Skip to main content
SpringerLink
Log in

Genomic Identification of CYP450 Enzymes and New Insights into Their Response to Diverse Abiotic Stresses in Brassica napus

  • RESEARCH
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

Cytochrome P450 (CYP450) proteins are a large group of monooxygenase that play important roles in the biosynthesis of secondary metabolites and degradation of xenobiotics. However, the responses of CYP450 family to abiotic stresses have not been characterized in Brassica napus (B. napus). In this study, we identified a total of 384 CYP450 genes in Darmor-bzh, the rapeseed culture whose genome was wildly used as a reference for gene clone. The structure and localization analyses showed that BnaCYP450 genes have integrated heme-binding motif, contain 1–10 exons, unevenly distributed across all the 19 chromosomes, and mainly localized on chloroplast. Cis-regulation element analysis suggested that BnaCYP450 genes were transcriptionally regulated by hormone and multiple stress response signals. Transcript expression analyses identified 108, 85, 96, and 86 BnaCYP450s differentially expressed genes (DEGs) in response to salt stress, potassium deficiency, nitrogen stress, and cadmium toxicity, respectively. Gene ontology (GO) enrichment analysis indicated that these BnaCYP450 DEGs mainly enriched in molecular function of ion binding and oxidoreductase activity and the biological process of secondary product metabolism. Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis showed that they mainly involved in the pathway of isoflavonoid biosynthesis. Differential expression of BnaCYP450s to multiple abiotic stresses revealed the functional diversity of BnaCYP450 family in B. napus. This study gave a basic understanding of CYP450 genes in B. napus and provides multiple core BnaCYP450 genetic resources for improving plant resistance to multiple abiotic stresses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

Data Availability

No datasets were generated or analysed during the current study.

References

  • Ahanger MA, Agarwal RM (2017) Salinity stress induced alterations in antioxidant metabolism and nitrogen assimilation in wheat (Triticum aestivum L) as influenced by potassium supplementation. Plant Physiol Biochem 115:449–460

    Article  CAS  PubMed  Google Scholar 

  • Bak S, Beisson F, Bishop G, Hamberger B, Höfer R, Paquette S, Werck-Reichhart D (2011) Cytochromes p450. Arabidopsis Book 9:e0144

    Article  PubMed  PubMed Central  Google Scholar 

  • Chalhoub B, Denoeud F, Liu SY, Parkin IAP, Tang HB, Wang XY, Chiquet J et al (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345(6199):950–953

    Article  CAS  PubMed  Google Scholar 

  • Collu G, Unver N, Peltenburg-Looman AM, van der Heijden R, Verpoorte R, Memelink J (2001) Geraniol 10-hydroxylase, a cytochrome P450 enzyme involved in terpenoid indole alkaloid biosynthesis. FEBS Lett 508(2):215–220

    Article  CAS  PubMed  Google Scholar 

  • Du Y, Chu H, Chu IK, Lo C (2010) CYP93G2 is a flavanone 2-hydroxylase required for C-glycosylflavone biosynthesis in rice. Plant Physiol 154(1):324–333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng YN, Cui JQ, Zhou T, Liu Y, Yue CP, Huang JY, Hua YP (2020) Comprehensive dissection into morpho-physiologic responses, ionomic homeostasis, and transcriptomic profiling reveals the systematic resistance of allotetraploid rapeseed to salinity. BMC Plant Biol 20(1):534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frey M, Schmauder K, Pateraki I, Spring O (2018) Biosynthesis of eupatolide-A metabolic route for sesquiterpene lactone formation involving the P450 enzyme CYP71DD6. ACS Chem Biol 13(6):1536–1543

    Article  CAS  PubMed  Google Scholar 

  • Geisler K, Hughes RK, Sainsbury F, Lomonossoff GP, Rejzek M, Fairhurst S, Olsen CE, Motawi MS, Melton RE, Hemmings AM, Bak S, Osbourn A (2013) Biochemical analysis of a multifunctional cytochrome P450 (CYP51) enzyme required for synthesis of antimicrobial triterpenes in plants. Proc Natl Acad Sci USA 110(35):E3360–E3367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hua YP, Zhou T, Song HX, Guan CY, Zhang ZH (2018) Integrated genomic and transcriptomic insights into the two-component high-affinity nitrate transporters in allotetraploid rapeseed. Plant Soil 427:245–268

