Skip to main content
SpringerLink
Log in

Integration of transcriptome and metabolome analyses reveals the role of OsSPL10 in rice defense against brown planthopper

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

OsSPL10 is a negative regulator of rice defense against BPH, knockout of OsSPL10 enhances BPH resistance through upregulation of defense-related genes and accumulation of secondary metabolites.

Abstract

Rice (Oryza sativa L.), one of the most important staple foods worldwide, is frequently attacked by various herbivores, including brown planthopper (BPH, Nilaparvata lugens). BPH is a typical monophagous, phloem-sucking herbivore that has been a substantial threat to rice production and global food security. Understanding the regulatory mechanism of defense responses to BPH is essential for improving BPH resistance in rice. In this study, a SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE 10 (OsSPL10) transcription factor was found to play a negative role in the defenses of rice against BPH. To gain insights into the molecular and biochemical mechanisms of OsSPL10, we performed combined analyses of transcriptome and metabolome, and revealed that knockout of OsSPL10 gene improved rice resistance against BPH by enhancing the direct and indirect defenses. Genes involved in plant hormone signal transduction, MAPK signaling pathway, phenylpropanoid biosynthesis, and plant–pathogen interaction pathway were significantly upregulated in spl10 mutant. Moreover, spl10 mutant exhibited increased accumulation of defense-related secondary metabolites in the phenylpropanoid and terpenoid pathways. Our findings reveal a novel role for OsSPL10 gene in regulating the rice defense responses, which can be used as a potential target for genetic improvement of BPH resistance in rice.

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
Fig. 7

Similar content being viewed by others

Data availability

All data supporting the conclusions of this article are provided within the article (and its Additional files).

References

  • Barros J, Serrani-Yarce JC, Chen F, Baxter D, Venables BJ, Dixon RA (2016) Role of bifunctional ammonia-lyase in grass cell wall biosynthesis. Nature Plants 2:16050

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Chen H, Yuan JS, Kollner TG, Chen Y, Guo Y, Zhuang X, Chen X, Zhang YJ, Fu J, Nebenfuhr A, Guo Z, Chen F (2018) The rice terpene synthase gene OsTPS19 functions as an (S)-limonene synthase in planta, and its overexpression leads to enhanced resistance to the blast fungus Magnaporthe oryzae. Plant Biotechnol J 16:1778–1787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen S, Sun B, Shi Z, Miao X, Li H (2022) Identification of the rice genes and metabolites involved in dual resistance against brown planthopper and rice blast fungus. Plant Cell Environ 45:1914–1929

    Article  CAS  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 

  • 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  PubMed Central  Google Scholar 

  • Garg R, Tyagi AK, Jain M (2012) Microarray analysis reveals overlapping and specific transcriptional responses to different plant hormones in rice. Plant Signal Behav 7:951–956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo J, Xu C, Wu D, Zhao Y, Qiu Y, Wang X, Ouyang Y, Cai B, Liu X, Jing S, Shangguan X, Wang H, Ma Y, Hu L, Wu Y, Shi S, Wang W, Zhu L, Xu X, Chen R, Feng Y, Du B, He G (2018) Bph6 encodes an exocyst-localized protein and confers broad resistance to planthoppers in rice. Nat Genet 50:297–306

    Article  CAS  PubMed  Google Scholar 

  • He J, Liu Y, Yuan D, Duan M, Liu Y, Shen Z, Yang C, Qiu Z, Liu D, Wen P, Huang J, Fan D, Xiao S, Xin Y, Chen X, Jiang L, Wang H, Yuan L, Wan J (2019) An R2R3 MYB transcription factor confers brown planthopper resistance by regulating the phenylalanine ammonia-lyase pathway in rice. Proc Natl Acad Sci USA 117:271–277

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu L, Ye M, Li R, Lou Y (2016) OsWRKY53, a versatile switch in regulating herbivore-induced defense responses in rice. Plant Signal Behav 11:e1169357

    Article  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 

  • Hu X, Su S, Liu Q, Jiao Y, Peng Y, Li Y, Turlings TC (2020) Caterpillar-induced rice volatiles provide enemy-free space for the offspring of the brown planthopper. Elife. https://doi.org/10.7554/eLife.55421

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang Z, He G, Shu L, Li X, Zhang Q (2001) Identification and mapping of two brown planthopper resistance genes in rice. Theor Appl Genet 102:929–934

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kishi-Kaboshi M, Seo S, Takahashi A, Hirochika H (2018) The MAMP-responsive MYB transcription factors MYB30, MYB55 and MYB110 activate the HCAA synthesis pathway and enhance immunity in rice. Plant Cell Physiol 59:903–915

    Article  CAS  PubMed  Google Scholar 

  • Lan T, Zheng Y, Su Z, Yu S, Song H, Zheng X, Lin G, Wu W (2019) OsSPL10, a SBP-box gene, plays a dual role in salt tolerance and trichome formation in rice (Oryza sativa L). G3 (bethesda) 9:4107–4114

    Article  CAS  PubMed  Google Scholar 

  • Lefevere H, Bauters L, Gheysen G (2020) Salicylic acid biosynthesis in plants. Front Plant Sci 11:338

