Biological Functions of Antioxidants in Plant Transformation

Tag : zinc selenite

Antioxidants and the control of tissue browning and necrosis inplant transformation. Since 1996, tissue browning/necrosisassociated with Agrobaterium-mediated transformation have beenreported in different types of explants of both dicotyledonous andmonocotyledonous species. The examples include the browning/necrosis occurred in embryogenic calli and leaf disks of grape (Puand Goodman 1992; Perl et al. 1996; Das et al. 2002), cotyledonarynodes of soybean (Olhoft et al. 200la, b), hypocotyls ofcauliflower (Chakrabarty et al. 2002), leaf segments of C.plantagineum (Toldi et al. 2002), epicotyl sections of peanut(Zheng et al. 2005), and cotyledons of tomato (Dan et al. 2004),leaf spindle sections of sugarcane (Enriquez-Obregon et al. 1997,1998; Gustavo et al. 1998), shoot meristem sections, and calli ofrice (Enriquez-Obregon et al. 1999), and suspension cells, immatureembryos, and embryogenic calli of corn (Hansen 2000). From thesereports, it seems that dicotyledonous species are more susceptibleto tissue browning/ necrosis than monocotyledonous plants, but itcan be controlled by the use of antioxidants PVPP, DTT, ascorbicacid, cysteine, glutathione, selenite, tocopherol, or lipoic acid(Table 2). It appears that ascorbic acid and cysteine are suitableto minimize browning/necrosis for both dicotyletonary andmonocotyledonary plant species, but the rest of the antioxidantswas largely experimented with dicotyletonous plants. Table 1.Antioxidants used in plant tissue culture
Perl et al. (1996) found that short exposures of embryogenic calliof Vitis vinifera cv. Superior seedless to a diluted solution ofAgrobacterium resulted in tissue necrosis. The necrosis seemed tobe oxygen-dependent and correlated with elevated levels ofperoxides. Therefore, the inclusion of both 1% PVPP and 2 mg/l DTTin coculture medium was found to improve expiant viability duringand after cocultivation. They observed that the necrosis of theembryogenic calli was completely inhibited by these antioxidantswhile Agrobacterium virulence was not affected. These antioxidantsenabled the recovery of stable transgenic grape plants resistant tohygromycin. In another study Das et al. (2002) successfully used 1%PVPP and 2 mg/l DTT to control browning and necrosis in grape leaftissue expiants in a coculture medium during Agrobacterium-mediatedtransformation.
Table 2. Antioxidants used in plant transformation
It was found that the coculture of sugarcane leaf spindle sectionswith A. tumefaciens induced a rapid necrosis of the tissue(Enriquez-Obregon et al. 1997, 1998; Gustave et al. 1998). Tominimize the necrosis, the leaf spindle expiants were incubated ina liquid medium containing 15 mg/1 ascorbic acid, 40 mg/1 cysteine,and 2 mg/1 silver nitrate for 60 h in the dark prior to inoculationwith Agrobacterium and then cocultured in a cocultivation mediumwith the same antioxidants at the same concentrations,respectively, after the inoculation with Agrobacterium. By doingso, the percentage of the expiant viability was increased from 10%(without the antioxidants) to 90%. In addition, the percentage ofGUS positive expiants was increased from 0% (without theantioxidants) to 100%. Enriquez-Obregon et al. (1999) alsoinvestigated the effects of the three compounds on the necrosis ofshoot meristem expiants prior to infection in rice transformation.The expiants, which were incubated in a liquid medium containing 20mg/1 ascorbic acid, 40 mg/1 cysteine, and 5 mg/1 silver nitrate for6 h in the dark, had an average of 6% of the each expiant areaproducing the necrosis, but the explants without the antioxidanttreatment had 80% of the each expiant area producing the necrosis.The antioxidant treatment increased rice transformation efficiencyfrom 17% without the antioxidant treatment to 30%. Similarly,Olhoft et al. (2001a, b) increased Agrobacterium infection from 37%(without cysteine) to 91% in the soybean cotyledonary node regionby including 400 mg/l cysteine in cocultivation medium,subsequently, resulting in a twofold increase in transformationefficiency (2.1% with cysteine vs. 0.9% without cysteine).Browning/necrosis on the expiant tissues was also reduced. Thestudies also showed that the frequency of transformed cells wasincreased only when cysteine was present during cocultivation ofAgrobacterium and cotyledonary-node explants. Later, the authorsreported the cocultivation medium with 3.3 mM cysteine, plus 1 mMDTT resulted a significant higher transformation efficiency (12.7%)than that either with cysteine alone (7.7%) or no cysteine (0.7%)when using hygromycin B selection (Olhoft et al. 2003). Applying400 mg/1 cysteine in the coculture medium increased both thefrequency of transient a-glucuronidase (GUS) expression in targetcells of com (56% with cysteine vs. 17% without cysteine) and thestable transformation frequency (6.2% with cysteine vs. 0.2%without cysteine) (Frame et al. 2002). However, cysteine reducedthe percentage of the immature zygotic embryos giving rise toembryogenic Type II callus from 99% when noninfected immaturezygotic embryos incubated on cocultivation medium without cysteineto 52% when the embryos cultured on cocultivation medium containingcysteine (Frame et al. 2002). Zeng et al. (2004) further confirmedthat the inclusion of 400 mg/l cysteine in a cocultivation mediumincreased stable transformation from 0.2% (without cysteine) to5.9% in soybean Agrobacterium-mediated transformation.
