Function of hydroxycinnamoyl transferases for the biosynthesis of phenolamides in rice resistance to <i>Magnaporthe oryzae</i>

Hong Fang; Fan Zhang; Chongyang Zhang; Dan Wang; Shuangqian Shen; Feng He; Hui Tao; Ruyi Wang; Min Wang; Debao Wang; Xionglun Liu; Jie Luo; Guo-Liang Wang; Yuese Ning

doi:10.1016/j.jgg.2022.02.008

Function of hydroxycinnamoyl transferases for the biosynthesis of phenolamides in rice resistance to Magnaporthe oryzae

doi: 10.1016/j.jgg.2022.02.008

a. College of Agronomy, Hunan Agricultural University, Changsha, Hunan 410128, China;
b. State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China;
c. National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan, Hubei 430070, China;
d. College of Tropical Crops, Hainan University, Haikou, Hainan 572208, China;
e. Department of Plant Pathology, The Ohio State University, Columbus, OH 43210, USA

基金项目:

This work was supported by grants from the National Natural Science Foundation of China (32161143009, 31822041 and 31972225) to Y.N., the National Natural Science Foundation of China (U20A2021) to R.W. and the National Natural Science Foundation of China (31801692) to F.Z.

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通讯作者:
Yuese Ning,E-mail:ningyuese@caas.cn

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出版历程
- 收稿日期: 2021-11-13
- 修回日期: 2022-02-04
- 录用日期: 2022-02-06
- 网络出版日期: 2023-03-17

Function of hydroxycinnamoyl transferases for the biosynthesis of phenolamides in rice resistance to Magnaporthe oryzae

a. College of Agronomy, Hunan Agricultural University, Changsha, Hunan 410128, China;
b. State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China;
c. National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan, Hubei 430070, China;
d. College of Tropical Crops, Hainan University, Haikou, Hainan 572208, China;
e. Department of Plant Pathology, The Ohio State University, Columbus, OH 43210, USA

Funds:

摘要

摘要: Phenolamide (PA) metabolites play important roles in the interaction between plants and pathogens. The putrescine hydroxycinnamoyl transferase genes OsPHT3 and OsPHT4 positively regulate rice cell death and resistance to Magnaporthe oryzae. The bZIP transcription factor APIP5, a negative regulator of cell death and rice immunity, directly binds to the OsPHT4 promoter to regulate putrescine-derived PAs. Whether other hydroxycinnamoyl transferase (HT) genes also participate in APIP5-mediated immunity remains unclear. Surprisingly, we find that genes encoding agmatine hydroxycinnamoyl transferases OsAHT1 and OsAHT2, tryptamine hydroxycinnamoyl transferases OsTBT1 and OsTBT2, and tyramine hydroxycinnamoyl transferases OsTHT1 and OsTHT2, responsible for the biosynthesis of polyamine-derived PAs are all up-regulated in APIP5-RNAi transgenic plants compared with segregated wild-type rice. Furthermore, both OsAHT1/2 and OsTBT1/2 are induced during M.oryzae infection, showing expression patterns similar to those previously reported for OsTHT1/2 and OsPHT3/4. Transgenic plants overexpressing either OsAHT2-GFP or OsTBT1-GFP show enhanced resistance against M.oryzae and accumulated more PA metabolites and lignin compared with wild-type plants. Interestingly, as demonstrated for OsPHT4, APIP5 directly binds to the promoters of OsAHT1/2, OsTBT1/2, and OsTHT1/2, repressing their transcription. Together, these results indicate that the HT genes are common targets of APIP5 and that PAs play critical roles in rice immunity.
- Hydroxycinnamoyl transferases /
- Phenolamides /
- Magnaporthe oryzae /
- bZIP transcription factor /
- Lignin
Abstract: Phenolamide (PA) metabolites play important roles in the interaction between plants and pathogens. The putrescine hydroxycinnamoyl transferase genes OsPHT3 and OsPHT4 positively regulate rice cell death and resistance to Magnaporthe oryzae. The bZIP transcription factor APIP5, a negative regulator of cell death and rice immunity, directly binds to the OsPHT4 promoter to regulate putrescine-derived PAs. Whether other hydroxycinnamoyl transferase (HT) genes also participate in APIP5-mediated immunity remains unclear. Surprisingly, we find that genes encoding agmatine hydroxycinnamoyl transferases OsAHT1 and OsAHT2, tryptamine hydroxycinnamoyl transferases OsTBT1 and OsTBT2, and tyramine hydroxycinnamoyl transferases OsTHT1 and OsTHT2, responsible for the biosynthesis of polyamine-derived PAs are all up-regulated in APIP5-RNAi transgenic plants compared with segregated wild-type rice. Furthermore, both OsAHT1/2 and OsTBT1/2 are induced during M.oryzae infection, showing expression patterns similar to those previously reported for OsTHT1/2 and OsPHT3/4. Transgenic plants overexpressing either OsAHT2-GFP or OsTBT1-GFP show enhanced resistance against M.oryzae and accumulated more PA metabolites and lignin compared with wild-type plants. Interestingly, as demonstrated for OsPHT4, APIP5 directly binds to the promoters of OsAHT1/2, OsTBT1/2, and OsTHT1/2, repressing their transcription. Together, these results indicate that the HT genes are common targets of APIP5 and that PAs play critical roles in rice immunity.
- Hydroxycinnamoyl transferases /
- Phenolamides /
- Magnaporthe oryzae /
- bZIP transcription factor /
- Lignin