    Article  PubMed  PubMed Central  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  PubMed  PubMed Central  Google Scholar 

  • Li J, Tang B, Li Y, Li C, Guo M, Chen H, Han S, Li J, Lou Q, Sun W, Wang P, Guo H, Ye W, Zhang Z, Zhang H, Yu S, Zhang L, Li Z (2021) Rice SPL10 positively regulates trichome development through expression of HL6 and auxin-related genes. J Integr Plant Biol 63:1521–1537

    Article  CAS  PubMed  Google Scholar 

  • Liao Z, Wang L, Li C, Cao M, Wang J, Yao Z, Zhou S, Zhou G, Zhang D, Lou Y (2022) The lipoxygenase gene OsRCI-1 is involved in the biosynthesis of herbivore-induced JAs and regulates plant defense and growth in rice. Plant Cell Environ 45:2827–2840

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Bai X, Wang X, Chu C (2007) OsWRKY71, a rice transcription factor, is involved in rice defense response. J Plant Physiol 164:969–979

    Article  CAS  PubMed  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 

  • Lou Y, Zhang G, Zhang W, Hu Y, Zhang J (2013) Biological control of rice insect pests in China. Biol Control 67:8–20

    Article  Google Scholar 

  • Lu J, Li J, Ju H, Liu X, Erb M, Wang X, Lou Y (2014) Contrasting effects of ethylene biosynthesis on induced plant resistance against a chewing and a piercing-sucking herbivore in rice. Mol Plant 7:1670–1682

    Article  CAS  PubMed  Google Scholar 

  • Ma F, Yang X, Shi Z, Miao X (2020) Novel crosstalk between ethylene- and jasmonic acid-pathway responses to a piercing-sucking insect in rice. New Phyto 225:474–487

    Article  CAS  Google Scholar 

  • Munawar A, Zhang Y, Zhong J, Ge Y, Abou El-Ela AS, Mao Z, Ntiri ES, Mao LJ, Zhu Z, Zhou W (2022) Heat stress affects potato’s volatile emissions that mediate agronomically important trophic interactions. Plant Cell Environ 45:3036–3051

    Article  CAS  PubMed  Google Scholar 

  • Nagata T (1984) Insecticide resistance in the brown planthopper. Chin J Entomol 4:117–124

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pan G, Liu Y, Ji L, Zhang X, He J, Huang J, Qiu Z, Liu D, Sun Z, Xu T, Liu L, Wang C, Jiang L, Cheng X, Wan J (2018) Brassinosteroids mediate susceptibility to brown planthopper by integrating with the salicylic acid and jasmonic acid pathways in rice. J Exp Bot 69:4433–4442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi S, Wang H, Nie L, Tan D, Zhou C, Zhang Q, Li Y, Du B, Guo J, Huang J, Wu D, Zheng X, Guan W, Shan J, Zhu L, Chen R, Xue L, Walling LL, He G (2021) Bph30 confers resistance to brown planthopper by fortifying sclerenchyma in rice leaf sheaths. Mol Plant 14:1714–1732

    Article  CAS  PubMed  Google Scholar 

  • Tan J, Wu Y, Guo J, Li H, Zhu L, Chen R, He G, Du B (2020) A combined microRNA and transcriptome analyses illuminates the resistance response of rice against brown planthopper. BMC Genomics 21:144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Li S, Liu Q, Wu K, Zhang J, Wang S, Wang Y, Chen X, Zhang Y, Gao C, Wang F, Huang H, Fu X (2015) The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality. Nat Genet 47:949–954

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Yang D, Ma F, Zhu M, Shi Z, Miao X (2019) OsHLH61-OsbHLH96 influences rice defense to brown planthopper through regulating the pathogen-related genes. Rice 12:9

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu F, Duan Z, Xu P, Yan Q, Meng M, Cao M, Jones CS, Zong X, Zhou P, Wang Y, Luo K, Wang S, Yan Z, Wang P, Di H, Ouyang Z, Wang Y, Zhang J (2022) Genome and systems biology of Melilotus albus provides insights into coumarins biosynthesis. Plant Biotechnol J 20:592–609

    Article  CAS  PubMed  Google Scholar 

  • Xiao Y, Wang Q, Erb M, Turlings TC, Ge L, Hu L, Li J, Han X, Zhang T, Lu J, Zhang G, Lou Y (2012) Specific herbivore-induced volatiles defend plants and determine insect community composition in the field. Ecol Lett 15:1130–1139

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Wang X, Zu H, Zeng X, Baldwin IT, Lou Y, Li R (2021) Molecular dissection of rice phytohormone signaling involved in resistance to a piercing-sucking herbivore. New Phyto 230:1639–1652

    Article  CAS  Google Scholar 

  • Yao S, Kang J, Guo G, Yang Z, Huang Y, Lan Y, Zhou T, Wang L, Wei C, Xu Z, Li Y (2022) The key micronutrient copper orchestrates broad-spectrum virus resistance in rice. Sci Adv 8:eabm0660

