The molecular structure of plant sporopollenin

Li, Fu-Shuang; Phyo, Pyae; Jacobowitz, Joseph; Hong, Mei; Weng, Jing-Ke

doi:10.1038/s41477-018-0330-7

The molecular structure of plant sporopollenin

Journal Article · Sun Dec 16 23:00:00 EST 2018 · Nature Plants (Online)

DOI:https://doi.org/10.1038/s41477-018-0330-7· OSTI ID:1617031

Li, Fu-Shuang ^[1]; ^[2]; Jacobowitz, Joseph ^[3]; Hong, Mei ^[2]; ^[3]

Whitehead Institute for Biomedical Research, Cambridge, MA (United States); Massachusetts Institute of Technology
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Whitehead Institute for Biomedical Research, Cambridge, MA (United States); Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)

Sporopollenin is a ubiquitous and extremely chemically inert biopolymer that constitutes the outer wall of all land-plant spores and pollen grains. Sporopollenin protects the vulnerable plant gametes against a wide range of environmental assaults, and is considered as a prerequisite for the migration of early plants onto land2. Despite its importance, the chemical structure of plant sporopollenin has remained elusive1. Using a newly developed thioacidolysis degradative method together with state-of-the-art solid-state NMR techniques, we determined the detailed molecular structure of pine sporopollenin. We show here that pine sporopollenin is primarily composed of aliphatic-polyketide-derived polyvinyl alcohol units and 7-O-p-coumaroylated C16 aliphatic units, crosslinked through a distinctive dioxane moiety featuring an acetal. Naringenin was also identified as a minor component of pine sporopollenin. This discovery answers the long-standing question about the chemical makeup of plant sporopollenin, laying the foundation for future explorations of sporopollenin biosynthesis and for design of new biomimetic polymers with desirable inert properties.

View Accepted Manuscript (DOE)

Research Organization:: Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: SC0001090

OSTI ID:: 1617031

Alternate ID(s):: OSTI ID: 1566613

Journal Information:: Nature Plants (Online), Journal Name: Nature Plants (Online) Journal Issue: 1 Vol. 5; ISSN 2055-0278

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (43)

