Dual Roles of GSNOR1 in Cell Death and Immunity in Tetraploid Nicotiana tabacum
S-nitrosoglutathione reductase 1 (GSNOR1) is the key enzyme that regulates cellular homeostasis of S-nitrosylation. Although extensively studied in Arabidopsis, the roles of GSNOR1 in tetraploid Nicotiana species have not been investigated previously. To study the function of NtGSNOR1, we knocked ou...
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Frontiers Media S.A.
2021-02-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2021.596234/full |
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| author | Zhen-Chao Li Qian-Wei Ren Yan Guo Jie Ran Xiao-Tian Ren Ni-Ni Wu Hui-Yang Xu Xia Liu Xia Liu Jian-Zhong Liu Jian-Zhong Liu |
| author_facet | Zhen-Chao Li Qian-Wei Ren Yan Guo Jie Ran Xiao-Tian Ren Ni-Ni Wu Hui-Yang Xu Xia Liu Xia Liu Jian-Zhong Liu Jian-Zhong Liu |
| author_sort | Zhen-Chao Li |
| collection | DOAJ |
| description | S-nitrosoglutathione reductase 1 (GSNOR1) is the key enzyme that regulates cellular homeostasis of S-nitrosylation. Although extensively studied in Arabidopsis, the roles of GSNOR1 in tetraploid Nicotiana species have not been investigated previously. To study the function of NtGSNOR1, we knocked out two NtGSNOR1 genes simultaneously in Nicotiana tabacum using clustered regularly interspaced short palindromic repeats (CRISPR)/caspase 9 (Cas9) technology. To our surprise, spontaneous cell death occurred on the leaves of the CRISPR/Cas9 lines but not on those of the wild-type (WT) plants, suggesting that NtGSNOR1 negatively regulates cell death. The natural cell death on the CRISPR/Cas9 lines could be a result from interactions between overaccumulated nitric oxide (NO) and hydrogen peroxide (H2O2). This spontaneous cell death phenotype was not affected by knocking out two Enhanced disease susceptibility 1 genes (NtEDS11a/1b) and thus was independent of the salicylic acid (SA) pathway. Unexpectedly, we found that the NtGSNOR1a/1b knockout plants displayed a significantly (p < 0.001) enhanced resistance to paraquat-induced cell death compared to WT plants, suggesting that NtGSNOR1 functions as a positive regulator of the paraquat-induced cell death. The increased resistance to the paraquat-induced cell death of the NtGSNOR1a/1b knockout plants was correlated with the reduced level of H2O2 accumulation. Interestingly, whereas the N gene-mediated resistance to Tobacco mosaic virus (TMV) was significantly enhanced (p < 0.001), the resistance to Pseudomonas syringae pv. tomato DC3000 was significantly reduced (p < 0.01) in the NtGSNOR1a/1b knockout lines. In summary, our results indicate that NtGSNOR1 functions as both positive and negative regulator of cell death under different conditions and displays distinct effects on resistance against viral and bacterial pathogens. |
| first_indexed | 2024-12-13T23:24:08Z |
| format | Article |
| id | doaj.art-528acf03edde414494e0e72e8da2a158 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-13T23:24:08Z |
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| series | Frontiers in Plant Science |
| spelling | doaj.art-528acf03edde414494e0e72e8da2a1582022-12-21T23:27:35ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-02-011210.3389/fpls.2021.596234596234Dual Roles of GSNOR1 in Cell Death and Immunity in Tetraploid Nicotiana tabacumZhen-Chao Li0Qian-Wei Ren1Yan Guo2Jie Ran3Xiao-Tian Ren4Ni-Ni Wu5Hui-Yang Xu6Xia Liu7Xia Liu8Jian-Zhong Liu9Jian-Zhong Liu10College of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua, ChinaCollege of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua, ChinaCollege of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua, ChinaCollege of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua, ChinaCollege of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua, ChinaCollege