A novel TF molecular switch-mechanism found in two contrasting ecotypes of a psammophyte, Agriophyllum squarrosum, in regulating transcriptional drought memory
Abstract Background Prior drought stress may change plants response patterns and subsequently increase their tolerance to the same condition, which can be referred to as “drought memory” and proved essential for plants well-being. However, the mechanism of transcriptional drought memory in psammophy...
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| Format: | Article |
| Language: | English |
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BMC
2023-03-01
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| Series: | BMC Plant Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12870-023-04154-6 |
| _version_ | 1797853940676558848 |
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| author | Tingzhou Fang Chaoju Qian Bachir Goudia Daoura Xia Yan Xingke Fan Pengshu Zhao Yuqiu Liao Liang Shi Yuxiao Chang Xiao-Fei Ma |
| author_facet | Tingzhou Fang Chaoju Qian Bachir Goudia Daoura Xia Yan Xingke Fan Pengshu Zhao Yuqiu Liao Liang Shi Yuxiao Chang Xiao-Fei Ma |
| author_sort | Tingzhou Fang |
| collection | DOAJ |
| description | Abstract Background Prior drought stress may change plants response patterns and subsequently increase their tolerance to the same condition, which can be referred to as “drought memory” and proved essential for plants well-being. However, the mechanism of transcriptional drought memory in psammophytes remains unclear. Agriophyllum squarrosum, a pioneer species on mobile dunes, is widely spread in Northern China’s vast desert areas with outstanding ability of water use efficiency. Here we conducted dehydration-rehydration treatment on A. squarrosum semi-arid land ecotype AEX and arid land ecotype WW to dissect the drought memory mechanism of A. squarrosum, and to determine the discrepancy in drought memory of two contrasting ecotypes that had long adapted to water heterogeneity. Result Physiological traits monitoring unveiled the stronger ability and longer duration in drought memory of WW than that of AEX. A total of 1,642 and 1,339 drought memory genes (DMGs) were identified in ecotype AEX and WW, respectively. Furthermore, shared DMGs among A. squarrosum and the previously studied species depicted that drought memory commonalities in higher plants embraced pathways like primary and secondary metabolisms; while drought memory characteristics in A. squarrosum were mainly related to response to heat, high light intensity, hydrogen peroxide, and dehydration, which might be due to local adaptation to desert circumstances. Heat shock proteins (HSPs) occupied the center of the protein-protein interaction (PPI) network in drought memory transcription factors (TF), thus playing a key regulatory role in A. squarrosum drought memory. Co-expression analysis of drought memory TFs and DMGs uncovered a novel regulating module, whereby pairs of TFs might function as molecular switches in regulating DMG transforming between high and low expression levels, thus promoting drought memory reset. Conclusion Based on the co-expression analysis, protein-protein interaction prediction, and drought memory metabolic network construction, a novel regulatory module of transcriptional drought memory in A. squarrosum was hypothesized here, whereby recurrent drought signal is activated by primary TF switches, then amplified by secondary amplifiers, and thus regulates downstream complicated metabolic networks. The present research provided valuable molecular resources on plants’ stress-resistance basis and shed light on drought memory in A. squarrosum. |
| first_indexed | 2024-04-09T19:57:51Z |
| format | Article |
| id | doaj.art-b8c63aa396d743eca07315d7658d704b |
| institution | Directory Open Access Journal |
| issn | 1471-2229 |
| language | English |
| last_indexed | 2024-04-09T19:57:51Z |
| publishDate | 2023-03-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Plant Biology |
| spelling | doaj.art-b8c63aa396d743eca07315d7658d704b2023-04-03T05:21:59ZengBMCBMC Plant Biology1471-22292023-03-0123111810.1186/s12870-023-04154-6A novel TF molecular switch-mechanism found in two contrasting ecotypes of a psammophyte, Agriophyllum squarrosum, in regulating transcriptional drought memoryTingzhou Fang0Chaoju Qian1Bachir Goudia Daoura2Xia Yan3Xingke Fan4Pengshu Zhao5Yuqiu Liao6Liang Shi7Yuxiao Chang8Xiao-Fei Ma9Key Laboratory of Ecological Safety and Sustainable Development in Arid Lands, Northwest Institute of Eco-Environment and Resources, Chinese Academy of SciencesKey Laboratory of Ecological Safety and Sustainable Development in Arid Lands, Northwest Institute of Eco-Environment and Resources, Chinese Academy of SciencesDepartment of Biology, Faculty of Sciences and Technology, Dan Dicko Dankoulodo UniversityKey Laboratory of Eco-hydrology of Inland River Basin, Northwest Institute of Eco- Environment and Resources, Chinese Academy of SciencesKey Laboratory of Ecological Safety and Sustainable Development in Arid Lands, Northwest Institute of Eco-Environment