Flavin-Containing Monooxygenases ( FMO ) Genes in Garlic  Allium sativum  L.: Genome-Wide Identification, Characterization, and Expression Analysis in Response to  Fusarium proliferatum

O. K. Anisimova; Анисимова О. К.; A. V. Shchennikova; Щенникова А. В.; E. Z. Kochieva; Кочиева Е. З.; M. A. Filyushin; Филюшин М. А.

doi:10.31857/S0016675823070020

Flavin-Containing Monooxygenases (FMO) Genes in Garlic Allium sativum L.: Genome-Wide Identification, Characterization, and Expression Analysis in Response to Fusarium proliferatum

Authors: Anisimova O.K.¹, Shchennikova A.V.¹, Kochieva E.Z.¹, Filyushin M.A.¹
Affiliations:
1. Federal Research Centre “Fundamentals of Biotechnology” of the Russian Academy of Sciences
Issue: Vol 59, No 7 (2023)
Pages: 755-771
Section: ГЕНЕТИКА РАСТЕНИЙ
URL: https://journals.rcsi.science/0016-6758/article/view/134616
DOI: https://doi.org/10.31857/S0016675823070020
EDN: https://elibrary.ru/QISHHL
ID: 134616

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Abstract

In this study, 39 flavin-containing monooxygenase genes were identified in the garlic (Allium sativum L.) genome. The distribution of AsFMOs into three phylogenetic clades associated with N-oxygenation (22 proteins), auxin biosynthesis (13 proteins), and S-oxygenation (4 proteins) has been shown. FAD and NADPH binding, FMO-identifying, and FATGY motifs were found in the AsFMO sequences. AsFMOs transcripts were present in all garlic organs with a maximum in roots, leaves, peduncle, and aerial bulbs. In response to infection with the pathogenic fungus Fusarium proliferatum, differential expression of clade I genes (AsFMO4, AsFMO11, AsFMO12, and AsFMO35) was detected in the roots of cv. Sarmat and Strelets, contrasting in Fusarium rot resistance. At the same time, the expression response of the clade III AsFMO18 gene involved in the alliin biosynthesis was similar for both cultivars, regardless of their resistance/susceptibility to Fusarium. This suggests the clades I and III genes redundancy in plant responses to infection. The AsFMO35 coding and regulatory sequences were analyzed in the Sarmat and Strelets cultivars. It was shown that the AsFMO35 promoter differs in the presence of the ABA-associated cis-regulatory element ABRE in cv. Strelets susceptible to Fusarium rot.

Keywords

garlic, Allium sativum L., flavin-containing monooxygenase, Fusarium rot, expression analysis.

