Skip to main content

Advertisement

SpringerLink
Log in

Silencing of miR156 confers enhanced resistance to brown planthopper in rice

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Silencing of miR156 in rice confers enhanced resistance to brown planthopper through reducing JA and JA-Ile biosynthesis.

Rice brown planthopper (BPH, Nilaparvata lugens Stål) threatens the sustainability of rice production and global food security. Due to the rapid adaptation of BPH to current germplasms in rice, development of novel types of resistant germplasms becomes increasingly important. Plant ontogenetic defense against pathogen and herbivores offers a broad spectrum and durable resistance, and has been experimentally tested in many plants; however, the underlying molecular mechanism remains unclear. miR156 is the master regulator of ontogeny in plants; modulation of miR156 is, therefore, expected to cause corresponding changes in BPH resistance. To test this hypothesis, we silenced miR156 using a target mimicry method in rice, and analyzed the resistance of miR156-silenced plants (MIM156) to BPH. MIM156 plants exhibited enhanced resistance to BPH based on analyses of honeydew excretion, nymph survival, fecundity of BPH, and the survival ratio of rice plants after BPH infestation. Molecular analysis indicated that the expression of MPK3, MPK6, and WRKY70, three genes involved in BPH resistance and jasmonic acid (JA) signaling, was altered in MIM156 plants. The JA and bioactive jasmonoyl-isoleucine levels and the expression of genes involved in JA biosynthesis were significantly reduced in MIM156 plants. Restoration of JA level by exogenous application increased the number of BPH feeding on MIM156 plants and reduced its resistance to BPH. Our findings suggest that miR156 negatively regulates BPH resistance by increasing JA level in rice; therefore, modulation of miR156-SPLs’ pathway may offer a promising way to breed rice varieties with enhanced resistance against BPH and elite agronomically important traits.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

BPH:

Brown planthopper

MIM156:

Mimicry156

JA:

Jasmonic acid

JA-Ile:

Jasmonoyl-isoleucine

SA:

Salicylic acid

Et:

Ethylene

SPL :

SQUAMOSA PROMOTER BINDING PROTEIN-LIKE genes

LOX:

Lipoxygenase

References

  • Alamgir KM, Hojo Y, Christeller JT, Fukumoto K, Isshiki R, Shinya T, Baldwin IT, Galis I (2016) Systematic analysis of rice (Oryza sativa) metabolic responses to herbivory. Plant Cell Environ 39:453–466

    Article  CAS  PubMed  Google Scholar 

  • Asai K, Satoh N, Sasaki H, Satoh H, Nagato Y (2002) A rice heterochronic mutant, mori1, is defective in the juvenile-adult phase change. Development 129:265–273

    CAS  PubMed  Google Scholar 

  • Atamian HS, Eulgem T, Kaloshian I (2012) SlWRKY70 is required for Mi-1-mediated resistance to aphids and nematodes in tomato. Planta 235:299–309

    Article  CAS  PubMed  Google Scholar 

  • Baqu M, Kersha WJ (1993) Effect of plant age on host preference, honeydew production and fecundity of Nilaparvata lugens (Stål) (Horn., Delphacidae) on rice cultivars. J Appl Entomol 116:133–138

    Article  Google Scholar 

  • Barton K, Hanley M (2013) Seedling–herbivore interactions: insights into plant defence and regeneration patterns. Ann Bot 112:643–650

    Article  PubMed  PubMed Central  Google Scholar 

  • Barton K, Koricheva J (2010) The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. Am Nat 175:481–493

    Article  PubMed  Google Scholar 

  • Beydler B, Osadchuk K, Cheng CL, Manak JR, Irish EE (2016) The juvenile phase of maize sees upregulation of stress-response genes and is extended by exogenous jasmonic acid. Plant Physiol 171:2648–2658

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bhattarai KK, Atamian HS, Kaloshian I, Eulgem T (2010) WRKY72-type transcription factors contribute to basal immunity in tomato and Arabidopsis as well as gene-for-gene resistance mediated by the tomato R gene Mi-1. Plant J 63:229–240

    Article  CAS  PubMed  Google Scholar 

  • Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448

    Article  PubMed  Google Scholar 

  • Cheng X, Zhu L, He G (2013) Towards understanding of molecular interactions between rice and the brown planthopper. Mol Plant 6:621–634

    Article  CAS  PubMed  Google Scholar 

  • Cho SK, Young SC, Sung JP, Jeong SS, Hyok JK, Kyung HK (1998) Efficient transformation of Korean rice cultivars (Oryza sative L.) mediated by Agrobacterium tumefaciens. J Plant Biol 41:262–268

    Article  Google Scholar 

  • Chuck G, Cigan AM, Saeteurn K, Hake S (2007) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39:544–549

