Arabidopsis aldehyde oxidase 3, known to oxidize abscisic aldehyde to abscisic acid, protects leaves from aldehyde toxicity
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
34587326
DOI
10.1111/tpj.15521
Knihovny.cz E-zdroje
- Klíčová slova
- Arabidopsis, abscisic acid, aldehyde oxidase, reactive aldehydes, senescence,
- MeSH
- aldehydoxidasa genetika metabolismus MeSH
- aldehydy metabolismus toxicita MeSH
- Arabidopsis genetika fyziologie MeSH
- chlorofyl metabolismus MeSH
- kyselina abscisová metabolismus MeSH
- listy rostlin genetika fyziologie MeSH
- oxidace-redukce MeSH
- proteiny huseníčku genetika metabolismus MeSH
- regulátory růstu rostlin metabolismus MeSH
- senescence rostlin MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- AAO3 protein, Arabidopsis MeSH Prohlížeč
- aldehydoxidasa MeSH
- aldehydy MeSH
- chlorofyl MeSH
- kyselina abscisová MeSH
- proteiny huseníčku MeSH
- regulátory růstu rostlin MeSH
The Arabidopsis thaliana aldehyde oxidase 3 (AAO3) catalyzes the oxidation of abscisic aldehyde (ABal) to abscisic acid (ABA). Besides ABal, plants generate other aldehydes that can be toxic above a certain threshold. AAO3 knockout mutants (aao3) exhibited earlier senescence but equivalent relative water content compared with wild-type (WT) during normal growth or upon application of UV-C irradiation. Aldehyde profiling in leaves of 24-day-old plants revealed higher accumulation of acrolein, crotonaldehyde, 3Z-hexenal, hexanal and acetaldehyde in aao3 mutants compared with WT leaves. Similarly, higher levels of acrolein, benzaldehyde, crotonaldehyde, propionaldehyde, trans-2-hexenal and acetaldehyde were accumulated in aao3 mutants upon UV-C irradiation. Aldehydes application to plants hastened profuse senescence symptoms and higher accumulation of aldehydes, such as acrolein, benzaldehyde and 4-hydroxy-2-nonenal, in aao3 mutant leaves as compared with WT. The senescence symptoms included greater decrease in chlorophyll content and increase in transcript expression of the early senescence marker genes, Senescence-Related-Gene1, Stay-Green-Protein2 as well as NAC-LIKE, ACTIVATED-BY AP3/P1. Notably, although aao3 had lower ABA content than WT, members of the ABA-responding genes SnRKs were expressed at similar levels in aao3 and WT. Moreover, the other ABA-deficient mutants [aba2 and 9-cis-poxycarotenoid dioxygenase3-2 (nced3-2), that has functional AAO3] exhibited similar aldehydes accumulation and chlorophyll content like WT under normal growth conditions or UV-C irradiation. These results indicate that the absence of AAO3 oxidation activity and not the lower ABA and its associated function is responsible for the earlier senescence symptoms in aao3 mutant.
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 and Cell Physiology, 39, 1281-1286.
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.
Bekturova, A., Oshanova, D., Tiwari, P., Nurbekova, Z., Kurmanbayeva, A., Soltabayeva, A. et al. (2021) Adenosine 5' phosphosulfate reductase and sulfite oxidase regulate sulfite-induced water loss in Arabidopsis. Journal of Experimental Botany, 72, 6447-6466. https://doi.org/10.1093/jxb/erab249.
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.
Biswas, M.S. & Mano, J. (2016) Reactive carbonyl species activate caspase-3-like protease to initiate programmed cell death in plants. Plant and Cell Physiology, 57, 1432-1442.
Biswas, 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.
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. Journal of Biological Chemistry, 276, 40381-40384.
Böttcher, 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.
Boudsocq, M., Barbier-Brygoo, H. & Laurière, C. (2004) Identification of nine sucrose nonfermenting 1-related protein kinases 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana. Journal of Biological Chemistry, 279, 41758-41766.
Bower, P., Brown, H. & Purves, W. (1978) Cucumber seedling indole acetaldehyde oxidase. Plant Physiology, 61, 107-110.
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.
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.
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.
Clough, S.J. & Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal, 16, 735-743.
Esterbauer, H., Shaur, R.J. & Zollner, H. (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radical Biology and Medicine, 11, 81-128.
Gill, S.S. & Tuteja, N. (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48, 909-930.
González-Guzmán, A.M., Apostolova, N., Bellés, J.M., Barrero, J.M., Piqueras, P., Ponce, M.R. et al. (2012) The Short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. The Plant Cell, 14, 1833-1846.
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.
Gratao, P.L., Polle, P., Lea, P.J. & Azevedo, R.A. (2005) Making the life of heavy metal-stressed plants a little easier. Functional Plant Biology, 32, 481-494.
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.
Islam, M.M., Ye, W., Matsushima, D., Rhaman, M.S., Munemasa, S., Okuma, E. et al. (2019) Reactive carbonyl species function as signal mediators downstream of H2O2 production and regulate [Ca2+]cyt elevation in ABA signal pathway in Arabidopsis guard cells. Plant and Cell Physiology, 60, 1146-1159.
