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Research Article | Open Access

Rice sl-MH-1 mutant induces cell death and confers blast resistance via the synergistic roles of signaling systems

Dagang Tiana()Yan LinaShengping LibYiyang CaobGang LiaXinrui GuoaZiqiang ChenaZaijie ChenaFeng Wanga()Zonghua Wangb
Fujian Key Laboratory of Genetic Engineering for Agriculture, Biotechnology Research Institute, Fujian Academy of Agricultural Sciences, Fuzhou 350003, Fujian, China
State Key Laboratory of Ecological Control of Fujian-Taiwan Crop Pests, Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Plant Immunity Center, Fujian Agriculture and Forestry University, Fuzhou 350003, Fujian, China
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Abstract

Serotonin is ubiquitous across all forms of life and functions in responses to biotic and abiotic stresses. In rice, the conversion of tryptamine to serotonin is catalyzed by Sekiguchi lesion (SL). Previous studies have identified an sl mutation (a null mutation of SL) in several rice varieties and confirmed its increase of resistance and cell death. However, a systematic understanding of the reprogrammed cellular processes causing cell death and resistance is lacking. We performed a multi-omics analysis to clarify the fundamental mechanisms at the protein, gene transcript, and metabolite levels. We found that cell death and Magnaporthe oryzae (M. oryzae) infection of the sl-MH-1 mutant activated plant hormone signal transduction involving salicylic acid (SA), jasmonic acid (JA), and abscisic acid (ABA) in multiple regulatory layers. We characterized the dynamic changes of several key hormone levels during disease progression and under the cell death conditions and showed that SA and JA positively regulated rice cell death and disease resistance. SL-overexpressing lines confirmed that the sl-MH-1 mutant positively regulated rice resistance to M. oryzae. Our studies shed light on cell death and facilitate further mechanistic dissection of programmed cell death in rice.

References

[1]

M.A.U. Asad, S.A. Zakari, Q. Zhao, L. Zhou, Y. Ye, F. Cheng, Abiotic stresses intervene with ABA signaling to induce destructive metabolic pathways leading to death: premature leaf senescence in plants, Int. J. Mol. Sci. 20 (2019) 256.

[2]

K. Apel, H. Hirt, Reactive oxygen species: metabolism, oxidative stress, and signal transduction, Annu. Rev. Plant Biol. 55 (2004) 373-399.

[3]

M. Fujita, Y. Fujita, Y. Noutoshi, F. Takahashi, Y. Narusaka, K. Yamaguchi-Shinozaki, K. Shinozaki, Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks, Curr. Opin. Plant Biol. 9 (2006) 436-442.

[4]

K. Hayashi, Y. Fujita, T. Ashizawa, F. Suzuki, Y. Nagamura, Y. Hayano-Saito, Serotonin attenuates biotic stress and leads to lesion browning caused by a hypersensitive response to Magnaporthe oryzae penetration in rice, Plant J. 85 (2016) 46-56.

[5]

M.C. de Pinto, F. Tommasi, L. de Gara, Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco bright-yellow 2 cells, Plant Physiol 130 (2002) 698-708.

[6]

D. Tian, F. Yang, Y. Niu, Y. Lin, Z. Chen, G. Li, Q. Luo, F. Wang, M. Wang, Loss function of SL (sekiguchi lesion) in the rice cultivar Minghui 86 leads to enhanced resistance to (hemi)biotrophic pathogens, BMC Plant Biol. 20 (2020) 507.

[7]

R. Pelagio-Flores, R. Ortiz-Castro, A. Mendez-Bravo, L. Macias-Rodriguez, J. Lopez-Bucio, Serotonin, a tryptophan-derived signal conserved in plants and animals, regulates root system architecture probably acting as a natural auxin inhibitor in Arabidopsis thaliana, Plant Cell Physiol. 52 (2011) 490–508.

[8]

T. Fujiwara, S. Maisonneuve, M. Isshiki, M. Mizutani, L. Chen, H.L. Wong, T. Kawasaki, K. Shimamoto, Sekiguchi lesion gene encodes a cytochrome P450 monooxygenase that catalyzes conversion of tryptamine to serotonin in rice, J. Biol. Chem. 285 (2010) 11308-11313.

[9]

H.P. Lu, T. Luo, H.W. Fu, L. Wang, Y.Y. Tan, J.Z. Huang, Q. Wang, G.Y. Ye, A.M.R. Gatehouse, Y.G. Lou, Q.Y. Shu, Resistance of rice to insect pests mediated by suppression of serotonin biosynthesis, Nat. Plants 4 (2018) 338-344.

[10]

M. Ueno, H. Shibata, J. Kihara, Y. Honda, S. Arase, Increased tryptophan decarboxylase and monoamine oxidase activities induce Sekiguchi lesion formation in rice infected with Magnaporthe grisea, Plant J. 36 (2003) 215-228.

