发育过程及其分期. 中国水稻科学, 2001, 15(1): 21-28.

Feng J H, Lu Y G, Liu X D, Xu X B. Pollen development and its stages in rice (Oryza sativa L.). Chinese Journal of Rice Science, 2001, 15(1): 21-28. (in Chinese)

[19]刘向东, 徐是雄, 卢永根. 水稻胚囊壁的形成与发育观察. 植物学报, 1997, 39(11): 895-990.

Liu X D, Xu S X, Lu Y G. Formation and development of embryosac wall in rice. Acta Botanica Sinica, 1997, 39(11): 895-990. (in Chinese)

[20]程杏安, 黄劲飞, 胡美英, 胡黎明, 张彦博. 印楝素A诱导Sf9细胞凋亡的显微和超微形态化. 华南农业大学学报, 2010, 31: 53-58.

Cheng X A, Huang J F, Hu M Y, Hu L M, Zhang Y B. Morphological changes of microstructure and ultra-structure of apoptotic Sf9 cells induced by azadirachtin A. Journal of South China Agricultural University, 2010, 31: 53-58. (in Chinese)

[21]Yoshimoto K, Takano Y, Sakai Y. Autophagy in plants and phytopathogens. FEBS Letters, 2010, 584: 1350-1358.

[22]Matile P, Winkenbach F. Function of lysosomes and lysosomal enzymes in the senescing corolla of the morning glory (Ipomoeapurpurea). Journal of Experimental Botany, 1971, 22: 759-771.

[23]Smith M T, Saks Y, Van Staden J. Ultrastructural changes in the petals of senescing flowers of Dianthus caryophyllus L.. Annals of Botany, 1992, 69: 277-285.

[24]Filonova L H, Bozhkov P V, Brukhin V B, Daniel G, Zhivotovsky B, Arnold S V. Two waves of programmed cell death occur during formation and development of somatic embryos in the gymnosperm, Norway spruce. Journal of Cell Biology, 2000, 113: 4399-4411.

[25]Bell P R. Megaspore abortion: A consequence of selective apoptosis. International Journal of Plant Sciences, 1996, 157: 1-7.

[26]赵莎, 姚家玲. 光敏核不育水稻花粉发育的细胞学研究与PCD检测. 华中农业大学学报, 2007, 26(3): 283-288.

Zhao S, Yao J L. Cytological study and PCD assay on pollen development of photoperiod sensitive genic male sterile rice. Journal of Huazhong Agricultural University, 2007, 26(3): 283-288. (in Chinese)

[27]Li X W, Gao X Q, Wei Y, Deng L, Ouyang Y, Chen G, Li X, Zhang  Q, Wu C. Rice apoptosis inhibitors 5 coupled with two DEAD-Box Adenosine 5′-Triphosphate-Dependent RNA helicases regulates tapetum degeneration. The Plant Cell, 2011, 23: 1416-1434.

[28]陈朱希昭, 陈耀堂, 高信曾. 太谷核不育小麦花药组织和小孢子发生的超微结构研究. 植物学报, 1984, 26(3): 235-240.

Chenzhu X Z, Chen Y T, Gao X Z. Ultra-structure of anther tissue and microsporogenesis in Taigu nuclear male-sterile wheat. Acta Botanica Sinica, 1984, 26(3): 235-240. (in Chinese)

[29]Tian H Q, Kuang A, Musgrave M E, Russell S D. Calcium distribution in fertile and sterile anthers of a photoperiod-sensitivegenic male-sterile rice. Planta, 1998, 204: 183-192.

[30]Papini A, Mosti S, Brighigna L. Programmed cell death events during tapetum development of angiosperms. Protoplasma, 1999, 207: 213-221.

[31]Simonsen A, Stenmark H. Self-eating from an ER-associated cup. Journal of Cell Biology, 2008, 182: 621-622.

[32]Yen W L, Shintani T, Nair U, Cao Y, Li Z, Hughson F M, Baba M, Klionsky D J. The conserved oligomeric golgi complex is involved in double-membrane vesicle formation during autophagy. Journal of Cell Biology, 2010, 188: 101-114.

[33]Orsi A, Razi M, Dooley H C, Robinson D, Weston A E, Collinson L M, Tooze S A. Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, are required for autophagy. Molecular Biology of the Cell, 2012, 23: 1860-1873.

[34]Hailey D W, Rambold A S, Satpute-Krishnan P, Mitra K, Sougrat R, Kim P K, Lippincott-Schwartz J. Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell, 2010, 141: 656-667.

[35]English L, Chemali M, Duron J, Rondeau C, Laplante A, Gingras D, Alexander D, Leib D, Norbury C, Lippe R, Desjardins M. Autophagy enhances the presentation of endogenous viral antigens on MHC class I molecules during HSV-1 infection. Nature Immunology, 2009, 10: 480-487.

[36]English L, Chemali M, Desjardins M. Nuclear membrane-derived autophagy, a novel process that participates in the presentation of endogenous viral antigens during HSV-1 infection. Autophagy, 2009, 5: 1026-1029.
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