Osa-miR1873 fine-tunes rice immunity against Magnaporthe oryzae and yield traits.
Journal
Journal of integrative plant biology
ISSN: 1744-7909
Titre abrégé: J Integr Plant Biol
Pays: China (Republic : 1949- )
ID NLM: 101250502
Informations de publication
Date de publication:
Aug 2020
Aug 2020
Historique:
received:
19
09
2019
accepted:
20
12
2019
pubmed:
22
12
2019
medline:
7
4
2021
entrez:
22
12
2019
Statut:
ppublish
Résumé
MicroRNAs (miRNAs) are known to fine-tune growth, development, and stress-induced responses. Osa-miR1873 is a rice-specific miRNA targeting LOC_Os05g01790. Here, we show that Osa-miR1873 fine-tunes rice immunity against Magnaporthe oryzae and yield traits via LOC_Os05g01790. Osa-miR1873 was significantly upregulated in a susceptible accession but downregulated in a resistance accession at 24 h post-inoculation (hpi) of M. oryzae. Overexpressing Osa-miR1873 enhanced susceptibility to M. oryzae and compromised induction of defense responses. In contrast, blocking Osa-miR1873 through target mimicry compromised susceptibility to M. oryzae and enhanced induction of defense responses. Altered expression of Osa-miR1873 also resulted in some defects in yield traits, including grain numbers and seed setting rate. Moreover, overexpression of the target gene LOC_Os05g01790 increased rice blast disease resistance but severely penalized growth and yield. Taken together, we demonstrate that Osa-miR1873 fine-tunes the rice immunity-growth trade-off via LOC_Os05g01790, and blocking Osa-miR1873 could improve blast disease resistance without significant yield penalty. Thus, the Osa-miR1873-LOC_Os05g01790 regulatory module is valuable in balancing yield traits and blast resistance.
Substances chimiques
MicroRNAs
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1213-1226Subventions
Organisme : National Natural Science Foundation of China
ID : 31430072
Organisme : National Natural Science Foundation of China
ID : 31672090
Informations de copyright
© 2019 The Authors. Journal of Integrative Plant Biology Published by John Wiley & Sons Australia, Ltd on behalf of Institute of Botany, Chinese Academy of Sciences.
Références
Baldrich P, Campo S, Wu MT, Liu TT, Hsing YI, San Segundo B (2015) MicroRNA-mediated regulation of gene expression in the response of rice plants to fungal elicitors. RNA Biol 12: 847-863
Bialas A, Zess EK, De la Concepcion JC, Franceschetti M, Pennington HG, Yoshida K, Upson JL, Chanclud E, Wu CH, Langner T, Maqbool A, Varden FA, Derevnina L, Belhaj K, Fujisaki K, Saitoh H, Terauchi R, Banfield MJ, Kamoun S (2018) Lessons in effector and NLR biology of plant-microbe systems. Mol Plant Microbe Interact 31: 34-45
Campo S, Peris-Peris C, Sire C, Moreno AB, Donaire L, Zytnicki M, Notredame C, Llave C, San Segundo B (2013) Identification of a novel microRNA (miRNA) from rice that targets an alternatively spliced transcript of the Nramp6 (Natural resistance-associated macrophage protein 6) gene involved in pathogen resistance. New Phytol 199: 212-227
Chandran V, Wang H, Gao F, Cao XL, Chen YP, Li GB, Zhu Y, Yang XM, Zhang LL, Zhao ZX, Zhao JH, Wang YG, Li S, Fan J, Li Y, Zhao JQ, Li SQ, Wang WM (2019) miR396-OsGRFs module balances growth and rice blast disease-resistance. Front Plant Sci 9: 01999
