How eriophyid mites shape metal metabolism in leaf galls on Tilia cordata

Abstract

Introduction

Galls are remarkable examples of biochemical, physiological and morphological changes in plant organs induced by various organisms, including bacteria, fungi, nematodes and arthropods (Mani, 2013; Ferreira et al., 2019). The mechanisms of gall induction and development, especially those induced by arthropods, are not well understood, and many questions remain open (reviewed by Harris & Pitzschke, 2020). The evolutionary advantage of producing galls can be explained by three main hypotheses: the nutritional hypothesis stating that galls provide high-quality nutrient-rich tissue available directly to the galler over the whole associated life cycle; the protection (enemy) hypothesis stating that galls provide a safe place against biotic stress such as predators and pathogens; and the microenvironment hypothesis stating that galls protect the gallers from abiotic stress (temperature, UV radiation, etc.) allowing optimal conditions for reproduction and growth (Price et al., 1987; Stone & Schönrogge, 2003; Harris & Pitzschke, 2020).

Arthropod-induced galls can have different anatomical features, from simple tissue swelling, to complex, fascinating neoformed structures (Larew, 1981; Mani, 2013; Ferreira et al., 2019). Most galling-inducing arthropods are highly host-specific and often limited to one tissue type, such as leaf bud, stem or roots (Rohfritsch, 1992). Galls are induced by active compounds, cecidogens, excreted during feeding (saliva) or oviposition (Raman, 2011). Although the exact mechanisms of gall initiation and development are not fully known, some active molecules have been identified, including hormones, effector proteins and small RNAs (Little et al., 2007; Petanović & Kielkiewicz, 2010a; Medina et al., 2017; Harris & Pitzschke, 2020). Accumulation of growth-regulating hormones contributes to morphological changes (cell hypertrophy and tissue hyperplasia) during gall development (Petanović & Kielkiewicz, 2010b; Giron et al., 2016; Oliveira et al., 2016; Harris & Pitzschke, 2020).

The chemical composition of the galls differs from the surrounding host tissue, and it is manipulated to benefit the galler. Most of the studies on gall chemical modifications investigated the accumulation and distribution of primary and secondary metabolites. Galls developing on photosynthetically active tissues act as newly formed sinks, with inhibited photosynthetic activity but with the active import of photoassimilates (Zorić et al., 2019; Jiang et al., 2021). Tissue-specific accumulation of phenolic compounds has been observed as well, mostly in the outer layers of the galls with decreased content in the nutritive tissue, as well as increased lignification (in line with their antioxidative properties and structural support, respectively; Nyman & Julkunen-Tiitto, 2000; Guedes et al., 2019).

However, although essential for all organisms, the metabolism of macro- and micronutrients in plant–galler interactions remains underexplored. Transition metals (Fe, Cu, Zn, Ni, Mn and Mo) are required for plant (and arthropod) development and survival. They have a broad range of functions in overall metabolism, including gene regulation, post-translational protein modifications, enzyme activation and redox reactions (Andresen et al., 2018; He et al., 2021; Arriola et al., 2024). Among the available literature, the majority is related to measuring the total metal concentrations in the galls (e.g. Bagatto & Shorthouse, 1991, 1994a; Arriola et al., 2024). Mineral distribution in insect galls has been demonstrated in only a few studies so far, not quantitatively because of the methods used, and without deeper insight into their functional role, transport or binding (Bagatto & Shorthouse, 1994b; Anand & Ramani, 2021).

Highly specialised mites (genera from families Phytoptidae and Eriophyidae) can induce galls in different organs – leaves, buds, stems or fruits – by feeding (Chetverikov et al., 2015). These mites are economically important pests of crops (apple, pear, walnut, cherries, maple and grapevine), grasses and ornamental crops, including plants in urban ecosystems such as linden, poplar, willow, ash, alder and elm. They can considerably affect crop physiology and production (De Lillo et al., 2018; Jiang et al., 2021). The type of mite leaf galls varies from erinea (felt-like masses due to abnormal hair development), blister galls (pocket or warty galls), to marginal leaf roll galls, vein galls and nail (pouch) galls (Westphal & Manson, 1996). The mechanisms of eriophyid mite gall formation and their interaction with the host are not well documented. It is known that gall initiation is triggered by the saliva of overwintering female eriophyid mites (Petanović & Kielkiewicz, 2010a,b; Chetverikov et al., 2015). These deutogyne females overwinter beneath the bud scales. They start feeding and inducing galls for laying eggs in emerging leaves in early spring. Inside the galls, several generations of male and female mites are present during summer, but in early autumn overwintering females are produced, which will not lay eggs until the spring of the following year. Early mite gall development includes intense proliferation of epidermal cells and de-differentiation of cells from parenchyma to meristematic cells. With gall maturation the proliferation decreases, and lignification occurs (Petanović & Kielkiewicz, 2010a,b; Chetverikov et al., 2015).

Recent reports show that trace metals (e.g. Zn, Fe) are essential in plant–pathogen interactions. The mechanisms of metal-based immunity involve metalloproteins, low molecular weight (LMW) ligands and phytohormone accumulation (Morina et al., 2021; Morina & Küpper, 2022; Kuvelja et al., 2024). We hypothesise that micronutrients have an important role in plant response to the galler and gall development and that micronutrients have differential tissue distribution in the galls related to their function to accommodate the needs of the mites. This is different from the defence response to pathogens because gallers can hijack the plant proteasome, minimise/manipulate the defence responses of the host and suppress the immune system (Ithal et al., 2007; Tooker et al., 2008).