    Article  CAS  Google Scholar 

  • Hua YP, Zhou T, Huang JY, Yue CP, Song HX, Guan CY, Zhang ZH (2020) Genome-wide differential DNA methylation and miRNA expression profiling reveals epigenetic regulatory mechanisms underlying nitrogen-limitation-triggered adaptation and use efficiency enhancement in allotetraploid rapeseed. Int J Mol Sci 21(22):8453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koo AJ, Cooke TF, Howe GA (2011) Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-L-isoleucine. Proc Natl Acad Sci USA 108(22):9298–9303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krishnamurthy P, Vishal B, Ho WJ, Lok FCJ, Lee FSM, Kumar PP (2020) Regulation of a cytochrome P450 gene CYP94B1 by WRKY33 transcription factor controls apoplastic barrier formation in roots to confer salt tolerance. Plant Physiol 184(4):2199–2215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lam PY, Zhu FY, Chan WL, Liu H, Lo C (2014) Cytochrome P450 93G1 is a flavone synthase II that channels flavanones to the biosynthesis of tricin O-linked conjugates in rice. Plant Physiol 165(3):1315–1327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li L, Cheng H, Gai J, Yu D (2007) Genome-wide identification and characterization of putative cytochrome P450 genes in the model legume Medicago truncatula. Planta 226(1):109–123

    Article  CAS  PubMed  Google Scholar 

  • Liao Q, Jian SF, Song HX, Guan CY, Lepo JE, Ismail AM, Zhang ZH (2019) Balance between nitrogen use efficiency and cadmium tolerance in Brassica napus and Arabidopsis thaliana. Plant Sci 284:57–66

    Article  CAS  PubMed  Google Scholar 

  • Liu CJ, Huhman D, Sumner LW, Dixon RA (2003) Regiospecific hydroxylation of isoflavones by cytochrome p450 81E enzymes from Medicago truncatula. Plant J 36(4):471–484

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Boachon B, Lugan R, Tavares R, Erhardt M, Mutterer J, Demais V, Pateyron S, Brunaud V, Ohnishi T, Pencik A, Achard P, Gong F, Hedden P, Werck-Reichhart D, Renault H (2015) A conserved cytochrome P450 evolved in seed plants regulates flower maturation. Mol Plant 8(12):1751–1765

    Article  CAS  PubMed  Google Scholar 

  • Magwanga RO, Lu P, Kirungu JN, Dong Q, Cai X, Zhou Z, Wang X, Hou Y, Xu Y, Peng R, Agong SG, Wang K, Fang L (2019) Knockdown of cytochrome P450 genes Gh_D07G1197 and Gh_A13G2057 on chromosomes D07 and A13 reveals their putative role in enhancing drought and salt stress tolerance in Gossypium hirsutum. Genes (basel) 10(3):226

    Article  CAS  PubMed  Google Scholar 

  • Malik WA, Wang X, Wang X, Shu N, Cui R, Chen X, Wang D, Lu X, Yin Z, Wang J, Ye W (2020) Genome-wide expression analysis suggests glutaredoxin genes response to various stresses in cotton. Int J Biol Macromol 153:470–491

    Article  CAS  PubMed  Google Scholar 

  • McAllister CH, Beatty PH, Good AG (2012) Engineering nitrogen use efficient crop plants: the current status. Plant Biotechnol J 10(9):1011–1025

    Article  CAS  PubMed  Google Scholar 

  • Miettinen K, Pollier J, Buyst D, Arendt P, Csuk R, Sommerwerk S, Moses T, Mertens J, Sonawane PD, Pauwels L, Aharoni A, Martins J, Nelson DR, Goossens A (2017) The ancient CYP716 family is a major contributor to the diversification of eudicot triterpenoid biosynthesis. Nat Commun 8:14153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morant M, Bak S, Møller BL, Werck-Reichhart D (2003) Plant cytochromes P450: tools for pharmacology, plant protection and phytoremediation. Curr Opin Biotechnol 14(2):151–162