and Resources, Chinese Academy of SciencesKey Laboratory of Ecological Safety and Sustainable Development in Arid Lands, Northwest Institute of Eco-Environment and Resources, Chinese Academy of SciencesKey Laboratory of Ecological Safety and Sustainable Development in Arid Lands, Northwest Institute of Eco-Environment and Resources, Chinese Academy of SciencesKey Laboratory of Ecological Safety and Sustainable Development in Arid Lands, Northwest Institute of Eco-Environment and Resources, Chinese Academy of SciencesAgricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural ScienceKey Laboratory of Ecological Safety and Sustainable Development in Arid Lands, Northwest Institute of Eco-Environment and Resources, Chinese Academy of SciencesAbstract Background Prior drought stress may change plants response patterns and subsequently increase their tolerance to the same condition, which can be referred to as “drought memory” and proved essential for plants well-being. However, the mechanism of transcriptional drought memory in psammophytes remains unclear. Agriophyllum squarrosum, a pioneer species on mobile dunes, is widely spread in Northern China’s vast desert areas with outstanding ability of water use efficiency. Here we conducted dehydration-rehydration treatment on A. squarrosum semi-arid land ecotype AEX and arid land ecotype WW to dissect the drought memory mechanism of A. squarrosum, and to determine the discrepancy in drought memory of two contrasting ecotypes that had long adapted to water heterogeneity. Result Physiological traits monitoring unveiled the stronger ability and longer duration in drought memory of WW than that of AEX. A total of 1,642 and 1,339 drought memory genes (DMGs) were identified in ecotype AEX and WW, respectively. Furthermore, shared DMGs among A. squarrosum and the previously studied species depicted that drought memory commonalities in higher plants embraced pathways like primary and secondary metabolisms; while drought memory characteristics in A. squarrosum were mainly related to response to heat, high light intensity, hydrogen peroxide, and dehydration, which might be due to local adaptation to desert circumstances. Heat shock proteins (HSPs) occupied the center of the protein-protein interaction (PPI) network in drought memory transcription factors (TF), thus playing a key regulatory role in A. squarrosum drought memory. Co-expression analysis of drought memory TFs and DMGs uncovered a novel regulating module, whereby pairs of TFs might function as molecular switches in regulating DMG transforming between high and low expression levels, thus promoting drought memory reset. Conclusion Based on the co-expression analysis, protein-protein interaction prediction, and drought memory metabolic network construction, a novel regulatory module of transcriptional drought memory in A. squarrosum was hypothesized here, whereby recurrent drought signal is activated by primary TF switches, then amplified by secondary amplifiers, and thus regulates downstream complicated metabolic networks. The present research provided valuable molecular resources on plants’ stress-resistance basis and shed light on drought memory in A. squarrosum.https://doi.org/10.1186/s12870-023-04154-6Drought memoryAgriophyllum squarrosumMolecular switchComparative transcriptomicsPsammophytesLocal adaptation |
| spellingShingle | Tingzhou Fang Chaoju Qian Bachir Goudia Daoura Xia Yan Xingke Fan Pengshu Zhao Yuqiu Liao Liang Shi Yuxiao Chang Xiao-Fei Ma A novel TF molecular switch-mechanism found in two contrasting ecotypes of a psammophyte, Agriophyllum squarrosum, in regulating transcriptional drought memory BMC Plant Biology Drought memory Agriophyllum squarrosum Molecular switch Comparative transcriptomics Psammophytes Local adaptation |
| title | A novel TF molecular switch-mechanism found in two contrasting ecotypes of a psammophyte, Agriophyllum squarrosum, in regulating transcriptional drought memory |
| title_full | A novel TF molecular switch-mechanism found in two contrasting ecotypes of a psammophyte, Agriophyllum squarrosum, in regulating transcriptional drought memory |
| title_fullStr | A novel TF molecular switch-mechanism found in two contrasting ecotypes of a psammophyte, Agriophyllum squarrosum, in regulating transcriptional drought memory |
| title_full_unstemmed | A novel TF molecular switch-mechanism found in two contrasting ecotypes of a psammophyte, Agriophyllum squarrosum, in regulating transcriptional drought memory |
| title_short | A novel TF molecular switch-mechanism found in two contrasting ecotypes of a psammophyte, Agriophyllum squarrosum, in regulating transcriptional drought memory |
| title_sort | novel tf molecular switch mechanism found in two contrasting ecotypes of a psammophyte agriophyllum squarrosum in regulating transcriptional drought memory |
| topic | Drought memory Agriophyllum squarrosum Molecular switch Comparative transcriptomics Psammophytes Local adaptation |
| url | https://doi.org/10.1186/s12870-023-04154-6 |
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