Loss of Sterol Biosynthesis in Economically Important Plant Pests and Pathogens: A Review of a Potential Target for Pest Control

Abstract

Sterol biosynthesis is a crucial metabolic pathway in plants and various plant pathogens. Their vital physiological role in multicellular organisms and their effects on growth and reproduction underline their importance as membrane compounds, hormone precursors, and signaling molecules. Insects, nematodes, and oomycetes of the Peronosporales group, which harbor important agricultural pests and pathogens, have lost the ability to synthesize their own sterols. These organisms rely on the acquisition of sterols from their host and are dependent on the sterol composition of the host. It is thought that sterol-synthesizing enzymes were lost during co-evolution with the hosts, which provided the organisms with sufficient amounts of the required sterols. To meet the essential requirements of these organisms, some sterol auxotrophs retained a few remaining sterol-modifying enzymes. Several molecular and biochemical investigations have suggested promising avenues for pest and pathogen control by targeting host sterol composition, sterol uptake, or sterol modification in organisms that have lost the ability to biosynthesize sterol de novo. This review examines the loss of sterol biosynthesis de novo in insects, nematodes, and oomycetes with the aim of investigating the sterol metabolic constraints and sterol acquisition of these organisms. This will shed light on its potential as a control target for the management of sterol-dependent organisms in a comprehensive agronomic approach.

Keywords: auxotroph; biochemical pathway; control strategies; insects; nematodes; oomycetes.

Figure 1

(A) Chemical structure of 5α-cholesten-3β-ol (cholesterol). Carbon numbering according to IUPAC-IUB 1989 using the sterane structure, with each ring labeled from A to D. (B) The amphipathic side chain at C-17 of phytosterol can be modified at C-24 as highlighted in green, with stigmasterol at the top, β-sitosterol in the middle, and campesterol at the bottom. (C) The crucial double bonds in the B-ring are labeled with the delta symbol (Δ).

Figure 2

Schematic representation of enzymatic steps from Acetyl-Coa leading to the Δ5 sterol biosynthetic pathway, illustrating the lanosterol (LSS, in invertebrates) biosynthesis route leading to cholesterol and the cycloartenol (CAS, in plants) biosynthesis route leading to stigmasterol. With the exception of FDFT1, farnesyl-diphosphate farnesyltransferase 1, all enzymatic abbreviations and EC numbers for vertebrate and plant enzymes are detailed in Table 1. Each enzymatic reaction is highlighted in red on the corresponding chemical structures. The first cyclic products of each sterol biosynthesis pathway, as well as the final sterols, are highlighted in bold.

Figure 3

Predicted sitosterol-to-cholesterol conversion pathway, namely the phytosterol dealkylation pathway. Each enzymatic reaction is highlighted in red on the corresponding chemical structures. The enzyme 24-dehydrocholesterol reductase (DHCR24) is the only confirmed reaction within this pathway.

Figure 4

Predicted (stellasterol)ergosterol-to-brassicasterol conversion pathway through the enzymes PcErg3 (C-5 sterol desaturase) and PcDhcr7 (Δ7-sterol reductase). Each enzymatic reaction is highlighted in red on the corresponding chemical structures.