Deng Y, Zhai K, Xie Z, Yang D, Zhu X, Liu J, Wang X, Qin P, Yang Y, Zhang G, Li Q, Zhang J, Wu S, Milazzo J, Mao B, Wang E, Xie H, Tharreau D, He Z (2017) Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science 355: 962-965
Diao Z, Yu M, Zheng S, Lin J, Lai C, Zhang W, Wu W (2014) A preliminary study on the functions of miR1873 in Rice (Oryza sativa L.). Mol Plant Breed 12: 1133-1138. (in Chinese with an English abstract)
Dong S, Zhang J, Sun D, Liu H, Yang Q, Wang H, Chen Z, Wang J (2018) Identification of Magnaporthe oryzae-elicited rice novel miRNAs and their targets by miRNA and degradome sequencing. Eur J Plant Pathol 151: 629-647
Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, Garcia JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39: 1033-1037
Kong LA, Yang J, Li GT, Qi LL, Zhang YJ, Wang CF, Zhao WS, Xu JR, Peng YL (2012) Different chitin synthase genes are required for various developmental and plant infection processes in the rice blast fungus Magnaporthe oryzae. PLoS Pathog 8: e1002526
Li Y, Cao XL, Zhu Y, Yang XM, Zhang KN, Xiao ZY, Wang H, Zhao JH, Zhang LL, Li GB, Zheng YP, Fan J, Wang J, Chen XQ, Wu XJ, Zhao JQ, Dong OX, Chen XW, Chern M, Wang WM (2019a) Osa-miR398b boosts H2O2 production and rice blast disease-resistance via multiple superoxide dismutases. New Phytol 222: 1507-1522
Li Y, Jeyakumar JMJ, Feng Q, Zhao Z-X, Fan J, Khaskheli MI, Wang W-M (2019b) The roles of rice microRNAs in rice-Magnaporthe oryzae interaction. Phytopathol Res 1: 33
Li Y, Lu YG, Shi Y, Wu L, Xu YJ, Huang F, Guo XY, Zhang Y, Fan J, Zhao JQ, Zhang HY, Xu PZ, Zhou JM, Wu XJ, Wang PR, Wang WM (2014) Multiple rice microRNAs are involved in immunity against the blast fungus Magnaporthe oryzae. Plant Physiol 164: 1077-1092
Li Y, Zhao SL, Li JL, Hu XH, Wang H, Cao XL, Xu YJ, Zhao ZX, Xiao ZY, Yang N, Fan J, Huang F, Wang WM (2017) Osa-miR169 negatively regulates rice immunity against the blast fungus Magnaporthe oryzae. Front Plant Sci 8: 2
Lin ZZ, Jiang WW, Wang JL, Lei CL (2001) Research and utilization of universally susceptible property of Japonica rice variety Lijiangxintuanheigu. Sci Agric Sin 34: 116-117
Liu B, Li JF, Ao Y, Qu J, Li Z, Su J, Zhang Y, Liu J, Feng D, Qi K, He Y, Wang J, Wang HB (2012) Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 24: 3406-3419
Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312: 436-439
Navarro L, Jay F, Nomura K, He SY, Voinnet O (2008) Suppression of the microRNA pathway by bacterial effector proteins. Science 321: 964-967
Park CH, Chen S, Shirsekar G, Zhou B, Khang CH, Songkumarn P, Afzal AJ, Ning Y, Wang R, Bellizzi M, Valent B, Wang GL (2012) The Magnaporthe oryzae effector AvrPiz-t targets the RING E3 ubiquitin ligase APIP6 to suppress pathogen-associated molecular pattern-triggered immunity in rice. Plant Cell 24: 4748-4762
Peris-Peris C, Serra-Cardona A, Sánchez-Sanuy F, Campo S, Ariño J, Segundo BS (2017) Two NRAMP6 isoforms function as iron and manganese transporters and contribute to disease resistance in rice. Mol Plant Microbe Interact 30: 385-398