Chiral discrimination of secondary alcohols by both ¹ H-NMR and HPLC after labeling with a chiral derivatization reagent, 2-(2,3-anthracenedicarboximide)cyclohexane carboxylic acid Ohtaki, Takashi; Akasaka, Kazuaki; Kabuto, Chizuko Chirality, Vol. 17, Issue S1 https://doi.org/10.1002/chir.20141	journal	January 2005
Highly Potent Chiral Labeling Reagents for the Discrimination of Chiral Alcohols* Imaizumi, Keiichirou; Terasima, Hanae; Akasaka, Kazuaki Analytical Sciences, Vol. 19, Issue 9 https://doi.org/10.2116/analsci.19.1243	journal	January 2003
Development of Highly Potent Chiral Discrimination Methods That Solve the Problems of Diastereomer Method Ohrui, Hiroshi Analytical Sciences, Vol. 24, Issue 1 https://doi.org/10.2116/analsci.24.31	journal	January 2008
The Chalcone Synthase Superfamily of Type III Polyketide Synthases Austin, Michael B.; Noel, Joseph P. ChemInform, Vol. 34, Issue 17 https://doi.org/10.1002/chin.200317284	journal	April 2003
ChemInform Abstract: TMDS as a Dual-Purpose Reductant in the Regioselective Ring Cleavage of Hexopyranosyl Acetals to Ethers. Zhang, Yin-Jie; Dayoub, Wissam; Chen, Guo-Rong ChemInform, Vol. 43, Issue 35 https://doi.org/10.1002/chin.201235215	journal	August 2012
TMDS as a Dual-Purpose Reductant in the Regioselective Ring Cleavage of Hexopyranosyl Acetals to Ethers Zhang, Yin-Jie; Dayoub, Wissam; Chen, Guo-Rong European Journal of Organic Chemistry, Vol. 2012, Issue 10 https://doi.org/10.1002/ejoc.201101682	journal	February 2012
Incorporation of Oleic Acid into Sporopollenin and Its Inhibition by the Chloroacetamide Herbicide Metazachlor Couderchet, Michel; Schmalfuß, Jochen; Böger, Peter Pesticide Biochemistry and Physiology, Vol. 55, Issue 3 https://doi.org/10.1006/pest.1996.0048	journal	July 1996
Thioacidolysis Rolando, C.; Monties, B.; Lapierre, C. Methods in Lignin Chemistry https://doi.org/10.1007/978-3-642-74065-7_23	book	January 1992
p-coumaric acid ? a monomer in the sporopollenin skeleton Wehling, K.; Niester, Ch.; Boon, J. J. Planta, Vol. 181, Issue 1 https://doi.org/10.1007/BF00202338	journal	April 1990
p-Coumaric acid ? a monomer in the sporopollenin skeleton Wehling, K.; Niester, Ch.; Boon, J. J. Planta, Vol. 179, Issue 3 https://doi.org/10.1007/bf00391083	journal	October 1989
Sporopollenin monomer biosynthesis in arabidopsis Kim, Sung Soo; Douglas, Carl J. Journal of Plant Biology, Vol. 56, Issue 1 https://doi.org/10.1007/s12374-012-0385-3	journal	February 2013
Novel p-coumaric acid esters from Pinus densiflora pollen Shibuya, Tsuyoshi; Funamizu, Makoto; Kitahara, Yoshio Phytochemistry, Vol. 17, Issue 5 https://doi.org/10.1016/S0031-9422(00)88660-4	journal	January 1978
1H NMR analysis of sporopollenin from Typha Angustifolia Ahlers, Friedhelm; Thom, Ina; Lambert, Jörg Phytochemistry, Vol. 50, Issue 6 https://doi.org/10.1016/S0031-9422(98)00225-8	journal	March 1999
Methylene spectral editing in solid-state 13C NMR by three-spin coherence selection Mao, J. -D.; Schmidt-Rohr, K. Journal of Magnetic Resonance, Vol. 176, Issue 1 https://doi.org/10.1016/j.jmr.2005.04.016	journal	September 2005
Quantitative solid-state 13C NMR with signal enhancement by multiple cross polarization Johnson, Robert L.; Schmidt-Rohr, Klaus Journal of Magnetic Resonance, Vol. 239 https://doi.org/10.1016/j.jmr.2013.11.009	journal	February 2014
Characterization of a nitrogen-rich fulvic acid and its precursor algae from solid state NMR Mao, Jingdong; Cory, Rose M.; McKnight, Diane M. Organic Geochemistry, Vol. 38, Issue 8 https://doi.org/10.1016/j.orggeochem.2007.04.005	journal	August 2007
Degradation of poly(vinyl butyral) and its stabilization by bases Liu, Rong; He, Bobing; Chen, Xian Polymer Degradation and Stability, Vol. 93, Issue 4 https://doi.org/10.1016/j.polymdegradstab.2008.01.008	journal	April 2008
Multidimensional solid-state NMR spectroscopy of plant cell walls Wang, Tuo; Phyo, Pyae; Hong, Mei Solid State Nuclear Magnetic Resonance, Vol. 78 https://doi.org/10.1016/j.ssnmr.2016.08.001	journal	September 2016
Phenols as Integrated Compounds of Sporopollenin from Pinus Pollen Schulze Osthoff, K.; Wiermann, R. Journal of Plant Physiology, Vol. 131, Issue 1-2 https://doi.org/10.1016/s0176-1617(87)80262-6	journal	November 1987
Studies on Sporopollenin Biosynthesis in Cucurbita maxima (DUCH.) — II. The Involvement of Aliphatic Metabolism Meuter-Gerhards, Andrea; Riegert, Stefanie; Wiermann, Rolf Journal of Plant Physiology, Vol. 154, Issue 4 https://doi.org/10.1016/s0176-1617(99)80279-x	journal	April 1999
Direct Determination of Hydroxymethyl Conformations of Plant Cell Wall Cellulose Using ¹ H Polarization Transfer Solid-State NMR Phyo, Pyae; Wang, Tuo; Yang, Yu Biomacromolecules, Vol. 19, Issue 5 https://doi.org/10.1021/acs.biomac.8b00039	journal	December 2017
Lignin Functionalization through Chemical Demethylation: Preparation and Tannin-Like Properties of Demethylated Guaiacyl-Type Synthetic Lignins Sawamura, Kaori; Tobimatsu, Yuki; Kamitakahara, Hiroshi ACS Sustainable Chemistry & Engineering, Vol. 5, Issue 6 https://doi.org/10.1021/acssuschemeng.7b00748	journal	May 2017
