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Pectin is a vital component of plant cell walls and its methylation process is regulated by pectin methylesterase inhibitors (PMEIs). PMEIs regulate the structural and functional modifications of cell walls in plants and play an important role in plant processes such as seed germination, fruit ripening, and stress response. Although the PMEI gene family has been well characterized in model plants, the understanding of its molecular evolution and biological functions in watermelon remains limited. In this study, 60 ClPMEI genes were identified and characterized, revealing their dispersion on multiple chromosomes. Based on a systematic developmental analysis, these genes were classified into three subfamilies, which was further supported by the exon, intron, and conserved motif distribution. Analysis of cis-elements and expression patterns indicated that ClPMEIs might be involved in regulating the tolerance of watermelon to various abiotic stresses. Moreover, distinct ClPMEI genes exhibit specific functions under different abiotic stresses. For example, ClPMEI51 and ClPMEI54 showed a significant upregulation in expression levels during the late stage of drought treatments, whereas ClPMEI3 and ClPMEI12 displayed a significant downregulation under low-temperature induction. Subcellular localization prediction and analysis revealed that the ClPMEI family member proteins were localized to the cell membrane. This study provided an important foundation for the further exploration of the functions of ClPMEI genes in watermelon.

Male sterility is a valuable trait for watermelon breeding, as watermelon hybrids exhibit obvious heterosis. However, the underlying regulatory mechanism is still largely unknown, especially regarding the related non-coding genes. In the present study, approximately 1035 differentially expressed genes (DEGs), as well as 80 DE-lncRNAs and 10 DE-miRNAs, were identified, with the overwhelming majority down-regulated in male-sterile floral buds. Enrichment analyses revealed that the general phenylpropanoid pathway as well as its related metabolisms was predicted to be altered in a mutant compared to its fertile progenitor. Meanwhile, the conserved genetic pathway DYT1-TDF1-AMS-MS188-MS1, as well as the causal gene ClAMT1 for the male-sterile mutant Se18, was substantially disrupted during male reproductive development. In addition, some targets of the key regulators AMS and MS188 in tapetum development were also down-regulated at a transcriptional level, such as ABCG26 (Cla004479), ACOS5 (Cla022956), CYP703A2 (Cla021151), PKSA (Cla021099), and TKPR1 (Cla002563). Considering lncRNAs may act as functional endogenous target mimics of miRNAs, competitive endogenous RNA networks were subsequently constructed, with the most complex one containing three DE-miRNAs, two DE-lncRNAs, and 21 DEGs. Collectively, these findings not only contribute to a better understanding of genetic regulatory networks underlying male sterility in watermelon, but also provide valuable candidates for future research.

Grafting is widely used to increase plant defense responses to various stresses. Grafting-induced cold tolerance is associated with the increase of the antioxidant potential of plants; however, the underlying mechanisms remain unclear. Here, we found that pumpkin rootstocks promote antioxidant enzyme activities and alleviate cold-induced oxidative damage, accompanied by increased abscisic acid (ABA), melatonin, and methyl jasmonate (MeJA) levels in leaves. Increased ABA accumulation in leaves was attributed partly to the increased ABA levels in rootstocks. ABA induced antioxidant enzymes activities and the accumulation of melatonin and MeJA, while inhibition of ABA synthesis blocked the rootstock-induced antioxidant activity and the accumulation of melatonin and MeJA under cold stress. Melatonin and MeJA application also enhanced ABA accumulation in leaves after cold exposure, whereas inhibition of melatonin or MeJA synthesis attenuated the rootstock-induced increase of ABA. Moreover, melatonin and MeJA application alleviated cold-induced oxidative stress, but inhibition of melatonin or MeJA synthesis lowered the rootstock- or ABA-induced antioxidant potential and tolerance to cold. These findings indicate that ABA plays an important role in the grafting-induced cold tolerance by promoting the accumulation of melatonin and MeJA, which in turn, promote ABA accumulation, forming a positive feedback loop.

Transcriptional regulation of cold-responsive genes is crucial for exogenous melatonin-mediated cold tolerance in plants. Nonetheless, how melatonin regulates cold-responsive genes is largely unknown. In this study, we found that exogenous melatonin improved cold tolerance in watermelon by regulating expression of microRNAs (miRNAs). We identified a set of miRNAs that were regulated by melatonin under unstressed or cold conditions. Importantly, mRNA-seq analysis revealed that melatonin-induced downregulation of some miRNAs, such as miR159-5p, miR858, miR8029-3p, and novel-m0048-3p correlated with the upregulation of target genes involved in signal transduction (CDPK, BHLH, WRKY, MYB, and DREB) and protection/detoxification (LEA and MDAR) under cold stress. These results suggest that miRNAs may be involved in melatonin-mediated cold tolerance in watermelon by negatively regulating the expression of target mRNAs.

Melatonin, a pleiotropic signal molecule, has been shown to play important roles in the regulation of plant growth, development, and responses to environmental stresses. Since a few species have been investigated to unveil the effect of exogenous melatonin on salt stress, the underlying mechanism of melatonin-mediated salt stress tolerance in other plant species still remains largely unknown. In this study, the effects of melatonin on leaf photosynthesis and redox homeostasis in watermelon were examined under salt stress (300 mM NaCl) along with different doses of melatonin (50, 150, and 500 mM) pretreatment. NaCl stress inhibited photosynthesis and increased accumulation of reactive oxygen species and membrane damage in leaves of watermelon seedlings. However, pretreatment with melatonin on roots alleviated NaCl-induced decrease in photosynthetic rate and oxidative stress in a dose-dependent manner. The protection of photosynthesis by melatonin was closely associated with the inhibition of stomatal closure and improved light energy absorption and electron transport in photosystem II, while the reduction of oxidative stress by melatonin was attributed to the improved redox homeostasis coupled with the enhanced activities of antioxidant enzymes. This study unraveled crucial role of melatonin in salt stress mitigation and thus can be implicated in the management of salinity in watermelon cultivation. [ABSTRACT FROM AUTHOR]