The evolution of the phenylpropanoid pathway entailed pronounced radiations and divergences of enzyme families.
evo-physio
evolution of gene families
phenylpropanoid biosynthesis
plant evolution
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
revised:
11
06
2021
received:
26
01
2021
accepted:
21
06
2021
pubmed:
25
6
2021
medline:
28
12
2021
entrez:
24
6
2021
Statut:
ppublish
Résumé
Land plants constantly respond to fluctuations in their environment. Part of their response is the production of a diverse repertoire of specialized metabolites. One of the foremost sources for metabolites relevant to environmental responses is the phenylpropanoid pathway, which was long thought to be a land-plant-specific adaptation shaped by selective forces in the terrestrial habitat. Recent data have, however, revealed that streptophyte algae, the algal relatives of land plants, have candidates for the genetic toolkit for phenylpropanoid biosynthesis and produce phenylpropanoid-derived metabolites. Using phylogenetic and sequence analyses, we here show that the enzyme families that orchestrate pivotal steps in phenylpropanoid biosynthesis have independently undergone pronounced radiations and divergence in multiple lineages of major groups of land plants; sister to many of these radiated gene families are streptophyte algal candidates for these enzymes. These radiations suggest a high evolutionary versatility in the enzyme families involved in the phenylpropanoid-derived metabolism across embryophytes. We suggest that this versatility likely translates into functional divergence, and may explain the key to one of the defining traits of embryophytes: a rich specialized metabolism.
Substances chimiques
Enzymes
0
Phenylpropionates
0
Plant Proteins
0
Cytochrome P-450 Enzyme System
9035-51-2
Alcohol Oxidoreductases
EC 1.1.-
cinnamyl alcohol dehydrogenase
EC 1.1.1.195
Methyltransferases
EC 2.1.1.-
caffeoyl-CoA O-methyltransferase
EC 2.1.1.104
Phenylalanine Ammonia-Lyase
EC 4.3.1.24
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
975-1002Informations de copyright
© 2021 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Amborella Genome Project (2013) The Amborella genome and the evolution of flowering plants. Science, 342, 1241089.
Argout, X., Salse, J., Aury, J.-M., Guiltinan, M.J., Droc, G., Gouzy, J. et al. (2011) The genome of Theobroma cacao. Nature Genetics, 43, 101-108.
Aschauer, P., Rengachari, S., Lichtenegger, J., Schittmayer, M., Das, K. M., Mayer, N. et al. (2016) Crystal structure of the Saccharomyces cerevisiae monoglyceride lipase Yju3p. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, 1861, 462-470. https://doi.org/10.1016/j.bbalip.2016.02.005
Baedecker, M. & Schulz, G.E. (2002) Structures of two histidine ammonia-lyase modifications and implications for the catalytic mechanism. European Journal of Biochemistry, 269, 1790-1797.
Banks, J.a., Nishiyama, T., Hasebe, M., Bowman, J.l., Gribskov, M., dePamphilis, C. et al. (2011) The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science, 332, 960-963.
Barakat, A., Bagniewska-Zadworna, A., Choi, A., Plakkat, U., DiLoreto, D.S., Yellanki, P. et al. (2009) The cinnamyl alcohol dehydrogenase gene family in Populus: phylogeny, organization, and expression. BMC Plant Biology, 9, 26.
Barakate, A., Stephens, J., Goldie, A., Hunter, W.N., Marshall, D., Hancock, R.D. et al. (2011) Syringyl lignin is unaltered by severe sinapyl alcohol dehydrogenase suppression in tobacco. The Plant Cell, 23, 4492-4506.
Barros, J. & Dixon, R.A. (2020) Plant phenylalanine/tyrosine ammonia-lyases. Trends in Plant Science, 25, 66-79.
Barros, J., Serrani-Yarce, J.C., Chen, F., Baxter, D., Venables, B.J. & Dixon, R.A. (2016) Role of bifunctional ammonia-lyase in grass cell wall biosynthesis. Nature Plants, 2, 16050.
Bednarek, P., Schneider, B., Svatoš, A., Oldham, N.J. & Hahlbrock, K. (2005) Structural complexity, differential response to infection, and tissue specficity of indolic and phenylpropanoid secondary metabolism in Arabidopsis roots. Plant Physiology, 138, 1058-1070.
Berens, M.L., Berry, H.M., Mine, A., Argueso, C.T. & Tsuda, K. (2017) Evolution of hormone signaling networks in plant defense. Annual Review of Phytopathology, 55, 401-425.