Structure and Interactions of Plant Cell-Wall Polysaccharides by Two- and Three-Dimensional Magic-Angle-Spinning Solid-State NMR Dick-Pérez, Marilú; Zhang, Yuan; Hayes, Jennifer Biochemistry, Vol. 50, Issue 6 https://doi.org/10.1021/bi101795q	journal	February 2011
The Assignment of Absolute Configuration by NMR ^† Seco, José Manuel; Quiñoá, Emilio; Riguera, Ricardo Chemical Reviews, Vol. 104, Issue 1 https://doi.org/10.1021/cr000665j	journal	January 2004
Accurate Quantification of Aromaticity and Nonprotonated Aromatic Carbon Fraction in Natural Organic Matter by ¹³ C Solid-State Nuclear Magnetic Resonance Mao, J. -D.; Schmidt-Rohr, K. Environmental Science & Technology, Vol. 38, Issue 9 https://doi.org/10.1021/es034770x	journal	May 2004
Abundant and Stable Char Residues in Soils: Implications for Soil Fertility and Carbon Sequestration Mao, J. -D.; Johnson, R. L.; Lehmann, J. Environmental Science & Technology, Vol. 46, Issue 17 https://doi.org/10.1021/es301107c	journal	August 2012
Isolation and Identification of Oligomers from Partial Degradation of Lime Fruit Cutin Tian, Shiying; Fang, Xiuhua; Wang, Weimin Journal of Agricultural and Food Chemistry, Vol. 56, Issue 21 https://doi.org/10.1021/jf801028g	journal	October 2008
Preparation, Isolation, and Characterization of Cutin Monomers and Oligomers from Tomato Peels Osman, Stanley F.; Irwin, Peter; Fett, William F. Journal of Agricultural and Food Chemistry, Vol. 47, Issue 2 https://doi.org/10.1021/jf980693r	journal	February 1999
Whole plant cell wall characterization using solution-state 2D NMR Mansfield, Shawn D.; Kim, Hoon; Lu, Fachuang Nature Protocols, Vol. 7, Issue 9 https://doi.org/10.1038/nprot.2012.064	journal	August 2012
The chalcone synthase superfamily of type III polyketide synthases Austin, Michael B.; Noel, Joseph P. Natural Product Reports, Vol. 20, Issue 1 https://doi.org/10.1039/b100917f	journal	December 2002
Environmentally benign metal triflate-catalyzed reductive cleavage of the C–O bond of acetals to ethers Zhang, Yin-Jie; Dayoub, Wissam; Chen, Guo-Rong Green Chemistry, Vol. 13, Issue 10 https://doi.org/10.1039/c1gc15636e	journal	January 2011
Non-degradative dissolution and acetylation of ball-milled plant cell walls: high-resolution solution-state NMR Lu, Fachuang; Ralph, John The Plant Journal, Vol. 35, Issue 4 https://doi.org/10.1046/j.1365-313x.2003.01817.x	journal	August 2003
Tracer Experiments on Sporopollenin Biosynthesis: An overview Gubatz, S.; Rittscher, M.; Meuter, A. Grana, Vol. 32, Issue sup001 https://doi.org/10.1080/00173139309427447	journal	January 1993
CYP704B1 Is a Long-Chain Fatty Acid ω -Hydroxylase Essential for Sporopollenin Synthesis in Pollen of Arabidopsis Dobritsa, Anna A.; Shrestha, Jay; Morant, Marc Plant Physiology, Vol. 151, Issue 2 https://doi.org/10.1104/pp.109.144469	journal	August 2009
Gradients in Wall Mechanics and Polysaccharides along Growing Inflorescence Stems Phyo, Pyae; Wang, Tuo; Kiemle, Sarah N. Plant Physiology, Vol. 175, Issue 4 https://doi.org/10.1104/pp.17.01270	journal	October 2017
High Resolution Solid State ¹³ C NMR Spectroscopy of Sporopollenins from Different Plant Taxa Guilford, William J.; Schneider, Diane M.; Labovitz, Jeffrey Plant Physiology, Vol. 86, Issue 1 https://doi.org/10.1104/pp.86.1.134	journal	January 1988
CYP703 Is an Ancient Cytochrome P450 in Land Plants Catalyzing in-Chain Hydroxylation of Lauric Acid to Provide Building Blocks for Sporopollenin Synthesis in Pollen Morant, Marc; Jørgensen, Kirsten; Schaller, Hubert The Plant Cell, Vol. 19, Issue 5 https://doi.org/10.1105/tpc.106.045948	journal	May 2007
A Novel Fatty Acyl-CoA Synthetase Is Required for Pollen Development and Sporopollenin Biosynthesis in Arabidopsis de Azevedo Souza, Clarice; Kim, Sung Soo; Koch, Stefanie The Plant Cell, Vol. 21, Issue 2 https://doi.org/10.1105/tpc.108.062513	journal	February 2009
LAP6/POLYKETIDE SYNTHASE A and LAP5/POLYKETIDE SYNTHASE B Encode Hydroxyalkyl α-Pyrone Synthases Required for Pollen Development and Sporopollenin Biosynthesis in Arabidopsis thaliana Kim, Sung Soo; Grienenberger, Etienne; Lallemand, Benjamin The Plant Cell, Vol. 22, Issue 12 https://doi.org/10.1105/tpc.110.080028	journal	December 2010
Analysis of TETRAKETIDE α-PYRONE REDUCTASE Function in Arabidopsis thaliana Reveals a Previously Unknown, but Conserved, Biochemical Pathway in Sporopollenin Monomer Biosynthesis Grienenberger, Etienne; Kim, Sung Soo; Lallemand, Benjamin The Plant Cell, Vol. 22, Issue 12 https://doi.org/10.1105/tpc.110.080036	journal	December 2010
The origin and evolution of lignin biosynthesis: Tansley review Weng, Jing-Ke; Chapple, Clint New Phytologist, Vol. 187, Issue 2 https://doi.org/10.1111/j.1469-8137.2010.03327.x	journal	June 2010
The Rise of Chemodiversity in Plants Weng, Jing-Ke; Philippe, Ryan N.; Noel, Joseph P. Science, Vol. 336, Issue 6089 https://doi.org/10.1126/science.1217411	journal	June 2012
Acetylation and Silylation of Piperidine Solubilized Sporopollenin from Pollen of Typha angustifolia L. Ahlers, Friedhelm; Lambert, Jörg; Wiermann, Rolf Zeitschrift für Naturforschung C, Vol. 58, Issue 11-12 https://doi.org/10.1515/znc-2003-11-1210	journal	December 2003

