Mannose Induces an Endonuclease Responsible for DNA Laddering in Plant Cells

Joshua C. Stein¹ and Geneviève Hansen^*

Novartis Agribusiness Biotechnology Research, 3054 Cornwallis Road, Research Triangle Park, Durham, North Carolina 27709

The effect of D-mannose (Man) on plant cells was studied in two different systems: Arabidopsis roots and maize (Zea mays) suspension-cultured cells. In both systems, exposure to D-Man was associated with a subset of features characteristic of apoptosis, as assessed by oligonucleosomal fragmentation and microscopy analysis. Furthermore, D-Man induced the release of cytochrome c from mitochondria. The specificity of D-Man was evaluated by comparing the effects of diastereomers such as L-Man, D-glucose, and D-galactose. Of these treatments, only D-Man caused a reduction in final fresh weight with concomitant oligonucleosomal fragmentation. Man-induced DNA laddering coincided with the activation of a DNase in maize cytosolic extracts and with the appearance of single 35-kD band detected using an in-gel DNase assay. The DNase activity was further confirmed by using covalently closed circular plasmid DNA as a substrate. It appears that D-Man, a safe and readily accessible compound, offers remarkable features for the study of apoptosis in plant cells.

Plant Physiol. (1999) 121: 71-80
Copyright Clearance Center:   0032-0889/99/121//10
© 1999 American Society of Plant Physiologists

This article has been cited by other articles:

				L. Zhang, Y. Li, D. Xing, and C. Gao Characterization of mitochondrial dynamics and subcellular localization of ROS reveal that HsfA2 alleviates oxidative damage caused by heat stress in Arabidopsis J. Exp. Bot., May 1, 2009; 60(7): 2073 - 2091. [Abstract] [Full Text] [PDF]

				L. Zhang and D. Xing Methyl Jasmonate Induces Production of Reactive Oxygen Species and Alterations in Mitochondrial Dynamics that Precede Photosynthetic Dysfunction and Subsequent Cell Death Plant Cell Physiol., July 1, 2008; 49(7): 1092 - 1111. [Abstract] [Full Text] [PDF]

				A. K. Azad, T. Ishikawa, T. Ishikawa, Y. Sawa, and H. Shibata Intracellular energy depletion triggers programmed cell death during petal senescence in tulip J. Exp. Bot., May 31, 2008; (2008) ern066v1. [Abstract] [Full Text] [PDF]

				T. J. Reape, E. M. Molony, and P. F. McCabe Programmed cell death in plants: distinguishing between different modes J. Exp. Bot., February 5, 2008; (2008) erm258v1. [Abstract] [Full Text] [PDF]

				L. L. Torres and G. L. Salerno A metabolic pathway leading to mannosylfructose biosynthesis in Agrobacterium tumefaciens uncovers a family of mannosyltransferases PNAS, September 4, 2007; 104(36): 14318 - 14323. [Abstract] [Full Text] [PDF]

				L. Lombardi, S. Casani, N. Ceccarelli, L. Galleschi, P. Picciarelli, and R. Lorenzi Programmed cell death of the nucellus during Sechium edule Sw. seed development is associated with activation of caspase-like proteases J. Exp. Bot., August 28, 2007; (2007) erm137v1. [Abstract] [Full Text] [PDF]

				R. A. Vacca, D. Valenti, A. Bobba, R. S. Merafina, S. Passarella, and E. Marra 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 Physiology, May 1, 2006; 141(1): 208 - 219. [Abstract] [Full Text] [PDF]

				D. C. Logan The mitochondrial compartment J. Exp. Bot., March 1, 2006; 57(6): 1225 - 1243. [Abstract] [Full Text] [PDF]

				J. M. R. Faria, J. Buitink, A. A. M. van Lammeren, and H. W. M. Hilhorst Changes in DNA and microtubules during loss and re-establishment of desiccation tolerance in germinating Medicago truncatula seeds J. Exp. Bot., August 1, 2005; 56(418): 2119 - 2130. [Abstract] [Full Text] [PDF]

				E. A. A. da Silva, P. E. Toorop, J. Nijsse, J. D. Bewley, and H. W. M. Hilhorst Exogenous gibberellins inhibit coffee (Coffea arabica cv. Rubi) seed germination and cause cell death in the embryo J. Exp. Bot., March 1, 2005; 56(413): 1029 - 1038. [Abstract] [Full Text] [PDF]

				G. C. Pagnussat, H.-J. Yu, Q. A. Ngo, S. Rajani, S. Mayalagu, C. S. Johnson, A. Capron, L.-F. Xie, D. Ye, and V. Sundaresan Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis Development, February 1, 2005; 132(3): 603 - 614. [Abstract] [Full Text] [PDF]

