Osa-miR162a fine-tunes rice resistance to Magnaporthe oryzae and Yield

Rice - Tập 13 - Trang 1-13 - 2020
Xu-Pu Li1,2, Xiao-Chun Ma1,2, He Wang1,2, Yong Zhu1,2, Xin-Xian Liu1,2, Ting-Ting Li1,2, Ya-Ping Zheng1,2, Ji-Qun Zhao1,2, Ji-Wei Zhang1,2, Yan-Yan Huang1,2, Mei Pu1,2, Hui Feng1,2, Jing Fan1,2, Yan Li1,2, Wen-Ming Wang1,2
1State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University, Chengdu, China
2Rice Research Institute and Key Lab for Major Crop Diseases, Sichuan Agricultural University, Chengdu, China

Tóm tắt

MicroRNAs (miRNAs) play essential roles in rice immunity against Magnaporthe oryzae, the causative agent of rice blast disease. Here we demonstrate that Osa-miR162a fine-tunes rice immunity against M. oryzae and yield traits. Overexpression of Osa-miR162a enhances rice resistance to M. oryzae accompanying enhanced induction of defense-related genes and accumulation of hydrogen peroxide (H2O2). In contrast, blocking Osa-miR162 by overexpressing a target mimic of Osa-miR162a enhances susceptibility to blast fungus associating with compromised induction of defense-related gene expression and H2O2 accumulation. Moreover, the transgenic lines overexpressing Osa-miR162a display decreased seed setting rate resulting in slight reduced yield per plant, whereas the transgenic lines blocking Osa-miR162 show an increased number of grains per panicle, resulting in increased yield per plant. Altered accumulation of Osa-miR162 had a limited impact on the expression of rice Dicer-like 1 (OsDCL1) in these transgenic lines showing normal gross morphology, and silencing of OsDCL1 led to enhanced resistance to blast fungus similar to that caused by overexpression of Osa-miR162a, suggesting the involvement of OsDCL1 in Osa-miR162a-regulated resistance. Together, our results indicate that Osa-miR162a is involved in rice immunity against M. oryzae and fine-tunes resistance and yield.

