OsERF7 Negatively Regulates Resistance to Sheath Blight Disease by Inhibiting Phytoalexin Biosynthesis
Received date: 2024-10-02
Accepted date: 2024-12-30
Online published: 2025-06-16
Ethylene response factors (ERFs) are plant transcription agents that play a pivotal role in disease resistance through the ethylene signaling pathway. However, whether and how ERFs regulate resistance to sheath blight (ShB), caused by Rhizoctonia solani in rice, remains largely unknown. Here, we demonstrated that OsERF7 negatively regulates rice resistance to ShB by inhibiting phytoalexin biosynthesis. Overexpression of OsERF7 (OsERF7OE) significantly decreased ShB resistance, whereas knockout of OsERF7 (oserf7) enhanced it. Mechanistically, antioxidant enzyme activities are significantly reduced in OsERF7OE plants, but increased in oserf7 plants. Furthermore, transcriptome analysis revealed that oserf7 plants exhibited significant upregulation of pathogenesis-related (PR) and phytoalexin biosynthesis genes upon R. solani infection. Consistently, transcript levels of phytoalexin biosynthesis genes, including OsKSL7, OsKSL8, OsKOL5, and OsCPS4, were significantly elevated in oserf7 plants, but reduced in OsERF7OE plants in response to R. solani infection. Electrophoretic mobility shift assays and dual-luciferase (LUC) reporter assays further confirmed that OsERF7 directly binds to the promoters of OsKSL8, OsKOL5, and OsCPS4, thereby repressing their expression. In summary, our study revealed that OsERF7 negatively regulated rice resistance to ShB primarily by inhibiting phytoalexin biosynthesis.
Key words： rice; sheath blight; OsERF7; phytoalexin
Xie Yuhao, Xie Wenya, Zhao Jianhua, Xue Xiang, Cao Wenlei, Shi Xiaopin, Wang Zhou, Wang Yiwen, Wang Guangda, Feng Zhiming, Hu Keming, Chen Xijun, Chen Zongxiang, Zuo Shimin . OsERF7 Negatively Regulates Resistance to Sheath Blight Disease by Inhibiting Phytoalexin Biosynthesis[J]. Rice Science, 2025 , 32(3) : 367 -379 . DOI: 10.1016/j.rsci.2024.12.014
| [1] | Ahuja I, Kissen R, Bones A M. 2012. Phytoalexins in defense against pathogens. Trends Plant Sci, 17(2): 73-90. |
| [2] | Bera S, Purkayastha R P. 1999. Multicomponent coordinated defence response of rice to Rhizoctonia solani causing sheath blight. Curr Sci, 76(10): 1376-1384. |
| [3] | Bian S Q, Li Z, Song S J, et al. 2024. Enhancing crop resilience: Insights from labdane-related diterpenoid phytoalexin research in rice (Oryza sativa L.). Curr Issues Mol Biol, 46(9): 10677-10695. |
| [4] | Cao W L, Zhang H M, Zhou Y, et al. 2022. Suppressing chlorophyll degradation by silencing OsNYC3 improves rice resistance to Rhizoctonia solani, the causal agent of sheath blight. Plant Biotechnol J, 20(2): 335-349. |
| [5] | Chen X J, Chen Y, Zhang L N, et al. 2016. Overexpression of OsPGIP1 enhances rice resistance to sheath blight. Plant Dis, 100(2): 388-395. |
| [6] | Cheng H T, Liu H B, Deng Y, et al. 2015. The WRKY45-2 WRKY13 WRKY42 transcriptional regulatory cascade is required for rice resistance to fungal pathogen. Plant Physiol, 167(3): 1087-1099. |
| [7] | Gao Y, Xue C Y, Liu J M, et al. 2021. Sheath blight resistance in rice is negatively regulated by WRKY53 via SWEET2a activation. Biochem Biophys Res Commun, 585: 117-123. |
| [8] | Guo J P, Xu C X, Wu D, et al. 2018. Bph6 encodes an exocyst-localized protein and confers broad resistance to planthoppers in rice. Nat Genet, 50(2): 297-306. |
| [9] | Hasegawa M, Mitsuhara I, Seo S, et al. 2010. Phytoalexin accumulation in the interaction between rice and the blast fungus. Mol Plant Microbe Interact, 23(8): 1000-1011. |
| [10] | Hong Y B, Wang H, Gao Y Z, et al. 2022. ERF transcription factor OsBIERF3 positively contributes to immunity against fungal and bacterial diseases but negatively regulates cold tolerance in rice. Int J Mol Sci, 23(2): 606. |