    Article  CAS  PubMed  Google Scholar 

  • Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, Fitt GP, Sewelam N, Schenk PM, Manners JM, Kazan K (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225–2245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du B, Zhang W, Liu B, Hu J, Wei Z, Shi Z, He R, Zhu L, Chen R, Han B, He G (2009) Identification and characterization of Bph14, a gene conferring resistance to brown planthopper in rice. Proc Natl Acad Sci USA 106:22163–22168

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gallagher KD, Kenmore PE, Sogawa K (1994) Judicial use of insecticides deter planthopper outbreaks and extend the life of resistant varieties in Southeast Asian rice. In: Denno RF, Perfect JR (eds) Planthoppers: their ecology and management. Chapman & Hall, New York, pp 599–614

    Chapter  Google Scholar 

  • Guo C, Yao L, You C, Wang S, Cui J, Ge X, Ma H (2016) MID1 plays an important role in response to drought stress during reproductive development. Plant J 88:280–293

    Article  CAS  PubMed  Google Scholar 

  • Hibara K, Isono M, Mimura M, Sentoku N, Kojima M, Sakakibara H, Kitomi Y, Yoshikawa T, Itoh J, Nagato Y (2016) Jasmonate regulates juvenile-to-adult phase transition in rice. Development 143:3407–3416

    Article  CAS  PubMed  Google Scholar 

  • Hu L, Ye M, Li R, Zhang T, Zhou G, Wang Q, Lu J, Lou Y (2015) The rice transcription factor WRKY53 suppresses herbivore-induced defenses by acting as a negative feedback modulator of mitogen-activated protein kinase activity. Plant Physiol 169:2907–2921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu L, Wu Y, Wu D, Rao W, Guo J, Ma Y, Wang Z, Shangguan X, Wang H, Xu C, Huang J, Shi S, Chen R, Du B, Zhu L, He G (2017) The coiled-coil and nucleotide binding domains of BROWN PLANTHOPPER RESISTANCE14 function in signaling and resistance against planthopper in rice. Plant Cell 29:3157–3185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang D, Qiu Y, Zhang Y, Huang F, Meng J, Wei S, Li R, Chen B (2013) Fine mapping and characterization of BPH27, a brown planthopper resistance gene from wild rice (Oryza rufipogon Griff.). Theor Appl Genet 126:219–229

    Article  CAS  PubMed  Google Scholar 

  • Jiao Y, Wang Y, Xue D, Jing W, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42:541–544

    Article  CAS  PubMed  Google Scholar 

  • Kaur H, Heinzel N, Schottner M, Baldwin IT, Galis I (2010) R2R3-NaMYB8 regulates the accumulation of phenylpropanoid–polyamine conjugates, which are essential for local and systemic defense against insect herbivores in Nicotiana attenuata. Plant Physiol 152:1731–1747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ketipearachchi Y, Kaneda C, Nakamura C (1998) Adaptation of the brown planthopper (BPH), Nilaparvata lugens (Stål) (Homoptera: Delphacidae) to BPH resistant rice cultivara carring bph8 or Bph9. Appl Entomol Zool 33:497–505

    Article  Google Scholar 

  • Kobayashi T, Yamamoto K, Suetsugu Y, Kuwazaki S, Hattori M, Jairin J, Sanada-Morimura S, Matsumura M (2014) Genetic mapping of the rice resistance-breaking gene of the brown planthopper Nilaparvata lugens. Proc Biol Sci 281:20140726

    Article  PubMed  PubMed Central  Google Scholar 

  • Kramell R, Schmidt J, Schneider G, Sembdner G, Schreiber K (1988) Synthesis of n-(jasmonoyl) amino acid conjugates. Tetrahedron 44:5791–5807

    Article  CAS  Google Scholar 

  • Kurotani K, Hayashi K, Hatanaka S, Toda Y, Ogawa D, Ichikawa H, Ishimaru Y, Tashita R, Suzuki T, Ueda M (2015) Elevated levels of CYP94 family gene expression alleviate the jasmonate response and enhance salt tolerance in rice. Plant Cell Physiol 56:779–789

    Article  CAS  PubMed  Google Scholar 

  • Lang TN, Buu BC (2003) Genetic and physical maps of gene Bph10 controlling brown plant hopper resistance in rice (Oryza sativa L.). Omonrice 11:35–41

    Google Scholar 

  • Li R, Zhang J, Li J, Zhou G, Wang Q, Bian W, Erb M, Lou Y (2015) Prioritizing plant defence over growth through WRKY regulation facilitates infestation by non-target herbivores. Elife 4:e04805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ling K, Tiongco E, Aguiero V (1977) Transmission of rice ragged stunt disease. Int Rice Res Newsl Int Rice Res Inst 2:11–12

