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In plants, salicylic acid (SA) hydroxylation regulates SA homoeostasis, playing an essential role during plant development and response to pathogens. This reaction is catalysed by SA hydroxylase enzymes, which hydroxylate SA producing 2,3-dihydroxybenzoic acid (2,3-DHBA) and/or 2,5-dihydroxybenzoic acid (2,5-DHBA). Several SA hydroxylases have recently been identified and characterised from different plant species, but no such activity has yet been reported in maize. In this work, we describe the identification and characterisation of a new SA hydroxylase in maize plants. This enzyme, with high sequence similarity to previously described SA hydroxylases from Arabidopsis and rice, converts SA into 2,5-DHBA; however, it has different kinetic properties to those of previously characterised enzymes, and it also catalysers the conversion of the flavonoid dihydroquercetin into quercetin in in vitro activity assays, suggesting that the maize enzyme may have different roles in vivo to those previously reported from other species. Despite this, ZmS5H can complement the pathogen resistance and the early senescence phenotypes of Arabidopsis s3h mutant plants. Finally, we characterised a maize mutant in the S5H gene (s5h Mu ) that has altered growth, senescence and increased resistance against Colletotrichum graminicola infection, showing not only alterations in SA and 2,5-DHBA but also in flavonol levels. Together, the results presented here provide evidence that SA hydroxylases in different plant species have evolved to show differences in catalytic properties that may be important to fine tune SA levels and other phenolic compounds such as flavonols, to regulate different aspects of plant development and pathogen defence.

Titel:	A maize enzyme from the 2-oxoglutarate-dependent oxygenase family with unique kinetic properties, mediates resistance against pathogens and regulates senescence.
Autor/in / Beteiligte Person:	Serra, P ; Aramburu, SR ; Petrich, J ; Campos-Bermudez, VA ; Ferreyra, MLF ; Casati, P
Link:	Full Text Finder (Volltext)
Zeitschrift:	Plant, cell & environment, 2024-04-30
Veröffentlichung:	Ahead of Print, 2024
Medientyp:	academicJournal
ISSN:	1365-3040 (electronic)
DOI:	10.1111/pce.14929
Sonstiges:	Nachgewiesen in: MEDLINE Sprachen: English Publication Type: Journal Article Language: English [Plant Cell Environ] 2024 Apr 30. <i>Date of Electronic Publication: </i>2024 Apr 30. References: Abreu, M.E. & Munne‐Bosch, S. (2009) Salicylic acid deficiency in NahG transgenic lines and sid2 mutants increases seed yield in the annual plant Arabidopsis thaliana. Journal of Experimental Botany, 60, 1261–1271. ; Aledo, J.C. (2022) renz: an R package for the analysis of enzyme kinetic data. BMC Bioinformatics, 23, 182. Available from: https://doi.org/10.1186/s12859-022-04729-4. ; Bartsch, M., Bednarek, P., Vivancos, P.D., Schneider, B., von Roepenack‐Lahaye, E., Foyer, C.H. et al. (2010) Accumulation of isochorismate‐derived 2,3‐Dihydroxybenzoic 3‐O‐β‐d‐Xyloside in arabidopsis resistance to pathogens and ageing of leaves. Journal of Biological Chemistry, 285, 25654–25665. ; Bresson, J., Bieker, S., Riester, L., Doll, J. & Zentgraf, U. (2018) A guideline for leaf senescence analyses: from quantification to physiological and molecular investigations. Journal of Experimental Botany, 69, 769–786. ; Casati, P., & Walbot, V. (2005) Differential accumulation of maysin and rhamnosylisoorientin in leaves of high‐altitudes landraces of maize after UV‐B exposure. Plant, Cell & Environment, 28, 788–799. ; Chapman, B. & Chang, J. (2000) Biopython: python tools for computational biology. ACM SIGBIO Newsletter, 20, 15–19. ; 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. ; Curtis, M.D. & Grossniklaus, U. (2003) A gateway cloning vector set for highthroughput functional analysis of genes in planta. Plant Physiology, 133, 462–469. ; Dean, J.V., Mohammed, L.A. & Fitzpatrick, T. (2005) The formation, vacuolar localization, and