Berland, H., Albert, N.W., Stavland, A., Jordheim, M., McGhie, T.K., Zhou, Y. et al. (2019) Auronidins are a previously unreported class of flavonoid pigments that challenges when anthocyanin biosynthesis evolved in plants. Proceedings of the National Academy of Sciences of the United States of America, 116, 20232-20239.
Blanc, G., Agarkova, I., Grimwood, J., Kuo, A., Brueggeman, A., Dunigan, D.D. et al. (2012) The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation. Genome Biology, 13, R39.
Blázquez, M.A., Nelson, D.C. & Weijers, D. (2020) Evolution of plant hormone response pathways. Annual Review of Plant Biology, 71, 327-353.
Booij-James, I.S., Dube, S.K., Jansen, M.A.K., Edelman, M. & Mattoo, A.K. (2000) Ultraviolet-B radiation impacts light-mediated turnover of the photosystem II reaction center heterodimer in Arabidopsis mutants altered in phenolic metabolism. Plant Physiology, 124, 1275-1284.
Bowman, J.L., Kohchi, T., Yamato, K.T., Jenkins, J., Shu, S., Ishizaki, K. et al. (2017) Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell, 171, 287-304.
Byeon, Y., Lee, H.J., Lee, H.Y. & Back, K. (2016) Cloning and functional characterization of the Arabidopsis N-acetylserotonin O-methyltransferase responsible for melatonin synthesis. Journal of Pineal Research, 60, 65-73.
Carella, P., Gogleva, A., Hoey, D.J., Bridgen, A.J., Stolze, S.C., Nakagami, H. et al. (2019) Conserved biochemical defenses underpin host responses to oomycete infection in an early-divergent land plant lineage. Current Biology, 29, 2282-2294.e5.
Cheng, S., Xian, W., Fu, Y., Marin, B., Keller, J., Wu, T. et al. (2019) Genomes of subaerial Zygnematophyceae provide insights into land plant evolution. Cell, 179, 1057-1067.e14.
Chezem, W.R., Memon, A., Li, F.-S., Weng, J.-K. & Clay, N.K. (2017) SG2-type R2R3-MYB transcription factor MYB15 controls defense-induced lignification and basal immunity in Arabidopsis. The Plant Cell, 29, 1907-1926.
Clayton, W.A., Albert, N.W., Thrimawithana, A.H., McGhie, T.K., Deroles, S.C., Schwinn, K.E. et al. (2018) UVR8-mediated induction of flavonoid biosynthesis for UVB tolerance is conserved between the liverwort Marchantia polymorpha and flowering plants. The Plant Journal, 96, 503-517.
Costa, M.A., Bedgar, D.L., Moinuddin, S.G.A., Kim, K.-W., Cardenas, C.L., Cochrane, F.C. et al. (2005) Characterization in vitro and in vivo of the putative multigene 4-coumarate:CoA ligase network in Arabidopsis: syringyl lignin and sinapate/sinapyl alcohol derivative formation. Phytochemistry, 66, 2072-2091.
Danielsson, M., Lundén, K., Elfstrand, M., Hu, J., Zhao, T., Arnerup, J. et al. (2011) Chemical and transcriptional responses of Norway spruce genotypes with different susceptibility to Heterobasidion spp. infection. BMC Plant Biology, 11, 154.
D'Auria, J.C. (2006) Acyltransferases in plants: a good time to be BAHD. Current Opinion in Plant Biology, 9, 331-340.
de Azevedo Souza, C., Kim, S.S., Koch, S., Kienow, L., Schneider, K., McKim, S.M. et al. (2009) A novel fatty acyl-CoA synthetase is required for pollen development and sporopollenin biosynthesis in Arabidopsis. The Plant Cell, 21, 507-525.
