Parasitic-plant parasite utilizes flowering pathways at unconventional stages to form stem-derived galls

Abstract

Galls induced by various organisms exhibit diverse morphological and physiological characteristics, involving complex plant-insect interactions. Most transcriptome analyses to date have focused on leaf-derived galls. To better understand gall formation mechanisms, we investigated stem-derived galls induced by the weevil Smicronyx madaranus on the parasitic plant Cuscuta campestris at gene expression, cellular, and physiological levels. 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 early 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 stem cell induction and maintenance are involved in various gall types. Like leaf- derived galls, the expression of genes related to floral organ development increased through the gall development. However, their expression patterns were dramatically different: downstream genes in the flowering pathway were highly expressed at the initial gall stage, whereas upstream genes were highly expressed later. This suggests that the weevil might activate the flowering pathway at unconventional stages, potentially rerouting the typical flowering cascade to influence gall development. Unlike the decrease in photosynthesis-related genes in leaf-derived galls, we observed an increase in these genes in galls formed on the stem of the holoparasitic plant. Shading experiments confirmed that photosynthesis is crucial for both gall growth and the weevil. This study highlights how gall-inducers can co-opt host resources and genetic pathways, offering new insights into the complexity of plant-insect interactions.