RNA-seq-based comparative transcriptome analysis reveals the role of CsPrx73 in waterlogging-triggered adventitious root formation in cucumber

Abstract

Abiotic stressors like waterlogging are detrimental to cucumber development and growth. However, comprehension of the highly complex molecular mechanism underlying waterlogging can provide an opportunity to enhance cucumber tolerance under waterlogging stress. We examined the hypocotyl and stage-specific transcriptomes of the waterlogging-tolerant YZ026A and the waterlogging-sensitive YZ106A, which had different adventitious rooting ability under waterlogging. YZ026A performed better under waterlogging stress by altering its antioxidative machinery and demonstrated a greater superoxide ion (O₂⁻) scavenging ability. KEGG pathway enrichment analysis showed that a high number of differentially expressed genes (DEGs) were enriched in phenylpropanoid biosynthesis. By pairwise comparison and weighted gene co-expression network analysis analysis, 2616 DEGs were obtained which were categorized into 11 gene co-expression modules. Amongst the 11 modules, black was identified as the common module and yielded a novel key regulatory gene, CsPrx73. Transgenic cucumber plants overexpressing CsPrx73 enhance adventitious root (AR) formation under waterlogging conditions and increase reactive oxygen species (ROS) scavenging. Silencing of CsPrx73 expression by virus-induced gene silencing adversely affects AR formation under the waterlogging condition. Our results also indicated that CsERF7-3, a waterlogging-responsive ERF transcription factor, can directly bind to the ATCTA-box motif in the CsPrx73 promoter to initiate its expression. Overexpression of CsERF7-3 enhanced CsPrx73 expression and AR formation. On the contrary, CsERF7-3-silenced plants decreased CsPrx73 expression and rooting ability. In conclusion, our study demonstrates a novel CsERF7-3-CsPrx73 module that allows cucumbers to adapt more efficiently to waterlogging stress by promoting AR production and ROS scavenging.

Acknowledgements

This work was funded by the science and technology plan project of Guizhou Province [(2019) 4318] and [(2021) 239], the science and technology plan project of Guiyang City [2021]3-22, and first-class discipline of Kaili University (Horticulture) [grant number 202102]. We are very grateful to the experimenters and analysts at Biomarker Inc. (www.biomarker.com.cn) who took part in this study.

Author contributions

Y.S.W. and Q.Y.Z. designed the experiments, J.Y.G. and Q.Y.Z. collected samples and took part in conducting experiments, Y.S.W. and Q.Y.Z. took part in analyzing the data, and Y.S.W. wrote the paper.

Data availability statement

The draft genome sequence was deposited in the China National Center for Bioinformation Database (https://bigd.big.ac.cn/gsub/, accession number CRA011290). The clean raw data of the long-read and short-read transcriptomes of young stems, young roots, young leaves, calyxes, petals, stamens, young berries, coloring berries, and mature berries were also deposited in the China National Center for Bioinformation Database (https://bigd.big.ac.cn/gsub/, accession numbers CRA011285 and CRA012463).

Conflict of interest

The authors declare no conflicts of interest.

Supplementary data

Supplementary data are available at Horticulture Research online.

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