[11]

A. Ishihara, Y. Hashimoto, C. Tanaka, J.G. Dubouzet, T. Nakao, F. Matsuda, T. Nishioka, H. Miyagawa, K. Wakasa, The tryptophan pathway is involved in the defense responses of rice against pathogenic infection via serotonin production, Plant J. 54 (2008) 481-495.

[12]

X. Gao, Z. Chen, Y. Song, Z. Chen, D. Tian, Y. Lin, S. Yang, S. Chen, F. Wang, Identification and gene mapping of a runaway cell death mutant rcd1 in rice, Mol. Plant Breed. 13 (2015) 1433-1440 (in Chinese with English Abstract).

[13]

Y. Cui, Y. Peng, Q. Zhang, S. Xia, B. Ruan, Q. Xu, X. Yu, T. Zhou, H. Liu, D. Zeng, G. Zhang, Z. Gao, J. Hu, L. Zhu, L. Shen, L. Guo, Q. Qian, D. Ren, Disruption of EARLY LESION LEAF 1, encoding a cytochrome P450 monooxygenase, induces ROS accumulation and cell death in rice, Plant J. 105 (2021) 942-956.

[14]

L. van Oudenhove, B. Devreese, A review on recent developments in mass spectrometry instrumentation and quantitative tools advancing bacterial proteomics, Appl. Microbiol. Biot. 97 (2013) 4749-4762.

[15]

A. Otto, D. Becher, F. Schmidt, Quantitative proteomics in the field of microbiology, Proteomics 14 (2014) 547-565.

[16]

F.J. Perez-Llarena, G. Bou, Proteomics as a tool for studying bacterial virulence and antimicrobial resistance, Front. Microbiol. 7 (2016) 410.

[17]

D. Tian, L. Yang, Z. Chen, Z. Chen, F. Wang, Y. Zhou, Y. Luo, L. Yang, S. Chen, Proteomic analysis of the defense response to Magnaporthe oryzae in rice harboring the blast resistance gene Piz-t, Rice 11 (2018) 47.

[18]

M. Brosché, T. Blomster, J. Salojärvi, F. Cui, N. Sipari, J. Leppälä, A. Lamminmäki, G. Tomai, S. Narayanasamy, R.A. Reddy, M. Keinänen, K. Overmyer, J. Kangasjärvi, M.A. Torres, Transcriptomics and functional genomics of ROS-induced cell death regulation by Radical-Induced Cell Death1, PLoS Genet. 10 (2014) e1004112.

[19]

Z. Zhang, A. Lenk, M.X. Andersson, T. Gjetting, C. Pedersen, M.E. Nielsen, M.A. Newman, B.H. Hou, S.C. Somerville, H. Thordal-Christensen, A lesion-mimic syntaxin double mutant in Arabidopsis reveals novel complexity of pathogen defense signalin, Mol. Plant 1 (2008) 510-527.

[20]

L. Li, X. Shi, F. Zheng, D. Wu, A.A. Li, F.Y. Sun, C.C. Li, J.C. Wu, T. Li, Transcriptome analysis of Dlm mutants reveals the potential formation mechanism of lesion mimic in wheat, Eur. J. Plant Pathol. 146 (2016) 987-997.

[21]

R. Lowe, N. Shirley, M. Bleackley, S. Dolan, T. Shafee, Transcriptomics technologies, PLoS Comput. Biol. 13 (2017) e1005457.

[22]

P. Jain, P.K. Singh, R. Kapoor, A. Khanna, A.U. Solanke, S.G. Krishnan, A.K. Singh, V. Sharma, T.R. Sharma, Understanding host-pathogen interactions with expression profiling of NILs carrying rice-blast resistance Pi9 gene, Front. Plant Sci. 8 (2017) 93.

[23]

P. Jain, H. Dubey, P.K. Singh, A.U. Solanke, A.K. Singh, T.R. Sharma, Deciphering signalling network in broad spectrum near isogenic lines of rice resistant to Magnaporthe oryzae, Sci. Rep. 9 (2019) 16939.

[24]

W.S. Suharti, A. Nose, S.H. Zheng, Metabolite profiling of sheath blight disease resistance in rice: in the case of positive ion mode analysis by CE/TOF-MS, Plant Prod. Sci. 19 (2016) 279-290.

[25]

K. Floková, D. Tarkowská, O. Miersch, M. Strnad, C. Wasternack, O. Novák, UHPLC-MS/MS based target profiling of stress-induced phytohormones, Phytochemistry 105 (2014) 147-157.