References

Thodberg S., Jakobsen Neilson E.H. The “Green” FMOs: diversity, functionality and application of plant flavoproteins // Catalysts. 2020. V. 10. Article 329. https://doi.org/10.3390/catal10030329
Van Berkel W.J.H., Kamerbeek N.M., Fraaije M.W. Flavoprotein monooxygenases, A diverse class of oxidative biocatalysts // J. Biotechnol. 2006. V. 124. P. 670–689. https://doi.org/10.1016/j.jbiotec.2006.03.044
Schlaich N.L. Flavin-containing monooxygenases in plants: looking beyond detox // Trends Plant Sci. 2007. V. 12. P. 412–418. https://doi.org/10.1016/j.tplants.2007.08.009
Ziegler D.M. Flavin-containing monooxygenases: Catalytic mechanism and substrate specificities // Drug Metab. Rev. 1988. V. 19. P. 1–32.
Ziegler D.M. An overview of the mechanism, substrate specificities, and structure of FMOs // Drug Metab. Rev. 2002. V. 34. P. 503–511. https://doi.org/10.1081/dmr-120005650
Yanni S.B., Annaert P.P., Augustijns P. et al. Role of flavin-containing monooxygenase in oxidative metabolism of voriconazole by human liver microsomes // Drug Metab. Dispos. 2008. V. 36. P. 1119–1125. https://doi.org/10.1124/dmd.107.019646
Rossner R., Kaeberlein M., Leiser S.F. Flavin-containing monooxygenases in aging and disease: Emerging roles for ancient enzymes // J. Biol. Chem. 2017. V. 292. P. 11138–11146. https://doi.org/10.1074/jbc.R117.779678
Krueger S.K., Williams D.E. Mammalian flavin-containing monooxygenases: Structure/function, genetic polymorphisms and role in drug metabolism // Pharmacol. Ther. 2005. V. 106. P. 357–387. https://doi.org/10.1016/j.pharmthera.2005.01.001
Zhao Y., Christensen S.K., Fankhauser C. et al. A role for flavin monooxygenase-like enzymes in auxin biosynthesis // Science. 2001. V. 291. P. 306–309. https://doi.org/10.1126/science.291.5502.306
Won C., Shen X., Mashiguchi K. et al. Conversion of tryptophan to indole-3-acetic acid by tryptophan aminotransferases of Arabidopsis and YUCCAs in Arabidopsis // Proc. Natl Acad. Sci. USA. 2011. V. 108(45). P. 18518–18523. https://doi.org/10.1073/pnas.1108436108
Hartmann M., Zeier T., Bernsdorff F. et al. Flavin monooxygenase-generated N-hydroxypipecolic acid is a critical element of plant systemic immunity // Cell. 2018. V. 173(2). P. 456–469. https://doi.org/10.1016/j.cell.2018.02.049
Halkier B.A., Gershenzon J. Biology and biochemistry of glucosinolates // Annu. Rev. Plant Biol. 2006. V. 57. P. 303–333. https://doi.org/10.1146/annurev.arplant.57.032905.105228
Kong W., Li J., Yu Q. et al. Two novel flavin-containing monooxygenases involved in biosynthesis of aliphatic glucosinolates // Front. Plant Sci. 2016. V. 7. Article 1292. https://doi.org/10.3389/fpls.2016.01292
Yoshimoto N., Onuma M., Mizuno S. et al. Identification of a flavin-containing S-oxygenating monooxygenase involved in alliin biosynthesis in garlic // Plant J. 2015. V. 83. P. 941–951. https://doi.org/10.1111/tpj.12954
Yoshimoto N., Saito K. S-Alk(en)ylcysteine sulfoxides in the genus Allium: Proposed biosynthesis, chemical conversion, and bioactivities // J. Exp. Bot. 2019. V. 70. P. 4123–4137. https://doi.org/10.1093/jxb/erz243
Mishina T.E., Zeier J. The Arabidopsis flavin-dependent monooxygenase fmo1 is an essential component of biologically induced systemic acquired resistance // Plant Physiol. 2006. V. 141. P. 1666–1675. https://doi.org/10.1104/pp.106.081257
Sun X., Zhu S., Li N. et al. A chromosome-level genome assembly of garlic (Allium sativum) provides insights into genome evolution and allicin biosynthesis // Mol. Plant. 2020. V. 13. P. 1328–1339. https://doi.org/10.1016/j.molp.2020.07.019
Filyushin M.A., Anisimova O.K., Kochieva E.Z., Shchennikova A.V. Genome-wide identification and expression of chitinase class I genes in garlic (Allium sativum L.) cultivars resistant and susceptible to Fusarium proliferatum // Plants. 2021. V. 10. Article 720. https://doi.org/10.3390/plants10040720
Анисимова О.К., Щенникова А.В., Кочиева Е.З., Филюшин М.А. Идентификация генов монодегидроаскорбатредуктаз (MDHAR) чеснока (Allium sativum L.) и их участие в ответе на заражение Fusarium proliferatum // Генетика. 2022. Т. 58. № 7. С. 754–764. https://doi.org/10.31857/S0016675822070037
Anisimova O.K., Seredin T.M., Danilova O.A., Filyushin M.A. First report of Fusarium proliferatum causing garlic clove rot in Russian federation // Plant Dis. 2021. V. 105. P. 3308. https://doi.org/10.1094/PDIS-12-20-2743-PDN
Tchórzewska D., Deryło K., Błaszczyk L., Winiarczyk K. Tubulin cytoskeleton during microsporogenesis in the male-sterile genotype of Allium sativum and fertile Allium ampeloprasum L. // Plant Reprod. 2015. V. 28. P. 171–182. https://doi.org/10.1007/s00497-015-0268-0
Qin M., Wang J., Zhang T. et al. Genome-wide identification and analysis on YUCCA gene family in Isatis indigotica Fort. and IiYUCCA6-1 functional exploration // Int. J. Mol. Sci. 2020. V. 21. Article 2188. https://doi.org/10.3390/ijms21062188
Hansen B.G., Kliebenstein D.J., Halkier B.A. Identification of a flavin-monooxygenase as the S-oxygenating enzyme in aliphatic glucosinolate biosynthesis in Arabidopsis // Plant J. 2007. V. 50. P. 902–910. https://doi.org/10.1111/j.1365-313X.2007.03101.x
Eswaramoorthy S., Bonanno J.B., Burley S.K., Swaminathan S. Mechanism of action of a flavin-containing monooxygenase // Proc. Natl Acad. Sci. USA. 2006. V. 103. P. 9832–9837. https://doi.org/10.1073/pnas.0602398103
Li R., Zhu F., Duan D. Function analysis and stress-mediated cis-element identification in the promoter region of VqMYB15 // Plant Signal Behav. 2020. V. 15. Article 1773664. https://doi.org/10.1080/15592324.2020.1773664
Nakashima K., Yamaguchi-Shinozaki K. ABA signaling in stress-response and seed development // Plant Cell Rep. 2013. V. 32. P. 959–970. https://doi.org/10.1007/s00299-013-1418-1