The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
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Capsicum annuum NAC4 (CaNAC4) Is a Transcription Factor with Roles in Biotic and Abiotic Stresses

  • Guogeng Jia (Department of Applied Biology, Chungnam National University) ;
  • Khaing Shwe Zin Thinn (Department of Applied Biology, Chungnam National University) ;
  • Sun Ha Kim (Department of Applied Biology, Chungnam National University) ;
  • Jiyoung Min (Department of Applied Biology, Chungnam National University) ;
  • Sang-Keun Oh (Department of Applied Biology, Chungnam National University)
  • Received : 2024.07.22
  • Accepted : 2024.08.29
  • Published : 2024.10.01
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Abstract

Transcription factors (TFs) regulate gene expression by binding to DNA. The NAC gene family in plants consists of crucial TFs that influence plant development and stress responses. The whole genome of Capsicum annuum shows over 100 NAC genes (CaNAC). Functional characteristics of the most CaNAC TFs are unknown. In this study, we identified CaNAC4, a novel NAC TF in C. annuum. CaNAC4 expression increased after inoculation with the pathogens, Xanthomonas axonopodis pv. vesicatoria race 3 and X. axonopodis pv. glycines 8ra, and following treatment with the plant hormones, salicylic acid and abscisic acid. We investigated the functional characteristics of the CaNAC4 gene and its roles in salt tolerance and anti-pathogen defense in transgenic Nicotiana benthamiana. For salt stress analysis, the leaf discs of wild-type and CaNAC4-transgenic N. benthamiana plants were exposed to different concentrations of sodium chloride. Chlorophyll loss was more severe in salt stress-treated wild-type plants than in CaNAC4-transgenic plants. To analyze the role of CaNAC4 in anti-pathogen defense, a spore suspension of Botrytis cinerea was used to infect the leaves. The disease caused by B. cinerea gradually increased in severity, and the symptoms were clearer in the CaNAC4-transgenic lines. We also investigated hypersensitive response (HR) in CaNAC4-transgenic plants. The results showed a stronger HR in wild-type plants after infiltration with the apoptosis regulator, BAX. In conclusion, our results suggest that CaNAC4 may enhance salt tolerance and act as a negative regulator of biotic stress in plants.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea (NRF) funded by the MEST (NRF-2017R1D1A1B03035692).

References

  1. Baek, D., Nam, J., Koo, Y. D., Kim, D. H., Lee, J., Jeong, J. C., Kwak, S.-S., Chung, W. S., Lim, C. O., Bahk, J. D., Hong, J. C., Lee, S. Y., Kawai-Yamada, M., Uchimiya, H. and Yun, D.-J. 2004. Bax-induced cell death of Arabidopsis is meditated through reactive oxygen-dependent and -independent processes. Plant Mol. Biol. 56:15-27.
  2. Cerda, R., Avelino, J., Gary, C., Tixier, P., Lechevallier, E. and Allinne, C. 2017. Primary and secondary yield losses caused by pests and diseases: assessment and modeling in coffee. PLoS ONE 12:e0169133.
  3. Cramer, G. R., Urano, K., Delrot, S., Pezzotti, M. and Shinozaki, K. 2011. Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol. 11:163.
  4. Diao, W., Snyder, J. C., Wang, S., Liu, J., Pan, B., Guo, G., Ge, W. and Dawood, M. H. S. A. 2018. Genome-wide analyses of the NAC transcription factor gene family in pepper (Capsicum annuum L.): chromosome location, phylogeny, structure, expression patterns, cis-elements in the promoter, and interaction network. Int. J. Mol Sci. 19:1028.
  5. Erpen, L., Devi, H. S., Grosser, J. W. and Dutt, M. 2018. Potential use of the DREB/ERF, MYB, NAC and WRKY transcription factors to improve abiotic and biotic stress in transgenic plants. Plant Cell Tissue Organ Cult. 132:1-25.
  6. Gong, L., Zhang, H., Liu, X., Gan, X., Nie, F., Yang, W., Zhang, L., Chen, Y., Song, Y. and Zhang, H. 2020. Ectopic expression of HaNAC1, an ATAF transcription factor from Haloxylon ammodendron, improves growth and drought tolerance in transgenic Arabidopsis. Plant Physiol. Biochem. 151:535-544.