    Google Scholar 

  • Liu Y, Wu H, Chen H, Liu Y, He J, Kang H, Sun Z, Pan G, Wang Q, Hu J, Zhou F, Zhou K, Zheng X, Ren Y, Chen L, Wang Y, Zhao Z, Lin Q, Wu F, Zhang X, Guo X, Cheng X, Jiang L, Wu C, Wang H, Wan J (2015) A gene cluster encoding lectin receptor kinases confers broad-spectrum and durable insect resistance in rice. Nat Biotechnol 33:301–305

    Article  CAS  PubMed  Google Scholar 

  • Lu J, Ju H, Zhou G, Zhu C, Erb M, Wang X, Wang P, Lou Y (2011) An EAR-motif-containing ERF transcription factor affects herbivore-induced signaling, defense and resistance in rice. Plant J 68:583–596

    Article  CAS  PubMed  Google Scholar 

  • Luo Y, Guo Z, Li L (2013) Evolutionary conservation of microRNA regulatory programs in plant flower development. Dev Biol 380:133–144

    Article  CAS  PubMed  Google Scholar 

  • Lv W, Du B, Shangguan X, Zhao Y, Pan Y, Zhu L, He Y, He G (2014) BAC and RNA sequencing reveal the brown planthopper resistance gene BPH15 in a recombination cold spot that mediates a unique defense mechanism. BMC Genomics 15:674

    Article  PubMed  PubMed Central  Google Scholar 

  • Mao YB, Liu YQ, Chen DY, Chen FY, Fang X, Hong GJ, Wang LJ, Wang JW, Chen XY (2017) Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance. Nat Commun 8:13925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miura K, Ikeda M, Matsubara A, Song XJ, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42:545–549

    Article  CAS  PubMed  Google Scholar 

  • Normile D (2008) Reinventing rice to feed the world. Science 321:330–333

    Article  CAS  PubMed  Google Scholar 

  • Poethig RS (1990) Phase change and the regulation of shoot morphogenesis in plants. Science 250:923–930

    Article  CAS  PubMed  Google Scholar 

  • Rahman ML, Jiang W, Chu SH, Qiao Y, Ham TH, Woo MO, Lee J, Khanam MS, Chin JH, Jeung JU, Brar DS, Jena KK, Koh HJ (2009) High-resolution mapping of two rice brown planthopper resistance genes, Bph20(t) and Bph21(t), originating from Oryza minuta. Theor Appl Genet 119:1237–1246

    Article  PubMed  Google Scholar 

  • Rivera CT, Ou SH, Lida TT (1966) Grassy stunt disease of rice and its transmission by Nilaparvata lugens Stål. Plant Dis Rep 50:453–456

    Google Scholar 

  • Sharma PN, Torii A, Takumi S, Mori N, Nakamura C (2004) Marker-assisted pyramiding of brown planthopper (Nilaparvata lugens Stål) resistance genes Bph1 and Bph2 on rice chromosome 12. Hereditas 140:61–69

    Article  PubMed  Google Scholar 

  • Skibbe M, Qu N, Galis I, Baldwin IT (2008) Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell 20:1984–2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sogawa K, Mittler T, Radovsky F, Resh V (1982) The rice brown planthopper: feeding physiology and host plant interactions. Annu Rev Entomol 27:49–73

    Article  CAS  Google Scholar 

  • Tamura Y, Hattori M, Yoshioka H, Yoshioka M, Takahashi A, Wu J, Sentoku N, Yasui H (2014) Map-based cloning and characterization of a brown planthopper resistance gene BPH26 from Oryza sativa L. ssp. indica cultivar ADR52. Sci Rep 4:5872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka K, Endo S, Kazano H (2000) Toxicity of insecticides to predators of rice planthoppers: spiders, the mirid bug and the dryinid wasp. Appl Entomol Zool 35:177–187

    Article  CAS  Google Scholar 

  • van Dam NM, Horn M, Mares M, Baldwin IT (2001) Ontogeny constrains systemic protease inhibitor response in Nicotiana attenuata. J Chem Ecol 27:547–568

    Article  PubMed  Google Scholar 

  • Wang Y, Li J (2005) The plant architecture of rice (Oryza sativa). Plant Mol Biol 59:75–84

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Halitschke R, Kang JH, Berg A, Harnisch F, Baldwin IT (2007) Independently silencing two JAR family members impairs levels of trypsin proteinase inhibitors but not nicotine. Planta 226:159–167

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Wu K, Yuan Q, Liu X, Liu Z, Lin X, Zeng R, Zhu H, Dong G, Qian Q (2012) Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet 44:950–954. https://doi.org/10.1038/ng.2327

