Influence of cell wall polymers and their modifying enzymes during plant-aphid interactions

Abstract

Aphids are a major issue for commercial crops. These pests drain phloem nutrients and transmit ~50% of the known insect-borne viral diseases. During aphid feeding, trophic structures called stylets advance toward the phloem intercellularly, disrupting cell wall polymers. It is thought that cell wall-modifying enzymes (CWMEs) present in aphid saliva facilitate stylet penetration through this intercellular polymer network. Additionally, different studies have demonstrated that host settling preference, feeding behavior, and colony performance of aphids are influenced by modulating the CWME expression levels in host plants. CWMEs have been described as critical defensive elements for plants, but also as a key virulence factor for plant pathogens. However, whether CWMEs are elements of the plant defense mechanisms or the aphid infestation process remains unclear. Therefore, in order to better consider the function of CWMEs and cell wall-derived damage-associated molecular patterns (DAMPs) during plant-aphid interactions, the present review integrates different hypotheses, perspectives, and experimental evidence in the field of plant-aphid interactions and discusses similarities to other well-characterized models such as the fungi-plant pathosystems from the host and the attacker perspectives.

Keywords: Aphid; callose; cell wall; cellulose; damage-associated molecular pattern (DAMP); hemicellulose; homogalacturonan; methanol; oligogalacturonides.

Fig. 1.

Stylet penetration through the cell wall matrix induces changes on its constituent polymers. (A) Transversal section of the head and mouthpart of an adult Myzus persicae aphid feeding on an Arabidopsis leaf. Scale bar=100 µm. (B) Close up of (A) showing the stylet bundle of M. persicae penetrating the host between epidermal cells (Ec). Scale bar=20 µm. (C) Longitudinal section of the body of an adult M. persicae aphid feeding on an Arabidopsis leaf. Scale bar=100 µm. (D) Close up of (C) showing a section of the stylet penetrating intercellularly. Scale bar=20 µm. (E) and (F) Immunolabeling of the slices shown in bright field in (C) and (D), respectively. The monoclonal antibody LM19 was used to target de-methylesterified HG (green) (Verhertbruggen et al., 2009). The images reveal a zone of HG de-methylesterification (dme-HG) surrounding the stylet pathway. Calcofluor white was applied to reveal cell walls (magenta). Scale bar=50 µm (E) and 20 µm (F).Images (A–F) were visualized with a Leica confocal microscope model TCS LSI.

Fig. 2.

Illustrative model showing the main changes described in the HG pectic domain during aphid infestation and its hypothesized defensive role. (1a) Due to the rise in global PME activity (plant PMEs plus salivary PMEs from aphids), the abundance of de-methylesterified HG increases during aphid feeding. (1b) As a product of PME activity, methanol emissions increase, possibly acting as an attractant signal or antibiotic molecule depending on its concentration and timing. (2) Due to the increase in global PL activity and the presence of PG activity in the salivary secretion of aphids, the de-methylesterified HG chains could become depolymerized, leading to the production of OGs. (3) Both methanol and OGs produced during aphid feeding could be recognized as DAMP signals by the host plant, triggering defense responses against the attacker.