Endogenous Plant Cell Wall Digestion: A Key Mechanism in Insect Evolution

Abstract

The prevailing view that insects lack endogenous enzymes for plant cell wall (PCW) digestion had led to the hypothesis that PCW digestion evolved independently in different insect taxa through the establishment of symbiotic relationships with microorganisms. However, recent studies reporting endogenous PCW-degrading genes and enzymes for several insects, including phylogenetically basal insects and closely related arthropod groups, challenge this hypothesis. Here, we summarize the molecular and biochemical evidence on the mechanisms of PCW digestion in insects to analyze its evolutionary pathways. The evidence reveals that the symbiotic-independent mechanism may be the ancestral mechanism for PCW digestion. We discuss the implications of this alternative hypothesis in the evolution of plant-insect interactions and suggest that changes in the composition of lignocellulolytic complexes were involved in the evolution of feeding habits and diet specializations in insects, playing important roles in the evolution of plant-insect interactions and in the diversification of insects.

A Salivary Endo-β-1,4-Glucanase Acts as an Effector That Enables the Brown Planthopper to Feed on Rice

“…4, B and C). NlEG1 expression in the fat body might be related to the detoxification of plant defense chemicals, as has been reported for some PCW-degrading enzymes in insects (Calderón-Cortés et al, 2012). Further research will be necessary to elucidate these roles in NlEG1.…”

“…Thus far, endogenous endob-1,4-glucanases have been reported in 16 insect orders; most belong to the GHF 9 and are expressed mainly in the salivary glands and midguts (Calderón-Cortés et al, 2012). NlEG1 also is classified as a GHF 9 protein and is most highly expressed in the midgut and salivary glands of BPH ( Fig.…”

“…Plant cell walls (PCWs), for instance, are thick, rigid structures that consist mainly of a pectin-embedded network of cellulose and hemicellulose (Calderón-Cortés et al, 2012); these structures not only act as physical defenses against herbivores by enhancing the mechanical hardness of plant tissues but also reduce the digestibility of food for herbivores (Santiago et al, 2013), thereby functioning as the first layer of defense against herbivores. Herbivores can secrete salivary PCW-degrading enzymes such as cellulases (consisting of endo-b-1,4-glucanases and b-glucosidases) and pectinases to degrade PCWs (Backus et al, 2012;Calderón-Cortés et al, 2012). Herbivores also can secrete other effectors to overcome plant defenses.…”

Horizontal gene transfer in the acquisition of novel traits by metazoans

“…Despite the fact that some authors consider some plant cell wall-degrading enzymes were present in the last common ancestor of bilaterian metazoans [55] the phylogenetic distance between the two presumptive prokaryotic donors for the HhMAN1 in H. hampei and xylanase genes in P. cochleariae suggest that these cases are bona fide examples of horizontal gene transfer in insects. Further studies will probably reveal more examples of acquired genes related to plant feeding in herbivorous Coleoptera.…”

The genome of the mustard leaf beetle encodes two active xylanases originally acquired from bacteria through horizontal gene transfer

“…These enzymes were long thought to be absent in animals, until the first endogenous cellulase from a termite was characterized [2]. Since then, endogenous genes encoding many and diverse PCWDEs have been found in other animals such as plantparasitic nematodes [3], springtails [4], mussels [5,6], bdelloid rotifers [7] and insects, particularly phytophagous beetles from the superfamilies Chrysomeloidea and Curculionoidea [8]. Interestingly, PCWDEs are absent from the genomes characterized to date of herbivorous insects and notorious crop pests from the order Lepidoptera (butterflies and moths; [9][10][11]).…”