Phloem transcriptome signatures underpin the physiological differentiation of the pedicel, stalk and fruit of cucumber (Cucumis sativusL.)

Abstract

Cucumber is one of the most important vegetables grown worldwide due to its important economic and nutritional value. The cucumber fruit consists morphologically of the undesirable stalk and the tasty fruit; however, physiological differentiation of these two parts and the underlying molecular basis remain largely unknown. Here we characterized the physiological differences among the pedicel, stalk and fruit, and compared the respective phloem transcriptomes using laser capture microdissection coupled with RNA sequencing (RNA-Seq). We found that the pedicel was characterized by minor cell expansion and a high concentration of stachyose, the stalk showed rapid cell expansion and high raffinose accumulation, and the fruit featured transition from cell division to cell expansion and high levels of monosaccharides. Analyses of transcriptome data indicated that cell wall- and calcium ion binding-related genes contributed to the cell expansion in the pedicel and stalk, whereas genes implicated in cell cycle and hormone actions regulated the transition from cell division to cell expansion in the fruit. Differential sugar distribution in these three phloem-connected tissues resulted from tissue-specific sugar metabolism and transport. Enrichment of transcription factors in the stalk and fruit may facilitate nutrient accumulation in these sink organs. As such, phloem-located gene expression partially orchestrated physiological differentiation of the pedicel, stalk and fruit in cucumber. In addition, we identified 432 cucumber-unique genes and five phloem markers guiding future functional studies.