AAO2 impairment enhances aldehyde detoxification by AAO3 in Arabidopsis leaves exposed to UV-C or Rose-Bengal

. 2024 Oct ; 120 (1) : 272-288. [epub] 20240827

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39190782

Grantová podpora
CZ.02.1.01/0.0/0.0/16_019/0000827 European Regional Development Fund-Project
757/12 Israel Center of Research Excellence (Plant Adaptation)

Among the three active aldehyde oxidases in Arabidopsis thaliana leaves (AAO1-3), AAO3, which catalyzes the oxidation of abscisic-aldehyde to abscisic-acid, was shown recently to function as a reactive aldehyde detoxifier. Notably, aao2KO mutants exhibited less senescence symptoms and lower aldehyde accumulation, such as acrolein, benzaldehyde, and 4-hydroxyl-2-nonenal (HNE) than in wild-type leaves exposed to UV-C or Rose-Bengal. The effect of AAO2 expression absence on aldehyde detoxification by AAO3 and/or AAO1 was studied by comparing the response of wild-type plants to the response of single-functioning aao1 mutant (aao1S), aao2KO mutants, and single-functioning aao3 mutants (aao3Ss). Notably, aao3Ss exhibited similar aldehyde accumulation and chlorophyll content to aao2KO treated with UV-C or Rose-Bengal. In contrast, wild-type and aao1S exhibited higher aldehyde accumulation that resulted in lower remaining chlorophyll than in aao2KO leaves, indicating that the absence of active AAO2 enhanced AAO3 detoxification activity in aao2KO mutants. In support of this notion, employing abscisic-aldehyde as a specific substrate marker for AAO3 activity revealed enhanced AAO3 activity in aao2KO and aao3Ss leaves compared to wild-type treated with UV-C or Rose-Bengal. The similar abscisic-acid level accumulated in leaves of unstressed or stressed genotypes indicates that aldehyde detoxification by AAO3 is the cause for better stress resistance in aao2KO mutants. Employing the sulfuration process (known to activate aldehyde oxidases) in wild-type, aao2KO, and molybdenum-cofactor sulfurase (aba3-1) mutant plants revealed that the active AAO2 in WT employs sulfuration processes essential for AAO3 activity level, resulting in the lower AAO3 activity in WT than AAO3 activity in aao2KO.

Erratum v

PubMed

Zobrazit více v PubMed

Akaba, S., Leydecker, M.T., Moureaux, T., Oritani, T. & Koshiba, T. (1998) Aldehyde oxidase in wild type and aba1 mutant leaves of Nicotiana plumbaginifolia. Plant & Cell Physiology, 39, 1281–1286. Available from: https://doi.org/10.1093/oxfordjournals.pcp.a029331

Akaba, S., Mitsunori, S., Dohmae, N., Takio, K., Sekimoto, H., Kamiya, Y. et al. (1999) Production of homo‐ and hetero‐dimeric isozymes from two aldehyde oxidase genes of Arabidopsis thaliana. Journal of Biochemistry, 126, 395–401. Available from: https://doi.org/10.1093/oxfordjournals.jbchem.a022463

Bekturova, A., Oshanova, D., Tiwari, P., Nurbekova, Z., Kurmanbayeva, A., Soltabayeva, A. et al. (2021) Adenasine 5′ phosphosulfate reductase and sulfite oxidase regulate sulfite‐induced loss in Arabidopsis. Journal of Experimental Botany, 72, 6447–6466. Available from: https://doi.org/10.1093/jxb/erab249

Bindschedler, L.V. & Cramer, R. (2011) Quantitative plant proteomics. Proteomics, 11, 756–775. Available from: https://doi.org/10.1002/pmic.201000426

Biswas, M.S., Fukaki, H., Mori, I.C., Nakahara, K. & Mano, J. (2019) Reactive oxygen species and reactive carbonyl species constitute a feed‐forward loop in auxin signaling for lateral root formation. The Plant Journal, 100, 536–548. Available from: https://doi.org/10.1111/tpj.14456

Biswas, M.S. & Mano, J. (2015) Lipid peroxide‐derived short‐chain carbonyls mediate hydrogen peroxide‐induced and salt‐induced programmed cell death in plants. Plant Physiology, 168, 885–898. Available from: https://doi.org/10.1104/pp.115.256834