Adding glutathione to the selection medium reduced hyperhydricityof leaf expiants, increased leaf expiant viability, and increasedthe frequency of transformation from 13% (without glutathione) to45% in Agrobacteriummediated transformation of a desiccation-tolerant plant, Craterostigma plantagineum (Toldi et al. 2002).Zheng et al. (2005) investigated the effects of antioxidants,including ascorbic acid, sodium selenite, DL-a-tocopherol, andglutathione in a cocultivation medium, on ROS production,antioxidant activity, and stable transformation efficiency duringpeanut Agrobacterium-mediated transformation. They found thatglutathione, tocopherol, and selenite not only eliminated theformation of H^sub 2^O^sub 2^ produced in wound tissue duringpreparation of leaf expiants and their cocultivation with A.tumefaciens, but also decreased malondialdehyde (MDA) formation andenhanced the activities of the antioxidant enzymes such assuperoxide dismutase (SOD) and catalase (CAT). The inclusion of 100mg/l glutathione, 50 mg/l tocopherol, and 20 mg/l selenite in thecocultivation medium increased the transformation frequencies from3.9% (no antioxidant) to 14.6%, 10.3%, and 12.4%, respectively(Zheng et al. 2005).
Lipoic acid (LA) is a sulfur-containing compound involved inseveral multienzyme complexes such as pyruvate dehydrogenase, ct-ketoglutarate dehydrogenase, branched-chain keto aciddehydrogenase, and glycine decarboxylase complex (Packer et al.1995). In animals, free LA and dihydrolipoic acid are metabolicantioxidants that are able to scavenge most reactive oxygenspecies, to recycle other antioxidants such as vitamin C,glutathione, and vitamin B, and to increase the expression of genesinvolved in the regulation of normal growth and metabolism as wellas redox regulation of gene transcription (Packer et al. 1995;Packer and Tritschler 1996; Packer et al. 1997). Therefore, LA wasinvestigated in Agrobacteriummediated transformation across fivedifferent plant species, and it has significantly improved thetransformation methods, even for recalcitrant genotypes (Dan et al.2004; Dan 2006). Frequencies of independent transgenic plant eventswere increased in soybean from 0.6% to 3.6%, in potato from 3% to19%, in tomato from 28% to 94%, and in wheat from 2.9% to 5.4%. Thefrequency of putative transgenic embryo was increased in cottonfrom 41% to 61%. The frequencies of shoot escapes were reduced insoybean from 92% to 72%, in potato from 50% to 16%, and in tomatofrom 91% to 53%, under the optimal conditions. This study alsodemonstrated that an increase of the transformation frequency andreduction of escapes in tomato were accompanied by a twofoldreduction in the severity of the browning/necrosis ofAgrobacterium-toansfomied tissues, a twofold increase in thesurvivability of the transformed tissues, a fourfold increase inthe percentage of transgenic shoots, and a threefold reduction ofthe percentage of shoot escapes when using LA under optimalconditions. The application of LA in plant transformation hasdramatically solved the three common problems in planttransformation: browning/necrosis of the transformed tissues,recalcitrance, and shoot escapes, which severely limit the numberof transgenic plants produced.
Analysis of published information indicates that the antioxidantsused in plant transformation can be classified into two groupsbased on their biological function. The first group, consisting ofascorbic acid, cysteine, DTT, lipoic acid, and PVPP, functions toreduce expiant necrosis, increase viability of expiants, andimprove transformation efficiency while the other one, whichinclude glutathione, selenite, and alpha-tocopherol, reduceshyperhydricity and ROS and increases transformation efficiency(Table 2).
Programmed CeU Death Associated with ROS in Plant
Mechanism of plant cell death induced by Agrobacterium. Hansen(2000) reported that the cell death triggered by Agrobacterium spp.in maize tissues had several features of apoptosis, which were DNAfragmentation, and cytological changes, and cytochrome c release.She further showed the two antiapoptotic genes from baculovirus,p35, and lap had the ability to prevent the onset of the apoptosisin maize tissues. p35 is reported to act as a direct inhibitor ofcaspases whereas lap may act upstream to prevent activation ofcaspases. Caspases control most events of apoptosis in vertebratesand in invertebrates and are responsible, either directly orindirectly, for the cleavage of cellular proteins. The proteinsinclude nuclear proteins such as poly (ADP-ribose) polymerase, DNA-dependent protein kinase, and lamins, as well as actin (Nagata1997). The evidence that these genes could affect the reaction ofmaize cells to an apoptotic stimulus strongly indicates that plantmay have caspase-like proteases regulating apoptosis. A caspase-like proteolytic activity was also reported in tobacco plantsundergoing an HR triggered by an infection with Tobacco mosaicvirus (del Pozo and Lam 1998). Molecular identification of ROSsignaling during programmed cell death (PCD) in plant. One of thefirst genes identified and isolated in ROS-associated plant celldeath is LSDl that encodes a zinc-finger protein. This protein,together with two other zinc-finger proteins (LOLl and LOL2), couldact as a molecular rheostat, sensing changes in ROS homeostasis,thereby controlling apoptosis through the regulation of apoptoticgenes (Dietrich et al. 1997; Epple et al. 2003). The inactivationof the Arabidopsis Executerl gene completely abolished singletoxygeninduced cell death (Wagner et al. 2004). The chloroplasticprotein, which is encoded by Executerl, might perceive nonscavengedsinglet oxygen species within the chloroplast. Other importantstress signal transducers include mitogen-activated protein kinases(MAPKs) that act upstream of the oxidative burst during ozonetreatment and the HR (Ren et al. 2002; Samuel and Ellis 2002). Theprimary ROS activated tobacco MAPK is the salicylic acidinducedprotein kinase, which is required during harpindependent PCD(Samuel et al. 2005). A MAPKKK of alfalfe activates cell deathinduced by H^sub 2^O^sub 2^ through a specific MAPK-scaffoldingaction (Nakagami et al. 2004). A recent finding demonstrates theconserved Arabidopsis BCL2associated athanogene protein has beenshown to be induced by H^sub 2^O^sub 2^ and capable of provokingPCD in both yeast (Saccharomyces cerevisiae) and plants (Kang etal. 2006).
