Revisiting the histological patterns of storage tissues: beyond the limits of gall-inducing taxa

Abstract

Gall-inducing Aphididae may feed directly on phloem, whereas Eriophyidae and Nematoda feed on cells lining the gall chambers. We assume that a variation in structural complexity will occur within galls induced by each taxon, and that the complexity of the galls could be related to the types of storage tissue they have. Histological, histometric, and histochemical analyses were used to compare six gall systems with different levels of complexity. Such levels are not taxon-related, even though eriophyid galls are usually simpler than nematode and aphid galls. The histological features of galls allowed the classification of storage tissues into three types: typical nutritive tissues (TNT), common storage tissues (CST), and nutritive-like tissues (NLT). The TNT and NLT have cells with dense cytoplasm and a prominent nucleus. The CST cells are vacuolated, and may store starch and other energy-rich molecules, as do the NLT cells. In contrast to NLT or CST, the TNT serves as a direct food source for gall inducers, and it is present in nematode and some eriophyid galls. NLTs may be present in some aphid galls, but are not the direct feeding site. The CST occurs on galls of all three inducing taxa.

Structural, histochemical and photosynthetic profiles of galls induced by Eugeniamyia dispar (Diptera, Cecidomyiidae) on the leaves of Eugenia uniflora (Myrtaceae)

“…(Piperaceae), such proteins are associated with the high metabolism and oxidative stress caused by the gall-inducing insect (Schönrogge et al, 2000;Oliveira et al, 2011b;Bragança, Oliveira, & Isaias, 2017), which also occurs with galls induced by E. dispar on E. uniflora. The starch and reducing sugars detected in the cells around the larval chamber of galls induced by E. dispar may function as energetic resources for both gall-inducing insect nutrition and maintenance of the cell machinery of the gall, as proposed for other systems (Oliveira et al, 2011a;Isaias et al, 2014;Oliveira et al, 2016;Bragança et al, 2017;Ferreira et al, 2017). Although uncommon in the nutritive tissue, starch grains have been detected in galls induced by cecidomyiids (Oliveira et al, 2011a).…”

“…Galls induced by cecidomyiids commonly develop nutritive tissues around the larval chamber (Bronner, 1992;Ferreira et al, 2017). These nutritive tissues usually store proteins and reducing sugars that may be used as food by the gall-inducing insect larva (Bronner, 1992;Oliveira, Carneiro, Magalhaes, & Isaias, 2011a;Vecchi, Menezes, Oliveira, Ferreira, & Isaias, 2013;Ferreira et al, 2017). In galls induced by species of Cecidomyiidae on leaves of Aspidosperma spruceanum Benth ex Müll.…”

“…Among the changes caused by the feeding activity of gall-inducing insects is the accumulation of primary metabolites (Bronner, 1992). Cecidomyiid galls, for example, possess a histochemical gradient associated with a large accumulation of certain primary metabolites near the larval chamber, thereby forming nutritive tissue, while others (such as starch) accumulate more distant from the larval chamber and are known as reserve tissues (Bronner, 1992;Ferreira, Álvarez, Avritzer, & Isaias, 2017). In addition to nutritive tissue formation, structural and physiological alterations, such as decreases in the amount of chlorophyllous tissues, pigment content, gas exchange, and photosynthetic rates, have been detected in gall tissues (Florentine, Raman, & Dhileepan, 2005;Oliveira et al, 2011b;Oliveira, Moreira, Isaias, Martini, & Rezende, 2017).…”

The mechanism of plant gall induction by insects: revealing clues, facts, and consequences in a cross-kingdom complex interaction

“…Tissues near the inducing insect show cytological and morphological changes that benefit its feeding process and development. This tissue, also known as "nutritive tissue", commonly presents high concentrations of sugar (Nogueira et al, 2018), lipids, proteins, nitrogen, and other nutrients that provide a continuous source of food for the insect and show intense phosphatase activity (Miles, 1968;Rohfritsch & Shorthouse, 1982;Shorthouse & Rohfritsch, 1992;Raman, 2011, Oliveira & Isaias, 2010Oliveira et al, 2011;Nabity, Haus, Berenbaum, & Delucia, 2013;Huang et al, 2015;Oates et al, 2016;Ferreira et al, 2017;Isaias et al, 2018). Typical nutritive cells show a dense cytoplasm with abundant cell organelles, fragmented vacuoles, a hypertrophied nucleus and nucleolus, and dedifferentiated plastids clustered around the nucleus, as well as chloroplasts modified to varying degrees and modified cell walls (Shorthouse & Rohfritsch, 1992;Raman, 2011;.…”

“…Typical nutritive cells show a dense cytoplasm with abundant cell organelles, fragmented vacuoles, a hypertrophied nucleus and nucleolus, and dedifferentiated plastids clustered around the nucleus, as well as chloroplasts modified to varying degrees and modified cell walls (Shorthouse & Rohfritsch, 1992;Raman, 2011;. Ferreira et al (2017) compared six gall systems with different levels of structural complexity (aphids, mites, and Nematoda), using histometric and histochemical analyses. Based on the types of storage tissue, the authors proposed a classification of three types of storage tissues: typical nutritive tissues (TNT), common storage tissues (CST), and nutritive-like tissues (NLT).…”