Biswas, M.S. & Mano, J. (2016) Reactive carbonyl species activate caspase‐3‐like protease to initiate programmed cell death in plants. Plant & Cell Physiology, 57, 1432–1442. Available from: https://doi.org/10.1093/pcp/pcw053

Bittner, F., Oreb, M. & Mendel, R.R. (2001) ABA3 is a molybdenum cofactor sulfurase required for activation of aldehyde oxidase and xanthine dehydrogenase in Arabidopsis thaliana. The Journal of Biological Chemistry, 276, 40381–40384. Available from: https://doi.org/10.1074/jbc.C100472200

Bottcher, C., Chapman, A., Fellermeier, F., Choudhary, M., Scheel, D. & Glawischnig, E. (2014) The biosynthetic pathway of indole‐3‐carbaldehyde and indole‐3‐carboxylic acid derivatives in Arabidopsis. Plant Physiology, 165, 841–853. Available from: https://doi.org/10.1104/pp.114.235630

Bower, P., Brown, H. & Purves, W. (1978) Cucumber seedling indole acetaldehyde oxidase. Plant Physiology, 61, 107–110. Available from: https://doi.org/10.1104/pp.61.1.107

Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein‐dye binding. Analytical Biochemistry, 72, 248–254. Available from: https://doi.org/10.1016/0003‐2697(76)90527‐3

Brychkova, G., Alikulov, Z., Fluhr, R. & Sagi, M. (2008) A critical role for ureides in dark and senescence‐induced purine remobilization is unmasked in the Atxdh1 Arabidopsis mutant. The Plant Journal, 54, 496–509. Available from: https://doi.org/10.1111/j.1365‐313X.2008.03440.x

Brychkova, G., Xia, Z., Yang, G., Yesbergenova, Z., Zhang, Z., Davydov, O. et al. (2007) Sulfite oxidase protects plants against sulfur dioxide toxicity. The Plant Journal, 50, 696–709. Available from: https://doi.org/10.1111/j.1365‐313X.2007.03080.x

Clough, S.J. & Bent, A.F. (1998) Floral dip: a simplified method for agrobacterium‐mediated transformation of Arabidopsis thaliana. The Plant Journal., 6, 735–743. Available from: https://doi.org/10.1046/j.1365‐313x.1998.00343.x

González‐Guzmán, M., Abia, D., Salinas, J., Serrano, R. & Rodríguez, P.L. (2004) Two new alleles of the abscisic aldehyde oxidase 3 gene reveal its role in Abscisic acid biosynthesis in seeds. Plant Physiology, 135, 325–333. Available from: https://doi.org/10.1104/pp.103.036590

Graan, T. & Ort, D.R. (1984) Quantitation of the rapid electron donors to P700, the functional plastoquinone pool, and the ratio of the photosystems in spinach chloroplasts. The Journal of Biological Chemistry, 22, 14003–14010. Available from: https://doi.org/10.1016/S0021‐9258(18)89845‐3

Havaux, M. & Triantaphylides, C. (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends in Plant Science, 14, 219–228. Available from: https://doi.org/10.1016/j.tplants.2009.01.008

Ibdah, M., Chen, Y.T., Wilkerson, C.G. & Pichersky, E. (2009) An aldehyde oxidase in developing seeds of Arabidopsis converts benzaldehyde to benzoic acid. Plant Physiology, 150, 416–423. Available from: https://doi.org/10.1104/pp.109.135848

Keren, N., Berg, A., Van Kan, P.J., Levanon, H. and Ohad, I. (1997) Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: the role of back electron flow. Proceedings of the National Academy of Sciences of the United States of America, 94(4), 1579‐1584. https://doi.org/10.1073/pnas.94.4.1579

Knox, J.P. & Dodge, A.D. (1984) Photodynamic damage to plant leaf tissue by Rose Bengal. Plant Science Letters, 37, 3–7. Available from: https://doi.org/10.1016/0304‐4211(84)90194‐9