Mechanism to control programmed cell death associated with ROS inplant. Several recent studies have begun to unravel the possibleregulatory mechanisms of programmed cell death associated with ROSin plants (Breusegem and Dat 2006; Patel et al. 2006). The mostextensively studied form of plant PCD is HR to pathogen infection(Greenberg and Yao 2004; Soosaar et al. 2005). Recent evidenceindicates that autophagy, which is induced during the plant defenseresponse, is one mechanism by which HR-PCD is controlled (Liu etal. 2005). Autophagy is a process hi which cytosol and organellesare sequestered within doublemembrane vesicles that deliver thecontents to the lysosome/vacuole for degradation and recycling ofthe resulting macromolecules (Klionsky 2005). Several AuTophaGy(ATG) genes, which are required for autophagic activity, haveidentified via genetic screens in yeast (Levine and Klionsky 2004).The findings of Liu et al. (2005) imply that there is a prodeathsignal that moves out of the HR lesion into the surroundinguninfected tissue. Therefore, autophagy most likely alters theinduction, movement and/or recognition of the pro-PCD signal.Autophagy is not required for HR-PCD execution but is required tolimit PCD to the infection sites in plant and might prevent aprodeath signal from initiating PCD in healthy tissue (Liu et al.2005). Another study also suggests that autophagy has an anti-PCDfunction in innate immunity (Patel et al. 2006). However,examination of the function of ATG genes in other higher eukaryotesindicates that autophagy might have a dual role: pro- and/oranti-cell death (Yu et al. 2004; Boya et al. 2005; Pattingre et al.2005). The study from Torres and Dangl (2005) suggest that ROS andnitric oxide are possible candidates for a pro-PCD signal. Asextracellular ROS are produced before the onset of HR-PCD, ROS havebeen thought to function as pro- PCD signals, either by directlykilling the pathogen or by acting as signaling molecules thatmediate defense responses (Torres and Dangl 2005).
Apoptosis functions as an important defense strategy by host cellsagainst viral invasion. Many viruses contain the antiapoptoticgenes to block the defense-by-death response of host cells (Wang etal. 2004). The expression of antiapoptotic genes such as iap andp35 from baculoviruses, ced-9 from Caenorhabditis elegans and bcl-2from humans in tobacco, tomato, and passion fruit plant (Passifloraspp) suppressed the extensive cell death caused by fungal andbacterial pathogens and also enhanced resistance to some abioticstresses such as wounding, salt, cold, UV, and herbicides (Dickmanet al. 2001; Lincoln et al. 2002; Chen and Dickman 2004; Li andDickman 2004; Xu et al. 2004; Freitas et al. 2007). Particularly,baculovirus p35 and iap genes were expressed in com embryos andembryogenic calli and their expression reduced tissue browning 3 dafter cocultivation with A. tumefaciens (Hansen 2000). Theseantiapoptotic genes can be engineered to be expressed in plants forcontrolling tissue browning/ necrosis and enhancing planttransformation efficiency, especially in recalcitrant or poorlytransformable plant species.
Potential Mechanisms of Antioxidants for Improving PlantTransformation
Exposure of plant tissues to Agrobacterium during planttransformation leads to browning/necrosis of targeted cells/tissues, which affect transformation efficiency (Kuta and Tripathi2005). Browning/necrosis of targeted cells/tissues affects planttransformation in two ways. Browning/ necrosis may occur intransformed cells within expiant tissues, inhibiting regenerationof the transformed cells/ tissues. secondly, necrotic tissues areknown to accumulate antimicrobial substances (Goodman and Novacky1994), which may inhibit the potential of Agrobacterium to colonizeplant cells and transfer T-DNA. Thirdly, the active release ofchemical signals, which induce the vir genes in Agrobacterium,occurs only in living cells (Shaw et al. 1991). This also couldreduce the potential of Agrobacterium to transfer T-DNA intoplants. The inhibition of regeneration of transformed cells/tissuesmay promote growth of non-transformed cells/tissues even underselective pressures and, subsequently, result in production ofshoot escapes. With regard to Agrobaterium, the ROS, producedduring attempted transfection could be toxic enough to directlykill the attacking Agrobacterium (Wojtaszek 1997), therebysubsequently preventing Agrobacterium from colonizing plant cellsand transferring T-DNA into plants.
Perl et al. (1996) observed that elevated levels of peroxidaseactivity in grape tissues correlated with Agrobacterium-inducednecrosis in the host during Agrobacterium-mediated transformation.Peroxidase is known to mediate oxidative cross-linking ofstructural proteins in the cell wall (Somssich and Hahlbrock 1998),and the Agrobacterium-induced increase in peroxidase activity ingrape tissues could further confirm the role of oxidative burst inHR in plants to Agrobacterium infection. Deng et al. (1995)demonstrated that at least two genes residing within the T-DNAregion of Agrobacterium are responsible for inducing necrosis ingrape tissues. Furthermore, the aviR gene in Agrobacterium vitiswas found to be associated with Agrobacterium-induced HR (Zheng etal. 2003). aviR is homologous to luxR, which implies that the^groeactentww- induced HR is regulated by a quorum-sensingmechanism. The Agrobacterium-mdaced HR could lead to rapid andlarge generation of ROS in target plant cells, resulting in plantcells/tissues necrosis, oxidative stress on the invadingAgrobacterium cells, production of toxic antibacterial substances,and the deleterious effects on DNA molecules, especially at thesite of oxidative burst (Zheng et al. 2003). All of these factorscould significantly reduce the efficiency of stable transformationof plants.
Conclusion
Preliminary research on Agrobaterium-mduced plant cell death hasshown that Agrobacterium likely causes browning/necrosis oftransformed plant cells/tissues in vitro and ROS production duringAgrobacterium infection in vivo induces necrosis. The ROS couldkill the attacking Agrobacterium, thereby preventing Agrobacteriumfrom infecting plant cells/tissues and delivering T-DNA intoplants. Also, the necrosis prevents regeneration of transformedcells/ tissues.
Using antioxidants in plant tissue culture and transformationreduces the browning/necrosis of nontransformed and transformedcells/tissues and the frequencies of shoot escapes. In addition,the antioxidants increase the stable transformation efficienciesacross dicotyledonary and monocotyledonay plant species, indicatingtheir potential roles of controlling ROS for efficient productionof transgenic plants.
