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

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [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)

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.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
ORNL LDRD Director's R&D; USDOE
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
1356905
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 43 Vol. 113; ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)Copyright Statement
Country of Publication:
United States
Language:
English

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Orthogonal monoterpenoid biosynthesis in yeast constructed on an isomeric substrate journal August 2019
The hornwort genome and early land plant evolution journal February 2020
A Comprehensive Survey on the Terpene Synthase Gene Family Provides New Insight into Its Evolutionary Patterns journal July 2019
Oil body formation in Marchantia polymorpha is controlled by MpC1HDZ and serves as a defense against arthropod herbivores journal March 2020
Terpene Synthases as Metabolic Gatekeepers in the Evolution of Plant Terpenoid Chemical Diversity journal October 2019
Mechanistic Characterization of Two Chimeric Sesterterpene Synthases from Penicillium journal July 2017
Orthogonal monoterpenoid biosynthesis in yeast constructed on an isomeric substrate journal August 2019
The hornwort genome and early land plant evolution journal February 2020
De novo formation of an aggregation pheromone precursor by an isoprenyl diphosphate synthase-related terpene synthase in the harlequin bug journal August 2018
QM/MM free energy simulations of the reaction catalysed by ( 4S )-limonene synthase involving linalyl diphosphate (LPP) substrate journal March 2018
Emission and biosynthesis of volatile terpenoids from the plasmodial slime mold Physarum polycephalum journal January 2019
A terpene synthase-cytochrome P450 cluster in Dictyostelium discoideum produces a novel trisnorsesquiterpene journal May 2019