Koiwai, H., Nakaminami, K., Seo, M., Mitsuhashi, W., Toyomasu, T. & Koshiba, T. (2004) Tissue‐specific localization of an abscisic acid, enzyme AAO3, in Arabidopsis. Plant Physiology, 134, 1697–1707. Available from: https://doi.org/10.1104/pp.103.036970

Koshiba, T., Saito, E., Ono, N., Yamamoto, N. & Sato, M. (1996) Purification and properties of flavin‐ and molybdenum‐containing aldehyde oxidase from coleoptiles of maize. Plant Physiology, 110, 781–789. Available from: https://doi.org/10.1104/pp.110.3.781

Kurmanbayeva, A., Bekturova, A., Srivastava, S., Soltabayeva, A., Asatryan, A., Ventura, Y. et al. (2017) Higher novel l‐Cys degradation activity results in lower organic‐S and biomass in sarcocornia than the related Saltwort, Salicornia. Plant Physiology, 175, 272–289. Available from: https://doi.org/10.1104/pp.17.00780

Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680–685.

Mano, J. & Biswas, M.S. (2018) Analysis of reactive carbonyl species generated under oxidative stress. Methods in Molecular Biology, 1742, 117–124. Available from: https://doi.org/10.1007/978‐1‐4939‐7668‐3_11

Mano, J., Kanameda, S., Kuramitsu, R., Matsuura, N. & Yamauchi, Y. (2019) Detoxification of reactive carbonyl species by glutathione transferase tau isozymes. Frontiers in Plant Science, 10, 1–7. Available from: https://doi.org/10.3389/fpls.2019.00487

Mano, J., Nagata, M., Okamura, S., Shiraya, T. & Mitsui, T. (2014) Identification of oxidatively modified proteins in salt‐stressed Arabidopsis: a carbonyl‐targeted proteomics approach. Plant and Cell Physiology, 55, 1233–1244. Available from: https://doi.org/10.1093/pcp/pcu072

Mano, J., Tokushige, K., Mizoguchi, H., Fujii, H. & Khorobrykh, S. (2010) Accumulation of lipid peroxide‐derived, toxic α,β‐unsaturated aldehydes (E)‐2‐pentenal, acrolein and (E)‐2‐hexenal in leaves under photoinhibitory illumination. Plant Biotechnology, 27, 193–197. Available from: https://doi.org/10.5511/plantbiotechnology.27.193

Mano, J., Torii, Y., Hayashi, S., Takimoto, K., Matsui, K., Nakamura, K. et al. (2002) The NADPH:Quinone oxidoreductase P1‐ζ‐crystallin in Arabidopsis catalyzes the α,β‐hydrogenation of 2‐alkenals: detoxication of the lipid peroxide‐derived reactive aldehydes. Plant and Cell Physiology, 43, 1445–1455. Available from: https://doi.org/10.1093/pcp/pcf187

Matsui, K., Sugimoto, K., Kakumyan, P., Khorobrykh, S. & Mano, J. (2009) Volatile oxylipins formed under stress in plants. Methods in Molecular Biology, 580, 17–27. Available from: https://doi.org/10.1007/978‐1‐60761‐325‐1_2

Mendel, R.R. (2022) The history of the molybdenum cofactor—a personal view. Molecules, 27, 4934. Available from: https://doi.org/10.3390/molecules27154934

Nurbekova, Z., Srivastava, S., Standing, D., Kurmanbayeva, A., Bekturova, A., Soltabayeva, A. et al. (2021) Arabidopsis aldehyde oxidase 3, known to oxidize abscisic aldehyde to abscisic acid, protects leaves from aldehyde toxicity. The Plant Journal, 108, 1439–1455. Available from: https://doi.org/10.1111/tpj.15521

Oberschall, A., Deák, M., Török, K., Sass, L., Vass, I., Kovács, I. et al. (2000) A novel aldose/aldehyde reductase protects transgenic plants against lipid peroxidation under chemical and drought stresses. The Plant Journal, 24, 437–446.

