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Title: Microbial-type terpene synthase genes occur widely in nonseed land plants, but not in seed plants

Abstract

Here, the vast abundance of terpene natural products in nature is due to enzymes known as terpene synthases (TPSs) that convert acyclic prenyl diphosphate precursors into a multitude of cyclic and acyclic carbon skeletons. Yet the evolution of TPSs is not well understood at higher levels of classification. Microbial TPSs from bacteria and fungi are only distantly related to typical plant TPSs, whereas genes similar to microbial TPS genes have been recently identified in the lycophyte Selaginella moellendorffii. The goal of this study was to investigate the distribution, evolution, and biochemical functions of microbial terpene synthase-like (MTPSL) genes in other plants. By analyzing the transcriptomes of 1,103 plant species ranging from green algae to flowering plants, putative MTPSL genes were identified predominantly from nonseed plants, including liverworts, mosses, hornworts, lycophytes, and monilophytes. Directed searching for MTPSL genes in the sequenced genomes of a wide range of seed plants confirmed their general absence in this group. Among themselves, MTPSL proteins from nonseed plants form four major groups, with two of these more closely related to bacterial TPSs and the other two to fungal TPSs. Two of the four groups contain a canonical aspartate-rich “DDxxD” motif. The third group has a “DDxxxD”more » motif, and the fourth group has only the first two “DD” conserved in this motif. Upon heterologous expression, representative members from each of the four groups displayed diverse catalytic functions as monoterpene and sesquiterpene synthases, suggesting these are important for terpene formation in nonseed plants.« less

Authors:
 [1];  [2];  [3];  [4];  [1];  [1];  [5];  [6]; ORCiD logo [7];  [8];  [8];  [8];  [9];  [9];  [10];  [11];  [12]; ORCiD logo [13];  [3];  [1]
  1. Univ. of Tennessee, Knoxville, TN (United States)
  2. Univ. of Tennessee, Knoxville, TN (United States); Shaanxi Normal Univ., Xian (China)
  3. Max Planck Institute for Chemical Ecology, Jena (Germany)
  4. Univ. of Tennessee, Knoxville, TN (United States); Chinese Academy of Agricultural Sciences, Hangzhou (China)
  5. Southern Illinois Univ., Carbondale, IL (United States)
  6. Monash Univ., Melbourne, VIC (Australia)
  7. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  8. Beijing Genomics Institute - Shenzhen, Shenzhen (China)
  9. Univ. of California, Berkeley, CA (United States)
  10. Uppsala Univ., Uppsala (Sweden)
  11. Univ. of British Columbia, Vancouver, BC (Canada)
  12. New York Botanical Garden, Bronx, NY (United States)
  13. Beijing Genomics Institute - Shenzhen, Shenzhen (China); Univ. of Alberta, Edmonton, AB (Canada)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Laboratory Directed Research and Development (LDRD) Program
OSTI Identifier:
1356905
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 113; Journal Issue: 43; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; terpene synthase; specialized metabolism; nonseed plant; gene evolution

Citation Formats

Jia, Qidong, Li, Guanglin, Köllner, Tobias G., Fu, Jianyu, Chen, Xinlu, Xiong, Wangdan, Crandall-Stotler, Barbara J., Bowman, John L., Weston, David J., Zhang, Yong, Chen, Li, Xie, Yinlong, Li, Fay -Wei, Rothfels, Carl J., Larsson, Anders, Graham, Sean W., Stevenson, Dennis W., Wong, Gane Ka-Shu, Gershenzon, Jonathan, and Chen, Feng. Microbial-type terpene synthase genes occur widely in nonseed land plants, but not in seed plants. United States: N. p., 2016. Web. doi:10.1073/pnas.1607973113.
Jia, Qidong, Li, Guanglin, Köllner, Tobias G., Fu, Jianyu, Chen, Xinlu, Xiong, Wangdan, Crandall-Stotler, Barbara J., Bowman, John L., Weston, David J., Zhang, Yong, Chen, Li, Xie, Yinlong, Li, Fay -Wei, Rothfels, Carl J., Larsson, Anders, Graham, Sean W., Stevenson, Dennis W., Wong, Gane Ka-Shu, Gershenzon, Jonathan, & Chen, Feng. Microbial-type terpene synthase genes occur widely in nonseed land plants, but not in seed plants. United States. doi:10.1073/pnas.1607973113.
Jia, Qidong, Li, Guanglin, Köllner, Tobias G., Fu, Jianyu, Chen, Xinlu, Xiong, Wangdan, Crandall-Stotler, Barbara J., Bowman, John L., Weston, David J., Zhang, Yong, Chen, Li, Xie, Yinlong, Li, Fay -Wei, Rothfels, Carl J., Larsson, Anders, Graham, Sean W., Stevenson, Dennis W., Wong, Gane Ka-Shu, Gershenzon, Jonathan, and Chen, Feng. Mon . "Microbial-type terpene synthase genes occur widely in nonseed land plants, but not in seed plants". United States. doi:10.1073/pnas.1607973113. https://www.osti.gov/servlets/purl/1356905.
@article{osti_1356905,
title = {Microbial-type terpene synthase genes occur widely in nonseed land plants, but not in seed plants},
author = {Jia, Qidong and Li, Guanglin and Köllner, Tobias G. and Fu, Jianyu and Chen, Xinlu and Xiong, Wangdan and Crandall-Stotler, Barbara J. and Bowman, John L. and Weston, David J. and Zhang, Yong and Chen, Li and Xie, Yinlong and Li, Fay -Wei and Rothfels, Carl J. and Larsson, Anders and Graham, Sean W. and Stevenson, Dennis W. and Wong, Gane Ka-Shu and Gershenzon, Jonathan and Chen, Feng},
abstractNote = {Here, the vast abundance of terpene natural products in nature is due to enzymes known as terpene synthases (TPSs) that convert acyclic prenyl diphosphate precursors into a multitude of cyclic and acyclic carbon skeletons. Yet the evolution of TPSs is not well understood at higher levels of classification. Microbial TPSs from bacteria and fungi are only distantly related to typical plant TPSs, whereas genes similar to microbial TPS genes have been recently identified in the lycophyte Selaginella moellendorffii. The goal of this study was to investigate the distribution, evolution, and biochemical functions of microbial terpene synthase-like (MTPSL) genes in other plants. By analyzing the transcriptomes of 1,103 plant species ranging from green algae to flowering plants, putative MTPSL genes were identified predominantly from nonseed plants, including liverworts, mosses, hornworts, lycophytes, and monilophytes. Directed searching for MTPSL genes in the sequenced genomes of a wide range of seed plants confirmed their general absence in this group. Among themselves, MTPSL proteins from nonseed plants form four major groups, with two of these more closely related to bacterial TPSs and the other two to fungal TPSs. Two of the four groups contain a canonical aspartate-rich “DDxxD” motif. The third group has a “DDxxxD” motif, and the fourth group has only the first two “DD” conserved in this motif. Upon heterologous expression, representative members from each of the four groups displayed diverse catalytic functions as monoterpene and sesquiterpene synthases, suggesting these are important for terpene formation in nonseed plants.},
doi = {10.1073/pnas.1607973113},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 43,
volume = 113,
place = {United States},
year = {2016},
month = {10}
}

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    Works referencing / citing this record:

    The hornwort genome and early land plant evolution
    journal, February 2020