The Effects of Pharmacological Carbonic Anhydrase Suppression on Defence Responses of Potato Leaves To Phytophthora Infestans
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Abstract
In this study we proposed carbonic anhydrase (CA) as an important element of basal resistance during the potato (Solanum tuberosum L.)-Phytophthora infestans interaction. We found a different β-CA expression pattern in incompatible vs. compatible systems correlated in time with CA enzyme activity. Resistant potato leaves supplied with dorzolamide (an inhibitor of carbonate CA activity) and challenged with the pathogen showed an elevated nitric oxide (NO) synthesis, which was the most evident during the early phase of NO burst (at 3 hpi) during hypersensitive response (HR). In vitro application of dorzolamide and effective inhibitors of NO synthesis confirmed the implication of CA activity in NO metabolism during potato defense. To clarify how suppression of CA carbonate activity translates into the complexity of NO-related responses leading to potato resistance or susceptibility to an oomycete pathogen we analysed expression of NPR, PR1, and PAL.
Taken together, pharmacological damping of CA activity revealed a functional link between CA and NO-dependent signaling in potato defense against P. infestans manifested by accelerated NO formation and a modified salicylic acid defense pathway. The dorzolamide-mediated effective responses for basal resistance also delayed symptoms of late blight in the susceptible potato cultivar, without overcoming HR formation in the resistant one.
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Moroney JV, Bartlett SG, Samuelsson G. Carbonic anhydrases in plants and algae. Plant CellEnviron. 2001; 24: 141-153. Ref.: https://goo.gl/YTHFVd
DiMario RJ, Quebedeaux JC, Longstreth DJ, Dassanayake M, Hartman MM, et al. The cytoplasmic carbonic anhydrases βCA2 and βCA4 are required for optimal plant growth at low CO2. Plant Physiol. 2016; 171: 280-293. Ref.: https://goo.gl/nOYqS2
Badger MR, Price GD. The Role of Carbonic anhydrase in photosynthesis. Annu Rev Plant Physiol Plant Mol Biol. 1994; 45: 369-392. Ref.: https://goo.gl/DxgDJ7
Reed ML, Graham D. Carbonic anhydrase in plants: distribution, properties and possible physiological roles, In: Progress in phytochemistry, Pergamon Press, Oxford, Reinhold L, Harborne JB, Swaquin T. 1981; 7: 47-94.
Badger M. The roles of carbonic anhydrases in photosynthetic CO2 concentrating mechanisms. Photosynth Res. 2003; 77: 83-94. Ref.: https://goo.gl/ee26MF
Tobin AJ. Carbonic anhydrase from parsley leaves. J Biol Chem. 1970; 245: 2656-2666. Ref.: https://goo.gl/G1h6WD
Fabre N, Reiter IM, Becuwe-Linka N, Genty B, Rumeau D. Characterization and expression analysis of genes encoding alpha and beta carbonic anhydrases in Arabidopsis. Plant Cell Environ. 2007; 30: 617-629. Ref.: https://goo.gl/UQDkoH
Kaul T, Reddy PS, Mahanty S, Thirulogachandar V, Reddy RA, et al. Biochemical and molecular characterization of stress-induced β-carbonic anhydrase from a C(4) plant, Pennisetum glaucum. J Plant Physiol. 2011; 168: 601-610. Ref.: https://goo.gl/99FF4U
Pal A, Borthakur D. Tissue-specific differential expression of two β-carbonic anhydrases in Leucaena leucocephala under abiotic stress conditions. J Appl Biotechnol. 2014; 2: 43. Ref.: https://goo.gl/MI0gVx
