Glutathione S-transferase Activity Facilitates Rice Tolerance to the Barnyard Grass Root Exudate DIMBOA

Overview

Journal BMC Plant Biol

Publisher Biomed Central

Specialty Biology

Date 2024 Feb 16

PMID 38365588

Authors

Huabin Zhang

Dan Mu

Yushan Li

Xilin Li

Xue Yan

Ke Li

Yanyang Jiao

Jiayu Li

Hongmei Lin

Wenxiong Lin

Changxun Fang

Affiliations

Soon will be listed here.

Abstract

Background: In paddy fields, the noxious weed barnyard grass secretes 2,4-dihydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H)-one (DIMBOA) to interfere with rice growth. Rice is unable to synthesize DIMBOA. Rice cultivars with high or low levels of allelopathy may respond differently to DIMBOA.

Results: In this study, we found that low concentrations of DIMBOA (≤ 0.06 mM) promoted seedling growth in allelopathic rice PI312777, while DIMBOA (≤ 0.08 mM) had no significant influence on the nonallelopathic rice Lemont. DIMBOA treatment caused changes in the expression of a large number of glutathione S-transferase (GST) proteins, which resulting in enrichment of the glutathione metabolic pathway. This pathway facilitates plant detoxification of heterologous substances. The basal levels of GST activity in Lemont were significantly higher than those in PI312777, while GST activity in PI312777 was slightly induced by increasing DIMBOA concentrations. Overexpression of GST genes (Os09g0367700 and Os01g0949800) in these two cultivars enhanced rice resistance to DIMBOA.

Conclusions: Taken together, our results indicated that different rice accessions with different levels of allelopathy have variable tolerance to DIMBOA. Lemont had higher GST activity, which helped it tolerate DIMBOA, while PI312777 had lower GST activity that was more inducible. The enhancement of GST expression facilitates rice tolerance to DIMBOA toxins from barnyard grass root exudates.

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References

Baerson S, Sanchez-Moreiras A, Pedrol-Bonjoch N, Schulz M, Kagan I, Agarwal A . Detoxification and transcriptome response in Arabidopsis seedlings exposed to the allelochemical benzoxazolin-2(3H)-one. J Biol Chem. 2005; 280(23):21867-81. DOI: 10.1074/jbc.M500694200. View

Kong C, Zhao H, Xu X, Wang P, Gu Y . Activity and allelopathy of soil of flavone o-glycosides from rice. J Agric Food Chem. 2007; 55(15):6007-12. DOI: 10.1021/jf0703912. View

Chen T, Ma J, Liu Y, Chen Z, Xiao N, Lu Y . iProX in 2021: connecting proteomics data sharing with big data. Nucleic Acids Res. 2021; 50(D1):D1522-D1527. PMC: 8728291. DOI: 10.1093/nar/gkab1081. View

Fang C, Yang L, Chen W, Li L, Zhang P, Li Y . MYB57 transcriptionally regulates MAPK11 to interact with PAL2;3 and modulate rice allelopathy. J Exp Bot. 2019; 71(6):2127-2141. PMC: 7242072. DOI: 10.1093/jxb/erz540. View

Lallement P, Brouwer B, Keech O, Hecker A, Rouhier N . The still mysterious roles of cysteine-containing glutathione transferases in plants. Front Pharmacol. 2014; 5:192. PMC: 4138524. DOI: 10.3389/fphar.2014.00192. View

Treumann A, Thiede B . Isobaric protein and peptide quantification: perspectives and issues. Expert Rev Proteomics. 2010; 7(5):647-53. DOI: 10.1586/epr.10.29. View

Gaines T, Busi R, Kupper A . Can new herbicide discovery allow weed management to outpace resistance evolution?. Pest Manag Sci. 2021; 77(7):3036-3041. DOI: 10.1002/ps.6457. View

Cummins I, Wortley D, Sabbadin F, He Z, Coxon C, Straker H . Key role for a glutathione transferase in multiple-herbicide resistance in grass weeds. Proc Natl Acad Sci U S A. 2013; 110(15):5812-7. PMC: 3625300. DOI: 10.1073/pnas.1221179110. View

Ross P, Huang Y, Marchese J, Williamson B, Parker K, Hattan S . Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics. 2004; 3(12):1154-69. DOI: 10.1074/mcp.M400129-MCP200. View

10.

Wu H, Haig T, Pratley J, Lemerle D, An M . Allelochemicals in wheat (Triticum aestivum L.): production and exudation of 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one. J Chem Ecol. 2001; 27(8):1691-700. DOI: 10.1023/a:1010422727899. View

11.

Livak K, Schmittgen T . Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2002; 25(4):402-8. DOI: 10.1006/meth.2001.1262. View

12.

Bonnafe E, Sroda S, Budzinski H, Valiere A, Pedelluc J, Marty P . Responses of cytochrome P450, GST, and MXR in the mollusk Corbicula fluminea to the exposure to hospital wastewater effluents. Environ Sci Pollut Res Int. 2015; 22(14):11033-46. DOI: 10.1007/s11356-015-4309-x. View

13.

Zhang Q, Zheng X, Lin S, Gu C, Li L, Li J . Transcriptome analysis reveals that barnyard grass exudates increase the allelopathic potential of allelopathic and non-allelopathic rice (Oryza sativa) accessions. Rice (N Y). 2019; 12(1):30. PMC: 6502933. DOI: 10.1186/s12284-019-0290-1. View

14.

He H, Wang H, Fang C, Wu H, Guo X, Liu C . Barnyard grass stress up regulates the biosynthesis of phenolic compounds in allelopathic rice. J Plant Physiol. 2012; 169(17):1747-53. DOI: 10.1016/j.jplph.2012.06.018. View

15.

Nelson D, Koymans L, Kamataki T, Stegeman J, Feyereisen R, Waxman D . P450 superfamily: update on new sequences, gene mapping, accession numbers and nomenclature. Pharmacogenetics. 1996; 6(1):1-42. DOI: 10.1097/00008571-199602000-00002. View

16.

Guo L, Qiu J, Ye C, Jin G, Mao L, Zhang H . Echinochloa crus-galli genome analysis provides insight into its adaptation and invasiveness as a weed. Nat Commun. 2017; 8(1):1031. PMC: 5647321. DOI: 10.1038/s41467-017-01067-5. View

17.

Guo L, Qiu J, Li L, Lu B, Olsen K, Fan L . Genomic Clues for Crop-Weed Interactions and Evolution. Trends Plant Sci. 2018; 23(12):1102-1115. DOI: 10.1016/j.tplants.2018.09.009. View

18.

Ma J, Chen T, Wu S, Yang C, Bai M, Shu K . iProX: an integrated proteome resource. Nucleic Acids Res. 2018; 47(D1):D1211-D1217. PMC: 6323926. DOI: 10.1093/nar/gky869. View

19.

Wen B, Zhou R, Feng Q, Wang Q, Wang J, Liu S . IQuant: an automated pipeline for quantitative proteomics based upon isobaric tags. Proteomics. 2014; 14(20):2280-5. DOI: 10.1002/pmic.201300361. View

20.

Banerjee S, Goswami R . GST profile expression study in some selected plants: in silico approach. Mol Cell Biochem. 2010; 336(1-2):109-26. DOI: 10.1007/s11010-010-0384-y. View