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. 2020 Jan 7;117(1):271-277.
doi: 10.1073/pnas.1902771116. Epub 2019 Dec 17.

An R2R3 MYB transcription factor confers brown planthopper resistance by regulating the phenylalanine ammonia-lyase pathway in rice

Jun He  1 , Yuqiang Liu  1 , Dingyang Yuan  2 , Meijuan Duan  3 , Yanling Liu  1 , Zijie Shen  1 , Chunyan Yang  1 , Zeyu Qiu  1 , Daoming Liu  1 , Peizheng Wen  1 , Jie Huang  1 , Dejia Fan  1 , Shizhuo Xiao  1 , Yeyun Xin  2 , Xianian Chen  1 , Ling Jiang  1 , Haiyang Wang  4 , Longping Yuan  5 , Jianmin Wan  6   4
Affiliations

An R2R3 MYB transcription factor confers brown planthopper resistance by regulating the phenylalanine ammonia-lyase pathway in rice

Jun He et al. Proc Natl Acad Sci U S A. .

Abstract

Brown planthopper (BPH) is one of the most destructive insects affecting rice (Oryza sativa L.) production. Phenylalanine ammonia-lyase (PAL) is a key enzyme involved in plant defense against pathogens, but the role of PAL in insect resistance is still poorly understood. Here we show that expression of the majority of PALs in rice is significantly induced by BPH feeding. Knockdown of OsPALs significantly reduces BPH resistance, whereas overexpression of OsPAL8 in a susceptible rice cultivar significantly enhances its BPH resistance. We found that OsPALs mediate resistance to BPH by regulating the biosynthesis and accumulation of salicylic acid and lignin. Furthermore, we show that expression of OsPAL6 and OsPAL8 in response to BPH attack is directly up-regulated by OsMYB30, an R2R3 MYB transcription factor. Taken together, our results demonstrate that the phenylpropanoid pathway plays an important role in BPH resistance response, and provide valuable targets for genetic improvement of BPH resistance in rice.

Keywords: brown planthopper; lignin; phenylalanine ammonia-lyase; rice; salicylic acid.

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Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.
Fig. 1.
Altered expression of PALs significantly impacts BPH resistance. (A) qRT-PCR analysis of OsPAL expression in the RNAi knockdown transgenic lines. The expression values are presented relative to those in the background parent IR64. (B) The activity of OsPALs in IR64 and OsPAL knockdown lines. (C) Seedlings of IR64 and OsPAL knockdown plants not infested with BPH. (Scale bar, 10 cm.) (D) Representative image of IR64 and OsPAL knockdown plants 7 d after infestation (dpi) with BPH. (Scale bar, 10 cm.) (E) Seedling mortality rate of IR64 and OsPAL knockdown lines infested with BPH. Data were collected at 7 dpi. (F) qRT-PCR analysis of OsPAL8 expression in the transgenic lines overexpressing OsPAL8. Expression level of OsPAL8 in the background parent 02428 was set as 1. (G) Representative image of 02428 and plants overexpressing OsPAL8 infested with BPH at 7 dpi. (Scale bar, 10 cm.) (H) Seedling mortality rate of 02428 and plants overexpressing OsPAL8 infested with BPH. Data were collected 7 dpi. Values are means ± SD of 3 biological replicates, by Student’s t test (B, E, F, and H, **P < 0.01).
Fig. 2.
Fig. 2.
Lignin accumulation is associated with BPH resistance in rice. (A) Histochemical staining showing lignin accumulation in fresh leaf sheaths of IR64 and the OsPAL knockdown plants. (Scale bars, 50 μm.) (B) Lignin contents of IR64 and the OsPAL knockdown plants measured using the acetyl bromide method. (C) Histochemical staining showing lignin accumulation in fresh leaf sheaths of WT (02428) and the transgenic plants overexpressing OsPAL8. (Scale bars, 50 μm.) (D) Quantification of lignin content in fresh leaf sheaths of WT and plants overexpressing OsPAL8. (E) Histochemical staining showing lignin accumulation in fresh leaf sheaths of wild-type (WT) and lr-1 plants. (Scale bars, 50 μm.) (F) Quantification of lignin content in fresh leaf sheaths of WT and lr-1 plants. (G) Representative image of WT and lr-1 plants infested with BPH. (Scale bar, 10 cm.) (H) Seedling mortality rates of WT and lr-1 plants infested with BPH at 7 dpi. Values are means ± SD of 3 biological replicates (B, D, F, and H). *P < 0.05, **P < 0.01 in comparison with background parent or WT plant (Student’s t test).
Fig. 3.
Fig. 3.
OsPAL-mediated BPH resistance is associated with SA levels. SA level in the OsPAL knockdown lines (A) or plants overexpressing OsPAL8 (B). Error bars, mean ± SD of 3 biological replicates. *P < 0.05, **P < 0.01 in comparison with background parent (Student’s t-test). Representative image (C) and seedling mortality rate (D) of NahG#1 transgenic plants infested with BPH for 5 d after pretreatment with SA, BTH, Mock, and the background parent Nipponbare (NIP), respectively. (Scale bar, 10 cm.) Error bars, mean ± SD of 3 biological replicates. Different letters on the histograms indicate statistically significant differences at P < 0.05 estimated by one-way ANOVA. (E) Representative image and (F) mortality rates of the OsPAL knockdown lines infested with BPH for 7 d after pretreatment with SA, BTH, and Mock, respectively. (Scale bar, 10 cm.) Error bars, mean ± SD of at least 3 biological replicates. *P < 0.05, **P < 0.01 in comparison with IR64 (Student’s t-test).
Fig. 4.
Fig. 4.
OsPALs-mediated BPH resistance is regulated by OsMYB30. (A) Representative image of Osmyb30 mutants infested with BPH for 5 d. (Scale bars, 1 cm.) (B) Seedling mortality rates of WT and Osmyb30 mutants infested with BPH. Data were collected at 7 dpi. (C) Verification of the T-DNA insertion in the Osmyb30 mutant. The positions of the F, R, and TF primers are indicated as red arrows. (D) SA levels in WT and the Osmyb30 mutant plants. (E) Histochemical staining showing lignin accumulation in fresh leaf sheaths of WT and the Osmyb30 mutant plants. (Scale bar, 50 μm.) (F) qRT-PCR analysis of OsPAL6 and OsPAL8 expression in the Osmyb30 mutant. The expression values are presented relative to those in WT without BPH infestation. Error bars, mean ± SD of 3 biological replicates, by Student’s t-test (B and D, **P < 0.01).
Fig. 5.
Fig. 5.
OsMYB30 binds to the AC-like elements in the promoters of OsPAL6 and OsPAL8. (A) Coexpression of OsMYB30 with LUC driven by the OsPAL6 or OsPAL8 promoters in rice leaf protoplasts. Error bars, mean ± SD of 3 biological replicates. **P < 0.01 by Student’s t-test. (B) Evaluation of the binding of OsMYB30 to the AC6-I and AC8-I elements in the promoter of OsPAL6 and OsPAL8, using the Biacore T200 instrument. Error bars, mean ± SD of 3 biological replicates. (C) EMSA assay showing the binding of OsMYB30 to the AC6-I and AC8-I elements in the promoters of OsPAL6 and OsPAL8. Error bars, mean ± SD of 3 biological replicates.
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