  7. Guo, W.-L., Wang, S.-B., Chen, R.-G., Chen, B.-H., Du, X.-H., Yin, Y.-X., Gong, Z.-H. and Zhang, Y.-Y. 2015. Characterization and expression profile of CaNAC2 pepper gene. Front. Plant Sci. 6:755.
  8. Han, D., Du, M., Zhou, Z., Wang, S., Li, T., Han, J., Xu, T. and Yang, G. 2020. An NAC transcription factor gene from Malus baccata, MbNAC29, increases cold and high salinity tolerance in Arabidopsis. In Vitro Cell. Dev. Biol. Plant 56:588-599.
  9. He, X., Zhu, L., Xu, L., Guo, W. and Zhang, X. 2016. GhATAF1, a NAC transcription factor, confers abiotic and biotic stress responses by regulating phytohormonal signaling networks. Plant Cell Rep. 35:2167-2179.
  10. Ju, Y.-L., Min, Z., Yue, X.-F., Zhang, Y.-L., Zhang, J.-X., Zhang, Z.-Q. and Fang, Y.-L. 2020. Overexpression of grapevine VvNAC08 enhances drought tolerance in transgenic Arabidopsis. Plant Physiol. Biochem. 151:214-222.
  11. Kamble, P. N., Giri, S. P., Mane, R. S. and Tiwana, A. 2015. Estimation of chlorophyll content in young and adult leaves of some selected plants. Univers. J. Environ. Res. Technol. 5:306-310.
  12. Kim, S., Park, M., Yeom, S.-I., Kim, Y.-M., Lee, J. M., Lee, H.-A., Seo, E., Choi, J., Cheong, K., Kim, K.-T., Jung, K., Lee, G.-W., Oh, S.-K., Bae, C., Kim, S.-B., Lee, H.-Y., Kim, S.-Y., Kim, M.-S., Kang, B.-C., Jo, Y. D., Yang, H.-B., Jeong, H.-J., Kang, W.-H., Kwon, J.-K., Shin, C., Lim, J. Y., Park, J. H., Huh, J. H., Kim, J.-S., Kim, B.-D., Cohen, O., Paran, I., Suh, M. C., Lee, S. B., Kim, Y.-K., Shin, Y., Noh, S.-J., Park, J., Seo, Y. S., Kwon, S.-Y., Kim, H. A., Park, J. M., Kim, H.-J., Choi, S.-B., Bosland, P. W., Reeves, G., Jo, S.-H., Lee, B.-W., Cho, H.-T., Choi, H.-S., Lee, M.-S., Yu, Y., Choi, Y. D., Park, B.-S., van Deynze, A., Ashrafi, H., Hill, T., Kim, W. T., Pai, H.-S., Ahn, H. K., Yeam, I., Giovannoni, J. J., Rose, J. K. C., Sorensen, I., Lee, S.-J., Kim, R. W., Choi, I.-Y., Choi, B.-S., Lim, J.-S., Lee, Y.-H. and Choi, D. 2014. Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat. Genet. 46:270-278.
  13. Lee, M.-H., Jeon, H. S., Kim, H. G. and Park, O. K. 2017. An Arabidopsis NAC transcription factor NAC4 promotes pathogen-induced cell death under negative regulation by microRNA164. New Phytol. 214:343-360.
  14. Liang, K.-H., Wang, A.-B., Yuan, Y.-H., Miao, Y.-H. and Zhang, L.-Y. 2020. Picea wilsonii NAC transcription factor PwNAC30 negatively regulates abiotic stress tolerance in transgenic Arabidopsis. Plant Mol. Biol. Rep. 38:554-571.
  15. Liu, B., Ouyang, Z., Zhang, Y., Li, X., Hong, Y., Huang, L., Liu, S., Zhang, H., Li, D. and Song, F. 2014. Tomato NAC transcription factor SlSRN1 positively regulates defense response against biotic stress but negatively regulates abiotic stress response. PLoS ONE 9:e102067.