[26]

Y. Nehela, F. Hijaz, A.A. Elzaawely, H.M. El-Zahaby, N. Killiny, Phytohormone profiling of the sweet orange (Citrus sinensis (L.) Osbeck) leaves and roots using GC-MS-based method, J. Plant Physiol. 199 (2016) 12-17.

[27]

K. Maruyama, K. Urano, K. Yoshiwara, Y. Morishita, N. Sakurai, H. Suzuki, M. Kojima, H. Sakakibara, D. Shibata, K. Saito, K. Shinozaki, K. Yamaguchi-Shinozaki, Integrated analysis of the effects of cold and dehydration on rice metabolites, phytohormones, and gene transcripts, Plant Physiol. 164 (2014) 1759-1771.

[28]

D. Todaka, Y. u. Zhao, T. Yoshida, M. Kudo, S. Kidokoro, J. Mizoi, K. -S. Kodaira, Y. Takebayashi, M. Kojima, H. Sakakibara, K. Toyooka, M. Sato, A.R. Fernie, K. Shinozaki, K. Yamaguchi-Shinozaki, Temporal and spatial changes in gene expression, metabolite accumulation and phytohormone content in rice seedlings grown under drought stress conditions, Plant J. 90 (2017) 61-78.

[29]

W. Stacklies, H. Redestig, M. Scholz, D. Walther, J. Selbig, pcaMethods-a Bioconductor package providing PCA methods forincomplete data, Bioinformatics 23 (2007) 1164-1167.

[30]

B.H. Mevik, R. Wehrens, The plsPackage: principal component and partial least squares regression in R, J. Stat. Softw. 18 (2007) 1-23.

[31]

C. Ginestet, ggplot2: elegant graphics for data analysis, J. R. Stat. Soc. Series A 174 (2011) 245.

[32]

J. Han, Y. Liu, R. Wang, J. Yang, V. Ling, C.H. Borchers, Metabolic profiling of bile acids in human and mouse blood by LC-MS/MS in combination with phospholipid-depletion solid-phase extraction, Anal. Chem. 87 (2015) 1127-1136.

[33]

R. Zeng, M.U. Farooq, L. Wang, Y. Su, T. Zheng, X. Ye, X. Jia, J. Zhu, Study on differential protein expression in natural selenium-enriched and non-selenium-enriched rice based on iTRAQ quantitative proteomics, Biomolecules 9 (2019) 130.

[34]

S. Hou, S.W. Jones, L.H. Choe, E.T. Papoutsakis, K.H. Lee, Workflow for quantitative proteomic analysis of Clostridium acetobutylicum ATCC 824 using iTRAQ tags, Methods 61 (2013) 269-276.

[35]

C. Xie, X. Mao, J. Huang, Y. Ding, J. Wu, S. Dong, L. Kong, G. Gao, C.Y. Li, L. Wei, KOBAS: 2.0: a web server for annotation and identification of enriched pathways and diseases, Nucleic Acids Res. 39 (2011) W316-W322.

[36]

C. Trapnell, L. Pachter, S.L. Salzberg, TopHat: discovering splice junctions with RNA-Seq, Bioinformatics 25 (2009) 1105-1111.

[37]

B. Li, C.N. Dewey, RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome, BMC Bioinformatics 12 (2011) 323.

[38]

M.D. Robinson, D.J. McCarthy, G.K. Smyth, edgeR: a bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics 26 (2010) 139-140.

[39]

F. Zhu, D.H. Xi, S. Yuan, F. Xu, D.W. Zhang, H.H. Lin, Salicylic acid and jasmonic acid are essential for systemic resistance against tobacco mosaic virus in Nicotiana benthamiana, MPMI 27 (2014) 567-577.

[40]

J. Durner, J. Shah, D.F. Klessig, Salicylic acid and disease resistance in plants, Trends Plant Sci. 2 (1997) 266-274.

[41]

J. Fu, H. Liu, Y. Li, H. Yu, X. Li, J. Xiao, S. Wang, Manipulating broad-spectrum disease resistance by suppressing pathogen-induced auxin accumulation in rice, Plant Physiol. 155 (2011) 589-602.

[42]

C.G. Ren, C.C. Dai, Jasmonic acid is involved in the signaling pathway for fungal endophyte-induced volatile oil accumulation of Atractylodes lancea plantlets, BMC Plant Biol. 12 (2012) 128.

[43]

M.A. Hossain, S. Bhattacharjee, S.M. Armin, P. Qian, W. Xin, H.Y. Li, D.J. Burritt, M. Fujita, L.S. Tran, Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging, Front. Plant Sci. 6 (2015) 420.

[44]

N. Avonce, B. Leyman, J.O. Mascorro-Gallardo, P. Van Dijck, J.M. Thevelein, G. Iturriaga, The trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling, Plant Physiol. 136 (2004) 3649-3659.