Advancing Agrobacterium-mediated transformation technology requiresan understanding of the mechanisms of Agrobacterium- inducedbrowning/necrosis and the roles of antioxidants in facilitatingplant transformation. The functions of the antioxidants describedabove have raised important questions. Do ROS produce whenAgrobacterium infection takes place during in vitro transformation?Do the ROS cause the browning/necrosis of transformed cells/tissues? Do the antioxidants scavenge and/or down-regulate the ROSthrough regulating the expression of genes involving ROS-generatingsystems such as NADPH oxidase or pH-dependent cell wall peroxidase?Do the ROS scavenging and/or down-regulating activities prevent thebrowning/necrosis of transformed cells/tissues? Or do theantioxidants alter the expression of genes that play an importantrole in the regeneration of transformed cells/ tissues byregulating the production of ROS that damage cells/tissues, or byactivating other metabolic pathways? Once these questions areaddressed, we can control apoptotic responses during wounding andAgrobacterium infection in plant transformation more effectively.This will undoubtedly lead to the development of more efficientplant transformation systems.
Acknowledgments The author thanks Dr. Richard E. Veilleux and Ms.Helen J. Hodges for English editing of the manuscript.
Received: 21 July 2006 /Accepted: 4 February 2008 / Publishedonline: 18 March 2008 / Editor: P. Lakshmanan (c) The Society forIn Vitro Biology 2008
References
Badia Nkanka, K. Effect of vitamin E on in vitro propagation ofEucalyptus rudis, Larix x Eurolepis and Quercus borealis. Bulletindes Recherches Agronomiques de Gembloux 17 (3):219-226; 1982.
Bailey, E.; Deighton, N.; Clulow, S. A.; Goodman, B. A.; Benson, E.E. Changes in free radical profiles during the callogenesis ofresponsive and recalcitrant potato genotypes. Proc. R. Soc.Edinburgh, sect. B 102:243-246; 1994.
Benson, E. E. In vitro plant recalcitrance: an introduction. InVitro Cell. Dev. Biol. Plant 36:141-148; 2000a.
Benson, E. E. Do free radicals have a role in plant tissue culturerecalcitrance? In Vitro Cell. Dev. Biol. Plant 36:163-170; 2000b.
Benson, E. E.; Lynch, P. T.; Jones, J. Variation in free radical-mediated damage in rice cell suspensions with different embryogenicpotentials. Planta 188:296-305; 1992.
Benson, E. E.; Roubelakis-Angelakis, K. A. Fluorescent lipidperoxidation products and antioxidant enzymes in tissue cultures ofWtis vinifera L. Plant Sci. 84:83-90; 1992.
Benson, E. E.; Roubelakis-Angelakis, K. A. Oxidative stress inrecalcitrant tissue cultures of grapevine. Free Radie. Biol. Med.16:355-362; 1994.
Betteridge, D. J. What is oxidative stress? Metabolism 49:3-8;2000.
Boya, P.; Gonzalez-Polo, R. A.; Casares, N.; Perfetn'ni, J.L.;Dessen, P.; Larochette, N; Metivier, D.; Meley, D.; Souquere, S.;Yoshimori, T. et al. Inhibition of macroautophagy triggersapoptosis. Mol. Cell Biol. 25:1025-1040; 2005.
Bremner, D. H.; Magill, W. J.; Benson, E. E. An evaluation ofanalytical methods for the detection of secondary oxidationproducts in dedifferentiated plant cultures. Phyton 37:39-44; 1997.
Breusegem, F. V.; Dat, J. F. Reactive oxygen species in plant celldeath. Plant Physiol. 141(2):384-390; 2006.
Cervera, M.; Juarez, J.; Navarro, A.; Pina, J. A.; Duran-Vila, N.;Navarro, L.; Pena, L. Genetic transformation and regeneration ofmature tissue of woody finit plants bypassing the juvenile stage.Transgenic Res. 7:51-59; 1998.
Chakrabarty, D.; Park, S., Y.; Ali, M., B.; Shin, K., S.; Paek, K.,Y. Hyperhydricity in apple: ultrastuctural and physiologicalaspects. Tree Physiol. 26(3):377-388; 2006.
Chakrabarty, R.; Viswakarma, N.; Bhat, S. R.; Kirti, P. B.; Singh,B. D.; Chopra, V. L. Agrobacterium-mediated transformation ofcauliflower optimization of protocol and development of Bt-transgenic cauliflower. J. Biosci. 27:495-502; 2002.
Chance, B.; Sies, H.; Boveris, A. Hydroperoxide metabolism inmammalian organs. Physiol. Rev. 59:527-605; 1979.
Chen, S.; Dickman, M. B. Sci-family members localize to tobaccochloroplasts and inhibit programmed cell death induced bychloroplast-targeted herbicides. J. Exp. Bot. 8:1-7; 2004.
Chin, H., F.; Krishnapillay, B.; Alang, Z., C. Media for embryoculture of some tropical recalcitrant species. Pertanika 11(3):357-363; 1988.
Chung, J. D.; Lee, J. H.; Jee, S. O.; Kim, C. K. Effect of severaladditives on medium browning and mericlone growth of temperateCymbidium species. Korean Journal of Horticultural Science &Technology 16(2):239-241; 1998.
Dan, Y. A novel plant transformation technology-Lipoic acid. Invitro cell. Dev. Biol. Plant 42:18-A; 2006 (Abstract).
Dan, Y.; Munyikawa, T. R. I.; Kimberly, A. R.; Rommens, C. M. T.Use of lipoic acid in plant culture media. US Patent Pub. No.: US2004/0133938 A1; 2004.
Das, D.; Reddy, M.; Upadhyaya, K.; Sopory, S. An efficient leaf-disc culture method for the regeneration via somatic embryogenesisand transformation of grape (Vitis vinifera L.). Plant Cell Rep. 20(11):999-1005; 2002.
Davies, M. J.; Gilbert, B. C.; Haywood, R. M. Radical-induceddamage to bovine serum albumin: role of the cysteine residue. FreeRadie. Res. Commun. 18:353-367; 1993.
