Genome-Wide Identification of SWEET Genes in Cicer arietinum and Modulation of Its Expression in Endophytic Interactions with Serendipita indica

Sugar Will Eventually be Exported Transporters (SWEETs) are plant transporters involved in the efflux of sugars to the apoplast from high to low concentrations. Owing to their function, they have an important implication in plant–microbe interactions. Plants regulate their key sugar transporters during such interactions, as has been identified in several pathogenic and symbiotic interactions. However, it is still unclear whether plant SWEETs are involved in endophytic interactions with fungi such as Serendipita indica . This study identified SWEET genes in the leguminous crop Cicer arietinum (chickpea). We analyzed their gene structure, motif composition, chromosomal localization, and phylogenetic relationship with Arabidopsis thaliana, Oryza sativa, and Medicago truncatula . The expression of the CaSWEET genes was identified in C. arietinum roots colonized by S. indica . We found that the genes CaSWEET1b , CaSWEET2b , and CaSWEET4 were upregulated, whereas CaSWEET1a , CaSWEET12 , CaSWEET15c , and CaSWEET16 were downregulated. Though the SWEETs transport sugar to the fungal mycelia, some SWEET genes were downregulated. This intrigued us to inspect whether during C. arietinum - S. indica interaction, some miRNAs were synthesized by the plant that plays a role in the downregulation of the SWEET genes. We first identified the miRNAs from C. arietinum - S. indica interaction targeting CaSWEET genes. The identified miRNAs were validated using stem-loop RT-qPCR. One of the miRNAs, miR156, showed significantly higher expression and was identified to target the CaSWEET12 gene. The CaSWEET12 transporter was expressed in most of the C. arietinum tissues, but its expression was reduced during interaction with S. indica . This indicated that the plant regulates its sugar transport to S. indica by downregulating selective transporters to restrict its excessive growth on the plant. This study has thus provided insight into the miRNA-mediated regulation of plant SWEET genes in the case of C. arietinum - S. indica symbiosis, which can be used in future for functional validation and will benefit crop improvement.