A novel TF molecular switch-mechanism found in two contrasting ecotypes of a psammophyte, Agriophyllum squarrosum , in regulating transcriptional drought memory

BMC Plant Biology · 10 authors, 5 centres

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Using dehydration-rehydration treatments, physiological monitoring revealed that the arid ecotype WW exhibited a stronger and longer-lasting drought memory than ecotype AEX.

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Using dehydration-rehydration treatments, physiological monitoring revealed that the arid ecotype WW exhibited a stronger and longer-lasting drought memory than ecotype AEX. Transcriptomic analysis identified 1,642 drought memory genes in AEX and 1,339 in WW. The study proposes a model where primary transcription factor switches activate recurrent drought signals, which are amplified by secondary amplifiers to regulate downstream metabolic networks. Limitations include the need for further validation of the proposed transcription factor switch mechanism through techniques like yeast one-hybrid or co-immunoprecipitation. The findings provide molecular resources on plant stress resistance and illuminate drought memory mechanisms in this desert-adapted species.

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preclinical research

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ORIGINAL PAPER

PMC10061855

A novel TF molecular switch-mechanism found in two contrasting ecotypes of a psammophyte, Agriophyllum squarrosum , in regulating transcriptional drought memory

BMC Plant Biology

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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 . Supplementary Information The online version contains supplementary material available at 10.1186/s12870-023-04154-6.

CITATION EXPORT

Tingzhou Fang, Chaoju Qian, Bachir Goudia Daoura et al.. A novel TF molecular switch-mechanism found in two contrasting ecotypes of a psammophyte, Agriophyllum squarrosum, in regulating transcriptional drought memory. BMC Plant Biology. (2023). https://doi.org/10.1186/s12870-023-04154-6

AUTHORS

10 · 5 CENTRES

Tingzhou Fang, Chaoju Qian, Bachir Goudia Daoura, Xia Yan, Xingke Fan, Pengshu Zhao, Yuqiu Liao, Liang Shi, Yuxiao Chang, Xiao-Fei Ma

1grid.9227.e0000000119573309Key Laboratory of Ecological Safety and Sustainable Development in Arid Lands, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou, Gansu 730000 China
2grid.410726.60000 0004 1797 8419College of Resources and Environment, University of Chinese Academy of Sciences, Beijing, 100049 China
3Department of Biology, Faculty of Sciences and Technology, Dan Dicko Dankoulodo University, POBox 465, Maradi, Niger
4grid.9227.e0000000119573309Key Laboratory of Eco-hydrology of Inland River Basin, Northwest Institute of Eco- Environment and Resources, Chinese Academy of Sciences, Lanzhou, Gansu, 730000 China
5grid.488316.00000 0004 4912 1102Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Science, Shenzhen, 518000 China