  16. Lu, M., Sun, Q.-P., Zhang, D.-F., Wang, T.-Y. and Pan, J.-B. 2015. Identification of 7 stress-related NAC transcription factor members in maize (Zea mays L.) and characterization of the expression pattern of these genes. Biochem. Biophys. Res. Commun. 462:144-150.
  17. Nuruzzaman, M., Manimekalai, R., Sharoni, A. M., Satoh, K., Kondoh, H., Ooka, H. and Kikuchi, S. 2010. Genome-wide analysis of NAC transcription factor family in rice. Gene 465:30-44.
  18. Nuruzzaman, M., Sharoni, A. M. and Kikuchi, S. 2013. Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front. Microbiol. 4:248.
  19. Oh, S.-K., Baek, K.-H., Park, J. M., Yi, S. Y., Yu, S. H., Kamoun, S. and Choi, D. 2008. Capsicum annuum WRKY protein CaWRKY1 is a negative regulator of pathogen defense. New Phytol. 177:977-989.
  20. Oh, S.-K., Jang, H. A., Lee, S. S., Cho, H. S., Lee, D.-H., Choi, D. and Kwon, S.-Y. 2014. Cucumber Pti1-L is a cytoplasmic protein kinase involved in defense responses and salt tolerance. J. Plant Physiol. 171:817-822.
  21. Oh, S.-K., Lee, S., Yu, S. H. and Choi, D. 2005. Expression of a novel NAC domain-containing transcription factor (CaNAC1) is preferentially associated with incompatible interactions between chili pepper and pathogens. Planta 222:876-887.
  22. Ooka, H., Satoh, K., Doi, K., Nagata, T., Otomo, Y., Murakami, K., Matsubara, K., Osato, N., Kawai, J., Carninci, P., Hayashizaki, Y., Suzuki, K., Kojima, K., Takahara, Y., Yamamoto, K. and Kikuchi, S. 2003. Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res. 10:239-247.
  23. Peng, X., Zhao, Y., Li, X., Wu, M., Chai, W., Sheng, L., Wang, Y., Dong, Q., Jiang, H. and Cheng, B. 2015. Genomewide identification, classification and analysis of NAC type gene family in maize. J. Genet. 94:377-390.
  24. Puranik, S., Sahu, P. P., Srivastava, P. S. and Prasad, M. 2012. NAC proteins: regulation and role in stress tolerance. Trends Plant Sci. 17:369-381.
  25. Qin, C., Yu, C., Shen, Y., Fang, X., Chen, L., Min, J., Cheng, J., Zhao, S., Xu, M., Luo, Y., Yang, Y., Wu, Z., Mao, L., Wu, H., Ling-Hu, C., Zhou, H., Lin, H., Gonzalez-Morales, S., Trejo-Saavedra, D. L., Tian, H., Tang, X., Zhao, M., Huang, Z., Zhou, A., Yao, X., Cui, J., Li, W., Chen, Z., Feng, Y., Niu, Y., Bi, S., Yang, X., Li, W., Cai, H., Luo, X., Montes-Hernandez, S., Leyva-Gonzalez, M. A., Xiong, Z., He, X., Bai, L., Tan, S., Tang, X., Liu, D., Liu, J., Zhang, S., Chen, M., Zhang, L., Zhang, L., Zhang, Y., Liao, W., Zhang, Y., Wang, M., Lv, X., Wen, B., Liu, H., Luan, H., Zhang, Y., Yang, S., Wang, X., Xu, J., Li, X., Li, S., Wang, J., Palloix, A., Bosland, P. W., Li, Y., Krogh, A., Rivera-Bustamante, R. F., Herrera-Estrella, L., Yin, Y., Yu, J., Hu, K. and Zhang, Z. 2014. Whole-genome sequencing of cultivated and wild peppers provides insights into Capsicum domestication and specialization. Proc. Natl. Acad. Sci. U. S. A. 111:5135-5140.