De Clerck, O., Kao, S.-M., Bogaert, K.A., Blomme, J., Foflonker, F., Kwantes, M. et al. (2018) Insights into the evolution of multicellularity from the sea lettuce genome. Current Biology, 28, 2921-2933.e2925.
de Vries, J. & Archibald, J.M. (2018) Plant evolution: landmarks on the path to terrestrial life. New Phytologist, 217, 1428-1434.
de Vries, J., Curtis, B.A., Gould, S.B. & Archibald, J.M. (2018) Embryophyte stress signaling evolved in the algal progenitors of land plants. Proceedings of the National Academy of Sciences of the United States of America, 115, E3471-E3480.
de Vries, J., de Vries, S., Curtis, B.A., Zhou, H., Penny, S., Feussner, K. et al. (2020) Heat stress response in the closest algal relatives of land plants reveals conserved stress signalling circuits. The Plant Journal, 103, 1025-1048.
de Vries, J., de Vries, S., Slamovits, C.H., Rose, L.E. & Archibald, J.M. (2017) How embryophytic is the biosynthesis of phenylpropanoids and their derivatives in streptophyte algae? Plant and Cell Physiology, 58, 934-945.
de Vries, J. & Ischebeck, T. (2020) Ties between stress and lipid droplets pre-date seeds. Trends in Plant Science, 12, 1203-1214.
de Vries, S., Herrfurth, C., Li, F.-W., Feussner, I. & de Vries, J. (2021) An ancient route towards salicylic acid and its implications for the perpetual Trichormus-Azolla symbiosis. bioRxiv preprint https://doi.org/10.1101/2021.03.12.435107
Delwiche, C.F., Graham, L.E. & Thomson, N. (1989) Lignin-like compounds and sporopollenin in Coleochaete, an algal model for land plant ancestry. Science, 245, 399-401.
Devic, M., Guilleminot, J., Debeaujon, I., Bechtold, N., Bensaude, E., Koornneef, M. et al. (1999) The BANYULS gene encodes a DFR-like protein and is a marker of early seed coat development. The Plant Journal, 19, 387-398.
Dixon, R.A., Achnine, L., Kota, P., Liu, C.-J., Srinivasa Reddy, M.S. & Wang, L. (2002) The phenylpropanoid pathway and plant defence-a genomics perspective. Molecular Plant Pathology, 3, 371-390.
Dixon, R.A. & Paiva, N.L. (1995) Stress-induced phenylpropanoid metabolism. The Plant Cell, 7, 1085-1097.
Do, C.-T., Pollet, B., Thévenin, J., Sibout, R., Denoue, D., Barrière, Y. et al. (2007) Both caffeoyl coenzyme A 3-O-methyltransferase 1 and caffeic acid O-methyltransferase 1 are involved in redundant functions for lignin, flavonoids and sinapoyl malate biosynthesis in Arabidopsis. Planta, 226, 1117-1129.
Ehlting, J., Büttner, D., Wang, Q., Douglas, C.J., Somssich, I.E. & Kombrink, E. (1999) Three 4-coumarate:coenzyme A ligases in Arabidopsis thaliana represent two evolutionarily divergent classes in angiosperms. The Plant Journal, 19, 9-20.
Emiliani, G., Fondi, M., Fani, R. & Gribaldo, S. (2009) A horizontal gene transfer at the origin of phenylpropanoid metabolism: a key adaptation of plants to land. Biology Direct, 4, 7.
Eudes, A., Pereira, J.H., Yogiswara, S., Wang, G., Benites, V.T., Baidoo, E.E.K. et al. (2016) Exploiting the substrate promiscuity of hydroxycinnamoyl-CoA: shikimate hydroxycinnamoyl transferase to reduce lignin. Plant and Cell Physiology, 57, 568-579.
Fellenberg, C., Milkowski, C., Hause, B., Lange, P.-R., Böttcher, C., Schmidt, J. et al. (2008) Tapetum-specific location of a cation-dependent O-methyltransferase in Arabidopsis thaliana. The Plant Journal, 56, 132-145.
Ferrer, J.L., Zubieta, C., Dixon, R.A. & Noel, J.P. (2005) Crystal structures of alfalfa caffeoyl coenzyme A 3-O-methyltransferase. Plant Physiology, 137, 1009-1017.
Franks, N.P., Jenkins, A., Conti, E., Lieb, W.R. & Brick, P. (1998) Structural basis for the inhibition of firefly luciferase by a general anesthetic. Biophysical Journal, 75, 2205-2211.
Fürst-Jansen, J.M.R., de Vries, S. & de Vries, J. (2020) Evo-physio: on stress responses and the earliest land plants. Journal of Experimental Botany, 11, 3254-3269.
Goiris, K., Muylaert, K., Voorspoels, S., Noten, B., De Paepe, D., Baart, G.J.E. et al. (2014) Detection of flavonoids in microalgae from different evolutionary lineages. Journal of Phycology, 50, 483-492.
Gouy, M., Guindon, S. & Gascuel, O. (2010) SeaView Version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution, 27, 221-224.