Ross CA, Liu Y, Shen QJ (2007) The WRKY gene family in rice (Oryza sativa). J Integr Plant Biol 49: 827-842
Salvador-Guirao R, Hsing YI, San Segundo B (2018) The polycistronic miR166k-166h positively regulates rice immunity via post-transcriptional control of EIN2. Front Plant Sci 9: 337
Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H, Shibuya N (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64: 204-214
Song X, Li Y, Cao X, Qi Y (2019) MicroRNAs and their regulatory roles in plant-environment interactions. Annu Rev Plant Biol 70: 489-525
Tang J, Chu C (2017) MicroRNAs in crop improvement: Fine-tuners for complex traits. Nat Plants 3: 17077
Tsumematsu H, Yanoria MJT, Ebron LA, Hayashi N, Ando I, Kato H, Imbe T, Khush GS (2000) Development of monogenic lines of rice for blast resistance. Breed Sci 50: 229-234
Turner M, Adhikari S, Subramanian S (2013) Optimizing stem-loop qPCR assays through multiplexed cDNA synthesis of U6 and miRNAs. Plant Signal Behav 8: e24918
Wang BH, Ebbole DJ, Wang ZH (2017) The arms race between Magnaporthe oryzae and rice: diversity and interaction of Avr and R genes. J Integr Agric 16: 2746-2760
Wang J, Zhou L, Shi H, Chern M, Yu H, Yi H, He M, Yin J, Zhu X, Li Y, Li W, Liu J, Chen X, Qing H, Wang Y, Liu G, Wang W, Li P, Wu X, Zhu L, Zhou JM, Ronald PC, Li S, Li J (2018a) A single transcription factor promotes both yield and immunity in rice. Science 361: 1026-1028
Wang Z, Xia Y, Lin S, Wang Y, Guo B, Song X, Ding S, Zheng L, Feng R, Chen S, Bao Y, Sheng C, Zhang X, Wu J, Niu D, Jin H, Zhao H (2018b) Osa-miR164a targets OsNAC60 and negatively regulates rice immunity against the blast fungus Magnaporthe oryzae. Plant J 95: 584-597
Wu L, Zhang Q, Zhou H, Ni F, Wu X, Qi Y (2009) Rice microRNA effector complexes and targets. Plant Cell 21: 3421-3435
Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y (2010) DNA methylation mediated by a microRNA pathway. Mol Cell 38: 465-475
Xiao Z-Y, Wang Q-X, Wang H, Li J-L, Zhao S-L, Fan J, Li Y, Wang W-M (2017) MiR444b.2 regulates resistance to Magnaporthe oryzae and tillering in rice. Acta Phytopathol Sin 47: 511-522. (in Chinese with an English abstract)
Xie Z, Yan B, Shou J, Tang J, Wang X, Zhai K, Liu J, Li Q, Luo M, Deng Y, He Z (2019) A nucleotide-binding site-leucine-rich repeat receptor pair confers broad-spectrum disease resistance through physical association in rice. Philos Trans R Soc B Biol Sci 374: 20180308
Zhang H, Lang Z, Zhu JK (2018a) Dynamics and function of DNA methylation in plants. Nat Rev Mol Cell Biol 19: 489-506
Zhang X, Bao Y, Shan D, Wang Z, Song X, Wang J, He L, Wu L, Zhang Z, Niu D, Jin H, Zhao H (2018b) Magnaporthe oryzae induces the expression of a microRNA to suppress the immune response in rice. Plant Physiol 177: 352-368
Zhang X, Zhao H, Gao S, Wang W, Katiyar-Agarwal S, Huang H, Raikhel N, Jin H (2011) Arabidopsis Argonaute 2 regulates innate immunity via miRNA393(*)-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol Cell 42: 356-366
Zhao ZX, Feng Q, Cao XL, Zhu Y, Wang H, Chandran V, Fan J, Zhao JQ, Pu M, Li Y, Wang WM (2020) Osa-miR167d facilitates infection of Magnaporthe oryzae in rice. J Integr Plant Biol 62: 702-715