| [11] | Karmakar S, Molla K A, Chanda P K, et al. 2016. Green tissue-specific co-expression of chitinase and oxalate oxidase 4 genes in rice for enhanced resistance against sheath blight. Planta, 243(1): 115-130. |
| [12] | Karmakar S, Molla K A, Das K, et al. 2017. Dual gene expression cassette is superior than single gene cassette for enhancing sheath blight tolerance in transgenic rice. Sci Rep, 7(1): 7900. |
| [13] | Karmakar S, Datta K, Molla K A, et al. 2019. Proteo-metabolomic investigation of transgenic rice unravels metabolic alterations and accumulation of novel proteins potentially involved in defence against Rhizoctonia solani. Sci Rep, 9(1): 10461. |
| [14] | Koga J, Shimura M, Oshima K, et al. 1995. Phytocassanes A, B, C and D, novel diterpene phytoalexins from rice, Oryza sativa L. Tetrahedron, 51: 7907-7918. |
| [15] | Kumar V, Chaudhary P, Prasad A, et al. 2023. Jasmonic acid limits Rhizoctonia solani AG1-IA infection in rice by modulating reactive oxygen species homeostasis. Plant Physiol Biochem, 196: 520-530. |
| [16] | Li D Y, Li S, Wei S H, et al. 2021.Strategies to manage rice sheath blight: Lessons from interactions between rice and Rhizoctonia solani. Rice, 14(1): 21. |
| [17] | Li N, Wei S T, Chen J, et al. 2018. OsASR2 regulates the expression of a defence-related gene, Os2H16, by targeting the GT-1 cis-element. Plant Biotechnol J, 16(3): 771-783. |
| [18] | Liang X F, Moomaw E W, Rollins J A. 2015. Fungal oxalate decarboxylase activity contributes to Sclerotinia sclerotiorum early infection by affecting both compound appressoria development and function. Mol Plant Pathol, 16(8): 825-836. |
| [19] | Lin Y J, Zhang Q F. 2005. Optimising the tissue culture conditions for high efficiency transformation of indica rice. Plant Cell Rep, 23(8): 540-547. |
| [20] | Liu D F, Chen X J, Liu J Q, et al. 2012. The rice ERF transcription factor OsERF922 negatively regulates resistance to Magnaporthe oryzae and salt tolerance. J Exp Bot, 63(10): 3899-3911. |
| [21] | Liu J, Tang D Z. 2023. Plant immunity research in China. Phytopathol Res, 5(1): 37. |
| [22] | Liu J Z, Shen Y T, Cao H X, et al. 2022. OsbHLH057 targets the AATCA cis-element to regulate disease resistance and drought tolerance in rice. Plant Cell Rep, 41(5): 1285-1299. |
| [23] | Lu X, Zhang J, Brown B, et al. 2018. Inferring roles in defense from metabolic allocation of rice diterpenoids. Plant Cell, 30(5): 1119-1131. |
| [24] | Ma Z M, Hu L J, Jiang W Z. 2024. Understanding AP2/ERF transcription factor responses and tolerance to various abiotic stresses in plants: A comprehensive review. Int J Mol Sci, 25(2): 893. |
| [25] | Molla K A, Karmakar S, Chanda P K, et al. 2013. Rice oxalate oxidase gene driven by green tissue-specific promoter increases tolerance to sheath blight pathogen (Rhizoctonia solani) in transgenic rice. Mol Plant Pathol, 14(9): 910-922. |
| [26] | Molla K A, Karmakar S, Chanda P K, et al. 2016. Tissue-specific expression of Arabidopsis NPR1 gene in rice for sheath blight resistance without compromising phenotypic cost. Plant Sci, 250: 105-114. |
| [27] | Molla K A, Karmakar S, Molla J, et al. 2020. Understanding sheath blight resistance in rice: The road behind and the road ahead. Plant Biotechnol J, 18(4): 895-915. |
| [28] | Park H L, Yoo Y, Hahn T R, et al. 2014. Antimicrobial activity of UV-induced phenylamides from rice leaves. Molecules, 19(11): 18139-18151. |
| [29] | Park S, Moon J C, Park Y C, et al. 2014. Molecular dissection of the response of a rice leucine-rich repeat receptor-like kinase (LRR-RLK) gene to abiotic stresses. J Plant Physiol, 171(17): 1645-1653. |
| [30] | Peng X X, Hu Y J, Tang X K, 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(5): 1485-1498. |
