Gene duplication and subsequent functional diversification of sucrose hydrolase in Papilio xuthus

Insect Mol Biol. 2019 Dec;28(6):862-872. doi: 10.1111/imb.12603. Epub 2019 Jun 19.

Abstract

Sucrose is the main product of photosynthesis in plants, providing a rich carbon and energy source for the physiological growth and development of insects. In a previous study, we identified a novel sucrose hydrolase (SUH) in the larval midgut of moths. Intriguingly, there are two copies of Suh, namely Suh1 and Suh2, in several species of butterflies. However, the biochemical characteristics of SUHs in butterflies remain unclear. In this study, we found that this duplication and subsequent diversification produced two Suh genes in Papilio xuthus. These two PxSuh genes were significantly divergent in terms of their expression pattern and enzyme properties. PxSuh messenger RNA expression was highest during the larval stage, reduced in the prepupal and pupal stages and, for PxSuh1, slightly increased again in the adult. The observed levels of PxSuh2 were overall below those of PxSuh1 amongst the development stages examined. Compared with PxSUH2, which has maintained the original gene function of maltose hydrolysis, PxSUH1 exhibits substrate specificity for sucrose with an optimum enzyme activity occurring at an alkaline pH. The data show that PxSuh1 is evolutionarily adapted for effective functioning in an alkaline digestive system. Furthermore, we find that functional diversification of Suh facilitates P. xuthus to digestive carbohydrate of host plants. Thus, our findings offer new insights into the ecological and evolutionary adaptation of digestive enzymes in butterflies.

Keywords: Papilio xuthus; Lepidoptera; functional divergence; gene duplication; sucrose hydrolase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Butterflies / enzymology
  • Butterflies / genetics*
  • Butterflies / growth & development
  • Gene Duplication*
  • Hydrolases / genetics*
  • Hydrolases / metabolism
  • Insect Proteins / genetics*
  • Insect Proteins / metabolism
  • Larva / enzymology
  • Larva / growth & development
  • Pupa / enzymology
  • Pupa / growth & development
  • Sucrose / metabolism*

Substances

  • Insect Proteins
  • Sucrose
  • Hydrolases