Parasitic-Plant Parasite Rewires Flowering Pathways to Induce Stem-Derived Galls.

Abstract

Gall-inducing insects manipulate host plant development, redirecting cellular fate and physiological processes to form novel structures. This phenomenon is even more intriguing when the host itself is a holoparasitic plant with minimal photosynthetic capacity. In the stem of Cuscuta campestris, the weevil Smicronyx madaranus forms galls that unexpectedly activate photosynthesis, in contrast to the typical suppression of photosynthetic activity observed in leaf-derived galls. This reversal of the usual source-to-sink transition highlights a unique form of insect-induced organogenesis. To elucidate the underlying mechanisms, we performed transcriptomic, histological, and physiological analyses of these galls. RNA-seq across four developmental stages identified differentially expressed genes and associated gene ontology terms. Consistent with histological observations, genes related to cell division and the cell cycle were upregulated in early stage but decreased as the gall matured. Similar to leaf-derived galls, we found high expression of PLETHORA and meristem-related homeobox genes in early gall development, suggesting that induction of cell division is involved in various gall types. Interestingly, the expression of genes related to floral organ development increased through gall development. However, their expression patterns showed a marked temporal shift: Floral organ identity genes were highly expressed at the initial gall stage, whereas floral transition genes were activated later. This suggests that the weevil triggers ectopic activation of the flowering pathway in non-floral tissues, potentially redirecting the typical flowering cascade to drive gall formation. Consistent with previous findings, photosynthesis-related genes were highly expressed in later stage of galls, despite the host being a holoparasitic plant. Shading experiments confirmed that photosynthesis is crucial for both gall and the weevil growth. This study highlights how gall-inducers can co-opt host resources and genetic pathways, offering new insights into the complexity of plant-insect interactions.