Evolution, gene expression, and protein‒protein interaction analyses identify candidate CBL-CIPK signalling networks implicated in stress responses to cold and bacterial infection in citrus
Abstract Background Cold is a major abiotic stress and Huanglongbing and citrus canker disease are two devastating bacterial diseases for citrus. The Ca2+-CBL-CIPK network is known to regulate different types of stress signalling in plants. How do CBL–CIPK signalling networks function in response to...
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| Format: | Article |
| Language: | English |
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BMC
2022-09-01
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| Series: | BMC Plant Biology |
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| Online Access: | https://doi.org/10.1186/s12870-022-03809-0 |
| _version_ | 1811297523022692352 |
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| author | Cui Xiao Hu Zhang Fan Xie Zhi-Yong Pan Wen-Ming Qiu Zhu Tong Ze-Qiong Wang Xiu-Juan He Yu-Hai Xu Zhong-Hai Sun |
| author_facet | Cui Xiao Hu Zhang Fan Xie Zhi-Yong Pan Wen-Ming Qiu Zhu Tong Ze-Qiong Wang Xiu-Juan He Yu-Hai Xu Zhong-Hai Sun |
| author_sort | Cui Xiao |
| collection | DOAJ |
| description | Abstract Background Cold is a major abiotic stress and Huanglongbing and citrus canker disease are two devastating bacterial diseases for citrus. The Ca2+-CBL-CIPK network is known to regulate different types of stress signalling in plants. How do CBL–CIPK signalling networks function in response to cold and infection by CLas or Xcc in citrus? Results Eight calcineurin B-like proteins (CBLs) and seventeen CBL-interacting protein kinases (CIPKs) were identified from the cold-tolerant satsuma mandarin ‘Guijing2501’ (Citrus. unshiu) and CLas/Xcc-sensitive sweet orange (C. sinensis). Phylogenetic analysis revealed that both CBL and CIPK family members in citrus were classified into an ancient and a recent clade according to their conserved domain characteristics and/or intron/exon structures. Genome duplication analysis suggested that both tandem and segmental duplications contributed to the amplification of the CBL and CIPK gene families in citrus under intense purifying selection, and the duplication events only existed in the recent clades. Expression comparison of the duplicated gene pairs indicated that the duplicated CBL and CIPK genes underwent functional differentiation. Further expression analysis identified that CBL1, 5, 6, and 8 and CIPK2, 8, 12, 15, 16, and 17 were significantly regulated by multiple stresses, including cold, Xcc infection and/or CLas infection, in citrus, whereas CBL2/7 and CIPK1/4/5/11/13/14 were independently highly regulated by cold and CIPK3 was uniquely responsive to Xcc infection. The combination analyses of targeted Y2H assay and expression analysis revealed that CBL6-CIPK8 was the common signalling network in response to cold and Xcc infection, while CBL6/CBL8-CIPK14 was uniquely responsive to cold in citrus. Further stable transformation and cold tolerance assay indicated that overexpression of CuCIPK16 enhanced the cold tolerance of transgenic Arabidopsis with higher POD activity and lower MDA content. Conclusions In this study, evolution, gene expression and protein‒protein interaction analyses of citrus CBLs and CIPKs were comprehensively conducted over a genome-wide range. The results will facilitate future functional characterization of individual citrus CBLs and CIPKs under specific stresses and provide clues for the clarification of cold tolerance and disease susceptibility mechanisms in corresponding citrus cultivars. |
| first_indexed | 2024-04-13T06:05:38Z |
| format | Article |
| id | doaj.art-edc4cf1bfa8147a1a953d968680f3c3e |
| institution | Directory Open Access Journal |
| issn | 1471-2229 |
| language | English |
| last_indexed | 2024-04-13T06:05:38Z |
| publishDate | 2022-09-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Plant Biology |
| spelling | doaj.art-edc4cf1bfa8147a1a953d968680f3c3e2022-12-22T02:59:16ZengBMCBMC Plant Biology1471-22292022-09-0122111710.1186/s12870-022-03809-0Evolution, gene expression, and protein‒protein interaction analyses identify candidate CBL-CIPK signalling networks implicated in stress responses to cold and bacterial infection in citrusCui Xiao0Hu Zhang1Fan Xie2Zhi-Yong Pan3Wen-Ming Qiu4Zhu Tong5Ze-Qiong Wang6Xiu-Juan He7Yu-Hai Xu8Zhong-Hai Sun9Fruit and Tea Research Institute, Hubei Academy of Agricultural SciencesFruit and Tea Research Institute, Hubei Academy of Agricultural SciencesFruit and Tea Research Institute, Hubei Academy of Agricultural SciencesKey Laboratory of Horticultural Plant Biology (Ministry of Education), Huazhong Agricultural UniversityFruit and Tea Research