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参考文献(46)

Assuncao, A.G., Herrero, E., Lin, Y.F., Huettel, B., Talukdar, S., Smaczniak, C., Immink, R.G., van Eldik, M., Fiers, M., Schat, H., et al., 2010. Arabidopsis thaliana transcription factors bzip19 and bzip23 regulate the adaptation to zinc deficiency. Proc. Natl. Acad. Sci. U. S. A. 107, 10296-10301

Bhuiyan, N.H., Selvaraj, G., Wei, Y.,King, J., 2009. Gene expression profiling and silencing reveal that monolignol biosynthesis plays a critical role in penetration defence in wheat against powdery mildew invasion. J. Exp. Bot. 60, 509-521

Boycheva, S., Daviet, L., Wolfender, J.L.,Fitzpatrick, T.B., 2014. The rise of operon-like gene clusters in plants. Trends Plant Sci. 19, 447-459

Burhenne, K., Kristensen, B.K.,Rasmussen, S.K., 2003. A new class of n-hydroxycinnamoyltransferases. Purification, cloning, and expression of a barley agmatine coumaroyltransferase (ec 2.3.1.64). J. Biol. Chem. 278, 13919-13927

Campos, L., Lison, P., Lopez-Gresa, M.P., Rodrigo, I., Zacares, L., Conejero, V.,Belles, J.M., 2014. Transgenic tomato plants overexpressing tyramine n-hydroxycinnamoyltransferase exhibit elevated hydroxycinnamic acid amide levels and enhanced resistance to pseudomonas syringae. Mol. Plant Microbe Interact. 27, 1159-1169

Chen, W., Gao, Y., Xie, W., Gong, L., Lu, K., Wang, W., Li, Y., Liu, X., Zhang, H., Dong, H., et al., 2014. Genome-wide association analyses provide genetic and biochemical insights into natural variation in rice metabolism. Nat. Genet. 46, 714-721

Dean, R., Van Kan, J.A., Pretorius, Z.A., Hammond-Kosack, K.E., Di Pietro, A., Spanu, P.D., Rudd, J.J., Dickman, M., Kahmann, R., Ellis, J., et al., 2012. The top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 13, 414-430

Erb, M.,Kliebenstein, D.J., 2020. Plant secondary metabolites as defenses, regulators, and primary metabolites:The blurred functional trichotomy. Plant Physiol. 184, 39-52

Facchini, P.J., Hagel, J.,Zulak, K.G., 2002. Hydroxycinnamic acid amide metabolism:Physiology and biochemistry. Canadian Journal of Botany 80, 577-589

Fang, C., Fernie, A.R.,Luo, J., 2019. Exploring the diversity of plant metabolism. Trends Plant Sci. 24, 83-98

Fang, H., Shen, S., Wang, D., Zhang, F., Zhang, C., Wang, Z., Zhou, Q., Wang, R., Tao, H., He, F., et al., 2021. A monocot-specific hydroxycinnamoylputrescine gene cluster contributes to immunity and cell death in rice. Sci. Bull. 66, 2381-2391

Gerlin, L., Baroukh, C.,Genin, S., 2021. Polyamines:Double agents in disease and plant immunity. Trends Plant Sci. 26, 1061-1071

He, F., Zhang, F., Sun, W., Ning, Y.,Wang, G.L., 2018. A versatile vector toolkit for functional analysis of rice genes. Rice 11, 27

He, J., Liu, Y., Yuan, D., Duan, M., Liu, Y., Shen, Z., Yang, C., Qiu, Z., Liu, D., Wen, P., et al., 2020. An r2r3 myb transcription factor confers brown planthopper resistance by regulating the phenylalanine ammonia-lyase pathway in rice. Proc. Natl. Acad. Sci. U. S. A. 117, 271-277

Hellens, R.P., Allan, A.C., Friel, E.N., Bolitho, K., Grafton, K., Templeton, M.D., Karunairetnam, S., Gleave, A.P.,Laing, W.A., 2005. Transient expression vectors for functional genomics, quantification of promoter activity and rna silencing in plants. Plant Methods 1, 13