Dean, R. T; Gieseg, S.; Davies, M. J. Reactive species and theiraccumulation on radical-damage proteins. Trends Biochem. Sci.18:437- 441; 1993.
Deighton, N.; Magill, W. J.; Bremner, D. H.; Benson, E. E.Malondialdehyde and 4 hydroxy-2-nonenal in plant tissue cultures:LC- MS determination of 2,4 dinitrophenylhydrazone derivatives.Free Radie. Res. 27:255-265; 1997.
del Pozo, O.; Lam, E. Caspases and programmed cell death in thehypersensitive response of plants to pathogens. Curr. Biol. 8:1129-1132; 1998.
Deng, W.; Pu, X. A.; Goodman, R. N.; Gordon, M. P.; Nester, E. W.T-DNA genes responsible for inducing a necrotic response on grapevines. Mol. Plant Microb. Interact. 8:538-548; 1995.
Desjardins, Y; Gosselin, A. The effect of hormonal concentrations,culture medium and an antioxidant on the shoot- doubling time forthe raspberry cultivar Madawaska grown in vitro. Can. J. Plant.Sci. 67(3):863-869; 1987.
Dickman, M. B.; Park, V. K.; Oltersdorf, T.; Li, W.; Clemente, T.;French, R. Abrogation of disease development in plants expressinganimal anti-apoptotic genes. Proc. Natl. Acad. Sci. USA98:6957-6962; 2001.
Dietrich, R. A.; Richberg, M. H.; Schmidt, R.; Dean, C.; Dangl, J.L. A novel zinc finger protein is encoded by the Arabidopsis LSDlgene and functions as a negative regulator of plant cell death.Cell 88:685-694; 1997.
Dutta, G. S.; Datta, S. Antioxidant enzyme activities during invitro morphogenesis of gladiolus and the effect of application ofantioxidants on plant regeneration. Biol. Plant. 47(2): 179-183;2003.
Elias, P. S. Food irradiation. In: Kotsonis, F. N.; Mackey, M.;Hjelle, J., eds. Nutritional toxicology. New York: Raven Press;1994:149-180.
Enriquez-Obregon, G., A.; Prieto-Samsonov, D., L.; Riva, G., A.; dela Perez, M.; Selman-Housein, G.; Vazquez-Padron, R., I.Agrobacterium-mediated japonica rice transformation: a procedureassisted by an antinecrotic treatment. Plant Cell Tissue OrganCult. 59(3):159-168; 1999.
Enriquez-Obregon, G., A.; Trujillo, L., E.; Menendez, C.; Vazquez,R., I.; Tiel, K.; Dafhnis, F.; Arrieta, J.; Selman, G.; Hernandez,L. Sugarcane (Saccharum hybrid) genetic transformation mediated byAgrobacterium tumefaciens: production of transgenic plantsexpressing proteins with agronomic and industrial value. Plantgenetic engineering: towards the third millennium: Proceedings ofthe International Symposium on Plant Genetic Engineering, Havana,Cuba, 6-10 December, 2000, pp. 76-81.
Enriquez-Obregon, G. A.; Vazquez-Padron, R. I.; Prieto-Samsonov, D.L.; Perez, M.; Selman-Housein, G. Genetic transformation ofsugarcane by Agrobacterium tumefaciens using antioxidantscompounds. Biotecnol. Apl. 14:169-174; 1997.
Enriquez-Obregon, G. A.; Vazquez-Padron, R. I.; Prieto-Samsonov, D.L.; de a Riva, G. A.; Selman-Housein, G. Herbicide-resistantsugarcane (Saccharum qfficinarum L.) plants byAgrobacteriummediated transformation. Planta 206:20-27; 1998.
Epple, P.; Mack, A. A.; Morris, V. R. F.; Dangl, J. L. Antagonisticcontrol of oxidative stress-induced cell death in Arabidopsis bytwo related, plantspecific zinc finger proteins. Proc. Natl. Acad.Sci. USA 100:6831-6836; 2003.
Fahey, R. C. Protection of DNA by thiols. Pharmacol. Ther. 39:101-108; 1988.
Feng, F. Study on the control of browning of longan in vitroculture. South China Fruits 6:49-51; 2004.
Finkel, T. Oxygen radicals and signaling. Curr. Opin. Cell Biol.10:248-253; 1998.
Frame, B. R.; Shou, H.; Chikwamba, R. K.; Zhang, Z.; Xiang, C.;Fonger, T. M.; Pegg, S. E. K.; Li, B.; Nettleton, D. S.; Pei, D.;Wang, K. Agrobacterium tumefaciens-mediated transformation of maizeembryos using a standard binary vector system. Plant Physiol.129:13- 22; 2002.
Freitas, D. S. D.; Coelho, M. C. F.; Souza Jr, M. T.; Marques, A.;Ribeiro, B. M. Introduction of the anti-apoptotic baculovirus p35gene in passion fruit induces herbicide tolerance, reducedbacterial lesions, but does not inhibits passion fruit woodinessdisease progress induced by cowpea aphid-borne mosaic virus(CABMV). Biotechnol. Lett. 29:79-87; 2007.
Fridovich, I. Superoxide dismutases. An adaptation to aparamagnetic gas. J. Biol. Chem. 264:7761-7764; 1989.
Furchgott, R. F. A research trail over half a century. Ann. Rev.Pharmacol. Toxicol. 35:1-27; 1995.
Goodman, R. N.; Novacky, A. J. The hypersensitive reaction inplants to pathogens...a resistant phenomenon. St. Paul, Minnesota:APS PRESS; 1994:240.
Greenberg, J. T; Quo, A.; Klessig, D. F.; Ausubel, F. M. Programmedcell death in plants: a pathogen-triggered response activatedcoordinately with multiple defense functions. Cell 77:551- 563;1994.
Greenberg, J. T; Yao, N. The role and regulation of programmed celldeath in plant-pathogen interactions. Cell Microbiol. 6:201- 211;2004.