tonoplast transport of salicylic acid glucose conjugates in tobacco cell suspension cultures. Planta, 221, 287–296. ; Dempsey, D.A., Vlot, A.C., Wildermuth, M.C. & Klessig, D.F. (2011) Salicylic acid biosynthesis and metabolism. The Arabidopsis Book, 9, e0156. ; Dhar, N., Caruana, J., Erdem, I., Subbarao, K.V., Klosterman, S.J. & Raina, R. (2020) The Arabidopsis SENESCENCE‐ASSOCIATED GENE 13 regulates Dark‐Induced senescence and plays contrasting roles in defense against bacterial and fungal pathogens. Molecular Plant‐Microbe Interactions®, 33, 754–766. ; Falcone Ferreyra, M.L., Rius, S., Emiliani, J., Pourcel, L., Feller, A., Morohashi, K. et al. (2010) Cloning and characterization of a UV‐B inducible maize flavonol synthase. The Plant Journal, 62, 77–91. ; Falcone Ferreyra, M.L., Casas, M.I., Questa, J.I., Herrera, A.L., Deblasio, S., Wang, J. et al. (2012) Evolution and expression of tandem duplicated maize flavonol synthase genes. Frontiers in Plant Science, 3, 101. Available from: https://doi.org/10.3389/fpls.2012.00101. ; Falcone Ferreyra, M.L., Emiliani, J., Rodriguez, E.J., Campos‐Bermudez, V.A., Grotewold, E. & Casati, P. (2015) The identification of maize and arabidopsis type I FLAVONE SYNTHASEs links flavones with hormones and biotic interactions. Plant Physiology, 169, 1090–1107. ; Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S. et al. (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science, 261, 754–756. ; Gao, X., Zhang, J.Q., Zhang, X., Zhou, J., Jiang, Z., Huang, P. et al. (2019) Rice qGL3/OsPPKL1 functions with the GSK3/SHAGGY‐like kinase OsGSK3 to modulate brassinosteroid signaling. The Plant Cell, 31, 1077–1093. ; Garcion, C., Lohmann, A., Lamodière, E., Catinot, J., Buchala, A., Doermann, P. et al. (2008) Characterization and biological function of the ISOCHORISMATE SYNTHASE2 gene of arabidopsis. Plant Physiology, 147, 1279–1287. ; Guo, Y. & Gan, S. (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. The Plant Journal, 46, 601–612. ; Guo, Y., Ren, G., Zhang, K., Li, Z., Miao, Y. & Guo, H. (2021) Leaf senescence: progression, regulation, and application. Molecular Horticulture, 1, 5. ; Herrera‐Vasquez, A., Salinas, P. & Holuigue, L. (2015) Salicylic acid and reactive oxygen species interplay in the transcriptional control of defense genes expression. Frontiers of Plant Science, 6, 171. ; Hoopes, G.M., Hamilton, J.P., Wood, J.C., Esteban, E., Pasha, A., Vaillancourt, B. et al. (2019) An updated gene atlas for maize reveals organ‐specific and stress‐induced genes. The Plant Journal, 97, 1154–1167. ; Kawai, Y., Ono, E. & Mizutani, M. (2014) Evolution and diversity of the 2–oxoglutarate‐dependent dioxygenase superfamily in plants. The Plant Journal, 78, 328–343. ; Kumar, R., Bishop, E., Bridges, W.C., Tharayil, N. & Sekhon, R.S. (2019) Sugar partitioning and source‐sink interaction are key determinants of leaf senescence in maize. Plant, Cell & Environment, 42, 2597–2611. ; Lamb, C. & Dixon, R.A. (1997) The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology, 48, 251–275. ; Lefevere, H., Bauters, L. & Gheysen, G. (2020) Salicylic acid biosynthesis in plants. Frontiers in Plant Science, 11, 338. Available from: https://doi.org/10.3389/fpls.2020.00338. ; León, J., Shulaev, V., Yalpani, N., Lawton, M.A. & Raskin, I. (1995) Benzoic acid 2‐hydroxylase, a soluble oxygenase from tobacco, catalyzes salicylic acid biosynthesis. Proceedings of the National Academy of Sciences, 92, 10413–10417. ; Liang, B., Wang, H., Yang, C., Wang, L., Qi, L., Guo, Z. et al. (2022) Salicylic acid is required for broad‐spectrum disease resistance in rice. International Journal of Molecular Sciences, 23, 1354. ; Lim, E.K., Doucet, C.J., Li, Y., Elias, L., Worrall, D., Spencer, S.P. et al. (2002) The activity of arabidopsis glycosyltransferases toward salicylic acid, 4‐hydroxybenzoic acid, and other benzoates. Journal of Biological Chemistry, 277, 586–592. ; Love, A.J., Milner, J.J. & Sadanandom, A. (2008) Timing is everything: regulatory