of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua, ChinaCollege of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua, ChinaCollege of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua, ChinaZhejiang Provincial Key Laboratory of Biotechnology on Specialty Economic Plants, Zhejiang Normal University, Jinhua, ChinaCollege of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua, ChinaZhejiang Provincial Key Laboratory of Biotechnology on Specialty Economic Plants, Zhejiang Normal University, Jinhua, ChinaS-nitrosoglutathione reductase 1 (GSNOR1) is the key enzyme that regulates cellular homeostasis of S-nitrosylation. Although extensively studied in Arabidopsis, the roles of GSNOR1 in tetraploid Nicotiana species have not been investigated previously. To study the function of NtGSNOR1, we knocked out two NtGSNOR1 genes simultaneously in Nicotiana tabacum using clustered regularly interspaced short palindromic repeats (CRISPR)/caspase 9 (Cas9) technology. To our surprise, spontaneous cell death occurred on the leaves of the CRISPR/Cas9 lines but not on those of the wild-type (WT) plants, suggesting that NtGSNOR1 negatively regulates cell death. The natural cell death on the CRISPR/Cas9 lines could be a result from interactions between overaccumulated nitric oxide (NO) and hydrogen peroxide (H2O2). This spontaneous cell death phenotype was not affected by knocking out two Enhanced disease susceptibility 1 genes (NtEDS11a/1b) and thus was independent of the salicylic acid (SA) pathway. Unexpectedly, we found that the NtGSNOR1a/1b knockout plants displayed a significantly (p < 0.001) enhanced resistance to paraquat-induced cell death compared to WT plants, suggesting that NtGSNOR1 functions as a positive regulator of the paraquat-induced cell death. The increased resistance to the paraquat-induced cell death of the NtGSNOR1a/1b knockout plants was correlated with the reduced level of H2O2 accumulation. Interestingly, whereas the N gene-mediated resistance to Tobacco mosaic virus (TMV) was significantly enhanced (p < 0.001), the resistance to Pseudomonas syringae pv. tomato DC3000 was significantly reduced (p < 0.01) in the NtGSNOR1a/1b knockout lines. In summary, our results indicate that NtGSNOR1 functions as both positive and negative regulator of cell death under different conditions and displays distinct effects on resistance against viral and bacterial pathogens.https://www.frontiersin.org/articles/10.3389/fpls.2021.596234/fullcell deathdisease resistancenitric oxidehypersensitive responsesreactive oxygen speciesS-nitrosoglutathione reductase |
| spellingShingle | Zhen-Chao Li Qian-Wei Ren Yan Guo Jie Ran Xiao-Tian Ren Ni-Ni Wu Hui-Yang Xu Xia Liu Xia Liu Jian-Zhong Liu Jian-Zhong Liu Dual Roles of GSNOR1 in Cell Death and Immunity in Tetraploid Nicotiana tabacum Frontiers in Plant Science cell death disease resistance nitric oxide hypersensitive responses reactive oxygen species S-nitrosoglutathione reductase |
| title | Dual Roles of GSNOR1 in Cell Death and Immunity in Tetraploid Nicotiana tabacum |
| title_full | Dual Roles of GSNOR1 in Cell Death and Immunity in Tetraploid Nicotiana tabacum |
| title_fullStr | Dual Roles of GSNOR1 in Cell Death and Immunity in Tetraploid Nicotiana tabacum |
| title_full_unstemmed | Dual Roles of GSNOR1 in Cell Death and Immunity in Tetraploid Nicotiana tabacum |
| title_short | Dual Roles of GSNOR1 in Cell Death and Immunity in Tetraploid Nicotiana tabacum |
| title_sort | dual roles of gsnor1 in cell death and immunity in tetraploid nicotiana tabacum |
| topic | cell death disease resistance nitric oxide hypersensitive responses reactive oxygen species S-nitrosoglutathione reductase |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2021.596234/full |
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