[45]

I. Couee, C. Sulmon, G. Gouesbet, A. El Amrani, Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants, J. Exp. Bot. 57 (2006) 449–459.

[46]

E. Keunen, D. Peshev, J. Vangronsveld, W. van Den Ende, A. Cuypers, Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept, Plant Cell Environ. 36 (2013) 1242-1255.

[47]

E.E. Helliwell, Q. Wang, Y. Yang, Transgenic rice with inducible ethylene production exhibits broad-spectrum disease resistance to the fungal pathogens Magnaporthe oryzae and Rhizoctonia solani, Plant Biotechnol. J. 11 (2013) 33-42.

[48]

M. Riemann, K. Haga, T. Shimizu, K. Okada, S. Ando, S. Mochizuki, Y. Nishizawa, U. Yamanouchi, P. Nick, M. Yano, E. Minami, M. Takano, H. Yamane, M. Iino, Identification of rice allene oxide cyclase mutants and the function of jasmonate for defence against Magnaporthe oryzae, Plant J. 74 (2013) 226-238.

[49]

T. Shimizu, K. Miyamoto, K. Miyamoto, E. Minami, Y. Nishizawa, M. Iino, H. Nojiri, H. Yamane, K. Okada, OsJAR1 contributes mainly to biosynthesis of the stress-induced jasmonoyl-isoleucine involved in defense responses in rice, Biosci. Biotechnol. Biochem. 77 (2013) 1556-1564.

[50]

A.C. Vlot, D.A. Dempsey, D.F. Klessig, Salicylic Acid, a multifaceted hormone to combat disease, Annu. Rev. Phytopathol. 47 (2009) 177-206.

[51]

I. Ndamukong, A.A. Abdallat, C. Thurow, B. Fode, M. Zander, R. Weigel, C. Gatz, SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription, Plant J. 50 (2007) 128-139.

[52]

A. Attard, M. Gourgues, N. Callemeyn-Torre, H. Keller, The immediate activation of defense responses in Arabidopsis roots is not sufficient to prevent Phytophthora parasitica infection, New Phytol. 187 (2010) 449-460.

[53]

M. Koeck, A.R. Hardham, P.N. Dodds, The role of effectors of biotrophic and hemibiotrophic fungi in infection, Cell Microbiol. 13 (2011) 1849-1857.

[54]

C. Mao, S. Lu, B. Lv, B. Zhang, J. Shen, J. He, L. Luo, D. Xi, X. Chen, F. Ming, A rice NAC transcription factor promotes leaf senescence via ABA biosynthesis, Plant Physiol. 174 (2017) 1747-1763.

[55]

J.H. Kim, H.R. Woo, J. Kim, P.O. Lim, I.C. Lee, S.H. Choi, D. Hwang, H.G. Nam, Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis, Science 323 (2009) 1053-1057.

[56]

P. Qin, S. Fan, L. Deng, G. Zhong, S. Zhang, M. Li, W. Chen, G. Wang, B. Tu, Y. Wang, X. Chen, B. Ma, S. Li, LML1, encoding a conserved eukaryotic release factor 1 protein, regulates cell death and pathogen resistance by forming a conserved complex with SPL33 in rice, Plant Cell Physiol. 59 (2018) 887–902.

[57]

N. Bodenhausen, P. Reymond, Signaling pathways controlling induced resistance to insect herbivores in Arabidopsis, MPMI 20 (2007) 1406-1420.

[58]

X. Xiao, X. Cheng, K. Yin, H. Li, J.L. Qiu, Abscisic acid negatively regulates post-penetration resistance of Arabidopsis to the biotrophic powdery mildew fungus, Sci. China Life Sci. 60 (2017) 891-901.

[59]

A. Wingler, T.L. Delatte, L.E. O'Hara, L.F. Primavesi, D. Jhurreea, M.J. Paul, H. Schluepmann, Trehalose 6-phosphate is required for the onset of leaf senescence associated with high carbon availability, Plant Physiol. 158 (2012) 1241-1251.

[60]

Y. Jaillais, J. Chory, Unraveling the paradoxes of plant hormone signaling integration, Nat. Struct. Mol. Biol. 17 (2010) 642-645.

[61]

A. Verhage, S.C.M. van Wees, C.M.J. Pieterse, Plant immunity: it's the hormones talking, but what do they say? Plant Physiol. 154 (2010) 536-540.

The Crop Journal
Pages 1755-1766
Cite this article:
Tian D, Lin Y, Li S, et al. Rice sl-MH-1 mutant induces cell death and confers blast resistance via the synergistic roles of signaling systems. The Crop Journal, 2022, 10(6): 1755-1766. https://doi.org/10.1016/j.cj.2022.03.005
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