| Summary: | Watermelon (<i>Citrullus lanatus</i>) is an economically important fruit crop grown for consumption of its large edible fruit flesh. <i>Pentatricopeptide-repeat</i> (PPR) encoding genes, one of the large gene families in plants, are important RNA-binding proteins involved in the regulation of plant growth and development by influencing the expression of organellar mRNA transcripts. However, systematic information regarding the PPR gene family in watermelon remains largely unknown. In this comprehensive study, we identified and characterized a total of 422 <i>C. lanatus </i>PPR (<i>ClaPPR</i>) genes in the watermelon genome. Most <i>ClaPPRs</i> were intronless and were mapped across 12 chromosomes. Phylogenetic analysis showed that <i>ClaPPR</i> proteins could be divided into P and PLS subfamilies. Gene duplication analysis suggested that 11 pairs of segmentally duplicated genes existed. In-silico expression pattern analysis demonstrated that <i>ClaPPRs </i>may participate in the regulation of fruit development and ripening processes. Genotyping of 70 lines using 4 single nucleotide polymorphisms (SNPs) from 4 <i>ClaPPRs</i> resulted in match rates of over 0.87 for each validated SNPs in correlation with the unique phenotypes of flesh color, and could be used in differentiating red, yellow, or orange watermelons in breeding programs. Our results provide significant insights for a comprehensive understanding of <i>PPR</i> genes and recommend further studies on their roles in watermelon fruit growth and ripening, which could be utilized for cultivar development of watermelon.
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