Yu S, Zhang X, Guan Q, Takano T, Liu S. Expression of a carbonic anhydrase gene is induced by environmental stresses in Rice (Oryza sativa L.). Biotechnol Lett. 2007; 29: 89-94. Ref.: https://goo.gl/XyFgQz
Slaymaker DH, Navarre DA, Clark D, Del Pozo O, Martin GB, et al. The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response. Proc Natl Acad Sci U S A. 2002; 99: 11640-11645. Ref.: https://goo.gl/Jvy8W1
Wang YQ, Feechan A, Yun BW, Shafiei R, Hofmann A. S-Nitrosylation of AtSABP3 antagonizes the expression of plant immunity. J Biol Chem. 2009; 284: 2131-2137. Ref.: https://goo.gl/mzYzRF
Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Izbiańska K, Gzyl J, Jelonek T. Implication of peroxynitrite in defence responses of potato to Phytophthora infestans. Plant Pathol. 2015; 65: 754-766. Ref.: https://goo.gl/c13iic
Abramowski D, Arasimowicz-Jelonek M, Izbianska K, Billert H, Floryszak-Wieczorek J. Nitric oxide modulates redox-mediated defense in potato challenged with Phytophthora infestans. Eur J Plant Pathol. 2015; 143: 237-260. Ref.: https://goo.gl/uU1LN6
Kato H, Takemoto D, Kawakita K. Proteomic analysis of S-nitrosylated proteins in potato plant. Physiol Plant. 2013; 148: 371-386. Ref.: https://goo.gl/J77aZz
Chaki M, Valderrama R, Fernández-Ocaña AM, Carreras A, Gómez-Rodríguez MV, et al. High temperature triggers the metabolism of S-nitrosothiols in sunflower mediating a process of nitrosative stress which provokes the inhibition of ferredoxin-NADP reductase by tyrosine nitration. Plant Cell Environ. 2011; 34: 1803-1818. Ref.: https://goo.gl/VHju6f
Lozano-Juste J, Colom-Moreno R, Leon J. In vivo protein tyrosine nitration in Arabidopsis thaliana. J Exp Bot. 2011; 62: 3501-3517. Ref.: https://goo.gl/mQQ1zj
Restrepo S, Myers KL, del Pozo O, Martin GB, Hart AL, et al. Gene profiling of a compatible interaction between Phytophthora infestans and Solanum tuberosum suggests a role for carbonic anhydrase. Mol Plant-Microbe Interact. 2005; 18: 913-922. Ref.: https://goo.gl/DkK63s
Hoang CV, Chapman KD. Biochemical and molecular inhibition of plastidial carbonic anhydrase reduces the incorporation of acetate into lipids in cotton embryos and tobacco cell suspensions and leaves. Plant Physiol. 2002; 128: 1417-1427. Ref.: https://goo.gl/SlsBpI
Arasimowicz-Jelonek M, Kosmala A, Janus Ł, Abramowski D, Floryszak-Wieczorek J. The proteome response of potato leaves to priming agents and S-nitrosoglutathione. Plant Sci. 2013; 198: 83-90. Ref.: https://goo.gl/MQAc2e
Janus Ł, Milczarek G, Arasimowicz-Jelonek M, Abramowski D, Billert H, et al. Normoergic NO-dependent changes, triggered by a SAR inducer in potato, create more potent defense responses to Phytophthora infestans. Plant Sci.2013; 211: 23-34. Ref.: https://goo.gl/Jv7QUE
Aamand R, Dalsgaard T, Jensen FB, Simonsen U, Roepstorff A, et al. Generation of nitric oxide from nitrite by carbonic anhydrase: a possible link between metabolic activity and vasodilation. Am J Physiol Heart Circ Physiol.2009; 297: 2068-2074. Ref.: https://goo.gl/6roFif
Floryszak-Wieczorek J, Arasimowicz-Jelonek M, Abramowski D, Izbiańska K. Redox-sensing responses in the potato-Phytophthora infestans system. Oxidative stress and cell death in plants: Mechanisms and implications. Abstract book. 2013; 53.