Jensen, M.K., Hagedorn, H.P., Torres-Zabala, M., Grant, R.M., Rung, H.J., Collinge, B.D. et al. (2008) Transcriptional regulation by an NAC (NAM-ATF1,2-CUC2) transcription factor attenuates ABA signaling for efficient basal defence towards Blumeria graminis f. sp. hordei in Arabidopsis. The Plant Journal, 56, 867-880.
Kim, J., Kim, J.H., Lyu, J.I., Woo, H.R. & Lim, P.O. (2018) New insights into the regulation of leaf senescence in Arabidopsis. Journal of Experimental Botany, 69, 787-799.
Kirch, H.H., Nair, A. & Bartels, D. (2001) Novel ABA- and dehydration-inducible aldehyde dehydrogenase genes isolated from the resurrection plant Craterostigma plantagineum and Arabidopsis thaliana. The Plant Journal, 28, 555-567.
Koiwai, H., Akaba, S., Seo, M., Komano, T. & Koshiba, T. (2000) Functional expression of two Arabidopsis aldehyde oxidases in the yeast Pichia pastoris. Journal of Biochemistry, 127, 659-664.
Koiwai, H., Nakaminami, K., Seo, M., Mitsuhashi, W., Toyomasu, T. & Koshiba, T. (2004) Tissue-specific localization of an abscisic acid biosynthetic enzyme, AAO3, in Arabidopsis. Plant Physiology, 134, 1697-1707.
Koshiba, T., Saito, E., Ono, N., Yamamoto, N. & Satô, M. (1996) Purification and properties of flavin- and molybdenum-containing aldehyde oxidase from coleoptiles of maize. Plant Physiology, 110, 781-789.
Krispil, R., Tannenbaum, M., Sarusi-Portuguez, A., Loza, O., Raskina, O. & Hakim, O. (2020) The position and complex genomic architecture of plant T-DNA insertions revealed by 4SEE. International Journal of Molecular Sciences, 21, 2373. https://doi.org/10.3390/ijms21072373.
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.
Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
Mano, J. (2012) Reactive carbonyl species: Their production from lipid peroxides, action in environmental stress, and the detoxification mechanism. Plant Physiology and Biochemistry, 59, 90-97.
Mano, J. & Biswas, M.S. (2018) Analysis of reactive carbonyl species generated under oxidative stress. Methods in Molecular Biology, 1742, 117-124.
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.
Mano, J., Miyatake, F., Hiraoka, E. & Tamoi, M. (2009) Evaluation of the toxicity of stress-related aldehydes to photosynthesis in chloroplasts. Planta, 230, 639-648.
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 Journal, 27, 193-197.
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.
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.
Matsui, K., Sugimoto, K., Mano, J., Ozawa, R. & Takabayashi, J. (2012) Differential metabolisms of green leaf volatiles in injured and intact parts of a wounded leaf meet distinct ecophysiological requirements. PLoS One, 7, 1-10.
Mizoguchi, M., Umezawa, T., Nakashima, K., Kidokoro, S., Takasaki, H., Fujita, Y. et al. (2010) Two closely related subclass II SnRK2 protein kinases cooperatively regulate drought-inducible gene expression. Plant and Cell Physiology, 51, 842-847.
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.
Oshanova, D., Kurmanbayeva, A., Bekturova, A., Soltabayeva, A., Nurbekova, Z., Standing, D. et al. (2021) Level of sulfite oxidase activity affects sulfur and carbon metabolism in Arabidopsis. Frontiers in Plant Science, 12, 1-17.
Pucker, B., Kleinbolting, N. & Weisshaar, B. (2021) Large scale genomic rearragments in selected Arabidopsis thaliana T-DNA lines are caused by T-DNA insertion mutagensis. bioRxiv preprint., https://doi.org/10.1101/2021.03.03.433755
Rothe, G.M. (1974) Aldehyde oxidase isoenzymes (E.C.1.2.3.1) in potato tubers ( Solanum tuberosum ). Plant Cell Physiology, 15, 493-499.
Ruggiero, B., Koiwa, H., Manabe, Y., Quist, T.M., Inan, G., Saccardo, F. et al. (2020) 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.
Sade, N., Del Mar Rubio-Wilhelmi, M., Umnajkitikorn, K. & Blumwald, E. (2018) Stress-induced senescence and plant tolerance to abiotic stress. Journal of Experimental Botany, 69, 845-853.
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.
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.
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.
Schwartz, S.H., Leon-Kiloosterziel, K.M., Koornneef, M. & Zeevaart, J.A.D. (1997) Biochemical Characterization of the aba2 and aba3 mutants in Arabidopsis thaliana. Plant Physiology, 114, 161-166.
Seo, M., Akaba, S., Oritani, T., Delarue, M., Bellini, C., Caboche, M. et al. (1998) Higher activity of an aldehyde oxidase in the auxin-overproducing superroot1 mutant of Arabidopsis thaliana. Plant Physiology, 116, 687-693.
