Abstract
Watermelon (Citrullus lanatus (Thunb.) Matsum. & Nakai) is a non-climacteric fruit. The modern sweet-dessert watermelon is the result of years of cultivation and selection for fruits with desirable qualities. To date, the mechanisms of watermelon fruit ripening, and the role of abscisic acid (ABA) in this process, has not been well understood. We quantified levels of free and conjugated ABA contents in the fruits of cultivated watermelon (97103; C. lanatus subsp. vulgaris), semi-wild germplasm (PI179878; C. lanatus subsp. mucosospermus), and wild germplasm (PI296341-FR; C. lanatus subsp. lanatus). Results showed that ABA content in the fruits of 97103 and PI179878 increased during fruit development and ripening, but maintained a low steady state in the center flesh of PI296341-FR fruits. ABA levels in fruits were highest in 97103 and lowest in PI296341-FR, but no obvious differences in ABA levels were observed in seeds of these lines. Examination of 31 representative watermelon accessions, including different C. lanatus subspecies and ancestral species, showed a correlation between soluble solids content (SSC) and ABA levels in ripening fruits. Furthermore, injection of exogenous ABA or nordihydroguaiaretic acid (NDGA) into 97103 fruits promoted or inhibited ripening, respectively. Transcriptomic analyses showed that the expression levels of several genes involved in ABA metabolism and signaling, including Cla009779 (NCED), Cla005404 (NCED), Cla020673 (CYP707A), Cla006655 (UGT) and Cla020180 (SnRK2), varied significantly in cultivated and wild watermelon center flesh. Three SNPs (-738, C/A; -1681, C/T; -1832, G/T) in the promoter region of Cla020673 (CYP707A) and one single SNP (-701, G/A) in the promoter of Cla020180 (SnRK2) exhibited a high level of correlation with SSC variation in the 100 tested accessions. Our results not only demonstrate for the first time that ABA is involved in the regulation of watermelon fruit ripening, but also provide insights into the evolutionary mechanisms of this phenomenon.
Highlights
Due to its juicy, sweet and nutrient-rich flesh, watermelon (Citrullus lanatus (Thunb.) Matsum & Nakai) is among the most popular specialty fruits worldwide
abscisic acid (ABA) content is well correlated with watermelon fruit development and ripening To investigate the role of ABA in watermelon fruit development and ripening, levels of both free and conjugated ABA (ABA-GE) were quantified in different fruit tissues of 97103, PI179878 and PI296341-FR watermelons at distinct fruit development and ripening stages (1, 3, 5, 10, 18, 26, 34, 42 and 50 DAP)
The whole fruit ABA content was the highest in 97103, followed by PI179878 and lowest in PI296341-FR (Fig 1E). These results suggested that variation in the ABA contents in fruits, in the fleshy parts of the fruit, may be associated with watermelon fruit development and ripening
Summary
Sweet and nutrient-rich flesh, watermelon (Citrullus lanatus (Thunb.) Matsum & Nakai) is among the most popular specialty fruits worldwide. Given the differences in fruit morphology and composition between the fruits of the ancestral species and the modern sweet-dessert watermelon, it is obvious that several significant genetic changes have occurred during the domestication of this specialty crop. Despite the importance of these genetic changes, relatively little is known about the evolutionary events leading to the generation of the modern watermelon. This lack of knowledge is due to a lack of information on the genes involved in watermelon ripening, and due to a limited understanding of the physiology of watermelon fruit development
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