James WC. An illustrated serioes of assesment keys for plant diseases, their preparation and usage. Can Plant Dis Surv. 1971; 51: 39-65. Ref.: https://goo.gl/nVAfHa
Floryszak-Wieczorek J, Arasimowicz-Jelonek M, Milczarek G, Janus Ł, Pawlak-Sprada S, et al. Nitric oxide-mediated stress imprint in potato as an effect of exposure to a priming agent. Mol Plant Microbe Interact. 2012; 25: 1469-1477. Ref.: https://goo.gl/WfVyIk
Floryszak-Wieczorek J, Arasimowicz M, Milczarek G, Jelen H, Jackowiak H. Only an early nitric oxide burst and the following wave of secondary nitric oxide generation enhanced effective defence responses of pelargonium to a necrotrophic pathogen. New Phytol. 2007; 175: 718-730. Ref.: https://goo.gl/kIo5yH
Ciszewski A, Milczarek G. Electrochemical detection of nitric oxide using polymer modified electrodes. Talanta. 2003; 61: 11-26. Ref.: https://goo.gl/Keq3Bl
Li X, Hou J, Bai K, Yang X, Lin J, et al. Activity and distribution of carbonic anhydrase in leaf and ear parts of wheat (Triticum aestivum L.). Plant Sci. 2004; 166: 627-632. Ref.: https://goo.gl/fRkpvU
Chomcznski P, Sacchi N. Single-step method of RNA isolation by acid quanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987; 162: 156-159. Ref.: https://goo.gl/pPMqaM
Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, et al. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics. 2012; 13: 134. Ref.: https://goo.gl/Ul4fKq
Zhao S, Fernald RD. Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol. 2005; 12: 1047-1064. Ref.: https://goo.gl/1pWkir
Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001; 29: e45. Ref.: https://goo.gl/m6yWxi
Freytag S, Arabatzis N, Hahlbrock K, Schmelzer E. Reversible cytoplasmic rearrangements precede wall apposition, hypersensitive cell death and defense-related gene activation in potato/Phytophthora infestans interactions. Planta. 1994; 194: 123-135. Ref.: https://goo.gl/UnStrJ
Orłowska E, Fiil A, Kirk HG, Llorente B, Cvitanich C. Differential gene induction in resistant and susceptible potato cultivars at early stages of infection by Phytophthora infestans. Plant Cell Rep. 2012; 31: 187-203. Ref.: https://goo.gl/J5PgmE
Floryszak-Wieczorek J, Arasimowicz-Jelonek M. Contrasting regulation of NO and ROS in potato defense-associated metabolism in response to pathogens of different lifestyles. PLoS ONE. 2016; 11: e0163546. Ref.: https://goo.gl/mLeVGU
Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, et al. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci U S A. 2000; 97: 11655-11660. Ref.: https://goo.gl/2EMtiO
Frick UB, Schaller A. cDNA micrarray analysis of fusicoccin-induced changes in gene expression in tomato plants. Planta. 2002; 216: 83-94. Ref.: https://goo.gl/ov4jDj
Polesani M, Desario F, Ferrarini A, Zamboni A, Pezzotti M, et al. cDNA-AFLP analysis of plant and pathogen genes expressed in grapevine infected with Plasmopara viticola. BMC Genomics. 2008; 9: 142. Ref.: https://goo.gl/bdtgfe
Leitner M, Vandelle E, Gaupels F, Bellin D, Delledonne M. NO signals in the haze: nitric oxide signalling in plant defence. Curr Opin Plant Biol. 2009; 12: 451-458. Ref.: https://goo.gl/NqKiJ4
Delledonne M, Xia Y, Dixon RA, Lamb C. Nitric oxide functions as a signal in plant disease resistance. Nature. 1998; 394: 585-588. Ref.: https://goo.gl/wLVmaL
Kolbert Z, Sahin N, Erdei L. Early nitric oxide (NO) responses to osmotic stress in pea, Arabidopsis and wheat. Acta Biol Szeged. 2008; 52: 63-65. Ref.: https://goo.gl/J5LxLN
Kolbert Z, Ortega L, Erdei L. Involvement of nitrate reductase (NR) in osmotic stress-induced NO generation of Arabidopsis thaliana L. roots. J Plant Physiol. 2010; 167: 77-80. Ref.: https://goo.gl/6XWvX1
Huang J, Bellin D, Chen J, Fontanesi K, Klainfelder Delledonne M. Novel pathway in formation of NO from nitrite uder normoxic conditions in Arabidopsis. 4th Plant NO Club International Meeting. Edinburgh UK Book of Abstract. 2012.
Rumeau D, Cuine S, Fina L, Gault N, Nicole M, et al. Subcellular distribution of carbonic anhydrase in Solanum tuberosum L. leaves: Characterization of two compartment-specific isoforms. Planta. 1996; 199: 79-88. Ref.: https://goo.gl/QLY5nW
Winter H, Robinson DG, Heldt HW. Subcellular volumes and metabolite concentrations in spinach leaves. Planta. 1994; 193: 530-535. Ref.: https://goo.gl/YwlSLv