overlap in plant cell death. Trends in Plant Science, 13, 589–595. ; Low, Y.C., Lawton, M.A. & Di, R. (2020) Validation of barley 2OGO gene as a functional orthologue of arabidopsis DMR6 gene in fusarium head blight susceptibility. Scientific Reports, 10, 9935. ; McCarty, D.R., Mark Settles, A., Suzuki, M., Tan, B.C., Latshaw, S., Porch, T. et al. (2005) Steady‐state transposon mutagenesis in inbred maize. The Plant Journal, 44, 52–61. ; Métraux, J.P., Signer, H., Ryals, J., Ward, E., Wyss‐Benz, M., Gaudin, J. et al. (1990) Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science, 250, 1004–1006. ; Mou, Z., Fan, W. & Dong, X. (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell, 113, 935–944. ; Okonechnikov, K., Golosova, O. & Fursov, M., the UGENE team. (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics, 28, 1166–1167. ; Park, S.W., Kaimoyo, E., Kumar, D., Mosher, S. & Klessig, D.F. (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science, 318, 113–116. ; Payá, C., Minguillón, S., Hernández, M., Miguel, S.M., Campos, L., Rodrigo, I. et al. (2022) SlS5H silencing reveals specific pathogen‐triggered salicylic acid metabolism in tomato. BMC Plant Biology, 22, 549. ; Peng, X., Hu, Y., Tang, X., Zhou, P., Deng, X., Wang, H. et al. (2012) Constitutive expression of rice WRKY30 gene increases the endogenous jasmonic acid accumulation, PR gene expression and resistance to fungal pathogens in rice. Planta, 236, 1485–1498. ; Peng, Y., Yang, J., Li, X. & Zhang, Y. (2021) Salicylic acid: biosynthesis and signaling. Annual Review of Plant Biology, 72, 761–791. ; Pundir, S., Magrane, M., Martin, M.J. & O'Donovan, C. (2015) UniProt consortium. searching and navigating UniProt databases. Current Protocols in Bioinformatics, 50, 1.27. ; Raskin, I. (1992) Role of salicylic acid in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 43, 439–463. ; Rivas‐San vicente, M. & Plasencia, J. (2011) Salicylic acid beyond defence: its role in plant growth and development. Journal of Experimental Botany, 62, 3321–3338. ; Rozen, S. & Skaletsky, H. (2000) Primer3 on the WWW for general users and for biologist programmers. Methods in molecular biology (Clifton, N.J.), 132, 365–386. ; Salotti, I., Liang, Y.‐J., Ji, T. & Rossi, V. (2023) Development of a model for colletotrichum diseases with calibration for phylogenetic clades on different host plants. Frontiers in Plant Science, 14, 1069092. Available from: https://doi.org/10.3389/fpls.2023.1069092. ; Sambrook, J. & Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual, 1, 3rd Edition. New York: Cold Spring Harbor Laboratory Press. ; Sekhon, R.S., Lin, H., Childs, K.L., Hansey, C.N., Buell, C.R., De Leon, N. et al. (2011) Genome‐wide atlas of transcription during maize development. The Plant Journal, 66, 553–563. ; Sekhon, R.S., Childs, K.L., Santoro, N., Foster, C.E., Buell, C.R., de Leon, N. et al. (2012) Transcriptional and metabolic analysis of senescence induced by preventing pollination in maize. Plant Physiology, 159, 1730–1744. ; Sekhon, R.S., Saski, C., Kumar, R., Flinn, B.S., Luo, F., Beissinger, T.M. et al. (2019) Integrated Genome‐Scale analysis identifies novel genes and networks underlying senescence in maize. The Plant Cell, 31, 1968–1989. ; Settles, A.M., Holding, D.R., Tan, B.C., Latshaw, S.P., Liu, J., Suzuki, M. et al. (2007) Sequence‐indexed mutations in maize using the UniformMu transposon‐tagging population. BMC Genomics, 8, 116. ; Shimono, M., Sugano, S., Nakayama, A., Jiang, C.J., Ono, K., Toki, S. et al. (2007) Rice WRKY45 plays a crucial role in benzothiadiazoleinducible blast resistance. The Plant Cell, 19, 2064–2076. ; Silverman, P., Seskar, M., Kanter, D., Schweizer, P., Metraux, J.P. & Raskin, I. (1995) Salicylic acid in rice (biosynthesis, conjugation, and possible role). Plant Physiology, 108, 633–639. ; Sukno, S.A., García, M., Shaw, B.D. & Thon, M.R. (2008) Root infection and systemic colonization of maize by colletotrichum graminicola. Applied and Environmental Microbiology, 