Ammonium Uptake and Assimilation are Required for Rice Defense against Sheath Blight Disease

Abstract

Nitrogen (N) is an important nutrient for plant growth and yield production, and rice grown in paddy soil mainly uses ammonium (NH4+) as its N source. Previous studies have shown that N status is tightly connected to plant defense; however, the roles of NH4+ uptake and assimilation in rice sheath blight disease response have not been studied previously. Here, we analyzed the effects of different N sources on plant defense against Rhizoctonia solani. The results indicated that rice plants grown in N-free conditions had higher resistance to sheath blight than those grown under N conditions. In greater detail, rice plants cultured with glutamine as the sole N source were more susceptible to sheath blight disease compared to the groups using NH4+ and nitrate (NO3) as sole N sources. N deficiency severely inhibited plant growth; therefore, ammonium transporter 1;2 overexpressors (AMT1;2 OXs) were generated to test their growth and defense ability under low N conditions. AMT1;2 OXs increased N use efficiency and exhibited less susceptible symptoms to R. solani and highly induced the expression of PBZ1 compared to the wild-type controls upon infection of R. solani. Furthermore, the glutamine synthetase 1;1 (GS1;1) mutant (gs1;1) was more susceptible to R. solani infection than the wild-type control, and the genetic combination of AMT1;2 OX and gs1;1 revealed that AMT1;2 OX was less susceptible to R. solani and required GS1;1 activity. In addition, cellular NH4+ content was higher in AMT1;2 OX and gs1;1 plants, indicating that NH4+ was not directly controlling plant defense. In conclusion, the present study showed that the activation of NH4+ uptake and assimilation were required for rice resistance against sheath blight disease.

This is a preview of subscription content, access via your institution.

Abbreviations

AMT:

ammonium transporter

Os:

Oryza sativa

GS:

glutamine syn-thetase

N:

nitrogen

R. solani :

Rhizoctonia solani

OX:

overexpression

ORF:

open reading frame

PBZ1 :

Probenazole-inducible gene

References

  1. An, S., Park, S., Jeong, D.H., Lee, D.Y., Kang, H.G., Yu, J.H., Hur, J., Kim, S.R., Kim, Y.H., Lee, M., Han, S., Kim, S.J., Yang, J., Kim, E., Wi, S.J., Chung, H.S., Hong, J.P., Choe, V., Lee, H.K., Choi, J.H., Nam, J., Kim, S.R., Park, P.B., Park, K.Y., Kim, W.T., Choe, S., Lee, C.B., An, G. 2003. Generation and analysis of end sequence database for T-DNA tagging lines in rice. Plant Physiol. 133:2040–2047.

    CAS  Article  Google Scholar 

  2. Bloom, A.J. 1997. Nitrogen as a limiting factor: Crop acquisition of ammonium and nitrate. Ecology in Agriculture. 145–172.

  3. Brady, S.M., Burow, M., Busch, W., Carlborg, O., Denby, K.J., Glazebrook, J., Hamilton, E.S., Harmer, S.L., Haswell, E.S., Maloof, J.N., Springer, N.M., Kliebenstein, D.J. 2015. Reassess the t test: Interact with all Your Data via ANOVA. Plant Cell 27:2088–2094.

    CAS  Article  Google Scholar 

  4. Dou, M., Cheng, S., Zhao, B., Xuan, Y., Shao, M. 2016. The indeterminate domain protein ROC1 regulates chilling tolerance via activation of DREB1B/CBF1 in rice. Int. J. Mol. Sci. 17:233.

    Article  Google Scholar 

  5. Fagard, M., Launay, A., Clement, G., Courtial, J., Dellagi, A., Farjad, M., Krapp, A., Soulie, M.C., Masclaux-Daubresse, C. 2014. Nitrogen metabolism meets phytopathology. J. Exp. Bot. 65:5643–5656.

    CAS  Article  Google Scholar 

  6. Fernandez-Crespo, E., Scalschi, L., Llorens, E., Garcia-Agustin, P., Camanes, G. 2015. NH4+ protects tomato plants against Pseudomonas syringae by activation of systemic acquired acclimation. J. Exp. Bot. 66:6777–6790.

    CAS  Article  Google Scholar 

  7. Fukumorita, T., Chino, M. 1982. Sugar, amino acid and inorganic contents in rice phloem sap. Plant Cell Physiol. 23:273–283.

    CAS  Google Scholar 

  8. Hiei, Y., Ohta, S., Komari, T., Kumashiro, T. 1994. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6:271–282.

    CAS  Article  Google Scholar 

  9. Kadotani, N., Akagi, A., Takatsuji, H., Miwa, T., Igarashi, D. 2016. Exogenous proteinogenic amino acids induce systemic resistance in rice. BMC Plant Biol. 16:60.

    Article  Google Scholar 

  10. Kan, C.C., Chung, T.Y., Wu, H.Y., Juo, Y.A., Hsieh, M.H. 2017. Exogenous glutamate rapidly induces the expression of genes involved in metabolism and defense responses in rice roots. BMC Genomics 18:186.

