Morphometric analysis of young petiole galls on the narrow-leaf cottonwood, Populus angustifolia, by the sugarbeet root aphid, Pemphigus betae

Abstract

An insect-induced gall is a highly specialized structure resulting from atypical development of plant tissue induced by a reaction to the presence and activity of an insect. The insect induces a differentiation of tissues with features and functions of an ectopic organ, providing nutrition and protection to the galling insect from natural enemies and environmental stresses. In this anatomical and cytological study, we characterized how the gall-inducing aphid Pemphigus betae reshapes the leaf morphology of the narrow-leaf cottonwood Populus angustifolia to form a leaf fold gall. Young galls displayed a bend on one side of the midvein toward the center of the leaf and back to create a fold on the abaxial side of the leaf. This fold was formed abaxially by periclinal and anticlinal divisions, effectively eliminating intercellular spaces from the spongy parenchyma. Galls at this stage exhibited both cell hypertrophy and tissue hyperplasia. Cells on the adaxial surface were more numerous and smaller than cells near the abaxial surface were, creating the large fold that surrounds the insect. Mesophyll cells exhibited some features typical of nutritive cells induced by other galling insects, including conspicuous nucleolus, reduced and fragmented vacuole, smaller and degraded chloroplasts, and dense cytoplasm compared to ungalled tissue. Even though aphids feed on the contents of phloem and do not directly consume the gall tissue, they induce changes in the plant vascular system, which lead to nutrient accumulation to support the growing aphid numbers in mature galls.

Physiological response of Populus nigra ‘Italica’ to galling aphids feeding

“…A histological study of Pemphigus betae Doane leaf galls induced on Populus angustifolia (James) demonstrated modified structure of vascular bundles that facilitate aphid access to the phloem, eliminating the need for stylet penetration into or around cells (Richardson et al . 2017).…”

“…2012; Richardson et al . 2017; Kmieć et al . 2018; Kot & Kmieć 2020).…”

Insect Gallers and Their Plant Hosts: From Omics Data to Systems Biology

“…The nutritive tissue is organelle-rich, frequently including visible nucleoli, enlarged or fragmented vacuoles, dense cytoplasm, and high numbers of Golgi apparatus, endoplasmic reticulum, and ribosomes, which are traits indicative of the high metabolic status of these cells [17,18,19,20]. Secondly, this tissue comprises high concentrations of lipids, proteins, and carbohydrates, which supports its function as an enhanced source of nutrition to the developing insect [21,22]. …”

Oviposition of the Gall Wasp Leptocybe Invasa (Hymenoptera: Eulophidae) and Morphological Changes in Eucalyptus Spp. Genotypes Susceptible

“…Galls are alterations of plant tissues caused by gall-inducing stimuli contained in saliva injected during feeding by aphids, in maternal secretions injected during oviposition of sawflies, in larval secretions of unknown origin from cynipid galls wasps (ALMADA;FERNANDES 2011;RICHARDSON et al 2017). It causes cell hypertrophy and tissue hyperplasia (FERREIRA;MAGALHÃES et al 2014), responsible for the various structural gall shapes (ISAIAS et al 2013(ISAIAS et al , 2015.…”