Transcriptional evidence of pluripotency during development of the leaf gall formed by grape phylloxera (Daktulosphaira vitifoliae)

Abstract

Galls are structures formed by plants in response to stimuli by parasitic insects. Because galls require altered gene expression to change cell fates, their initiation requires pluripotent or ‘reactive’ cells. We used RNA sequencing to test three hypotheses about potential sources of pluripotency in the leaf gall formed by grape phylloxera (Daktulosphaira vitifoliae). We postulated that the insect might express ectopically genes regulating apical meristem pluripotency, exploit preexisting meristems, or induce callus cells de novo. We found that phylloxera exploits preexisting cambial and leaf meristems and promotes callus formation. Pluripotency gene expression increases as leaf cells differentiate, extending gall induction opportunity. Auxin regulates pluripotency gene expression. We found evidence of enhanced auxin synthesis and signaling in the gall and of cytokinin (CK) accumulation and signaling. However, we found no evidence for CK synthesis by the plant. Our results support the view that cellular pluripotency is central to gall development and point to sources of pluripotency in galls of an economically important insect. Results also implicate auxin and CK signaling as a means by which pluripotency is established and maintained in the developing gall.