Integrative View of the Diversity and Evolution of SWEET and SemiSWEET Sugar Transporters

Baolei Jia,Zhong Ji Pu,Lu Jiang Hao,Jie Zhang,Xiao Feng Zhu,Yuan Hu Xuan,Yu Xi Duan,Li-Qing Chen,Che Ok Jeon

doi:10.3389/fpls.2017.02178

Abstract

Sugars Will Eventually be Exported Transporter (SWEET) and SemiSWEET are recently characterized families of sugar transporters in eukaryotes and prokaryotes, respectively. SemiSWEETs contain 3 transmembrane helices (TMHs), while SWEETs contain 7. Here, we performed sequence-based comprehensive analyses for SWEETs and SemiSWEETs across the biosphere. In total, 3,249 proteins were identified and ≈60% proteins were found in green plants and Oomycota, which include a number of important plant pathogens. Protein sequence similarity networks indicate that proteins from different organisms are significantly clustered. Of note, SemiSWEETs with 3 or 4 TMHs that may fuse to SWEET were identified in plant genomes. 7-TMH SWEETs were found in bacteria, implying that SemiSWEET can be fused directly in prokaryote. 15-TMH extraSWEET and 25-TMH superSWEET were also observed in wild rice and oomycetes, respectively. The transporters can be classified into 4, 2, 2, and 2 clades in plants, Metazoa, unicellular eukaryotes, and prokaryotes, respectively. The consensus and coevolution of amino acids in SWEETs were identified by multiple sequence alignments. The functions of the highly conserved residues were analyzed by molecular dynamics analysis. The 19 most highly conserved residues in the SWEETs were further confirmed by point mutagenesis using SWEET1 from Arabidopsis thaliana. The results proved that the conserved residues located in the extrafacial gate (Y57, G58, G131, and P191), the substrate binding pocket (N73, N192, and W176), and the intrafacial gate (P43, Y83, F87, P145, M161, P162, and Q202) play important roles for substrate recognition and transport processes. Taken together, our analyses provide a foundation for understanding the diversity, classification, and evolution of SWEETs and SemiSWEETs using large-scale sequence analysis and further show that gene duplication and gene fusion are important factors driving the evolution of SWEETs.

Highlights

Sugars are ubiquitous compounds that play important roles in living organisms, including involvement in osmotic regulation, cell signaling, energy storage, and carbon skeletons (Chen et al, 2015)
3 Sugars Will Eventually be Exported Transporter (SWEET) and 1 putative SemiSWEET were found in Fungi, while 2 SemiSWEETs were observed in Archaea (Hu et al, 2016)
We first performed a large-scale in silico analysis of SWEETs and SemiSWEETs, which revealed that these transporters are widely distributed in archaea, bacteria, and eukaryotes

Summary

Introduction

Sugars are ubiquitous compounds that play important roles in living organisms, including involvement in osmotic regulation, cell signaling, energy storage, and carbon skeletons (Chen et al, 2015). Organisms have evolved several mechanisms to transport sugars across membranes, and the understanding of carbohydrate transport processes that are facilitated by sugar transporters is becoming increasingly sophisticated (Lalonde et al, 2004; Chen et al, 2015). These transporters can be classified into mainly three superfamilies: major facilitator superfamily (MFS) transporters, sodium-solute symporter family (SSF) transporters, and the newly identified Sugars Will Eventually be Exported Transporters (SWEETs) and SemiSWEETs families (Chen et al, 2015). The bacterial SemiSWEETs possess 3 TMHs in total (Xuan et al, 2013)

Methods

Results

Conclusion