Integrated metabolomics and transcriptomics reveal that sugar transporter CiSWEET10a is indispensable for nut sizing and kernel filling in Carya illinoinensis

Pecan [ Carya illinoinensis (Wagenh.) K. Koch] kernels are composed of the embryo and cotyledons. Rapid nut sizing and kernel filling are key periods during which kernels acquire large quantities of nutrients to produce high-quality nuts. Hence, an understanding of the molecular regulation of assimilate partitioning is important for improving pecan nut quality. Transcriptomics analysis revealed that CiSWEET10a transcript abundance was significantly decreased in abscising nuts compared to persisting nuts. CiSWEET10a was expressed in the basal shuck sucrose unload zone of persisting nuts before the rapid nut sizing stage, and a large starch granule content was observed in the upper tissues of the zone. However, CiSWEET10a was not expressed, and starch granules were not detected in the same zones in abscising nuts, indicating that CiSWEET10a unloads and transports sucrose across this zone during rapid nut sizing. CiSWEET10a expression was the highest in the seed coat. During the kernel filling stage, the starch content was the highest in the seed coat, and the sucrose content was the highest in kernel. In transgenic rice, CiSWEET10a promoter-derived GUS activity was detected in the ovular vascular trace, nucellar projection, nucellar epidermis, nucellar layers, and aleurone layer of the caryopsis at 5 days after pollination (DAP). Transgenic rice overexpressing CiSWEET10a had a significantly decreased starch content in the pericarp at 5 DAP but significantly increased starch content in the caryopsis at 9 DAP. CiSWEET10a transported sucrose from the shell and middle septum through the seed coat to the developing endosperm and embryo during the kernel filling stage. These results show that CiSWEET10a is indispensable for nut sizing and kernel filling in pecan.