74(3), 823–832. ; Tamura, K., Stecher, G. & Kumar, S. (2021) MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38, 3022–3027. ; Thomas, H. (2013) Senescence, ageing and death of the whole plant. New Phytologist, 197, 696–711. ; Thomas, H. & Ougham, H. (2014) The stay‐green trait. Journal of Experimental Botany, 65, 3889–3900. ; Thomazella, D.P.T., Seong, K., Mackelprang, R., Dahlbeck, D., Geng, Y., Gill, U.S. et al. (2021) Loss of function of a DMR6 ortholog in tomato confers broad‐spectrum disease resistance. Proceedings of the National Academy of Sciences, 118, e2026152118. ; Tripathi, J.N., Ntui, V.O., Shah, T. & Tripathi, L. (2021) CRISPR/Cas9‐ mediated editing of DMR6 orthologue in banana (Musa spp.) confers enhanced resistance to bacterial disease. Plant Biotechnology Journal, 19, 1291–1293. ; Van Bel, M., Silvestri, F., Weitz, E.M., Kreft, L., Botzki, A., Coppens, F. et al. (2022) PLAZA 5.0: extending the scope and power of comparative and functional genomics in plants. Nucleic Acids Research, 50, D1468–D1474. ; Vatov, E., Ludewig, U., Zentgraf, U. (2021) Disparate dynamics of gene body and cis‐regulatory element evolutionillustrated for the senescence‐associated cysteine protease gene SAG12 of plants. Plants, 10(7), 1380. ; Vlot, A.C., Dempsey, D.A. & Klessig, D.F. (2009) Salicylic acid, a multifaceted hormone to combat disease. Annual Review of Phytopathology, 47, 177–206. ; Wildermuth, M.C., Dewdney, J., Wu, G. & Ausubel, F.M. (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature, 414(6863), 562–565. ; Wintermans, J.F.G.M. & De Mots, A. (1965) Spectrophotometric characteristics of chlorophylls a and b and their phenophytins in ethanol. Biochimica et Biophysica Acta (BBA) ‐ Biophysics including Photosynthesis, 109, 448–453. ; Xiong, E., Li, Z., Zhang, C., Zhang, J., Liu, Y., Peng, T. et al. (2021) A study of leaf‐senescence genes in rice based on a combination of genomics, proteomics and bioinformatics. Briefings in Bioinformatics, 22, bbaa305. Available from: https://doi.org/10.1093/bib/bbaa305. ; Yang, Z., Wang, C., Qiu, K., Chen, H., Li, Z., Li, X. et al. (2020) The transcription factor ZmNAC126 accelerates leaf senescence downstream of the ethylene signalling pathway in maize. Plant, Cell & Environment, 43, 2287–2300. ; Zeilmaker, T., Ludwig, N.R., Elberse, J., Seidl, M.F., Berke, L., Van Doorn, A. et al. (2015) Downy mildew resistant 6 and DMR6‐LIKE OXYGENASE 1 are partially redundant but distinct suppressors of immunity in arabidopsis. The Plant Journal, 81, 210–222. ; Zhang, K., Halitschke, R., Yin, C., Liu, C.J. & Gan, S.S. (2013) Salicylic acid 3‐hydroxylase regulates arabidopsis leaf longevity by mediating salicylic acid catabolism. Proceedings of the National Academy of Sciences, 110, 14807–14812. ; Zhang, W.Y., Xu, Y.C., Li, W.L., Yang, L., Yue, X., Zhang, X.S. et al. (2014) Transcriptional analyses of natural leaf senescence in maize. PLoS One, 9, e115617. ; Zhang, Y., Zhao, L., Zhao, J., Li, Y., Wang, J., Guo, R. et al. (2017) S5H/DMR6 encodes a salicylic acid 5‐hydroxylase that fine‐tunes salicylic acid homeostasis. Plant Physiology, 175, 1082–1093. ; Zhang, Y., Yu, Q., Gao, S., Yu, N., Zhao, L., Wang, J. et al. (2022) Disruption of the primary salicylic acid hydroxylases in rice enhances broad‐spectrum resistance against pathogens. Plant, Cell & Environment, 45, 2211–2225. ; Zhu Y.X., Ge C., Ma S., Liu X.Y., Liu M., Sun Y., et al. (2020) Maize ZmFNSI homologs interact with an NLR protein to modulate hypersensitive response. International Journal of Molecular Sciences. 21, 2529. Grant Information: Fondo para la Investigación Científica y Tecnológica Contributed Indexing: Keywords: flavonoids; flavonols; salycilic hydroxylase Entry Date(s): Date Created: 20240430 Latest Revision: 20240430 Update Code: 20240501

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A maize enzyme from the 2-oxoglutarate-dependent oxygenase family with unique kinetic properties, mediates resistance against pathogens and regulates senescence.