Rootstock–scion exchanging mRNAs participate in the pathways of amino acid and fatty acid metabolism in cucumber under early chilling stress

Abstract

Cucumber (Cucumis sativus L.) often experiences chilling stress that limits their growth and productivity. Grafting is widely used to improve abiotic stress resistance by alternating a vigorous root system, suggesting there exists systemic signals communication between distant organs. mRNAs are reported to be evolving in fortification strategies by long-distance signaling when plants suffering from chilling stress. However, the potential function of mobile mRNAs alleviating chilling stress in grafted cucumber is still unknown. Here, the physiological changes, mobile mRNAs profiling, transcriptomic and metabolomic changes in above- and underground tissues of all graft combinations of cucumber and pumpkin responding to chilling stress were established and analyzed comprehensively. The co-relationship between the cluster of chilling-induced pumpkin mobile mRNAs with Differentially Expressed Genes (DEGs) and Differentially Intensive Metabolites (DIMs) revealed that four key chilling-induced pumpkin mobile mRNAs were highly related to glycine, serine and threonine synthesis and fatty acid β-oxidative degradation metabolism in cucumber tissues of heterografts. The verification of mobile mRNAs, potential transport of metabolites and exogenous application of key metabolites of glycerophospholipid metabolism pathway in cucumber seedlings confirmed that the role of mobile mRNAs in regulating chilling responses in grafted cucumber. Our results build a link between the long-distance mRNAs of chilling-tolerant pumpkin and the fatty acid β-oxidative degradation metabolism of chilling-sensitive cucumber. It helps to uncover the mechanism of signaling interaction between scion and stock responding to chilling tolerant in grafted cucumber.

Pumpkin CmoDREB2A enhances salt tolerance of grafted cucumber through interaction with CmoNAC1 to regulate H2O2 and ABA signaling and K+/Na+ homeostasis

“…These signals also play a vital role in vegetable grafting, where overexpression of SlNCED1 in grafted tomato rootstocks promotes ABA generation and translocation to scion leaves, thus increasing salt tolerance [ 29 ]. Similarly, in grafted peppers, salt-tolerant rootstock enhances H 2 O 2 level in scion leaves to activate antioxidant capacity, as well as ABA production to promote leaf stomata closure, thereby improving its salt tolerance [ 27 ]. Cucumber grafts also benefit from pumpkin rootstock CmoNAC1 , which binds to CmoRBOHD1 and CmoNCED6 promoters, resulting in increased production and transport of H 2 O 2 and ABA to cucumber scions, promoting leaf stomatal closure and salt stress resistance [ 34 , 45 , 46 ].…”

“…This aspect of the investigation provides a comprehensive understanding beyond previous studies conducted in tobacco [ 44 ] and tomato [ 17 ]. Furthermore, the study uncovered that CmoDREB2A interacts with CmoNAC1 in promoting the production of H 2 O 2 and ABA signals in pumpkin rootstock, offering deeper insights compared to the studies conducted on grafted tomatoes [ 29 ] and grafted peppers [ 27 ]. Concurrently, the study advances the current understanding of CmoNAC1’s role in regulating H 2 O 2 and ABA signaling of grafted cucumbers [ 34 ].…”

“…Grafting cucumber onto pumpkin rootstock has proven effective in improving its salt tolerance. Furthermore, both cucumber and pumpkin possess highly developed vascular tissues, making them suitable subjects for studying grafting signal transduction [ 26 , 27 ]. The key mechanisms through which grafting improves plant salt tolerance include: (i) upregulation of genes involved in H 2 O 2 and ABA synthesis in rootstock to facilitate the synthesis and transport of root signals to the shoot [ 28 , 29 ]; (ii) induction of mobile mRNA movement to the shoot [ 30 ]; (iii) restriction of Na + transport to the scion [ 31 ] and enhancement of K + absorption [ 32 ]; and (iv) increased activity of antioxidant enzymes and elevated proline content in the scion [ 33 , 34 ].…”

Transcriptome analysis reveals the effect of grafting on gossypol biosynthesis and gland formation in cotton

“…Grafting is a commonly used method in agriculture, which can improve the ability of plants to withstand external diseases and insect pests [ 47 ]. According to recent research reports, grafting can be used as an effective way to study plant molecular communication signals and the exchange of genetic material, Liu et al (2022) analyzed the metabolic mechanism of pumpkin rootstock mRNA signaling involved in regulating the cold tolerance of grafted cucumber [ 48 ]. Here, in the initial experiments, we measured the gland density and gossypol content after grafting.…”

Unveiling rootstock-induced dwarfing from comparative genomic analysis

“…The long-distance transport of mobile mRNAs between rootstock and scion also plays a significant role in regulating the traits of grafted plants (Liu et al 2022 ), but it has always been a challenge to identify mobile mRNAs between rootstock and scion in apple. To address this problem, the authors develop a bioinformatics tool called “RNAGlass” that integrates genomic and transcriptome data to accurately and effectively identify mobile mRNAs between rootstock and scion based on the assembled high-quality reference genome of the cultivated variety “Fuji”.…”