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Li S, Liu Q, Wu K, Zhang J, Wang S, Wang Y, Chen X, Zhang Y, Gao C (2015a) The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality. Nat Genet 47:949–954. https://doi.org/10.1038/ng.3352

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Cao L, Zhang Y, Cao C, Liu F, Huang F, Qiu Y, Li R, Lou X (2015b) Map-based cloning and characterization of BPH29, a B3 domain-containing recessive gene conferring brown planthopper resistance in rice. J Exp Bot 66:6035–6045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J, Hettenhausen C, Meldau S, Baldwin IT (2007) Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell 19:1096–1122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138:750–759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu H, Liu Y, He J, Liu Y, Jiang L, Liu L, Wang C, Cheng X, Wan J (2014) Fine mapping of brown planthopper (Nilaparvata lugens Stål) resistance gene Bph28(t) in rice (Oryza sativa L.). Mol Breed 33:909–918

    Article  CAS  Google Scholar 

  • Yang L, Zhang W (2016) Genetic and biochemical mechanisms of rice resistance to planthopper. Plant Cell Rep 35:1559–1572

    Article  CAS  Google Scholar 

  • Yang L, Han Y, Li P, Li F, Ali S, Hou M (2017) Silicon amendment is involved in the induction of plant defense responses to a phloem feeder. Sci Rep 7:4232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yara A, Phi CN, Matsumura M, Yoshimura A, Yasui H (2010) Development of near-isogenic lines for BPH25(t) and BPH26(t), which confer resistance to the brown planthopper, Nilaparvata lugens (Stål.) in indica rice ‘ADR52’. Breed Sci 60:639–647

    Article  Google Scholar 

  • Yu J, Lai Y, Wu X, Wu G, Guo C (2016) Overexpression of OsEm1 encoding a group I LEA protein confers enhanced drought tolerance in rice. Biochem Biophys Res Commun 478:703–709

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Huang J, Wang Z, Jing S, Wang Y, Ouyang Y, Cai B, Xin XF, Liu X, Zhang C, Pan Y, Ma R, Li Q, Jiang W, Zeng Y, Shangguan X, Wang H, Du B, Zhu L, Xu X, Feng YQ, He SY, Chen R, Zhang Q, He G (2016) Allelic diversity in an NLR gene BPH9 enables rice to combat planthopper variation. Proc Natl Acad Sci USA 113:12850–12855

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Han Z, Zhang X, Pang C (2003) Influence of rice varieties on the metabolizing enzymes of Nilaparvata lugens Stål. J Nanjing Agric Univ 26:24–28

    CAS  Google Scholar 

  • Zhou G, Qi J, Ren N, Cheng J, Erb M, Mao B, Lou Y (2009) Silencing OsHI-LOX makes rice more susceptible to chewing herbivores, but enhances resistance to a phloem feeder. Plant J 60:638–648

    Article  CAS  PubMed  Google Scholar 

  • Zhou G, Ren N, Qi J, Lu J, Xiang C, Ju H, Cheng J, Lou Y (2014) The 9-lipoxygenase Osr9-LOX1 interacts with the 13-lipoxygenase-mediated pathway to regulate resistance to chewing and piercing-sucking herbivores in rice. Physiol Plant 152:59–69

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by grants from the National Natural Science Foundation of China (31770209, 31770352, and 31500252) and Natural Science Foundation of Zhejiang Province (LY15C020004) to G. W. and C. G. This work was also partially supported by start-up funds from Zhejiang Agriculture and Forestry University (2012FR025 and 2013FR083) and the 1000 Youth Talents Program in China (2034020065) to G. W. and C. G. We thank members of the Wu laboratory for useful comments on this manuscript.

Author information

Author notes

  1. Yafei Ge, Junyou Han, and Guoxin Zhou have contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Subtropical Silviculture, School of Agriculture and Food Sciences, Zhejiang Agriculture and Forestry University, Hangzhou, 311300, China

    Yafei Ge, Guoxin Zhou, Yunmin Xu, Yue Ding, Min Shi, Changkui Guo & Gang Wu

  2. College of Plant Science, Jilin University, Changchun, 130062, China

    Junyou Han

Authors
  1. Yafei Ge
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Junyou Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guoxin Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yunmin Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yue Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Min Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Changkui Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Gang Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Changkui Guo or Gang Wu.

Ethics declarations

Conflict of interest

The authors declare that they do not have conflicts of interests.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 337 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ge, Y., Han, J., Zhou, G. et al. Silencing of miR156 confers enhanced resistance to brown planthopper in rice. Planta 248, 813–826 (2018). https://doi.org/10.1007/s00425-018-2942-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-018-2942-6

Keywords

Search

Navigation