Omarov, R.T., Akaba, S., Koshiba, T. & Lips, S.H. (1999) Aldehyde oxidase in roots, leaves and seeds of barley (Hordeum vulgare L.). Journal of Experimental Botany, 50, 63–69. Available from: https://doi.org/10.1093/jxb/50.330.63

Omarov, R.T., Sagi, M. & Lips, S.H. (1998) Regulation of aldehyde oxidase and nitrate reductase in roots of barley (Hordeum vulgare L.) by nitrogen source and salinity. Journal of Experimental Botany, 49, 897–902. Available from: https://doi.org/10.1093/jxb/49.322.897

Oshanova, D., Kurmanbayeva, A., Bekturova, A., Soltabayeva, A., Nurbekova, Z., Standing, S. et al. (2021) Level of sulfite oxidase activity affects sulfur and carbon metabolism in Arabidopsis. Frontiers in Plant Science, 12, 690830. Available from: https://doi.org/10.3389/fpls.2021.690830

Rothe, G.M. (1974) Aldehyde oxidase isoenzymes (E.C.1.2.3.1) in potato tubers (Solanum tuberosum). Plant and Cell Physiology, 15, 493–499. Available from: https://doi.org/10.1093/oxfordjournals.pcp.a075029

Ruggiero, B., Koiwa, H., Manabe, Y., Quist, T.M., Inan, G., Saccardo, F. et al. (2004) Uncoupling the effects of abscisic acid on plant growth and water relations. Analysis of sto1/nced3, an abscisic acid‐deficient but salt stress‐tolerant mutant in Arabidopsis. Plant Physiology, 136, 3134–3147. Available from: https://doi.org/10.1104/pp.104.046169

Sagi, M., Fluhr, R. & Lips, S.H. (1999) Aldehyde oxidase and xanthine dehydrogenase in a flacca tomato mutant with deficient abscisic acid and wilty phenotype. Plant Physiology, 120, 571–577. Available from: https://doi.org/10.1104/pp.120.2.571

Sagi, M., Omarov, R.T. & Lips, S.H. (1998) The Mo‐hydroxylases xanthine dehydrogenase and aldehyde oxidase in ryegrass as affected by nitrogen and salinity. Plant Science, 135, 125–135. Available from: https://doi.org/10.1016/S0168‐9452(98)00075‐2

Sagi, M., Scazzocchio, C. & Fluhr, R. (2002) The absence of molybdenum cofactor sulfuration is the primary cause of the flacca phenotype in tomato plants. The Plant Journal, 31, 305–317. Available from: https://doi.org/10.1046/j.1365‐313X.2002.01363.x

Seo, M., Koiwai, H., Akaba, S., Komano, T., Oritani, T., Kamiya, Y. et al. (2000) Abscisic aldehyde oxidase in leaves of Arabidopsis thaliana. The Plant Journal, 23, 481–488.

Seo, M. & Koshiba, T. (2002) Complex regulation of ABA biosynthesis in plants. Trends in Plant Science, 7, 41–48. Available from: https://doi.org/10.1016/S1360‐1385(01)02187‐2

Seo, M., Peeters, A.J.M., Koiwai, H., Oritani, T., Marion‐Poll, A., Zeevaart, J.A.D. et al. (2000) The Arabidopsis aldehyde oxidase 3 (AAO3) gene product catalyzes the final step in abscisic acid biosynthesis in leaves. Proceedings of the National Academy of Sciences, 97, 12908–12913. Available from: https://doi.org/10.1073/pnas.220426197

Soltabayeva, A., Bekturova, A., Kurmanbayeva, A., Oshanova, D., Nurbekova, Z., Srivastava, S. et al. (2022) Ureides are accumulated similarly in response to UV‐C irradiation and wounding in Arabidopsis leaves but are remobilized differently during recovery. Journal of Experimental Botany, 73(3), 1016–1032. Available from: https://doi.org/10.1093/jxb/erab441

Srivastava, S., Brychkova, G., Yarmolinsky, D., Soltabayeva, A., Samani, T. & Sagi, M. (2017) Aldehyde oxidase 4 plays a critical role in delaying silique senescence by catalyzing aldehyde detoxification. Plant Physiology, 173, 1977–1997. Available from: https://doi.org/10.1104/pp.16.01939

