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Positive Interaction between H₂O₂ and Ca²⁺ Mediates Melatonin-Induced CBF Pathway and Cold Tolerance in Watermelon (Citrullus lanatus L.).

ABSTRACT: Cold stress is a major environmental factor that detrimentally affects plant growth and development. Melatonin has been shown to confer plant tolerance to cold stress through activating the C-REPEAT BINDING FACTOR (CBF) pathway; however, the underlying modes that enable this function remain obscure. In this study, we investigated the role of H₂O₂ and Ca²⁺ signaling in the melatonin-induced CBF pathway and cold tolerance in watermelon (Citrullus lanatus L.) through pharmacological, physiological, and genetic approaches. According to the results, melatonin induced H₂O₂ accumulation, which was associated with the upregulation of respiratory burst oxidase homolog D (ClRBOHD) during the early response to cold stress in watermelon. Besides, melatonin and H₂O₂ induced the accumulation of cytoplasmic free Ca²⁺ ([Ca²⁺]_cyt) in response to cold. This was associated with the upregulation of cyclic nucleotide-gated ion channel 2 (ClCNGC2) in watermelon. However, blocking of Ca²⁺ influx channels abolished melatonin- or H₂O₂-induced CBF pathway and cold tolerance. Ca²⁺ also induced ClRBOHD expression and H₂O₂ accumulation in early response to cold stress in watermelon. Inhibition of H₂O₂ production in watermelon by RBOH inhibitor or in Arabidopsis by AtRBOHD knockout compromised melatonin-induced [Ca²⁺]_cyt accumulation and melatonin- or Ca²⁺-induced CBF pathway and cold tolerance. Overall, these findings indicate that melatonin induces RBOHD-dependent H₂O₂ generation in early response to cold stress. Increased H₂O₂ promotes [Ca²⁺]_cyt accumulation, which in turn induces H₂O₂ accumulation via RBOHD, forming a reciprocal positive-regulatory loop that mediates melatonin-induced CBF pathway and subsequent cold tolerance.

SUBMITTER: Chang J

PROVIDER: S-EPMC8471466 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Salt stress seriously reduced the yield and quality of watermelon and restricted the sustainable development of the watermelon industry. However, the molecular mechanism of watermelon in response to salt stress is still unclear. In this study, 150 mmol·L-1 NaCl was used to deal with the seedlings of salt-tolerant and salt-sensitive watermelon varieties. Physiological characteristics showed that salt stress significantly reduced the biomass of watermelon seedlings and the accumulation of K+ in roots and leaves and significantly increased the content of Na+, Cl-, and malondialdehyde (MDA). Compared with the salt-sensitive variety, the salt-tolerant variety had higher K+ accumulation, lower Cl-, Cl- accumulation, and MDA content in roots and leaves. Then, RNA-seq was performed on roots and leaves in normal culture and under 150 mmol·L-1 NaCl treatment. A total of 21,069 genes were identified by RNA-seq analysis, of which 1412 were genes encoding transcription factors (TFs). In the comparison groups of roots and leaves, 122 and 123 shared differentially expressed genes (DEGs) were obtained, respectively. Gene ontology (GO) annotation and KEGG enrichment results showed that there were many identical GO terms and KEGG pathways in roots and leaves, especially the pathways that related to sugar or energy (ATP or NADP+/NADPH). In addition, some DEGs related to salt tolerance were identified, such as plant hormone indole-3-acetic acid (IAA) and gibberellin (GA) signal transduction pathway-related genes, K+/Na+/Ca2+-related genes, lignin biosynthesis-related genes, etc. At the same time, we also identified some TFs related to salt tolerance, such as AP2-EREBP, bZIP, bHLH, MYB, NAC, OFP, TCP, and WRKY and found that these TFs had high correlation coefficients with salt tolerance-related genes, indicating that they might have a potential regulatory relationship. Interestingly, one TCP TF (Cla97C09G174040) co-exists both in roots and leaves, and it is speculated that it may be regulated by miR319 to improve the salt tolerance of watermelon.

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Positive Interaction between H₂O₂ and Ca²⁺ Mediates Melatonin-Induced CBF Pathway and Cold Tolerance in Watermelon (Citrullus lanatus L.).

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Positive Interaction between H2O2 and Ca2+ Mediates Melatonin-Induced CBF Pathway and Cold Tolerance in Watermelon (Citrullus lanatus L.).

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OmicsDI is part of the ELIXIR infrastructure

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Positive Interaction between H₂O₂ and Ca²⁺ Mediates Melatonin-Induced CBF Pathway and Cold Tolerance in Watermelon (Citrullus lanatus L.).