Genome-wide analysis of ATP-binding cassette transporters sheds light on the genes related to bioactive metabolite transportation in Salvia miltiorrhiza

Abstract

Background: ATP-binding cassette (ABC) transporters have been found in plants and play important roles in metabolic transport in cells, which affect the subcellular compartmentalisation and tissue distribution of these compounds in particular. The dry roots and rhizomes of Salvia miltiorrhiza Bunge, a widely used medicinal plant, known as Danshen in traditional Chinese medicine, contain biologically active secondary metabolites of tanshinone and salvianolic acid. Given an assembled and annotated genome and a set of transcriptome data of S. miltiorrhiza, we analysed and identified the candidate genes that likely involved in the bioactive metabolite transportation of this medicinal plant, starting with the members of the ABC transporter family.Results: A total of 114 genes encoding ABC transporters were identified in the genome of S. miltiorrhiza. All the ABC genes were divided into eight subfamilies, including 3ABCA, 31ABCB, 14ABCC, 2ABCD, 1ABCE, 7ABCF, 46ABCG and 10 ABCI. Gene expressional profiling analysis revealed the tissue-specific expression profiles of these ABC transporters, particularly the highly expressed transporters in the roots of S. miltiorrhiza, which might be involved in transporting bioactive compounds of this medicinal plant. Notably, 18 genes that were highly expressed in the roots of S. miltiorrhiza were selected and verified by quantitative reverse transcription polymerase chain reaction to determine the co-expression profiling of these candidate genes with the key enzyme genes involved in the tanshinone and salvianolic acid biosynthetic pathways. Finally, three ABC genes (SMil_00020022, SMil_00010949, SMil_00027268) and one gene (SMil_00016361) might be involved in tanshinone and salvianolic acid transport in cells, respectively. In addition, the biological functions of S. miltiorrhiza ABC transporters were predicted on the basis of the phylogenetic analysis and expressional profile exploration, including the transportation of lipids, hormones, ions and primary metabolites.Conclusions: Our systematic analyses on the ABC transporters in S. miltiorrhiza provided information on ABC proteins for the first time and revealed the candidate transporters involved in the bioactive compound transportation of this medicinal plant. The genome-wide identification, transcriptome profile analysis and their phylogenetic relationships would provide a new perspective on the function of ABC transporters in S. miltiorrhiza.

Plant Secondary Metabolite Transporters: Diversity, Functionality, and Their Modulation

“…In the recent past, genome-wide studies alone or in combination with RNA-Seq analysis followed by qRT-PCR validation have been successfully implemented to predict/identify potential transporters ( Wen et al, 2020 ; Sun et al, 2021 ). In addition, co-expression analysis using known biosynthesis pathway genes also assists in identifying co-regulatory transporters ( Biala et al, 2017 ; Larsen et al, 2017b ; Yan L. et al, 2021 ). Further, several web servers such as WoLF PSORT, Cell-PLoc 2.0, and TMHMM have been commonly used for the prediction of subcellular localization and transmembrane topology ( Wen et al, 2020 ; Mackon et al, 2021 ).…”

“…In order to achieve the elevated availability of the substrate, the upregulation of biosynthetic pathway genes is one of the ways which can probably induce the respective transporters in a substrate-dependent manner. Thus, keen attention has been paid to perform co-expression studies between various transporters such as NtMATE1, NtMATE2 ( Shoji et al, 2009 ), Nt-JAT1 ( Morita et al, 2009 ), SmABCC1, SmABCG46, SmABCG40, SmABCG4 ( Yan L. et al, 2021 ), and crucial genes from biosynthesis pathways of their substrates which have consistently shown positive co-regulatory mechanisms. In addition to altering the substrate biosynthesis pathway, the exogenous supply of substrate or substrate analogs also considerably affects the activity of transporters.…”