Complex meristematic activity induced by Eucecidoses minutanus on Schinus engleri turns shoots into galls

Premise Gall-inducing organisms change the development of their host plant organs, resulting in ontogenetic patterns not observed in the non-galled plants. Distinct taxa induce galls on Schinus spp., manipulating meristematic patterns in the host plant in distinct ways. Here we report ontogenetic novelties induced in the lateral buds of S. engleri by Eucecidoses minutanus, a Cecidosidae, whose galls have been poorly understood. Methods The anatomy, histochemistry, and histometry of galls in distinct phases of development, non-galled buds, and stems of Schinus engleri were analyzed in parallel with the instars of E. minutanus to detail the morphogenetic changes in the host with each larval stage. Results Ontogenetic phases of the galls were intricately associated with larval development. First and second-instar larvae induced pericycle and pith cells to dedifferentiate into the gall inner meristem, where hyperplasia and cell hypertrophy characterized the growth and development phase of the gall. The innermost layers were lipid-rich nutritive cells that lined the larval chamber. Additional vascular bundle rows were produced in young galls. Third and fourth instar-larvae were associated with the gall maturation phase: centripetal lignification of the outer parenchyma cell layers, epidermal stratification, and activation of a cambium-like meristem (CLM). The CLM activity resulted in new layers of nutritive cells that differentiated inward as the first layers of nutritive cells were consumed by E. minutanus larvae, and, also, in more parenchyma cell layers that formed outward. All tissues between the innermost layer of nutritive tissue that surround the gall chamber and the outermost layer of the dermal system that externally covers the gall form the gall wall, and increased in thickness until the end of gall maturation. Conclusions E. minutanus induces a structurally complex globoid stem gall, modifying all host plant tissues and stimulating a novel meristematic pattern in S. engleri. The gall developmental stages are each related to specific gall-inducing instars, as gall development progresses according to the development of E. minutanus.