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Luo T, Wang W, Cao T, Li R, Lou Y (2017) Silencing OsSLR1 enhances the resistance of rice to the brown planthopper Nilaparvata lugens. Plant Cell Environ 40:2147–2159

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Liu D, Gao D, Zhao W, Du H, Qiu Z, Huang J, Wen P, Wang Y, Li Q, Wang W, Xu H, He J, Liu Y, Wan J (2022) Cytokinin confers brown planthopper resistance by elevating jasmonic acid pathway in rice. Int J Mol Sci. https://doi.org/10.3390/ijms23115946

  • Zhao T, Liu J, Li HY, Lin JZ, Bian MD, Zhang CY, Zhang YX, Peng YC, Liu B, Lin C (2015) Using hybrid transcription factors to study gene function in rice. Sci China Life Sci 58:1160–1162

    Article  PubMed  Google Scholar 

  • Zhao Y, Huang J, Wang Z, Jing S, Wang Y, Ouyang Y, Cai B, Xin X-F, 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 Y-Q, 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  PubMed Central  Google Scholar 

  • Zhao S, Hong W, Wu J, Wang Y, Ji S, Zhu S, Wei C, Zhang J, Li Y (2017) A viral protein promotes host SAMS1 activity and ethylene production for the benefit of virus infection. Elife. https://doi.org/10.7554/eLife.27529

    Article  PubMed  PubMed Central  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

Funding

This work is supported by the National Natural Science Foundation of China (32101676, U2005208, 31971833), the Natural Science Foundation of Fujian Province, China (2021J05019, 2020J02030, 2021J01075), the Fujian Agriculture and Forestry University Natural Science Funds for Distinguished Young Scholar (xjq21001), Young Talents Special Project of Yunnan Xingdian Talent Support Plan (Grant No. XDYC-QNRC-2022–0717).

Author information

Author notes

  1. Long Lu and Zhongxiang Sun have contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, College of Agriculture, Fujian Agriculture and Forestry University, Fuzhou, 350002, People’s Republic of China

    Long Lu, Zhongxiang Sun, Rumeng Wang, Yifei Du, Zaoli Zhang, Tao Lan, Yuanyuan Song & Rensen Zeng

  2. State Key Laboratory of Conservation and Utilization of Biological Resources of Yunnan, College of Plant Protection, Yunnan Agricultural University, Kunming, 650201, People’s Republic of China

    Zhongxiang Sun

Authors
  1. Long Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhongxiang Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rumeng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yifei Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zaoli Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tao Lan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yuanyuan Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Rensen Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

LL and ZS performed most of the work and initiated the draft. RW, YD, and ZZ helped with some experiments and data analysis. RZ, YS and TL conceived the study, obtained funding, and revised the final version of the manuscript. All authors read and approved the final article.

Corresponding authors

Correspondence to Tao Lan, Yuanyuan Song or Rensen Zeng.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Communicated by Li Tian.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file 1:

Figure S1. Validation of nine DEGs using qRT-PCR. Figure S2. Principal component analysis (PCA) of all detected metabolites in spl10 and ZH11 seedlings at 0 (A), 6 (B), 24 (C), and 48h (D) after BPH infestation (Six biological replicates per treatment). Figure S3. Partial least squares-discriminant analysis (PLS-DA) of all detected metabolites in spl10 and ZH11 seedlings at 0 (A), 6 (B), 24 (C), and 48h (D) after BPH infestation (Six biological replicates per treatment). Figure S4. Metabolomic analysis of spl10 and ZH11 seedlings before and after BPH feeding. Figure S5. HMDB annotation for all DEMs between spl10 and ZH11 seedlings at different timepoints after BPH infestation. Figure S6. KEGG annotation for all DEMs between spl10 and ZH11 seedlings at different timepoints after BPH infestation. Figure S7. Correlation analysis of transcriptomic and metabolomic data from BPH-infested spl10 and ZH11 plants. Figure S8. Limonene showing the repellent role for BPH.

Supplementary file 2:

Table S1. List of DEGs between spl10 and ZH11 plants after BPH infestation.

Supplementary file 3:

Table S2. KEGG enrichment analysis of DEGs between spl10 and ZH11 plants at four timepoints after BPH infestation.

Supplementary file 4:

Table S3. GO enrichment analysis of DEGs between spl10 and ZH11 plants at four timepoints after BPH infestation.

Supplementary file 5:

Table S4. Expression changes of defensive phytohormone-responsive genes in spl10 mutant and ZH11 plants at different timepoints after BPH infestation.

Supplementary file 6:

Table S5. List of differentially expressed transcription factors (TFs) regulated by SPL10.

Supplementary file 7:

Table S6. List of differentially expressed metabolites between spl10 and ZH11 plants after BPH infestation.

Supplementary file 8:

Table S7. List of primers used in this study.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lu, L., Sun, Z., Wang, R. et al. Integration of transcriptome and metabolome analyses reveals the role of OsSPL10 in rice defense against brown planthopper. Plant Cell Rep 42, 2023–2038 (2023). https://doi.org/10.1007/s00299-023-03080-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-023-03080-z

Keywords

Search

Navigation