Tài liệu tham khảo

Campo S, Peris-Peris C, Sire C, Moreno AB, Donaire L, Zytnicki M, Notredame C, Llave C, Segundo BS (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 199:212–217 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 (2018) miR396-OsGRFs module balances growth and Rice blast disease-resistance. Front. Plant Sci 9:1999 Chen C, Ridzon DA, Broomer AJ, Zhou Z, Guegler KJ (2005) Real-time quantification of microRNAs by stem–loop RT–PCR. Nucleic Acids Res 33:e179 de Lima JC, Loss-Morais G, Margis R (2012) MicroRNAs play critical roles during plant development and in response to abiotic stresses. Genet Mol Biol 35:1069–1077 Ding D, Zhang L, Wang H, Liu Z, Zhang Z, Zheng Y (2009) Differential expression of miRNAs in response to salt stress in maize roots. Ann Bot 103:29–38 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 Kankanala P, Czymmek K, Valent B (2007) Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. Plant Cell 19:706–724 Katiyar-Agarwal S, Jin H (2010) Role of small RNAs in host-microbe interactions. Annu Rev Phytopathol 48:225–246 Kurihara Y, Watanabe Y (2004) Arabidopsis micro-RNA biogenesis through dicer-like 1 protein functions. Proc Natl Acad Sci U S A 101:12753–12758 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 H2 O2 production and rice blast disease-resistance via multiple superoxide dismutases. New Phytol. https://doi.org/10.1111/nph.15678 Li Y, Jeyakumar JMJ, Feng Q, Zhao ZX, Fan J, Khaskheli MK, Wang WM (2019b) The roles of rice microRNAs in rice-Magnaporthe oryzae interaction. Phytopathology Research Published: 18 November 2019. 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. Scientia Agricultura Sinjca 34:116–117 Liu B, Li P, Li X, Liu C, Cao S, Chu C, Cao X (2005) Loss of function of OsDCL1 affects microRNA accumulation and causes developmental defects in rice. Plant Physiol 139:296–305 Liu W, Wang GL (2016) Plant innate immunity in rice: a defense against pathogen infection. Natl Sci Rev 3:295–308 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 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 Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495 Pertermann R, Tamilarasan S, Gursinsky T, Gambino G, Schuck J, Weinholdt C, Lilie H, Grosse I, Golbik RP, Pantaleo V, Behrens SE (2018) A viral suppressor modulates the plant immune response early in infection by regulating MicroRNA activity. mBio 9. https://doi.org/10.1128/mBio.00419-18 Qiao Y, Jiang W, Lee J, Park B, Choi MS, Piao R, Woo MO, Roh JH, Han L, Paek NC, Seo HS, Koh HJ (2010) SPL28 encodes a clathrin-associated adaptor protein complex 1, medium subunit micro 1 (AP1M1) and is responsible for spotted leaf and early senescence in rice (Oryza sativa). New Phytol 185:258–274 Qu S, Guifu L, Bo Z, Maria B, Lirong Z, Liangying D, Bin H, Guo-Liang W (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 172:1901–1914 Salih H, Gong W, Mkulama M, Du X (2018) Genome-wide characterization, identification, and expression analysis of the WD40 protein family in cotton. Genome 61:539–547 Salvador-Guirao R, Baldrich P, Tomiyama S, Hsing YI, Okada K, San Segundo B (2019) OsDCL1a activation impairs phytoalexin biosynthesis and compromises disease resistance in rice. Ann Bot 123:79–93 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 Seo JK, Wu J, Lii Y, Li Y, Jin H (2013) Contribution of small RNA pathway components in plant immunity. Mol Plant Microbe Interact 26:617–625 Shi J, Li D, Li Y, Li X, Guo X, Luo Y, Lu Y, Zhang Q, Xu Y, Fan J, Huang F, Wang W (2015) Identification of rice blast resistance genes in the elite hybrid rice restorer line Yahui2115. Genome 58:91–97 Sun G, Stewart CN Jr, Xiao P, Zhang B (2012) MicroRNA expression analysis in the cellulosic biofuel crop switchgrass (Panicum virgatum) under abiotic stress. PLoS One 7:e32017 Tang J, Chu C (2017) MicroRNAs in crop improvement: fine-tuners for complex traits. Nat Plants 3:17077 Tian C, Zuo Z, Qiu JL (2015) Identification and characterization of ABA-responsive MicroRNAs in Rice. J Genet Genomics 42:393–402 Tijsterman M, Plasterk RH (2004) Dicers at RISC; the mechanism of RNAi. Cell 117:1–3 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 Varkonyi-Gasic E, Wu R, Wood M, Walton EF, Hellens RP (2007) Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods 3:12 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 (2018) Osa-miR164a targets OsNAC60 and negatively regulates rice immunity against the blast fungus Magnaporthe oryzae. Plant J. https://doi.org/10.1111/tpj.13972 Weiberg A, Wang M, Bellinger M, Jin H (2014) Small RNAs: a new paradigm in plant-microbe interactions. Annu Rev Phytopathol 52:495–516 Wu L, Zhang Q, Zhou H, Ni F, Wu X, Qi Y (2009) Rice MicroRNA effector complexes and targets. Plant Cell 21:3421–3435 Xiao S, Brown S, Patrick E, Brearley C, Turner JG (2003) Enhanced transcription of the Arabidopsis disease resistance genes RPW8.1 and RPW8.2 via a salicylic acid-dependent amplification circuit is required for hypersensitive cell death. Plant Cell 15:33–45 Xiao ZY, Wang WQ, Zhao SL, Wang H, Li JL, Huang F, Fan J, Li Y, Wang WM (2017) MiR444b.2 regulates resistance to Magnaporthe oryzae and tillering in rice. Acta Phytopathol Sin 47:511–522 Xie Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD, Zilberman D, Jacobsen SE, Carrington JC (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2:E104 Yamaguchi K, Yamada K, Ishikawa K, Yoshimura S, Hayashi N, Uchihashi K, Ishihama N, Kishi-Kaboshi M, Takahashi A, Tsuge S, Ochiai H, Tada Y, Shimamoto K, Yoshioka H, Kawasaki T (2013) A receptor-like cytoplasmic kinase targeted by a plant pathogen effector is directly phosphorylated by the chitin receptor and mediates Rice immunity. Cell Host Microbe 13:347–357 Yin Z, Chen J, Zeng L, Goh M, Leung H, Khush GS, Wang GL (2000) Characterizing rice lesion mimic mutants and identifying a mutant with broad-spectrum resistance to rice blast and bacterial blight. Mol Plant Microbe Interact 13:869–876 Yu Y, Jia T, Chen X (2017) The 'how' and 'where' of plant microRNAs. New Phytol 216:1002–1017 Zhang D, Liu M, Tang M, Dong B, Wu D, Zhang Z, Zhou B (2015) Repression of microRNA biogenesis by silencing of OsDCL1 activates the basal resistance to Magnaporthe oryzae in rice. Plant Sci 237:24–32 Zhang X, Bao Y, Shan D, Wang Z, Song X, Wang J, He L, Wu L, Zhang Z, Niu D, Jin H, Zhao H (2018a) Magnaporthe oryzae induces the expression of a MicroRNA to suppress the immune response in Rice. Plant Physiol 177:352–368 Zhang X, Bao Y, Shan D, Wang Z, Song X, Wang Z, Wang J, He L, Wu L, Zhang Z (2018b) Magnaporthe oryzae defeats rice defense by inducing miR319b and suppressing Jasmonic acid signaling. Plant Physiol 177:01665.02017 Zhao ZX, Feng Q, Cao XL, Zhu Y, Wang H, Chandran V, Fan J, Zhao JQ, Pu M, Li Y, Wang WM (2019) Osa-miR167d facilitates infection of Magnaporthe oryzae in rice. J Integr Plant Biol. https://doi.org/10.1111/jipb.12816 Zhou M, Gu LF, Li PC, Song XW, Wei LY, Chen ZY, Cao XF (2010) Degradome sequencing reveals endogenous small RNAtargets in rice (Oryza sativa L. ssp. indica). Front Biol 5:67–90 Zhou SX, Zhu Y, Wang LF, Zheng YP, Chen JF, Li TT, Yang XM, Wang H, Li XP, Ma XC, Zhao JQ, Pu M, Feng H, Li Y, Fan J, Zhang JW, Huang YY, Wang WM (2019) Osa-miR1873 fine-tunes rice immunity against Magnaporthe oryzae and yield traits. J Integr Plant Biol. https://doi.org/10.1111/jipb.12900