Gupta, S., D.; Datta, S. Antioxidant enzyme activities during invitro morphogenesis of gladiolus and the effect of application ofantioxidants on plant regeneration. Biol. Plant. 47(2):179-183;2003.
Gustavo, A. R.; Gonzalez-Cabrera, J.; Vazquez-Padron, R.;AyraPardo, C. Agrobacterium tumefaciens: a natural tool for planttransformation. Electronic J. Biotechnol. 1(3):118-133; 1998.
Halliwell, B. How to characterize a biological anti-oxidant. FreeRadie. Res. Commun. 9:1-32; 1990.
Halliwell, B.; Gutteridge, J. M. C. Role of free radicals andcatalytic metal ions in human disease: an overview. MethodsEnzymol. 186:1-85; 1990.
Halliwell, B. Antioxidants in human health and disease. Ann. Rev.Nutrition 16:33-50; 1996.
Halliwell, B. Antioxidant defence mechanisms: From the beginning tothe end (of the beginning). Free Radie. Res. 31:261-272; 1999.
Halliwell, B.; Aeschbach, R.; Loliger, J.; Aruoma, O. I. Thecharacterization of antioxidants. Food Chem. Toxicol. 33 (7):601-617(617); 1995.
Halliwell, B.; Gutteridge, J. M. C. Free Radicals Biology andMedicine. Oxford: Clarendon Press; 1989.
Hansen, G. Evidence for Agrobacterium-mduced apoptosis in maizecells. Mol. Plant-Microb Interact. 13:649-657; 2000.
Igene, J. O.; King, J. A.; Pearson, A. M.; Gray, J. I. Influence ofheme pigments, nitrates and non-heme iron on development ofwarmed-over flavor (WOF) in cooked meat. J. Agric. Food Chem.27:832- 842; 1979. James, D. J.; Passey, A. J.; Barbara, D. J.;Bevan, M. Genetic transformation of apple (Mains pumila Mill) usinga disarmed Tibinary vector. Plant Cell Rep. 7:658-661; 1989.
Kamata, H.; Hirata, H. Redox regulation of cellular signaling. CellSignal 11:1-14; 1999.
Kang, C. H.; Jung, W. Y.; Kang, Y. H.; Kim, J. Y; Kim, D. G.;Jeong, J. C.; Baek, D. W.; Jin, J. B.; Lee, J. Y; Kim, M. O. et al.AtBAG6, a novel calmodulin-binding protein, induces programmed celldeath in yeast and plants. Cell Death Differ. 13:84-95; 2006.
Kanner, J.; German, J. B.; Kinsella, J. E. Initiation of lipidperoxidation in biological systems. CRC Crit. Rev. Food Sci. Nutr.25:317-364; 1987.
Klionsky, D. J. The molecular machinery of autophagy: unansweredquestions. J. Cell Sci. 118:7-18; 2005.
Kuta, D. D.; Tripathi, L. Agrobacterium-mduced hypersensitivenecrotic reaction in plant cells: a resistance response againstAgrobacterium-mediated DNA transfer. Afr. J. Biotechnol. 4 (8):752-757; 2005.
Lee, K. W.; Lee, S. H.; Lee, D. G.; Woo, H. S.; Kim, D. H.; Choi,M. S.; Kim, K. Y; Lee, H. S.; Lee, B. H. Effect of plant growthregulators and antioxidants on callus induction and plantregeneration from seed culture of orchardgrass. Journal of theKorean Society of Grassland Science 25(3):191-198; 2005.
Levine, B.; Klionsky, D. J. Development by self-digestion:molecular mechanisms and biological functions of autophagy. Dev.Cell 6:463-477; 2004.
Li, W.; Dickman, M. B. Abiotic stress induces apoptotic-likefeatures in tobacco that is inhibited by expression of human Bcl-2.Biotechnol. Lett. 26:87-95; 2004.
Lincoln, J. E.; Richael, C.; Overduin, B.; Smith, K.; Bostock, R.;Gilchrist, D. G. Expression of the anti-apoptotic baculovirus p35gene in tomato blocks programmed cell death and provides broad-spectrum resistance to disease. Proc. Natl. Acad. Sci. USA 99:15217- 15221; 2002.
Liu, Y; Schiff, M.; Czymmek, K.; Talloczy, Z.; Levine, B.;DineshKumar, S. P.: Autophagy regulates programmed cell deathduring the plant innate immune response. Cell 121:567-577; 2005.
Marnett, L. J. Oxyradicals and DNA damage. Carcinogenesis 21:361-370; 2000.
Miller, D. K.; Smith, V. L.; Kanner, J.; Miller, D. D.; Lawless, H.T. Lipid oxidation and warmed-over aroma in cooked ground pork fromswine fed increasing levels of iron. J. Food Sci. 59:751-756; 1994.
Moore, G. A.; Jacono, C. C.; Neidigh, J. L.; Lawrence, S. D.;Cline, K. Agrobacterium-mediated transformation of citrus stemsegments and regeneration of transgenic plants. Plant Cell Rep.11:238-242; 1992.
Mourgues, F.; Chevreau, E.; Lambert, C.; Bondt, A. EfficientAgrobacterium-mediated transformation and recovery of transgenicplants from pear (Pyrus communis L.). Plant Cell Rep. 16:245-249;1996.
Mukai, K.; Morimoto, H.; Okauchi, Y.; Nagaoka, S. Kinetic study ofreactions between tocopheroxyl radicals and fatty acids. Lipids28:753-756; 1993.
Murkute, A., A.; Patil, S.; Mayakumari. Exudation and browning intissue culture of pomegranate. Agricultural Science Digest 23(1):29- 31; 2003.
Nagata, S. Apoptosis by death factor. Cell 85:817-827; 1997.
Nakagami H.; Kiegerl, S.; Hirt, H. OMTK1, a novel MAPKKK, channelsoxidative stress signaling through directMAPK interaction. J. Biol.Chem. 279: 26959-26966; 2004.
