Arabidopsis SWEET12 contributes to the regulation of sugar allocation and defense responses during interaction with Serendipita indica.

Abstract

Carbon availability is a central determinant of beneficial plant-fungal associations, and sugar transporters are key levers of this exchange. SWEETs (SUGARS WILL EVENTUALLY BE EXPORTED TRANSPORTER) are involved in transporting various kinds of sugars in plants; however, their functional roles in fungal symbiosis are not sufficiently explored. In this study, we investigate the functional relevance of Arabidopsis SWEETs in the interaction with the endophytic fungi, Serendipita indica. Transcript profiling of SWEET genes in response to S. indica and its major elicitor, cellotriose, revealed the early root-specific induction of SWEET12. Using a SWEET12 loss-of-function mutant, we demonstrate that the absence of SWEET12 disrupts the major outcomes of mutualism, including growth promotion, balanced colonization, sugar allocation, and the accumulation of defense phytohormones (jasmonic acid and salicylic acid). Transcriptome profiling further reveals that SWEET12 buffers whole-plant responses by coordinating genes linked to carbohydrate, nitrogen, and lipid metabolism, and by tuning defense signaling and nutrient transporter networks. Our findings indicate that SWEET12 is essential for balancing fungal colonization and host defense, thereby promoting plant growth. SWEET12 does so by acting as a sugar valve that meters sugar release to the apoplast, enabling the fungus to access carbon while preserving host sugar homeostasis and immune competence.