ThSCSP_12: Novel Effector in <i>Tilletia horrida</i> That Induces Cell Death and Defense Responses in Non-Host Plants
The basidiomycete fungus <i>Tilletia horrida</i> causes rice kernel smut (RKS), a crucial disease afflicting hybrid-rice-growing areas worldwide, which results in significant economic losses. However, few studies have investigated the pathogenic mechanisms and functions of effectors in &...
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MDPI AG
2022-11-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/23/23/14752 |
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| author | Xinyue Shu Desuo Yin Juan Liang Deze Xu Yuqi Jiang Ting Xiang Yuxuan Wang Chunhai Jiao Ping Li Aiping Zheng Aijun Wang |
| author_facet | Xinyue Shu Desuo Yin Juan Liang Deze Xu Yuqi Jiang Ting Xiang Yuxuan Wang Chunhai Jiao Ping Li Aiping Zheng Aijun Wang |
| author_sort | Xinyue Shu |
| collection | DOAJ |
| description | The basidiomycete fungus <i>Tilletia horrida</i> causes rice kernel smut (RKS), a crucial disease afflicting hybrid-rice-growing areas worldwide, which results in significant economic losses. However, few studies have investigated the pathogenic mechanisms and functions of effectors in <i>T. horrida</i>. In this study, we found that the candidate effector ThSCSP_12 caused cell necrosis in the leaves of <i>Nicotiana benthamiana</i>. The predicted signal peptide (SP) of this protein has a secreting function, which is required for ThSCSP_12 to induce cell death. The 1- 189 amino acid (aa) sequences of ThSCSP_12 are sufficient to confer it the ability to trigger cell death in <i>N. benthamiana</i>. The expression of ThSCSP_12 was induced and up-regulated during <i>T. horrida</i> infection. In addition, we also found that ThSCSP_12 localized in both the cytoplasm and nucleus of plant cells and that nuclear localization of this protein is required to induce cell death. Furthermore, the ability of ThSCSP_12 to trigger cell death in <i>N. benthamiana</i> depends on the (RAR1) protein required for Mla12 resistance but not on the suppressor of the G2 allele of Skp1 (SGT1), heat shock protein 90 (HSP90), or somatic embryogenesis receptor-like kinase (SERK3). Crucially, however, ThSCSP_12 induced a defense response in <i>N. benthamiana</i> leaves; yet, the expression of multiple defense-related genes was suppressed in response to heterologous expression in host plants. To sum up, these results strongly suggest that ThSCSP_12 operates as an effector in <i>T. horrida</i>–host interactions. |
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| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-09T17:46:46Z |
| publishDate | 2022-11-01 |
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| series | International Journal of Molecular Sciences |
| spelling | doaj.art-b664f82f8eef4d479eb7fcc1a737f9ae2023-11-24T11:07:26ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-11-0123231475210.3390/ijms232314752ThSCSP_12: Novel Effector in <i>Tilletia horrida</i> That Induces Cell Death and Defense Responses in Non-Host PlantsXinyue Shu0Desuo Yin1Juan Liang2Deze Xu3Yuqi Jiang4Ting Xiang5Yuxuan Wang6Chunhai Jiao7Ping Li8Aiping Zheng9Aijun Wang10College of Agronomy, Sichuan Agricultural University, Chengdu 611130, ChinaFood Crop Research Institute, Hubei Academy of Agriculture Sciences, Wuhan 430064, ChinaCollege of Agronomy, Sichuan Agricultural University, Chengdu 611130, ChinaFood Crop Research Institute, Hubei Academy of Agriculture Sciences, Wuhan 430064, ChinaCollege of Agronomy, Sichuan Agricultural University, Chengdu 611130, ChinaCollege of Agronomy, Sichuan Agricultural University, Chengdu 611130, ChinaCollege of Agronomy, Sichuan Agricultural University, Chengdu 611130, ChinaFood Crop Research Institute, Hubei Academy of Agriculture Sciences, Wuhan 430064, ChinaRice Research Institute, Sichuan Agricultural University, Chengdu 611130, ChinaCollege of Agronomy, Sichuan Agricultural University, Chengdu 611130, ChinaCollege of Agronomy, Sichuan Agricultural University, Chengdu 611130, ChinaThe basidiomycete fungus <i>Tilletia horrida</i> causes rice kernel smut (RKS), a crucial disease afflicting hybrid-rice-growing areas worldwide, which results in significant economic losses. However, few studies have investigated the pathogenic mechanisms and functions of effectors in <i>T. horrida</i>. In this study, we found that the candidate effector ThSCSP_12 caused cell necrosis in the leaves of <i>Nicotiana benthamiana</i>. The predicted signal peptide (SP) of this protein has a secreting function, which is required for ThSCSP_12 to induce cell death. The 1- 189 amino acid (aa) sequences of ThSCSP_12 are sufficient to confer it the ability to trigger cell death in <i>N. benthamiana</i>. The expression of ThSCSP_12 was induced and up-regulated during <i>T. horrida</i> infection. In addition, we also found that ThSCSP_12 localized in both the cytoplasm and nucleus of plant cells and that nuclear localization of this protein is required to induce cell death. Furthermore, the ability of ThSCSP_12 to trigger cell death in <i>N. benthamiana</i> depends on the (RAR1) protein required for Mla12 resistance but not on the suppressor of the G2 allele of Skp1 (SGT1), heat shock protein 90 (HSP90), or somatic embryogenesis receptor-like kinase (SERK3). Crucially, however, ThSCSP_12 induced a defense response in <i>N. benthamiana</i> leaves; yet, the expression of multiple defense-related genes was suppressed in response to heterologous expression in host plants. To sum up, these results strongly suggest that ThSCSP_12 operates as an effector in <i>T. horrida</i>–host interactions.https://www.mdpi.com/1422-0067/23/23/14752rice<i>Tilletia horrida</i>effectordefense responseinteractions |
| spellingShingle | Xinyue Shu Desuo Yin Juan Liang Deze Xu Yuqi Jiang Ting Xiang Yuxuan Wang Chunhai Jiao Ping Li Aiping Zheng Aijun Wang ThSCSP_12: Novel Effector in <i>Tilletia horrida</i> That Induces Cell Death and Defense Responses in Non-Host Plants International Journal of Molecular Sciences rice <i>Tilletia horrida</i> effector defense response interactions |
| title | ThSCSP_12: Novel Effector in <i>Tilletia horrida</i> That Induces Cell Death and Defense Responses in Non-Host Plants |
| title_full | ThSCSP_12: Novel Effector in <i>Tilletia horrida</i> That Induces Cell Death and Defense Responses in Non-Host Plants |
| title_fullStr | ThSCSP_12: Novel Effector in <i>Tilletia horrida</i> That Induces Cell Death and Defense Responses in Non-Host Plants |
| title_full_unstemmed | ThSCSP_12: Novel Effector in <i>Tilletia horrida</i> That Induces Cell Death and Defense Responses in Non-Host Plants |
| title_short | ThSCSP_12: Novel Effector in <i>Tilletia horrida</i> That Induces Cell Death and Defense Responses in Non-Host Plants |
| title_sort | thscsp 12 novel effector in i tilletia horrida i that induces cell death and defense responses in non host plants |
| topic | rice <i>Tilletia horrida</i> effector defense response interactions |
| url | https://www.mdpi.com/1422-0067/23/23/14752 |
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