    Article  CAS  PubMed  Google Scholar 

  • Morikawa T, Mizutani M, Aoki N, Watanabe B, Saga H, Saito S, Oikawa A, Suzuki H, Sakurai N, Shibata D, Wadano A, Sakata K, Ohta D (2006) Cytochrome P450 CYP710A encodes the sterol C-22 desaturase in Arabidopsis and tomato. Plant Cell 18(4):1008–1022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson DR, Werck-Reichhart D (2011) A P450-centric view of plant evolution. Plant J 66(1):194–211

    Article  CAS  PubMed  Google Scholar 

  • Nelson DR, Kamataki T, Waxman DJ, Guengerich FP, Estabrook RW, Feyereisen R, Gonzalez FJ, Coon MJ, Gunsalus IC, Gotoh O (1993) The P450 superfamily: update on new sequences, gene mapping, accession numbers, early trivial names of enzymes, and nomenclature. DNA Cell Biol 12(1):1–51

    Article  CAS  PubMed  Google Scholar 

  • Nelson DR, Schuler MA, Paquette SM, Werck-Reichhart D, Bak S (2004) Comparative genomics of rice and Arabidopsis. Analysis of 727 cytochrome P450 genes and pseudogenes from a monocot and a dicot. Plant Physiol 135(2):756–772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Omura T, Sato R (1964) The carbon monoxide-binding pigment of liver microsomes. I Evidence for Its Hemoprotein Nature 239:2370–2378

    CAS  Google Scholar 

  • Ono E, Nakai M, Fukui Y, Tomimori N, Fukuchi-Mizutan M, Saito M, Satake H, Tanaka T, Katsuta M, Umezawa T, Tanaka Y (2006) Formation of two methylenedioxy bridges by a Sesamum CYP81Q protein yielding a furofuran lignan, (+)-sesamin. Proc Natl Acad Sci USA 103(26):10116–10121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan Z, Baerson SR, Wang M, Bajsa-Hirschel J, Rimando AM, Wang X, Nanayakkara NPD, Noonan BP, Fromm ME, Dayan FE, Khan IA, Duke SO (2018) A cytochrome P450 CYP71 enzyme expressed in Sorghum bicolor root hair cells participates in the biosynthesis of the benzoquinone allelochemical sorgoleone. New Phytol 218(2):616–629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rai A, Singh R, Shirke PA, Tripathi RD, Trivedi PK, Chakrabarty D (2015) Expression of rice CYP450-like gene (Os08g01480) in Arabidopsis modulates regulatory network leading to heavy metal and other abiotic stress tolerance. PLoS ONE 10(9):e0138574

    Article  PubMed  PubMed Central  Google Scholar 

  • Ramamoorthy R, Jiang SY, Ramachandran S (2011) Oryza sativa cytochrome P450 family member OsCYP96B4 reduces plant height in a transcript dosage dependent manner. PLoS ONE 6(11):e28069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saito S, Hirai N, Matsumoto C, Ohigashi H, Ohta D, Sakata K, Mizutani M (2004) Arabidopsis CYP707As encode (+)-abscisic acid 8’-hydroxylase, a key enzyme in the oxidative catabolism of abscisic acid. Plant Physiol 2134(4):1439–1449

    Article  Google Scholar 

  • Shen C, Li X (2023) Genome-wide analysis of the P450 gene family in tea plant (Camellia sinensis) reveals functional diversity in abiotic stress. BMC Genomics 24(1):535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi J, Cui M, Yang L, Kim YJ, Zhang D (2015) Genetic and biochemical mechanisms of pollen wall development. Trends Plant Sci 20(11):741–753

    Article  CAS  PubMed  Google Scholar 

  • Vasav AP, Barvkar VT (2019) Phylogenomic analysis of cytochrome P450 multigene family and their differential expression analysis in Solanum lycopersicum L. suggested tissue specific promoters. BMC Genomics 20(1):116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vega A, O’Brien JA, Gutiérrez RA (2019) Nitrate and hormonal signaling crosstalk for plant growth and development. Curr Opin Plant Biol 52:155–163

