Co-evolution of insect proteases and plant protease inhibitors

Curr Protein Pept Sci. 2011 Aug;12(5):437-47. doi: 10.2174/138920311796391115.

Abstract

Plants are at the basis of the food chain, but there is no such thing as a "free lunch" for herbivores. To promote reproductive success, plants evolved multi-layered defensive tactics to avoid or discourage herbivory. To the detriment of plants, herbivores, in turn, evolved intricate strategies to find, eat, and successfully digest essential plant parts to raise their own offspring. In this battle the digestive tract is the arena determining final victory or defeat as measured by growth or starvation of the herbivore. Earlier, specific molecular opponents were identified as proteases and inhibitors: digestive proteases of herbivores evolved structural motifs to occlude plant protease inhibitors, or alternatively, the insects evolved proteases capable of specifically degrading the host plant inhibitors. In response plant inhibitors evolved hyper-variable and novel protein folds to remain active against potential herbivores. At the level of protease regulation in herbivorous insects, it was shown that inhibition-insensitive digestive proteases are up-regulated when sensitive proteases are inhibited. The way this regulation operates in mammals is known as negative feedback by gut-luminal factors, so-called 'monitor peptides' that are sensitive to the concentration of active enzymes. We propose that regulation of gut enzymes by endogenous luminal factors has been an open invitation to plants to "hijack" this regulation by evolving receptor antagonists, although yet these plant factors have not been identified. In future research the question of the co-evolution of insect proteases and plant inhibitors should, therefore, be better approached from a systems level keeping in mind that evolution is fundamentally opportunistic and that the plant's fitness is primarily improved by lowering the availability of essential amino acids to an herbivore by any available mechanism.

Publication types

  • Review

MeSH terms

  • Animals
  • Evolution, Molecular*
  • Gene Expression Regulation, Plant
  • Insecta / classification
  • Insecta / enzymology*
  • Peptide Hydrolases / chemistry
  • Peptide Hydrolases / metabolism*
  • Plant Proteins / chemistry
  • Plant Proteins / genetics
  • Plant Proteins / metabolism*
  • Plants / classification
  • Plants / genetics
  • Plants / metabolism*
  • Protease Inhibitors / chemistry
  • Protease Inhibitors / metabolism*
  • Structure-Activity Relationship

Substances

  • Plant Proteins
  • Protease Inhibitors
  • Peptide Hydrolases