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other·plant biology, plant genetics, plant physiology, ecology, agriculture·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 · 10 authors, 5 centres

AI SUMMARY

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POPULATIONAgriophyllum squarrosum plants of two contrasting ecotypes: semi-arid land ecotype AEX (from Horqin Sand Land, annual precipitation 485 mm) and arid land ecotype WW (from Tengger Desert, annual precipitation 166 mm)

INTERVENTIONThree rounds of dehydration-rehydration treatment (4 days water suspended followed by 5 days full rehydration per cycle)

COMPARISONComparison between ecotypes AEX and WW; comparison of drought memory genes (DMGs) between A. squarrosum and previously studied species (Arabidopsis thaliana, Zea mays, Panicum virgatum)

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TL;DR

This study investigated transcriptional drought memory in the desert plant Agriophyllum squarrosum, comparing a semi-arid ecotype (AEX) and an arid ecotype (WW) under recurring dehydration-rehydration cycles. The arid ecotype WW showed stronger and longer-lasting drought memory than AEX, and the authors identified a novel regulatory module where pairs of transcription factors may act as molecular switches controlling the expression of drought memory genes. These findings provide insights into how psammophytes adapt to recurrent drought and offer molecular resources for improving stress tolerance in crops.

Full summary

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**Background:** Prior drought stress can alter plant response patterns and increase tolerance to subsequent stress, a phenomenon known as 'drought memory.' While progress has been made in understanding drought memory in model plants, the mechanisms in psammophytes (sand-dune plants) remain largely unknown. Agriophyllum squarrosum is a pioneer annual plant widely distributed in Asian deserts with outstanding water use efficiency. This study aimed to dissect the drought memory mechanism of A. squarrosum and determine discrepancies between two ecotypes adapted to different water availability.

**Methods:** Two contrasting ecotypes were studied: AEX from a semi-arid site (Horqin Sand Land, 485 mm annual precipitation) and WW from an arid region (Tengger Desert, 166 mm annual precipitation). One-month-old seedlings were subjected to three rounds of dehydration-rehydration cycles (4 days water suspension followed by 5 days rehydration). Physiological measurements included soil moisture content (SMC), leaf relative water content (RWC), and water loss of isolated leaves. For transcriptomic analysis, mature leaves were collected from control (R0), first dehydration (S1), and third dehydration (S3) treatments. RNA sequencing generated 86.8 Gb clean reads (average 7.23 Gb per sample, Q30 average 94.2%), which were de novo assembled into 52,925 unigenes, with 32,488 (61.4%) annotated in at least one database. Drought memory genes (DMGs) were identified as drought-responsive genes with significantly different expression between S1 and S3, classified into four types: [+/+], [−/−], [+/−], and [−/+]. Ortholog groups were sought between A. squarrosum and three previously studied species (A. thaliana, Z. mays, P. virgatum). Co-expression analysis between drought memory transcription factors (TFs) and other DMGs was conducted using Pearson correlation coefficient. Protein-protein interaction (PPI) networks were constructed using STRING and visualized with Cytoscape.

**Key Results:** Physiological monitoring showed that WW had stronger and longer-lasting drought memory than AEX. In AEX, a consecutive decline of RWC in R2 and S3 was observed, indicating attenuation in drought memory function, while no such decline was found in WW. A total of 5,379 (12.5%) and 4,436 (10.7%) genes were drought-responsive in AEX and WW, respectively. DMGs comprised 1,776 (33.0%) of drought-responsive genes in AEX and 1,384 (31.2%) in WW. The [+/−] subgroup dominated in both ecotypes (48.4% in AEX, 39.9% in WW). Comparison across species identified 257 shared DMG ortholog groups (OGs) among all five tested species, 406 OGs unique to A. squarrosum, and 655 and 339 OGs unique to AEX and WW, respectively. Shared DMGs were enriched in phenylpropanoid biosynthesis, MAPK signaling, and saccharide metabolism. A. squarrosum-specific DMGs were enriched in responses to heat, high light intensity, hydrogen peroxide, and water deprivation. WW-unique DMGs were concentrated in photosynthesis-related functions. PPI network analysis revealed heat shock proteins (HSPs) as hub genes in both ecotypes. Co-expression analysis identified 17 TFs in AEX and 20 TFs in WW that showed 'on-off' controlling patterns, where pairs of TFs appeared to function as molecular switches regulating the expression of DMG sets. For example, in shared DMGs in AEX, a module of AsGBF3-AsODORANT1-AsWRKY53-AsARF19 controlled 30 DMGs; in WW, an AsNF-YA4-AsRAV1 module controlled 48 DMGs. DMGs subjected to TF switches included heat shock proteins, chaperonins, late embryogenesis abundant proteins, cytochrome P450, MAPKs, and glutathione S-transferases. Q-PCR validation of 10 TFs confirmed high correlation with RNA-seq data.

**Clinical Implications:** This is a plant biology study with no direct clinical implications. However, the findings provide valuable molecular resources for understanding stress resistance mechanisms in plants, which could inform breeding programs for drought-tolerant crops and pseudocereals, particularly for cultivation in sandy and arid lands. The proposed regulatory module—where TF pairs act as molecular switches controlling drought memory gene expression—offers a conceptual framework for understanding how plants balance growth and stress defense under recurring drought conditions.

PICO

PPOPULATION

Agriophyllum squarrosum plants of two contrasting ecotypes: semi-arid land ecotype AEX (from Horqin Sand Land, annual precipitation 485 mm) and arid land ecotype WW (from Tengger Desert, annual precipitation 166 mm)

IINTERVENTION

Three rounds of dehydration-rehydration treatment (4 days water suspended followed by 5 days full rehydration per cycle)

OOUTCOME

Physiological traits (leaf relative water content, water loss); transcriptomic profiles and identification of drought memory genes; protein-protein interaction networks; co-expression analysis of transcription factors and DMGs

STUDY TYPE

other

SPECIALTY

plant biology

SUMMARISED BY

AI pipeline

FIDELITY CHECK

76% · B

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