Functional and evolutionary implications of protein and metal content of leafhopper brochosomes

Feimin Yuan; Minjing Su; Tiantian Li; Yalin Zhang; Christopher H Dietrich; Michael D Webb; Cong Wei

doi:10.1016/j.ibmb.2023.103962

Functional and evolutionary implications of protein and metal content of leafhopper brochosomes

Insect Biochem Mol Biol. 2023 Jun:157:103962. doi: 10.1016/j.ibmb.2023.103962. Epub 2023 May 11.

Authors

Feimin Yuan¹, Minjing Su¹, Tiantian Li¹, Yalin Zhang¹, Christopher H Dietrich², Michael D Webb³, Cong Wei⁴

Affiliations

¹ Key Laboratory of Plant Protection Resources and Pest Management of the Ministry of Education, College of Plant Protection, Northwest A&F University, Yangling, Shaanxi, 712100, China.
² Illinois Natural History Survey, Prairie Research Institute, University of Illinois, Champaign, IL, 61820, USA.
³ Department of Science (Insects), The Natural History Museum, Cromwell Road, South Kensington, SW7 5BD, London, UK.
⁴ Key Laboratory of Plant Protection Resources and Pest Management of the Ministry of Education, College of Plant Protection, Northwest A&F University, Yangling, Shaanxi, 712100, China. Electronic address: congwei@nwsuaf.edu.cn.

PMID: 37178742
DOI: 10.1016/j.ibmb.2023.103962

Abstract

Brochosomes derived from the specialized glandular segments of the Malpighian tubules (MTs) form superhydrophobic coatings for insects of Membracoidea, and have multiple hypothetical functions. However, the constituents, biosynthesis and evolutionary origin of brochosomes remain poorly understood. We investigated general chemical and physical characteristics of the integumental brochosomes (IBs) of the leafhopper Psammotettix striatus, determined the constituents of IBs, identified the unigenes involved in brochosomal protein synthesis, and investigated the potential associations among brochosomal protein synthesis, amino acid composition of food source, and the possible roles of endosymbionts in brochosome production. The results show that IBs are mainly composed of glycine- and tyrosine-rich proteins and some metal elements, which contain both essential and non-essential amino acids (EAAs and NEAAs) for insects, including EAAs deficient in the sole food source. All 12 unigenes involved in synthesizing the 12 brochosomal proteins (BPs) with high confidence are exclusively highly expressed in the glandular segment of MTs, confirming that brochosomes are synthesized by this segment. The synthesis of BPs is one of the key synapomorphies of Membracoidea but may be lost secondarily in a few lineages. The synthesis of BPs might be related to the symbiosis of leafhoppers/treehoppers with endosymbionts that provide these insects with EAAs, including those are deficient in the sole diet (i.e., plant sap) and could only be made available by the symbionts. We hypothesize that the functional modification of MTs have combined with the application of BPs enabling Membracoidea to colonize and adapt to novel ecological niches, and evolve to the dramatic diversification of this hemipteran group (in particular the family Cicadellidae). This study highlights the importance of evolutionary plasticity and multiple functions of MTs in driving the adaptations and evolution of sap-sucking insects of Hemiptera.

Keywords: Biosynthesis; Diversification; Evolution; Evolutionary plasticity; Hemiptera; Malpighian tubules.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Amino Acids
Animals
Hemiptera* / genetics
Plants
Symbiosis

Substances

Amino Acids