Institute, Hubei Academy of Agricultural SciencesFruit and Tea Research Institute, Hubei Academy of Agricultural SciencesFruit and Tea Research Institute, Hubei Academy of Agricultural SciencesFruit and Tea Research Institute, Hubei Academy of Agricultural SciencesFruit and Tea Research Institute, Hubei Academy of Agricultural SciencesFruit and Tea Research Institute, Hubei Academy of Agricultural SciencesAbstract Background Cold is a major abiotic stress and Huanglongbing and citrus canker disease are two devastating bacterial diseases for citrus. The Ca2+-CBL-CIPK network is known to regulate different types of stress signalling in plants. How do CBL–CIPK signalling networks function in response to cold and infection by CLas or Xcc in citrus? Results Eight calcineurin B-like proteins (CBLs) and seventeen CBL-interacting protein kinases (CIPKs) were identified from the cold-tolerant satsuma mandarin ‘Guijing2501’ (Citrus. unshiu) and CLas/Xcc-sensitive sweet orange (C. sinensis). Phylogenetic analysis revealed that both CBL and CIPK family members in citrus were classified into an ancient and a recent clade according to their conserved domain characteristics and/or intron/exon structures. Genome duplication analysis suggested that both tandem and segmental duplications contributed to the amplification of the CBL and CIPK gene families in citrus under intense purifying selection, and the duplication events only existed in the recent clades. Expression comparison of the duplicated gene pairs indicated that the duplicated CBL and CIPK genes underwent functional differentiation. Further expression analysis identified that CBL1, 5, 6, and 8 and CIPK2, 8, 12, 15, 16, and 17 were significantly regulated by multiple stresses, including cold, Xcc infection and/or CLas infection, in citrus, whereas CBL2/7 and CIPK1/4/5/11/13/14 were independently highly regulated by cold and CIPK3 was uniquely responsive to Xcc infection. The combination analyses of targeted Y2H assay and expression analysis revealed that CBL6-CIPK8 was the common signalling network in response to cold and Xcc infection, while CBL6/CBL8-CIPK14 was uniquely responsive to cold in citrus. Further stable transformation and cold tolerance assay indicated that overexpression of CuCIPK16 enhanced the cold tolerance of transgenic Arabidopsis with higher POD activity and lower MDA content. Conclusions In this study, evolution, gene expression and protein‒protein interaction analyses of citrus CBLs and CIPKs were comprehensively conducted over a genome-wide range. The results will facilitate future functional characterization of individual citrus CBLs and CIPKs under specific stresses and provide clues for the clarification of cold tolerance and disease susceptibility mechanisms in corresponding citrus cultivars.https://doi.org/10.1186/s12870-022-03809-0CitrusCBL-CIPK interactionEvolutionExpression patternAbiotic and biotic stresses |
| spellingShingle | Cui Xiao Hu Zhang Fan Xie Zhi-Yong Pan Wen-Ming Qiu Zhu Tong Ze-Qiong Wang Xiu-Juan He Yu-Hai Xu Zhong-Hai Sun Evolution, gene expression, and protein‒protein interaction analyses identify candidate CBL-CIPK signalling networks implicated in stress responses to cold and bacterial infection in citrus BMC Plant Biology Citrus CBL-CIPK interaction Evolution Expression pattern Abiotic and biotic stresses |
| title | Evolution, gene expression, and protein‒protein interaction analyses identify candidate CBL-CIPK signalling networks implicated in stress responses to cold and bacterial infection in citrus |
| title_full | Evolution, gene expression, and protein‒protein interaction analyses identify candidate CBL-CIPK signalling networks implicated in stress responses to cold and bacterial infection in citrus |
| title_fullStr | Evolution, gene expression, and protein‒protein interaction analyses identify candidate CBL-CIPK signalling networks implicated in stress responses to cold and bacterial infection in citrus |
| title_full_unstemmed | Evolution, gene expression, and protein‒protein interaction analyses identify candidate CBL-CIPK signalling networks implicated in stress responses to cold and bacterial infection in citrus |
| title_short | Evolution, gene expression, and protein‒protein interaction analyses identify candidate CBL-CIPK signalling networks implicated in stress responses to cold and bacterial infection in citrus |
| title_sort | evolution gene expression and protein protein interaction analyses identify candidate cbl cipk signalling networks implicated in stress responses to cold and bacterial infection in citrus |
| topic | Citrus CBL-CIPK interaction Evolution Expression pattern Abiotic and biotic stresses |
| url | https://doi.org/10.1186/s12870-022-03809-0 |
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