Stiti, N., Adewale, I.O., Petersen, J., Bartels, D. & Kirch, H.H. (2011) Engineering the nucleotide coenzyme specificity and sulfhydryl redox sensitivity of two stress‐responsive aldehyde dehydrogenase isoenzymes of Arabidopsis thaliana. Biochemistry Journal, 434, 459–471. Available from: https://doi.org/10.1042/BJ20101337

Sunkar, R., Bartels, D. & Kirch, H.H. (2003) Overexpression of a stress‐inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance. The Plant Journal, 35, 452–464. Available from: https://doi.org/10.1046/j.1365‐313X.2003.01819.x

Sussmilch, F.C., Brodribb, T.J. & McAdam, A.M.S. (2017) Up‐regulation of NCED3 and ABA biosynthesis occur within minutes of a decrease in leaf turgor but AHK1 is not required. Journal of Experimental Botany, 68, 2913–2918. Available from: https://doi.org/10.1093/jxb/erx124

Triantaphylides, C., Krischke, M., Hoeberichts, F.A., Ksas, B., Gresser, G., Havaux, M. et al. (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiology, 148, 960–968. Available from: https://doi.org/10.1104/pp.108.125690

Turečková, V., Novak, O. & Strnad, M. (2009) Talanta Profiling ABA metabolites in Nicotiana tabacum L. leaves by ultra‐performance liquid chromatography – electrospray tandem mass spectrometry. Talanta, 80, 390–399. Available from: https://doi.org/10.1016/j.talanta.2009.06.027

Widhalm, J.R. & Dudareva, N. (2015) A familiar ring to it: biosynthesis of plant benzoic acids. Molecular Plant, 8, 83–97. Available from: https://doi.org/10.1016/j.molp.2014.12.001

Yamauchi, Y., Furutera, A., Seki, K., Toyoda, Y., Tanaka, K. & Sugimoto, Y. (2008) Malondialdehyde generated from peroxidized linolenic acid causes protein modification in heat‐stressed plants. Plant Physiology and Biochemistry, 46, 786–793. Available from: https://doi.org/10.1016/j.plaphy.2008.04.018

Yamauchi, Y., Hasegawa, A., Taninaka, A., Mizutani, M. & Sugimoto, Y. (2011) NADPH‐dependent reductases involved in the detoxification of reactive carbonyls in plants. The Journal of Biological Chemistry, 286, 6999–7009. Available from: https://doi.org/10.1074/jbc.M110.202226

Yarmolinsky, D., Brychkova, G., Fluhr, R. & Sagi, M. (2013) Sulfite reductase protects plants against sulfite toxicity. Plant Physiology, 161, 725–743. Available from: https://doi.org/10.1104/pp.112.207712

Yergaliyev, T.M., Nurbekova, Z., Mukiyanova, G., Akbassova, A., Sutula, M., Zhangazin, S. et al. (2016) The involvement of ROS producing aldehyde oxidase in plant response to Tombusvirus infection. Plant Physiology and Biochemistry, 109, 36–44. Available from: https://doi.org/10.1016/j.plaphy.2016.09.001

Yesbergenova, Z., Yang, G., Oron, E., Soffer, D., Fluhr, R. & Sagi, M. (2005) The plant Mo‐hydroxylases aldehyde oxidase and xanthine dehydrogenase have distinct reactive oxygen species signatures and are induced by drought and abscisic acid. The Plant Journal, 42, 862–876. Available from: https://doi.org/10.1111/j.1365‐313X.2005.02422.x

Yin, L., Mano, J., Wang, S., Tsuji, W. & Tanaka, K. (2010) The involvement of lipid peroxide‐derived aldehydes in aluminum toxicity of Tobacco roots. Plant Physiology, 152, 1406–1417.

Zdunek‐Zastocka, E., Omarov, R.T., Koshiba, T. & Lips, H.S. (2004) Activity and protein level of AO isoforms in pea plants (Pisum sativum L.) during vegetative development and in response to stress conditions. Journal of Experimental Botany, 55, 1361–1369.

Zdunek‐Zastocka, E. & Sobczak, M. (2013) Expression of Pisum sativum PsAO3 gene, which encodes an aldehyde oxidase utilizing abscisic aldehyde, is induced under progressively but not rapidly imposed drought stress. Plant Physiology and Biochemistry, 71, 57–66.

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...