Unveiling Molecular Mechanisms of Nitric Oxide-Induced Low-Temperature Tolerance in Cucumber by Transcriptome Profiling

Abstract

Cucumber (Cucumis sativus L.) is one of the most popular cultivated vegetable crops but it is intrinsically sensitive to cold stress due to its thermophilic nature. To explore the molecular mechanism of plant response to low temperature (LT) and the mitigation effect of exogenous nitric oxide (NO) on LT stress in cucumber, transcriptome changes in cucumber leaves were compared. The results showed that LT stress regulated the transcript level of genes related to the cell cycle, photosynthesis, flavonoid accumulation, lignin synthesis, active gibberellin (GA), phenylalanine metabolism, phytohormone ethylene and salicylic acid (SA) signaling in cucumber seedlings. Exogenous NO improved the LT tolerance of cucumber as reflected by increased maximum photochemical efficiency (Fv/Fm) and decreased chilling damage index (CI), electrolyte leakage and malondialdehyde (MDA) content, and altered transcript levels of genes related to phenylalanine metabolism, lignin synthesis, plant hormone (SA and ethylene) signal transduction, and cell cycle. In addition, we found four differentially expressed transcription factors (MYB63, WRKY21, HD-ZIP, and b-ZIP) and their target genes such as the light-harvesting complex I chlorophyll a/b binding protein 1 gene (LHCA1), light-harvesting complex II chlorophyll a/b binding protein 1, 3, and 5 genes (LHCB1, LHCB3, and LHCB5), chalcone synthase gene (CSH), ethylene-insensitive protein 3 gene (EIN3), peroxidase, phenylalanine ammonia-lyase gene (PAL), DNA replication licensing factor gene (MCM5 and MCM6), gibberellin 3 beta-dioxygenase gene (GA3ox), and regulatory protein gene (NPRI), which are potentially associated with plant responses to NO and LT stress. Notably, HD-ZIP and b-ZIP specifically responded to exogenous NO under LT stress. Taken together, these results demonstrate that cucumber seedlings respond to LT stress and exogenous NO by modulating the transcription of some key transcription factors and their downstream genes, thereby regulating photosynthesis, lignin synthesis, plant hormone signal transduction, phenylalanine metabolism, cell cycle, and GA synthesis. Our study unveiled potential molecular mechanisms of plant response to LT stress and indicated the possibility of NO application in cucumber production under LT stress, particularly in winter and early spring.

Transcriptome analysis revealed enrichment pathways and regulation of gene expression associated with somatic embryogenesis in Camellia sinensis

“…Knockdown of five genes of Lhcb1 in Arabidopsis resulted in chlorophyll loss and delayed growth 55 . Down-regulation of Lhcb1 , Lhcb3 and Lhcb5 genes expression levels in cucumber affected its photosynthesis 56 . In contrast, significant up-regulation of the five Lhcb1 genes during embryogenesis might contribute to their light capture and photosynthesis.…”

Transcriptome Analyses Revealed the Wax and Phenylpropanoid Biosynthesis Pathways Related to Disease Resistance in Rootstock-Grafted Cucumber

“…Recently, transcriptomics has become an essential tool for deciphering the molecular mechanisms underlying disease resistance in cucumber. Wu [ 45 ] used transcriptomic sequencing to examine the expression profiles of cucumber plants grown under low-temperature conditions. They found that low-temperature stress regulated the transcript levels of genes related to phenylalanine metabolism, the phytohormone ethylene, photosynthesis, flavonoid accumulation, lignin synthesis, cells, cycleactive gibberellin, and salicylic acid (SA) signaling in cucumber seedlings.…”

Transcriptomic Responses to Chilling Reveal Potential Chilling Tolerance Mechanisms in Cucumber

“…Transcriptome analysis identified 285 and 839 DEGs in chilling-tolerant (CC) and chilling-susceptible (R1461) cucumber cultivars, respectively ( Tables S3 and S4 ), suggesting that these genes may confer chilling tolerance in cucumber. GO analysis was used to analyze the functions of plant genes in response to low-temperature stress [ 5 , 27 , 28 , 35 , 39 ]. Previous studies found that chilling induces ethylene production in cucumber [ 14 , 15 ].…”

“…Transcriptomic analysis has been identified as an efficient experimental tool to investigate the genome functions and physiological regulation mechanisms of chilling stress [ 26 , 27 , 28 ]. Recently, physiological and transcriptome analysis has indicated that the interactions between auxin and hydrogen sulfide signaling are involved in cucumber chilling tolerance [ 3 ].…”

“…Recently, physiological and transcriptome analysis has indicated that the interactions between auxin and hydrogen sulfide signaling are involved in cucumber chilling tolerance [ 3 ]. In addition, transcriptome profiling uncovered that exogenous nitric oxide (NO) improves low-temperature tolerance in cucumber by modulating the expression of some key transcription factors and their target genes [ 27 ]. These results suggest that transcriptomic analysis plays an important role in dissecting the molecular mechanisms of plant responses to chilling stress.…”