				S. Chen and M. B. Dickman Bcl-2 family members localize to tobacco chloroplasts and inhibit programmed cell death induced by chloroplast-targeted herbicides J. Exp. Bot., December 1, 2004; 55(408): 2617 - 2623. [Abstract] [Full Text] [PDF]

				S. W. Yang, S. K. Kim, and W. T. Kim Perturbation of NgTRF1 Expression Induces Apoptosis-Like Cell Death in Tobacco BY-2 Cells and Implicates NgTRF1 in the Control of Telomere Length and Stability PLANT CELL, December 1, 2004; 16(12): 3370 - 3385. [Abstract] [Full Text] [PDF]

				J. Ito and H. Fukuda ZEN1 Is a Key Enzyme in the Degradation of Nuclear DNA during Programmed Cell Death of Tracheary Elements PLANT CELL, December 1, 2002; 14(12): 3201 - 3211. [Abstract] [Full Text] [PDF]

				E. VIROLAINEN, O. BLOKHINA, and K. FAGERSTEDT Ca2+-induced High Amplitude Swelling and Cytochrome c Release From Wheat (Triticum aestivum L.) Mitochondria Under Anoxic Stress Ann. Bot., October 1, 2002; 90(4): 509 - 516. [Abstract] [Full Text] [PDF]

				C. A. Christensen, S. W. Gorsich, R. H. Brown, L. G. Jones, J. Brown, J. M. Shaw, and G. N. Drews Mitochondrial GFA2 Is Required for Synergid Cell Death in Arabidopsis PLANT CELL, September 1, 2002; 14(9): 2215 - 2232. [Abstract] [Full Text] [PDF]

				F. Rolland, B. Moore, and J. Sheen Sugar Sensing and Signaling in Plants PLANT CELL, May 1, 2002; 14(90001): S185 - 205. [Full Text] [PDF]

				S.-B. Ning, L. Wang, and Y.-C. Song Identification of programmed cell death in situ in individual plant cells in vivo using a chromosome preparation technique J. Exp. Bot., April 1, 2002; 53(369): 651 - 658. [Abstract] [Full Text] [PDF]

				J. Balk and C. J. Leaver The PET1-CMS Mitochondrial Mutation in Sunflower Is Associated with Premature Programmed Cell Death and Cytochrome c Release PLANT CELL, August 1, 2001; 13(8): 1803 - 1818. [Abstract] [Full Text] [PDF]

				R. Brouquisse, A. Evrard, D. Rolin, P. Raymond, and C. Roby Regulation of Protein Degradation and Protease Expression by Mannose in Maize Root Tips. Pi Sequestration by Mannose May Hinder the Study of Its Signaling Properties Plant Physiology, March 1, 2001; 125(3): 1485 - 1498. [Abstract] [Full Text]

				W. Lukowitz, T. C. Nickle, D. W. Meinke, R. L. Last, P. L. Conklin, and C. R. Somerville Arabidopsis cyt1 mutants are deficient in a mannose-1-phosphate guanylyltransferase and point to a requirement of N-linked glycosylation for cellulose biosynthesis PNAS, February 15, 2001; (2001) 51625798. [Abstract] [Full Text]

				K. Obara, H. Kuriyama, and H. Fukuda Direct Evidence of Active and Rapid Nuclear Degradation Triggered by Vacuole Rupture during Programmed Cell Death in Zinnia Plant Physiology, February 1, 2001; 125(2): 615 - 626. [Abstract] [Full Text]

				P. Xu and M. J. Roossinck Cucumber Mosaic Virus D Satellite RNA-Induced Programmed Cell Death in Tomato PLANT CELL, July 1, 2000; 12(7): 1079 - 1092. [Abstract] [Full Text]

				Y. Xu and M. R. Hanson Programmed Cell Death during Pollination-Induced Petal Senescence in Petunia Plant Physiology, April 1, 2000; 122(4): 1323 - 1334. [Abstract] [Full Text]

				S. Arpagaus, A. Rawyler, and R. Braendle Occurrence and Characteristics of the Mitochondrial Permeability Transition in Plants J. Biol. Chem., January 11, 2002; 277(3): 1780 - 1787. [Abstract] [Full Text] [PDF]

				W. Lukowitz, T. C. Nickle, D. W. Meinke, R. L. Last, P. L. Conklin, and C. R. Somerville Arabidopsis cyt1 mutants are deficient in a mannose-1-phosphate guanylyltransferase and point to a requirement of N-linked glycosylation for cellulose biosynthesis PNAS, February 27, 2001; 98(5): 2262 - 2267. [Abstract] [Full Text] [PDF]