Cited By (5)

Lignin biosynthesis: old roads revisited and new roads explored Dixon, Richard A.; Barros, Jaime Open Biology, Vol. 9, Issue 12 https://doi.org/10.1098/rsob.190215	journal	December 2019
Rice pollen aperture formation is regulated by the interplay between OsINP1 and OsDAF1 Zhang, Xu; Zhao, Guochao; Tan, Qian Nature Plants, Vol. 6, Issue 4 https://doi.org/10.1038/s41477-020-0630-6	journal	April 2020
Exploiting pollen and sporopollenin for the sustainable production of microstructures Pomelli, Christian Silvio; D’Andrea, Felicia; Mezzetta, Andrea New Journal of Chemistry, Vol. 44, Issue 3 https://doi.org/10.1039/c9nj05082e	journal	January 2020
Chemical variations in Quercus pollen as a tool for taxonomic identification: Implications for long‐term ecological and biogeographical research Muthreich, Florian; Zimmermann, Boris; Birks, H. John B. Journal of Biogeography, Vol. 47, Issue 6 https://doi.org/10.1111/jbi.13817	journal	February 2020
Artificial pollen walls simulated by the tandem processes of phase separation and self‐assembly in vitro Gabarayeva, Nina I.; Grigorjeva, Valentina V.; Lavrentovich, Maxim O. New Phytologist, Vol. 225, Issue 5 https://doi.org/10.1111/nph.16318	journal	October 2019

Similar Records

The molecular structure of plant sporopollenin

Journal Article · Sun Dec 16 23:00:00 EST 2018 · Nature Plants (Online) · OSTI ID:1566613

Chemical structure of a sporinite from a lignite: Comparison with a synthetic sporinite transformed from sporopollenin

Conference · Tue Mar 31 23:00:00 EST 1987 · Prepr. Pap., Am. Chem. Soc., Div. Fuel Chem.; (United States) · OSTI ID:6396934

Chemical structure of a sporinite from a lignite: Comparison with a synthetic sporinite transformed from sporopollenin

Conference · Wed Dec 31 23:00:00 EST 1986 · OSTI ID:6387609

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
NMR

The molecular structure of plant sporopollenin

Citation Formats

References (43)

Cited By (5)

Similar Records

Related Subjects