Nomura, K.; Matsumoto, S.; Masuda, K.; Inoue, M. Reducedglutathione promotes callus growth and shoot development in a shoottip culture of apple root stock M.26. Plant Cell Rep. 17 (8):597-600; 1998.
Nordberg, J.; Amer, E. S. J. Reactive oxygen species, antioxidants,and the mammalian thioredoxin system. Free Radical Biol. Med.31:1287-1312; 2001.
Olhoft, P. M.; Flagel, L. E.; Donovan, C. M.; Somers, D. A.Efficient soybean transformation using hygromycin B selection inthe cotyledonary-node method. Planta 216:723-735; 2003.
Olhoft, P. M.; Lin, K.; Galbraith, J.; Nielsen, N. C.; Somers, D.A. The role of thiol compounds increasing Agrobacterium-mediatedtransformation of soybean cotyledonary-node cells. Plant Cell Rep.20:731-737; 2001a.
Olhoft, P. M.; Somers, D. A. 1-Cysteine increasesAgrobacteriummediated T-DNA delivery into soybean cotyledonary-nodecells. Plant Cell Rep. 20:706-711; 200 lb.
Packer, L.; Tritschler, H. Alpha-lipoic acid: The metabolicantioxidant. Free Radie. Biol. Med. 20: 625-626; 1996.
Packer, L.; Tritschler, H.; Wessel, K. Neuroprotection by themetabolic antioxidant alpha-lipoic acid. Free Radical Biol. Med.22:359-378; 1997.
Packer, L.; Witt, E.; Tritschler, H. Alpha-lipoic acid as abiological antioxidant. Free Rad. Biol. Med. 19:227-250; 1995.
Palmer, R. M. J.; Ferrige, A. G.; Moncada, S. Nitric oxide releaseaccounts for the biological activity of endothelium-derivedrelaxing factor. Nature 327:524-526; 1987.
Park, H. R.; Jung, H. H.; Kim, K. S. Ascorbic acid and citric acidreduce expiant darkening during shoot tip culture of Adonisamurensis. Hortic. Environ. Biotechnol. 47(1):41-44; 2006.
Patel, R. P.; McAndrew, J.; Sellak, H.; White, C. R.; Jo, H.;Freeman, B. A.; Darley-Usmar, V. M. Biological aspects of reactivenitrogen species. Biochim. Biophys. Acta 1411(2):385-400; 1999.
Patel, S.; Caplan, J.; Dinesh-Kumar, S. P. Autophagy in the controlof programmed cell death. Curr. Opin. Plant Biol. 9(4):391- 396;2006.
Pattingre, S.; Tassa, A.; Qu, X.; Garuti, R.; Liang, X. H.;Mizushima, N.; Packer, M.; Schneider, M. D.; Levine, B. Bcl-2antiapoptotic proteins inhibit Beclin !-dependent autophagy. Cell122:927-939; 2005.
Pena, L.; Cervera, M.; Juarez, J.; Navarro, A.; Pina, J. A.;Duran-Vila, N.; Navarro, L. Agrobacterium-mediated transformationof sweet orange and regeneration of transgenic plants. Plant CellRep. 14:616-619; 1995b.
Pena, L.; Cervera, M.; Juarez, J.; Navarro, A.; Pina, J. A.;Navarro, L.; Rep, P. C. Genetic transformation of lime (Citrusaurantifolia Swing.): factors affecting transformation andregeneration. Plant Cell Rep. 16:731-737; 1997.
Pena, L.; Cervera, M.; Juarez, J.; Ortega, C.; Pina, J. A.; Duran-Vila, N.; Navarre, L. High-efficiency Agmbacterium-mediatedtransformation and regeneration of citrus. Plant Sci. 104:183-191;1995a.
Perl, A.; Lotan, O.; Abu-Abied, M.; Holland, D. Establishment of anAgrobacterium-mediated transformation system for grape (Vitisvinifera L.): Establishment of an Agmbacterium-mediatedtransformation system for grape (Vitis vinifera L.): the role ofantioxidants during grape-Agrobacterium interactions. Nat.Biotechnol. 14(5):624-628; 1996.
Poleschuk, S. V.; Gorbatenko, I. Y. Effect of the syntheticantioxidant phenoxane on the regeneration and ontogeny of thetomato in vitro. Russ. Agric. Sci. 5(5):15-17; 1995.
Pu, X. A.; Goodman, R. N. Induction of necrosis by Agrobacteriumtumefaciens on grape explants. Physiol. Mol. Plant Pathol. 41:245-254; 1992.
Qiu, W., P.; Fekete, S.; Todd, T.; Kovacs, L. Facilitation ofmicroshoot tip propagation of Vitis aestivalis var. Norton bycombined application of an antioxidant and cytokinins. Am. J. Enol.Vitic. 55(1): 112-114; 2004.
Ramanathan, L.; Das, N. P. Natural products inhibit oxidativerancidity in salted cooked ground fish. J. Food Sci. 58:318-320;1993.
Ren, D.; Yang, H.; Zhang, S. Cell death mediated byMAPK isassociated with hydrogen peroxide production in Arabidopsis. J.Biol. Chem. 277:559-565; 2002.
Rhee, S. G. Redox signaling: hydrogen peroxide as intracellularmessenger. Exp. Mol. Med. 31:53-59; 1999.
Samuel, M. A.; Ellis, B. E. Double jeopardy: both overexpressionand suppression of a redox-activated plant-mitogen-activatedprotein kinase render tobacco plants ozone sensitive. Plant Cell14:2059- 2069; 2002.
Samuel, M.A.; Hall, H.; Krzymowska, M.; Drzewiecka, K.; Hennig, J.;Ellis, B.E. SIPK signaling controls multiple components ofharpin-induced cell death in tobacco. Plant J 42: 406-416; 2005.
Shaw, C. H.; Loake, G. J.; Brown, A. P.; Garrett, C. S. The earlyevents in Agrobacterium infection. In: Smith, C. J. ed.,Biochemistry and molecular biology of plant-pathogen interactions.Oxford: Clarendon Press; 1991:197-209.