    Article  CAS  PubMed  Google Scholar 

  • Vikhorev AV, Strygina KV, Khlestkina EK (2019) Duplicated flavonoid 3’-hydroxylase and flavonoid 3’, 5’-hydroxylase genes in barley genome. PeerJ 7:e6266

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang M, Yuan J, Qin L, Shi W, Xia G, Liu S (2020) TaCYP81D5, one member in a wheat cytochrome P450 gene cluster, confers salinity tolerance via reactive oxygen species scavenging. Plant Biotechnol J 18(3):791–804

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Zhang Y, Song M, Tang X, Huang S, Linhu B, Jin P, Guo W, Li F, Xing L, An R, Zhou X, Hao W, Mu J, Xie C (2023) Genome-wide identification of the cytochrome P450 superfamily genes and targeted editing of BnCYP704B1 confers male sterility in rapeseed. Plants (basel) 12(2):365

    Article  CAS  PubMed  Google Scholar 

  • Wang Y (2022) Multi-omics dissection of response mechanism under low potassium stress in rapeseed (Brassica napus L.). ZhengZhou University, p 000792

    Google Scholar 

  • Wei K, Chen H (2018) Global identification, structural analysis and expression characterization of cytochrome P450 monooxygenase superfamily in rice. BMC Genomics 19(1):35

    Article  PubMed  PubMed Central  Google Scholar 

  • Yasumoto S, Seki H, Shimizu Y, Fukushima EO, Muranaka T (2017) Functional characterization of CYP716 family P450 enzymes in triterpenoid biosynthesis in tomato. Front Plant Sci 8:21

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Li H, Li Q, Wang Z, Zeng W, Yin H, Qi K, Zou Y, Hu J, Huang B, Gu P, Qiao X, Zhang S (2023) Genome-wide identification, comparative analysis and functional roles in flavonoid biosynthesis of cytochrome P450 superfamily in pear (Pyrus spp.). BMC Genom Data 24(1):58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J, Li Z, Xiao G, Zhai M, Pan X, Huang R, Zhang H (2020) CYP71D8L is a key regulator involved in growth and stress responses by mediating gibberellin homeostasis in rice. J Exp Bot 71(3):1160–1170

    CAS  PubMed  Google Scholar 

  • Zhou T, Yue CP, Zhang TY, Liu Y, Huang JY, Hua YP (2021) Integrated ionomic and transcriptomic dissection reveals the core transporter genes responsive to varying cadmium abundances in allotetraploid rapeseed. BMC Plant Biol 21(1):372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zondlo SC, Irish VF (1999) CYP78A5 encodes a cytochrome P450 that marks the shoot apical meristem boundary in Arabidopsis. Plant J 19(3):259–268

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (No: 32202582) and the China Postdoctoral Science Foundation (No: 2021M692933).

Author information

Authors and Affiliations

  1. School of Agricultural Sciences, Zhengzhou University, Zhengzhou, 450001, China

    Haili Song, Yingpeng Hua, Ting Zhou & Yingna Feng

  2. School of Life Sciences, Zhengzhou University, Zhengzhou, 450001, China

    Caipeng Yue & JinYong Huang

Authors
  1. Haili Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yingpeng Hua
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ting Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Caipeng Yue
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. JinYong Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yingna Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Haili Song: Writing-original draft and validation. Yingpeng Hua: Conceptualization and data curation. Ting Zhou: Writing-review and editing. Caipeng Yue: Supervision. JinYong Huang: Supervision. Yingna Feng: Conceptualization and supervision.

Corresponding author

Correspondence to Yingna Feng.

Ethics declarations

Ethics Approval and Consent to Participate

Not applicable.

Consent for Publication

All authors approved the manuscript for publication.

Competing Interests

The authors declare no potential competing interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 981 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Song, H., Hua, Y., Zhou, T. et al. Genomic Identification of CYP450 Enzymes and New Insights into Their Response to Diverse Abiotic Stresses in Brassica napus. Plant Mol Biol Rep (2024). https://doi.org/10.1007/s11105-024-01448-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11105-024-01448-3

Keywords

Search

Navigation