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Identification, classification, and evolution of putative xylosyltransferases from algae

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Abstract

Xylosyltransferases (XylTs) play key roles in the biosynthesis of many different polysaccharides. These enzymes transfer d-xylose from UDP-xylose to substrate acceptors. In this study, we identified 30 XylTs from primary endosymbionts (green algae, red algae, and glaucophytes) and secondary or higher endosymbionts (brown algae, diatoms, Eustigmatophyceae, Pelagophyceae, and Cryptophyta). We performed comparative phylogenetic studies on key XylT subfamilies, and investigated the functional divergence of genes using RNA-Seq. Of the 30 XylTs, one β-1,4-XylT IRX14-related, one β-1,4 XylT IRX10L-related, and one xyloglucan 6-XylT 1-related gene were identified in the Charophyta, showing strong similarities to their land plant descendants. This implied the ancient occurrence of xylan and xyloglucan biosynthetic machineries in Charophyta. The other 27 XylTs were identified as UDP-d-xylose: l-fucose-α-1,3-d-XylT (FucXylT) type that specifically transferred d-xylose to fucose. We propose that FucXylTs originated from the last eukaryotic common ancestor, rather than being plant specific, because they are also distributed in Choanoflagellatea and Echinodermata. Considering the evidence from many aspects, we hypothesize that the FucXylTs likely participated in fucoidan biosynthesis in brown algae. We provide the first insights into the evolutionary history and functional divergence of FucXylT in algal biology.

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Funding

This work was supported by the national key research and development program of China (2018YFD0900703, 2016YFC1402102, 2018YFD0901503-8), Marine S&T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) (NO. 2018SDKJ0406-3); Financial Fund of the Ministry of Agriculture and Rural Affairs, P. R. of China (NFZX2018). Projects of International Exchange and Cooperation in Agriculture, Ministry of Agriculture and Rural Affairs of China-Science, Technology and Innovation Cooperation in Aquaculture with Tropical Countries along the Belt and Road; Shandong key Research and Development Plan (2018GHY115010); National Natural Science Foundation of China (41676145); China Agriculture Research System (CARS-50); Central Public-interest Scientific Institution Basal Research Fund, YSFRI, CAFS (20603022016001, 20603022019006); Taishan Scholars Funding of Shandong Province; Talent Projects of Distinguished Scientific Scholars in Agriculture.

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Authors and Affiliations

  1. Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, China

    Wentao Han, Xiao Fan, Linhong Teng, Xiaowen Zhang, Dong Xu & Naihao Ye

  2. Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, 201306, China

    Wentao Han

  3. Function Laboratory for Marine Fisheries Science and Food Production Processes,, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266071, China

    Wentao Han & Naihao Ye

  4. College of Life Science, Dezhou University, Dezhou, 253023, China

    Linhong Teng

  5. Biological Sciences, Flinders University, GPO Box 2100, Adelaide, SA, 5001, Australia

    Michelle Joyce Slade Kaczurowski

  6. Department of Food Science and Technology, University of Nebraska—Lincoln, Lincoln, Nebraska, USA

    Yanbin Yin

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  1. Wentao Han
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  2. Xiao Fan
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Contributions

N.Y. planned and designed the research. W.H., X.F., and L. T analyzed and interpreted the data for the work. W.H wrote the manuscript. M. J. S. K., X.D., X.Z., and Y. Y. revised it critically for important intellectual content.

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Correspondence to Naihao Ye.

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Supporting file S1

Sequence data of the 30 hits in target genomes (FASTA 18 kb)

Supporting table S1

The numbers of xylosyltransferase subfamily members found in 25 target genomes, including Glaucophyta, Cryptophyta, red algae, green algae, photosynthetic stramenopiles and non-photosynthetic oomycetes. The color indicates the count difference. The 12 xylosyltransferase’ hidden Markov models were downloaded from PANTHER (http://www.pantherdb.org). *Each subfamily belongs to the glycosyltransferase family. ** Only target proteins were counted. (XLSX 23 kb)

Supporting table S2

List of sequences used for phylogenetic analyses and their corresponding accession numbers. (XLSX 38 kb)

Supporting figure s1

Phylogeny of the xylosyltransferase domains of 225 proteins. The multiple sequence alignment of the xylosyltransferase protein domains was performed using Clustal Omega (http://www.ebi.ac.uk/Tools/msa/clustalo/). The phylogeny was constructed using the MEGA version 7.0 program (Kumar et al. 2016). Different subfamilies and GT families are represented by different colors. Black asterisks (*) denote proteins in our target genomes. (JPG 3218 kb)

Supporting figure S2

Phylogeny of the full-length IRX10L proteins. (JPG 525 kb)

Supporting figure S3

Phylogeny of the full-length IRX14 proteins. (JPG 557 kb)

Supporting figure S4

Phylogeny of the full-length XXT proteins. (JPG 640 kb)

Supporting figure S5

Phylogeny of the full-length FucXylT proteins. (JPG 1308 kb)

Supporting figure S6

Sequence identity and similarity levels among 11 FucXylT proteins. (JPG 345 kb)

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Han, W., Fan, X., Teng, L. et al. Identification, classification, and evolution of putative xylosyltransferases from algae. Protoplasma 256, 1119–1132 (2019). https://doi.org/10.1007/s00709-019-01358-2

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