title: Molecular evolutionary mechanisms driving functional diversification of α-glucosidase in Lepidoptera.
abstract: The digestive tract of lepidopteran insects is unique given its highly alkaline pH. The adaptive plasticity of digestive enzymes in this environment is crucial to the highly-efficient nutritional absorption in Lepidoptera. However, little is known about the molecular adaptation of digestive enzymes to this environment. Here, we show that lepidopteran α-glucosidase, a pivotal digestive enzyme, diverged into sucrose hydrolase (SUH) and other maltase subfamilies. SUH, which is specific for sucrose, was only detected in Lepidoptera. It suggests that lepidopteran insects have evolved an enhanced ability to hydrolyse sucrose, their major energy source. Gene duplications and exon-shuffling produced multiple copies of α-glucosidase in different microsyntenic regions. Furthermore, SUH showed significant functional divergence (FD) compared with maltase, which was affected by positive selection at specific lineages and codons. Nine sites, which were involved in both FD and positive selection, were located around the ligand-binding groove of SUH. These sites could be responsible for the ligand-binding preference and hydrolytic specificity of SUH for sucrose, and contribute to its conformational stability. Overall, our study demonstrated that positive selection is an important evolutionary force for the adaptive diversification of α-glucosidase, and for the exclusive presence of membrane-associated SUHs in the unique lepidopteran digestive tract.
authors.affiliation: College of Animal Sciences, Zhejiang University, Hangzhou 310058, China.
authors.forename: Xiaotong
authors.initials: X
authors.lastname: Li
authors.affiliation: College of Animal Sciences, Zhejiang University, Hangzhou 310058, China.
authors.forename: Liangen
authors.initials: L
authors.lastname: Shi
authors.affiliation: College of Animal Sciences, Zhejiang University, Hangzhou 310058, China.
authors.forename: Yanyan
authors.initials: Y
authors.lastname: Zhou
authors.affiliation: College of Animal Sciences, Zhejiang University, Hangzhou 310058, China.
authors.forename: Hongqing
authors.initials: H
authors.lastname: Xie
authors.affiliation: College of Animal Sciences, Zhejiang University, Hangzhou 310058, China.
authors.forename: Xiangping
authors.initials: X
authors.lastname: Dai
authors.affiliation: College of Animal Sciences, Zhejiang University, Hangzhou 310058, China.
authors.forename: Rongqiao
authors.initials: R
authors.lastname: Li
authors.affiliation: College of Animal Sciences, Zhejiang University, Hangzhou 310058, China.
authors.forename: Yuyin
authors.initials: Y
authors.lastname: Chen
authors.affiliation: College of Animal Sciences, Zhejiang University, Hangzhou 310058, China.
authors.forename: Huabing
authors.initials: H
authors.lastname: Wang
mesh_terms: D000818:Animals; D019143:Evolution, Molecular; D005091:Exons; D020440:Gene Duplication; D006867:Hydrolases / Q000235:genetics; D007438:Introns; D007915:Lepidoptera / Q000235:genetics; D010802:Phylogeny; D017434:Protein Structure, Tertiary; D012641:Selection, Genetic; D000520:alpha-Glucosidases / Q000235:genetics*
chemical_list: D006867:Hydrolases; D000520:alpha-Glucosidases