Seo, M., Aoki, H., Koiwai, H., Kamiya, Y., Nambara, E. & Koshiba, T. (2004) Comparative studies on the Arabidopsis aldehyde oxidase (AAO) gene family revealed a major role of AAO3 in ABA biosynthesis in seeds. Plant and Cell Physiology, 45, 1694-1703.
Seo, M., Koiwai, H., Akaba, S., Komano, T., Oritani, T., Kamiya, Y. et al. (2000a) 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.
Seo, M., Peeters, A.J.M., Koiwai, H., Oritani, T., Marion-Poll, A., Zeevaart, J.A.D. et al. (2000b) 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 U S A, 97, 12908-12913.
Shimizu, T., Kanno, Y., Suzuki, H., Watanabe, S.H. & Seo, M. (2021) Arabidopsis NPF4.6 and NPF5.1 control leaf stomatal aperture by regulating abscisic acid transport. Genes, 12, 885.
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.
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.
Thalmann, M., Pazmino, D., Seung, D., Horrer, D., Nigro, A., Meier, T. et al. (2016) Regulation of leaf starch degradation by abscisic acid is important for osmotic stress tolerance in plants. The Plant Cel, 28, 1860-1878.
Torres-Zabala, M., Truman, W., Bennet, H.M., Lafforgue, G., Wansfield, W.J. & Egea, P.R. et al., (2007) Pseudomonas Syringae pv.tomato hijacks the Arabidopsis abscisic acid signaling pathway to cause disease. The EMBO Journal, 26, 1434-1443.
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.
Umezawa, T., Okamoto, M., Kushiro, T., Nambara, E., Oono, Y., Seki, M. et al. (2006) CYP707A3, a major ABA 8 ¢ -hydroxylase involved in dehydration and rehydration response in Arabidopsis thaliana. The Plant Journal, 46, 171-182.
Umezawa, T., Yoshida, R., Maruyama, K., Yamaguchi-Shinozaki, K. & Shinozaki, K. (2004) SRK2C, a SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana. Proceedings of the National Academy of Sciences U S A, 101, 17306-17311.
Watanabe, S.H., Sato, M., Sawada, Y., Tanaka, M., Matsui, A., Kanno, Y. et al. (2018) Arabidopsis molybdenum cofactor sulfurase ABA3 contributes to anthocyanin accumulation and oxidative stress tolerance in ABA-dependent and independent ways. Scientific Reports, 8, 16592. https://doi.org/10.1038/s41598-018-34862-1.
Weber, H., Chételat, A., Reymond, P. & Farmer, E.E. (2004) Selective and powerful stress gene expression in Arabidopsis in response to malondialdehyde. The Plant Journal, 37, 877-888.
Weretilnyk, E.A. & Hanson, A.D. (1989) Betaine aldehyde dehydrogenase from spinach leaves: purification, in vitro translation of the mRNA, and regulation by salinity. Archives of Biochemistry and Biophysics, 271, 56-63.
Widhalm, J.R. & Dudareva, N. (2015) A familiar ring to it: Biosynthesis of plant benzoic acids. Molecular Plant, 8, 83-97.
Woude, L., Piotrowski, M., Klasse, G., Paulus, J., Krahn, D., Ninck, S. et al. (2021) The chemical compound 'Heatin' stimulates hypocotyl elongation and interferes with Arabidopsis NIT1-subfamily of nitrilases. The Plant Journal, 106, 1523-1540. https://doi.org/10.1111/tpj.15250.
Yalcinkaya, T., Uzilday, B., Ozgur, R. & Turkan, I. (2019) The roles of reactive carbonyl species in induction of antioxidant defence and ROS signalling in extreme halophytic model Eutrema parvulum and glycophytic model Arabidopsis thaliana. Environmental and Experimental Botany, 160, 81-91.
Yamauchi, Y., Hasegawa, A., Mizutani, M. & Sugimoto, Y. (2012) Chloroplastic NADPH-dependent alkenal/one oxidoreductase contributes to the detoxification of reactive carbonyls produced under oxidative stress. FEBS Letters, 586, 1208-1213.
Yamauchi, Y., Hasegawa, A., Taninaka, A., Mizutani, M. & Sugimoto, Y. (2011) NADPH-dependent reductases involved in the detoxification of reactive carbonyls in plants. Journal of Biological Chemistry, 286, 6999-7009.
Yang, J., Worley, E. & Udvardi, M. (2014) A NAP-AAO3 regulatory module promotes chlorophyll degradation via aba biosynthesis in arabidopsis leavesw open. The Plant Cell, 26, 4862-4874.
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.
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.
Yoshida, R., Umezawa, T., Mizoguchi, T., Takahashi, S., Takahashi, F. & Shinozaki, K. (2006) The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. Journal of Biological Chemistry, 281, 5310-5318.
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.
Zheng, M., Peng, T., Yang, T., Yan, J., Yang, K., Meng, D. et al. (2021) Arabidopsis MHP1, a homolog of yeast Mpo1, is involved in ABA signaling. Plant Science, 304, 110732. https://doi.org/10.1016/j.plantsci.2020.110732.