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

Abstract

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.

Alterations induced by Tortrimosaica polypodivora on the stems of Microgramma vacciniifolia: simple or complex galls?

“…The anatomical alterations induced by Tortrimosaica polypodivora in the stems of Microgramma squamulosa were described by Kraus et al (1993), including maintaining a layer of cells with meristematic features lining the gall chamber. This feature is commonly reported for galls induced by Lepidoptera on the leaves and stems of angiosperms, reported as nutritive tissues with lipid accumulation (Bedetti et al 2013;Vecchi et al 2013;Ferreira et al 2015Ferreira et al , 2022Rezende et al 2019;Guedes et al 2023). Other alterations reported for T. polypodivora-M. squamulosa galls include increased pericycle cell layers in the meristeles and sclereid-like cells lining the larval chambers in the galls in the final stages.…”

“…Histometric comparisons confirmed the occurrence of hyperplasia in the cortex and pericycle, cell hypotrophy in the pith cells, and hypertrophy in the width of the scales. SG revealed simple structural alterations, but the histochemical gradients demonstrated that despite maintaining the types of substances stored in the stem, the galling organism potentiates and induces the redistribution of the accumulated lipids and reducing sugars toward the larval chamber, essential for nutrition, as observed in other lepidopteran-induced galls (Bedetti et al 2013;Vecchi et al 2013;Rezende et al 2019;Ferreira et al 2019Ferreira et al , 2022. However, some compounds were not found in the nutritive tissues in all Lepidoptera galls, such as proteins and starch, demonstrating that the specific metabolism of the host species is essential for determining the histochemical features in nutritive cells (Guedes et al 2023).…”

“…DC. (Melastomataceae) (Rezende et al 2019), Schinus engleri F.A.Barkley (Ferreira et al 2022), and Schinus polygama (Cav.) Cabrera (Anacardiaceae) (Guedes et al 2023), while starch was only reported in the galls of Parthenium hyserophorus L. (Asteraceae) (Raman & Dhileepan 1999), reinforcing that the metabolic features of the host plants are essential in determining gall chemical features (Guedes et al 2023).…”

“…Despite the changes Kraus et al (1993) reported, which indicated a few changes in the stem organization, histochemical and histometric studies were not performed. Such kind of analyses were complementary in gall structural studies to understand other induced alterations, such as the differential accumulation of reserves in the nutritive tissues lining the gall chamber and the phenomena of cell hypertrophy and hyperplasia leading to gall formation, as reported in lepidopteran-angiosperm galls Bedetti et al 2013;Vecchi et al 2013;Ferreira et al 2015Ferreira et al , 2022Rezende et al 2019).…”

Can Molecularly Engineered Plant Galls Help to Ease the Problem of World Food Shortage (and Our Dependence on Pollinating Insects)?

“…This was shown using 14 C-labelling by Inbar et al [ 25 ], who studied galls formed on Pistacia palaestina by aphids of the family Pemphigidae. Starch, sugars and many other chemicals are being diverted from the phloem of the surrounding plant parts to the benefit of the developing insect [ 26 ]. Defensive low molecular weight phenolic substances present in the leaves of, for example, willows such as Salix spp.…”