Hu, Q., Min, L., Yang, X., Jin, S., Zhang, L., Li, Y., Ma, Y., Qi, X., Li, D., Liu, H., et al., 2018. Laccase ghlac1 modulates broad-spectrum biotic stress tolerance via manipulating phenylpropanoid pathway and jasmonic acid synthesis. Plant Physiol. 176, 1808-1823

Jakoby, M., Weisshaar, B., Droge-Laser, W., Vicente-Carbajosa, J., Tiedemann, J., Kroj, T.,Parcy, F., 2002. Bzip transcription factors in arabidopsis. Trends Plant Sci. 7, 106-111

Kang, S., Kang, K., Chung, G.C., Choi, D., Ishihara, A., Lee, D.S.,Back, K., 2006. Functional analysis of the amine substrate specificity domain of pepper tyramine and serotonin n-hydroxycinnamoyltransferases. Plant Physiol. 140, 704-715

Li, N., Lin, B., Wang, H., Li, X., Yang, F., Ding, X., Yan, J.,Chu, Z., 2019. Natural variation in zmfbl41 confers banded leaf and sheath blight resistance in maize. Nat. Genet. 51, 1540-1548

Liang, X., Chen, X., Li, C., Fan, J.,Guo, Z., 2017. Metabolic and transcriptional alternations for defense by interfering oswrky62 and oswrky76 transcriptions in rice. Sci. Rep. 7, 2474

Liu, J., Chen, X., Liang, X., Zhou, X., Yang, F., Liu, J., He, S.Y.,Guo, Z., 2016. Alternative splicing of rice wrky62 and wrky76 transcription factor genes in pathogen defense. Plant Physiol. 171, 1427-1442

Moreira-Vilar, F.C., Siqueira-Soares Rde, C., Finger-Teixeira, A., de Oliveira, D.M., Ferro, A.P., da Rocha, G.J., Ferrarese Mde, L., dos Santos, W.D.,Ferrarese-Filho, O., 2014. The acetyl bromide method is faster, simpler and presents best recovery of lignin in different herbaceous tissues than klason and thioglycolic acid methods. PLoS One 9, e110000

Morimoto, N., Ueno, K., Teraishi, M., Okumoto, Y., Mori, N.,Ishihara, A., 2018. Induced phenylamide accumulation in response to pathogen infection and hormone treatment in rice (oryza sativa). Biosci. Biotechnol. Biochem. 82, 407-416

Muroi, A., Ishihara, A., Tanaka, C., Ishizuka, A., Takabayashi, J., Miyoshi, H.,Nishioka, T., 2009. Accumulation of hydroxycinnamic acid amides induced by pathogen infection and identification of agmatine coumaroyltransferase in arabidopsis thaliana. Planta 230, 517-527

Obata, T.,Fernie, A.R., 2012. The use of metabolomics to dissect plant responses to abiotic stresses. Cell Mol. Life Sci. 69, 3225-3243

Peng, M., Gao, Y., Chen, W., Wang, W., Shen, S., Shi, J., Wang, C., Zhang, Y., Zou, L., Wang, S., et al., 2016. Evolutionarily distinct bahd n-acyltransferases are responsible for natural variation of aromatic amine conjugates in rice. Plant Cell 28, 1533-1550

Polturak, G.,Osbourn, A., 2021. Defense-related phenylpropanoid biosynthetic gene clusters in rice. Sci. Bull. 67, 13-16

Pushpa, D., Yogendra, K.N., Gunnaiah, R., Kushalappa, A.C.,Murphy, A., 2014. Identification of late blight resistance-related metabolites and genes in potato through nontargeted metabolomics. Plant Mol. Biol. Rep. 32, 584-595

Ranathunge, K., Schreiber, L.,Franke, R., 2011. Suberin research in the genomics era-new interest for an old polymer. Plant Sci. 180, 399-413

Schmidt, A., Grimm, R., Schmidt, J., Scheel, D., Strack, D.,Rosahl, S., 1999. Cloning and expression of a potato cdna encoding hydroxycinnamoyl-coa:Tyramine n-(hydroxycinnamoyl)transferase. J. Biol. Chem. 274, 4273-4280

Schmidt, A.,Strack, S.D., 1998. Elicitor-stimulated biosynthesis of hydroxycinnamoyltyramines in cell suspension cultures of solanum tuberosum. Planta 205, 51-55

Shen, S., Peng, M., Fang, H., Wang, Z., Zhou, S., Jing, X., Zhang, M., Yang, C., Guo, H., Li, Y., et al., 2021. An oryza specific hydroxycinnamoyl tyramine gene cluster contributes to enhanced disease resistance. Sci. Bull. 66, 2369-2380

