Anatomical and cytological diagnosis of phloem in insect galls

Abstract

Phloem cells transport water and photoassimilates along plant organs, as well as in neoformed organs induced by insects, the galls. The contents of phloem cells can also be the direct source of nutrition for gall inducers, as is the case of galls induced by Hemiptera. The central hypothesis of the thesis is that the feeding modes of galling insects imposes distinct modifications in the phloem with influence on the drain of photoassimilates and consequently on the differential development of galls. Our objective was to diagnose the responses of phloem cells to the feeding activity of different galling insects, in structural and ultrastructural levels, and compare the impact of galling endo- and exophytophagous insects on the phloem structure. From this perspective, and aiming to contribute to the knowledge of phloem responses to gall induction, we revised literature concerning phloem alterations, and found more studies on anatomical aspects, and the lower emphasis on researches involving immunocytochemistry, genetics, and cytology. The most common phloem response is the cell hypertrophy, predominantly in Hemiptera. Our main model of study is the economically important fruit species, Malus domestica Borkh. (Rosaceae) and the associated galling exophytophage Eriosoma lanigerum (Hausmann, 1802) (Hemiptera: Aphididae), that induces galls on roots and stems. The feeding activity of E. lanigerum influences the composition of cell walls both stem and root galls, especially concerning pectins, such as the homogalacturonans and arabinans, which are involved in parenchyma proliferation, favoring nutrient flow and water retention capacity. The xyloglucans and xylogalactorunans predominate in phloem of stem galls and can contribute to food resources to the E. lanigerum colony. In addition to the pectin composition, cytological changes in the phloem of stem galls on M. domestica favor the flow of nutritional resources toward the gall developmental site, consequently affecting the vigor of the apple trees. The changes in phloem cells of the stem galls induced by E. lanigerum were compared to endophytophage-induced galls for dormancy induced by the sap-sucking insect Pseudotectococcus rolliniae Hodgson & Gonçalves, 2004 (Hemiptera: Eriococcidae) on Annona dolabripetala Raddi (Annonaceae) and by the scraper-sucking Diptera: Cecidomyiidae in Celtis iguanaea (Jacq.) Sarg. (Cannabaceae). The hemiptera, such as E. lanigerum and P. rollinae, induced more pronounced phloem alterations in their host plants. In M. domestica, the callose in stem portion above the galls and P-protein in stem portions below the galls are two reactive responses that may interrupt the flow of photoassimilates otherwise mobilized toward the proximal region of the stem galls. In contrast in the stem galls induced by the endophytophagous P. rolliniae, the transport of photoassimilates is maintained. The maintenance of structural-functional characteristics of the phloem reveals absence of Cecidomyiidae on C. iguanae. Therefore, galls induced by hemipterans, with direct feeding on phloem cells, suffer more pronounced effects.