Tissue-specific regulation of a sugar transporter mediates both resistance and tolerance responses to attack from a leafminer in potato

Plants use two major defense strategies, resistance and tolerance, to counter herbivore attack; how these are coordinated remains poorly understood. Here, we demonstrate that damage by a specialist leafminer (<i>Phthorimaea operculella</i>) triggers tissue-specific responses in potato plants: compensatory growth in immature leaves, enabling tolerance, while resistance is induced in the mined leaf. The tissue-specific regulation of Sugars Will Eventually Be Exported Transporter 11 (SWEET11) mediates both responses. In unattacked sink leaves, SWEET11 is up-regulated, enhancing sugar import, promoting compensatory growth and herbivore tolerance. In contrast, SWEET11 is rapidly down-regulated in mined source leaves, inhibiting sugar export and increasing cellular sugar levels. The resulting sugar accumulations suppress SNF1-related protein kinase 1 (SnRK1) and thereby enhance herbivore resistance. SWEET11-mediated sugar signaling enhances jasmonic acid (JA)-mediated resistance by degrading MCPI1a and MCPI1b (metallocarboxypeptidase inhibitor 1), two JA-induced herbivory susceptibility factors. These findings reveal a dual role for sugar transport in regulating tissue-specific defense responses to herbivory.