  26. Rushton, P. J., Bokowiec, M. T., Han, S., Zhang, H., Brannock, J. F., Chen, X., Laudeman, T. W. and Timko, M. P. 2008. Tobacco transcription factors: novel insights into transcriptional regulation in the Solanaceae. Plant Physiol. 147:280-295.
  27. Shen, J., Lv, B., Luo, L., He, J., Mao, C., Xi, D. and Ming, F. 2017. The NAC-type transcription factor OsNAC2 regulates ABA-dependent genes and abiotic stress tolerance in rice. Sci. Rep. 7:40641.
  28. Strange, R. N. and Scott, P. R. 2005. Plant disease: a threat to global food security. Annu. Rev. Phytopathol. 43:83-116.
  29. Su, H., Zhang, S., Yin, Y., Zhu, D. and Han, L. 2015. Genome-wide analysis of NAM-ATAF1, 2-CUC2 transcription factor family in Solanum lycopersicum. J. Plant Biochem. Biotechnol. 24:176-183.
  30. Tran, L.-S. P., Nakashima, K., Sakuma, Y., Simpson, S. D., Fujita, Y., Maruyama, K., Fujita, M., Seki, M., Shinozaki, K. and Yamaguchi-Shinozaki, K. 2004. Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16:2481-2498.
  31. Tweneboah, S. and Oh, S.-K. 2017. Biological roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in solanaceous crops. J. Plant Biotechnol. 44:1-11.
  32. Tyagi, H., Jha, S., Sharma, M., Giri, J. and Tyagi, A. K. 2014. Rice SAPs are responsive to multiple biotic stresses and overexpression of OsSAP1, an A20/AN1 zinc-finger protein, enhances the basal resistance against pathogen infection in tobacco. Plant Sci. 225:68-76.
  33. Wang, G., Zhang, S., Ma, X., Wang, Y., Kong, F. and Meng, Q. 2016. A stress-associated NAC transcription factor (SlNAC35) from tomato plays a positive role in biotic and abiotic stresses. Physiol. Plant. 158:45-64.
  34. Wang, N., Zheng, Y., Xin, H., Fang, L. and Li, S. 2013. Comprehensive analysis of NAC domain transcription factor gene family in Vitis vinifera. Plant Cell Rep. 32:61-75.
  35. Wang, X., Basnayake, B. M. V. S., Zhang, H., Li, G., Li, W., Virk, N., Mengiste, T. and Song, F. 2009. The Arabidopsis ATAF1, a NAC transcription factor, is a negative regulator of defense responses against necrotrophic fungal and bacterial pathogens. Mol. Plant-Microbe Interact. 22:1227-1238.
  36. Wang, Y., Cao, S., Guan, C., Kong, X., Wang, Y., Cui, Y., Liu, B., Zhou, Y. and Zhang, Y. 2020. Overexpressing the NAC transcription factor LpNAC13 from Lilium pumilum in tobacco negatively regulates the drought response and positively regulates the salt response. Plant Physiol. Biochem. 149:96-110.
  37. Yan, J., Tong, T., Li, X., Chen, Q., Dai, M., Niu, F., Yang, M., Deyholos, M. K., Yang, B. and Jiang, Y.-Q. 2018. A novel NAC-type transcription factor, NAC87, from oilseed rape modulates reactive oxygen species accumulation and cell death. Plant Cell Physiol. 59:290-303.
  38. Yoon, Y., Seo, D. H., Shin, H., Kim, H. J., Kim, C. M. and Jang, G. 2020. The role of stress-responsive transcription factors in modulating abiotic stress tolerance in plants. Agronomy 10:788.
  39. Zhang, H., Ma, F., Wang, X., Liu, S., Saeed, U. H., Hou, X., Zhang, Y., Luo, D., Meng, Y., Zhang, W., Abid, K. and Chen, R. 2020. Molecular and functional characterization of CaNAC035, an NAC transcription factor from pepper (Capsicum annuum L.). Front. Plant Sci. 11:14.
  40. Zhao, Y., Chen, J., Tao, X., Zheng, X. and Mao, L. 2014. The possible role of BAX and BI-1 genes in chilling-induced cell death in cucumber fruit. Acta Physiol. Plant. 36:1345-1351.