Somssich, I. E.; Hahlbrock, K. Pathogen defense in plants-aparadigm of biological complexity. Trends Plant Sci. 3:86-90; 1998.
Soobratteea, M. A.; Neergheena, V. S.; Luximon-Rammaa, A.; Aruomab,O. I.; Bahoruna, T. Phenolics as potential antioxidant therapeuticagents: mechanism and actions. Mutat. Res. 579:200-213; 2005.
Soosaar, J.L.; Burch-Smith, T. M.; Dinesh-Kumar, S.P. Mechanisms ofplant resistance to viruses. Nat. Rev. Microbiol. 3:789-798; 2005.
Stipic, M.; Rotino, G. L.; Piro, F. Regeneration and genetictransformation attempts in the cauliflower 'Tardivo di Fano'.Italus Hortus 7(2):20-26; 2000.
Sundaresan, M.; Yu, Z. X.; Ferrans, V. J.; Irani, K.; Finkel, T.Requirement for generation of H2O2 for platelet-derived growthfactor signal transduction. Science 270:296-299; 1995.
Takayama, S.; Takai, A. Effect of antioxidant compound BHA ongrowth of potato shoots cultured in vitro. Journal of Society ofHigh Technology in Agriculture 16(1):11-15; 2004.
Tian, M.; Gu, Q.; Zhu, M. Y. The involvement of hydrogen peroxideand antioxidant enzymes in the process of shoot organogenesis ofstrawberry callus. Plant Sci. 165(4):701-707; 2003.
Tian, M.; Han, N.; Bian, H. W.; Zhu, M. Y. The possiblerelationship between the regeneration capacity and reactive oxygenspecies in the strawberry calli. Acta Horticulturae Sinica31(3):372- 374; 2004.
Toldi, O.; Toth, S.; Ponyi, T; Scott, P. An effective andreproducible transformation protocol for the model resurrectionplant Craterostigma plantagineum Hochst. Plant Cell Rep. 21(1):63-69; 2002.
Torres, M. A.; Dangl, J. L. Functions of the respiratory burstoxidase in biotic interactions, abiotic stress and development.Curr. Opin. Plant Biol. 8:397-403; 2005.
Toth, S.; Scott, P.; Sorvari, S.; Toldi, O. Effective andreproducible protocols for in vitro culturing and plantregeneration of the physiological model plant Ramonda myconi (L.)Rchb. Plant Sci. 166(4): 1027-1034; 2004. von Sonntag, C. Thechemical basis of radiation biology. London: Taylor and Francis;1987.
Wagner, D.; Przybyla, D.; op den Camp, R.; Kim, C.; Landgraf, F.;Lee, K. P.; Wursch, M.; Laloi, C.; Nater, M.; Hideg, E. et al. Thegenetic basis of singlet oxygen induced stress responses ofArabidopsis thaliana. Science 306:1183-1185; 2004.
Wang, Z. M.; Hu, L. B.; Yi, G. H.; Xu, H.; Qi, Y. P.; Yao, L. N.ORF390 of white spot syndrome virus genome is identified as a novelanti-apoptosis gene. Biochem. Biophys. Res. Commun. 325 (3):899-907; 2004.
Wojtaszek, P. Oxidative burst: an early plant response to pathogeninfection. Biochem. J. 322:681-691; 1997.
Wu, G.; Shortt, B. J.; Lawrence, E. B.; Levine, E. B.; Fitzsimons,K. C.; Shah, D. M. Disease resistance conferred by expression ofgene encoding H2O2-generating glucose oxidase in transgenic potatoplants. Plant Cell 7:1357-1368; 1995.
Wu, H. C.; Toit, E. S. D. Reducing oxidative browning during invitro establishment of Protea cynaroides. Scientia Horticulturae100(1/ 4):355-358; 2004.
Xu, P.; Rogers, S. J.; Roossinck, M. J. Expression of antiapoptoticgenes bcl-xL and ced-9 in tomato enhances tolerance to viralinducednecrosis and abiotic stress. Proc. Natl. Acad. Sci. USA101:15805-15810; 2004.
Yan, G. Q.; Tian, L. H.; Yang, L. Y. Studies on the browning incallus induction of Elaeagnus mollis. Acta Botanica Boreali-Occidentalia Sinica 24(8):1384-1389; 2004.
Yu, L.; Alva, A.; Su, H.; Dutt, P.; Freundt, E.; Welsh, S.;Baehrecke, E. H.; Lenardo, M. J. Regulation of an ATG7-beclin 1program of autophagic cell death by caspase-8. Science 304:1500-1502; 2004.
Zeng, P.; Vadnais, D. A.; Zhang, Z.; Polacco, J. C. Refinedglufosinate selection in Agrobacterium-mediated transformation ofsoybean Glycine max (L.) Merrill. Plant Cell Rep. 22(7):478-482;2004.
Zheng, D.; Zhang, H.; Carle, S.; Hao, G.; Holden, M. R.; Burr, T.J. A luxR homolog, aviR, in Agmbacterium vitis is associated withinduction of necrosis on grape and a hypersensitive response ontobacco. Mol. Plant Microbe Interact. 16:650-658; 2003.
Zheng, Q. S., Ju B., Liang L. K., Xiao X. H. Effects ofantioxidants on the plant regeneration and GUS expressive frequencyof peanut (Arachis hypogaea) expiants by Agrobacterium tumefaciens.Plant Cell Tissue Organ Cult 811: 83-89; 2005.
Ziv, M.; Halevy, A. H. Control of oxidative browning and in vitropropagation of Strelitzia reginae. HortScience 18(4):434-436; 1983.
Y. Dan (*)
Institute for Sustainable and Renewable Resources,
Institute for Advanced Learning and Research,
150 Slayton Avenue,
Danville, VA 24540, USA
e-mail: Yinghui.dan@ialr.org
Y. Dan
Department of Horticulture and Forestry,
Virginia Polytechnic Institute and State University,
Blacksburg, VA 24061, USA
Copyright Society for In Vitro Biology May/Jun 2008
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