| [31] | Peng X X, Wang H H, Jang J C, et al. 2016. OsWRKY80-OsWRKY 4 module as a positive regulatory circuit in rice resistance against Rhizoctonia solani. Rice, 9(1): 63. |
| [32] | Qu S H, Liu G F, Zhou B, et al. 2006. The broad-spectrum blast resistance gene Pi9 encodes a nucleotide-binding site-leucine-rich repeat protein and is a member of a multigene family in rice. Genetics, 172(3): 1901-1914. |
| [33] | Sayari M, Babaeizad V, Ghanbari M, et al. 2014. Expression of the pathogenesis related proteins, NH-1, PAL, and lipoxygenase in the Iranian Tarom and Khazar rice cultivars, in reaction to Rhizoctonia solani: The causal agent of rice sheath blight. J Plant Prot Res, 54(1): 36-43. |
| [34] | Tan J Y, Zhang X B, Shang H H, et al. 2023. ORYZA SATIVA SPOTTED-LEAF 41 (OsSPL41) negatively regulates plant immunity in rice. Rice Sci, 30(5): 426-436. |
| [35] | Tezuka D, Kawamata A, Kato H, et al. 2019. The rice ethylene response factor OsERF 83 positively regulates disease resistance to Magnaporthe oryzae. Plant Physiol Biochem, 135: 263-271. |
| [36] | Wang A J, Shu X Y, Jing X, et al. 2021. Identification of rice (Oryza sativa L.) genes involved in sheath blight resistance via a genome-wide association study. Plant Biotechnol J, 19(8): 1553-1566. |
| [37] | Wang F J, Wang C L, Liu P Q, et al. 2016. Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS One, 11(4): e0154027. |
| [38] | Wang L P, Fu J Y, Shen Q Q, et al. 2023. OsWRKY10 extensively activates multiple rice diterpenoid phytoalexin biosynthesis genes to enhance rice blast resistance. Plant J, 115(3): 758-771. |
| [39] | Wang Q, Hillwig M L, Wu Y S, et al. 2012. CYP701A8: A rice ent-kaurene oxidase paralog diverted to more specialized diterpenoid metabolism. Plant Physiol, 158(3): 1418-1425. |
| [40] | Wu L J, Han C, Wang H M, et al. 2024. OsbZIP53 negatively regulates immunity response by involving in reactive oxygen species and salicylic acid metabolism in rice. Rice Sci, 31(2): 190-202. |
| [41] | Xie W, Ding C Q, Hu H T, et al. 2022. Molecular events of rice AP2/ERF transcription factors. Int J Mol Sci, 23(19): 12013. |
| [42] | Xie W Y, Ke Y G, Cao J B, et al. 2021. Knock out of transcription factor WRKY53 thickens sclerenchyma cell walls, confers bacterial blight resistance. Plant Physiol, 187(3): 1746-1761. |
| [43] | Xie W Y, Cao W L, Lu S B, et al. 2023. Knockout of transcription factor OsERF65 enhances ROS scavenging ability and confers resistance to rice sheath blight. Mol Plant Pathol, 24(12): 1535-1551. |
| [44] | Xue X, Cao Z X, Zhang X T, et al. 2016. Overexpression of OsOSM1 enhances resistance to rice sheath blight. Plant Dis, 100(8): 1634-1642. |
| [45] | Yamamura C, Mizutani E, Okada K, et al. 2015. Diterpenoid phytoalexin factor, a bHLH transcription factor, plays a central role in the biosynthesis of diterpenoid phytoalexins in rice. Plant J, 84(6): 1100-1113. |
| [46] | Yang C, Li W, Cao J D, et al. 2017. Activation of ethylene signaling pathways enhances disease resistance by regulating ROS and phytoalexin production in rice. Plant J, 89(2): 338-353. |
| [47] | Yu J, Chai C Y, Ai G, et al. 2020. A Nicotiana benthamiana AP2/ERF transcription factor confers resistance to Phytophthora parasitica. Phytopathol Res, 2: 4. |
| [48] | Yuan D P, Xu X F, Hong W J, et al. 2020. Transcriptome analysis of rice leaves in response to Rhizoctonia solani infection and reveals a novel regulatory mechanism. Plant Biotechnol Rep, 14(5): 559-573. |
| [49] | Zhao X S, Zhang T B, Feng H J, et al. 2021. OsNBL1, a multi- organelle localized protein, plays essential roles in rice senescence, disease resistance, and salt tolerance. Rice, 14(1): 10. |
| [50] | Zuo S M, Yin Y J, Pan C H, et al. 2013. Fine mapping of qSB-11LE, the QTL that confers partial resistance to rice sheath blight. Theor Appl Genet, 126(5): 1257-1272. |
/
| 〈 |
|
〉 |