Shi, X., Long, Y., He, F., Zhang, C., Wang, R., Zhang, T., Wu, W., Hao, Z., Wang, Y., Wang, G.L., et al., 2018. The fungal pathogen magnaporthe oryzae suppresses innate immunity by modulating a host potassium channel. PLoS Pathog. 14, e1006878

St-Pierre, B.,Luca, V.D., 2000. Evolution of acyltransferase genes:Origin and diversification of the bahd superfamily of acyltransferases involved in secondary metabolism. Recent Advances in Phytochemistry 34, 285-315

Sulpice, R.,McKeown, P.C., 2015. Moving toward a comprehensive map of central plant metabolism. Annu. Rev. Plant Biol. 66, 187-210

Tao, H., Shi, X., He, F., Wang, D., Xiao, N., Fang, H., Wang, R., Zhang, F., Wang, M., Li, A., et al., 2021. Engineering broad-spectrum disease-resistant rice by editing multiple susceptibility genes. J. Integr. Plant Biol. 63, 1639-1648

Wang, J., Wang, R., Fang, H., Zhang, C., Zhang, F., Hao, Z., You, X., Shi, X., Park, C.H., Hua, K., et al., 2021. Two voz transcription factors link an e3 ligase and an nlr immune receptor to modulate immunity in rice. Mol. Plant 14, 253-266

Wang, R., Ning, Y., Shi, X., He, F., Zhang, C., Fan, J., Jiang, N., Zhang, Y., Zhang, T., Hu, Y., et al., 2016. Immunity to rice blast disease by suppression of effector-triggered necrosis. Curr. Biol. 26, 2399-2411

Wen, W., Li, D., Li, X., Gao, Y., Li, W., Li, H., Liu, J., Liu, H., Chen, W., Luo, J., et al., 2014. Metabolome-based genome-wide association study of maize kernel leads to novel biochemical insights. Nat. Commun. 5, 3438

Yang, Q., He, Y., Kabahuma, M., Chaya, T., Kelly, A., Borrego, E., Bian, Y., El Kasmi, F., Yang, L., Teixeira, P., et al., 2017. A gene encoding maize caffeoyl-coa o-methyltransferase confers quantitative resistance to multiple pathogens. Nat. Genet. 49, 1364-1372

Zeiss, D.R., Piater, L.A.,Dubery, I.A., 2021. Hydroxycinnamate amides:Intriguing conjugates of plant protective metabolites. Trends Plant Sci. 26, 184-195

Zhang, C., Fang, H., Shi, X., He, F., Wang, R., Fan, J., Bai, P., Wang, J., Park, C.H., Bellizzi, M., et al., 2020. A fungal effector and a rice nlr protein have antagonistic effects on a bowman-birk trypsin inhibitor. Plant Biotechnol. J. 18, 2354-2363

Zhang, X.,Liu, C.J., 2015. Multifaceted regulations of gateway enzyme phenylalanine ammonia-lyase in the biosynthesis of phenylpropanoids. Mol. Plant 8, 17-27

Zhao, Q., Tian, M., Li, Q., Cui, F., Liu, L., Yin, B.,Xie, Q., 2013. A plant-specific in vitro ubiquitination analysis system. Plant J. 74, 524-533

Zhou, X., Liao, H., Chern, M., Yin, J., Chen, Y., Wang, J., Zhu, X., Chen, Z., Yuan, C., Zhao, W., et al., 2018. Loss of function of a rice tpr-domain rna-binding protein confers broad-spectrum disease resistance. Proc. Natl. Acad. Sci. U. S. A. 115, 3174-3179

Zhu, X., Yin, J., Liang, S., Liang, R., Zhou, X., Chen, Z., Zhao, W., Wang, J., Li, W., He, M., et al., 2016. The multivesicular bodies (mvbs)-localized aaa atpase lrd6-6 inhibits immunity and cell death likely through regulating mvbs-mediated vesicular trafficking in rice. PLoS Genet. 12, e1006311

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Function of hydroxycinnamoyl transferases for the biosynthesis of phenolamides in rice resistance to Magnaporthe oryzae

doi: 10.1016/j.jgg.2022.02.008

通讯作者:
Yuese Ning,E-mail:ningyuese@caas.cn

计量

Function of hydroxycinnamoyl transferases for the biosynthesis of phenolamides in rice resistance to Magnaporthe oryzae

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留言板

Function of hydroxycinnamoyl transferases for the biosynthesis of phenolamides in rice resistance to Magnaporthe oryzae

doi: 10.1016/j.jgg.2022.02.008

通讯作者: Yuese Ning,E-mail:ningyuese@caas.cn

计量

出版历程

Function of hydroxycinnamoyl transferases for the biosynthesis of phenolamides in rice resistance to Magnaporthe oryzae

计量

出版历程

目录

通讯作者:
Yuese Ning,E-mail:ningyuese@caas.cn