    Article  Google Scholar 

  11. Koegel, S., Ait Lahmidi, N., Arnould, C., Chatagnier, O., Walder, F., Ineichen, K., Boller, T., Wipf, D., Wiemken, A., Courty, P.E. 2013. The family of ammonium transporters (AMT) in Sorghum bicolor: two AMT members are induced locally, but not systemically in roots colonized by arbuscular mycorrhizal fungi. New Phytol. 198:853–865.

    CAS  Article  Google Scholar 

  12. Liu, G., Ji, Y., Bhuiyan, N.H., Pilot, G., Selvaraj, G., Zou, J., Wei, Y. 2010. Amino acid homeostasis modulates salicylic acid-associated redox status and defense responses in Arabidopsis. Plant Cell. 22:3845–3863.

    CAS  Article  Google Scholar 

  13. Noctor, G., Foyer, C.H. 1998. A re-evaluation of the ATP: NADPH budget during C3 photosynthesis: a contribution from nitrate assimilation and its associated respiratory activity? J. Exp. Bot. 49:1895–1908.

    CAS  Google Scholar 

  14. Oliveira, I.C., Brears, T., Knight, T.J., Clark, A., Coruzzi, G.M. 2002. Overexpression of cytosolic glutamine synthetase. Relation to nitrogen, light, and photorespiration. Plant Physiol. 129:1170–1180.

    CAS  Article  Google Scholar 

  15. Pastor, V., Gamir, J., Camanes, G., Cerezo, M., Sanchez-Bel, P., Flors, V. 2014. Disruption of the ammonium transporter AMT1.1 alters basal defenses generating resistance against Pseudomonas syringae and Plectosphaerella cucumerina. Front. Plant Sci. 5:231.

    PubMed  PubMed Central  Google Scholar 

  16. Patterson, K., Cakmak, T., Cooper, A., Lager, I., Rasmusson, A.G., Escobar, M.A. 2010. Distinct signalling pathways and transcriptome response signatures differentiate ammonium and nitrate supplied plants. Plant Cell Eviron. 33:1486–1501.

    CAS  Google Scholar 

  17. Prasad, B., Eizenga, G.C. 2008. Rice sheath blight disease resistance identified in Oryza spp. Plant Dis. 92:1503–1509.

    CAS  Article  Google Scholar 

  18. Ranathunge, K., El-Kereamy, A., Gidda, S., Bi, Y.M., Rothstein, S.J. 2014. AMT1;1 transgenic rice plants with enhanced NH4(+) permeability show superior growth and higher yield under optimal and suboptimal NH4(+) conditions. J. Exp. Bot. 65:965–79.

    CAS  Article  Google Scholar 

  19. Savary, S., Castilla, N.P., Elazegui, F.A., McLaren, C.G., Ynalvez, M.A., Teng, P.S. 1995. Direct and indirect effects of nitrogen supply and disease source structure on rice sheath blight spread. Phytopathology. 85:959–965.

    Article  Google Scholar 

  20. Savary, S., Willocquet, L., Elazegui, F.A., Castilla, N.P., Teng, P.S. 2000. Rice pest constraints in tropical Asia: quantification of yield losses due to rice pests in a range of production situations. Plant Dis. 84.

  21. Scheideler, M., Schlaich, N.L., Fellenberg, K., Beissbarth, T., Hauser, N.C., Vingron, M., Slusarenko, A.J., Hoheisel, J.D. 2002. Monitoring the switch from housekeeping to pathogen defense metabolism in Arabidopsis thaliana using cDNA arrays. J. Biol. Chem. 277:10555–10561.

    CAS  Article  Google Scholar 

  22. Tabuchi, M., Sugiyama, K., Ishiyama, K., Inoue, E., Sato, T., Takahashi, H., Yamaya, T. 2005. Severe reduction in growth rate and grain filling of rice mutants lacking OsGS1;1, a cytosolic glutamine synthetase1;1. Plant J. 42:641–651.

    CAS  Article  Google Scholar 

  23. Ward, J.L., Forcat, S., Beckmann, M., Bennett, M., Miller, S.J., Baker, J.M., Hawkins, N.D., Vermeer, C.P., Lu, C., Lin, W., Truman, W.M., Beale, M.H., Draper, J., Mansfield, J.W., Grant, M. 2010. The metabolic transition during disease following infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato. Plant J. 63:443–457.

    CAS  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding authors

Correspondence to C. Zhang or Y. H. Wu or Y. J. Bai.

Additional information

Communicated by J. Zhang

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Chi, W.J., Wang, Z.Y., Liu, J.M. et al. Ammonium Uptake and Assimilation are Required for Rice Defense against Sheath Blight Disease. CEREAL RESEARCH COMMUNICATIONS 47, 98–110 (2019). https://doi.org/10.1556/0806.46.2018.056

Download citation

Keywords

  • AMT
  • assimilation
  • sheath blight
  • defense
  • GS1;1
  • rice