Combined metabolome and transcriptome profiling provides insights into dynamic molecular control of lemon (Citrus...

Lemon peels are crucial quality traits and important sources of nutraceuticals. However, the regulation of peel development remains largely misunderstood. Here, we delved into the dynamic molecular mechanisms that control smooth lemon peel formation through transcriptomics and metabolomics analyses of developing peels at five different stages, including C1 (30 DAF, day after flowering), C2 (60 DAF), C3 (90 DAF), C4 (120 DAF), and C5 (150 DAF).

Our analyses revealed that peel development is stage-specifically regulated, with the transition from stage C2 to stage C3 being the most critical period. Notably, major metabolic adjustments and transcriptional switches occurred between C2 and C3. Particularly, phytohormones and their related genes, flavonoids, terpenoids, phenolic acids, vitamin C, and citric acid were down-regulated at stage C3. Differentially expressed genes between the transition from C2 to C3 were mainly enriched in hydrolase activity, nucleic acid binding transcription, transcription factor activity, sequence-specific DNA binding and pathways such as plant hormone signal transduction, starch and sucrose metabolism, MAPK signaling pathway-plant, plant-pathogen interaction, and circadian rhythm-plant biosynthesis. Plant hormone signaling was crucial for peel development process. Specifically, we found that crosstalks between jasmonic acid, abscisic acid, salicylic acid, gibberellic acid, and ethylene dynamically and coordinately regulate peel development process. ABC transporter family genes and green-degrading promoting genes, including protein SGR1 (LOC18041639), ervatamin-C (LOC18051181), and many ethylene-responsive transcription factors were significantly induced from C2. Furthermore, we screened out stage-specific most regulated genes.

Our findings offer molecular understanding of peel formation process and fundamental resources for the functional dissection of its regulatory networks and for genomics-assisted control of peel shape and fruit quality in lemon.