Grienenberger, E., Kim, S.S., Lallemand, B., Geoffroy, P., Heintz, D., de Azevedo Souza, C. et al. (2010) Analysis of TETRAKETIDE α-PYRONE REDUCTASE function in Arabidopsis thaliana reveals a previously unknown, but conserved, biochemical pathway in sporopollenin monomer biosynthesis. The Plant Cell, 22, 4067-4083.
Gross, G.G., Stöckigt, J., Mansell, R.L. & Zenk, M.H. (1973) Three novel enzymes involved in the reduction of ferulic acid to coniferyl alcohol in higher plants: ferulate: CoA ligase, feruloyl-CoA reductase and coniferyl alcohol oxidoreductase. FEBS Letters, 31, 283-286.
Güngör, E., Brouwer, P., Dijkhuizen, L.W., Shaffar, D.C., Nierop, K.G.J., de Vos, R.C.H. et al. (2021) Azolla ferns testify: seed plants and ferns share a common ancestor for leucoanthocyanidin reductase enzymes. New Phytologist, 229, 1118-1132.
Guo, D.-M., Ran, J.-H. & Wang, X.-Q. (2010) Evolution of the Cinnamyl/Sinapyl Alcohol Dehydrogenase (CAD/SAD) gene family: the emergence of real lignin is associated with the origin of bona fide CAD. Journal of Molecular Evolution, 71, 202-218.
Ha, C.M., Escamilla-Trevino, L., Yarce, J.C.S., Kim, H., Ralph, J., Chen, F. et al. (2016) An essential role of caffeoyl shikimate esterase in monolignol biosynthesis in Medicago truncatula. The Plant Journal, 86, 363-375.
Hamberger, B., Ellis, M., Friedmann, M., de Azevedo Souza, C., Barbazuk, B. & Douglas, C.J. (2007) Genome-wide analyses of phenylpropanoid-related genes in Populus trichocarpa, Arabidopsis thaliana, and Oryza sativa: the Populus lignin toolbox and conservation and diversification of angiosperm gene families. Canadian Journal of Botany, 85, 1182-1201.
Hoffmann, L., Maury, S., Martz, F., Geoffroy, P. & Legrand, M. (2003) Purification, cloning, and properties of an acyltransferase controlling shikimate and quinate ester intermediates in phenylpropanoid metabolism. Journal of Biological Chemistry, 278, 95-103.
Hori, K., Maruyama, F., Fujisawa, T., Togashi, T., Yamamoto, N., Seo, M. et al. (2014) Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nature Communications, 5, 3978.
Hu, Y., Gai, Y., Yin, L., Wang, X., Feng, C., Feng, L. et al. (2010) Crystal structures of a Populus tomentosa 4-coumarate:CoA ligase shed light on its enzymatic mechanisms. The Plant Cell, 22, 3093-3104.
Huerta-Cepas, J., Serra, F. & Bork, P. (2016) ETE 3: Reconstruction, analysis, and visualization of phylogenomic data. Molecular Biology and Evolution, 33, 1635-1638.
Jahns, P. & Holzwarth, A.R. (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1817(1), 182-193.
Jiao, C., Sørensen, I., Sun, X., Sun, H., Behar, H., Alseekh, S. et al. (2020) The Penium margaritaceum genome: hallmarks of the origins of land plants. Cell, 181(P1097-1111), E12.
Jones, P., Binns, D., Chang, H.-y., Fraser, M., Li, W., McAnulla, C. et al. (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics, 30, 1236-1240.
Ju, C., Van de Poel, B., Cooper, E.D., Thierer, J.H., Gibbons, T.R., Delwiche, C.F. et al. (2015) Conservation of ethylene as a plant hormone over 450 million years of evolution. Nature Plants, 1, 14004.
Jun, S.-Y., Sattler, S.A., Cortez, G.S., Vermerris, W., Sattler, S.E. & Kang, C. (2018) Biochemical and structural analysis of substrate specificity of a Phenylalanine Ammonia-Lyase. Plant Physiology, 176, 1452-1468.
Kalyaanamoorthy, S., Minh, B.Q., Wong, T., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature methods, 14, 587-589.
Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular biology and evolution, 30, 772-780.
Kaur, H., Heinzel, N., Schöttner, M., Baldwin, I.T. & Gális, I. (2010) R2R3-NaMYB8 regulates the accumulation of phenylpropanoid-polyamine conjugates, which are essential for local and systemic defense against insect herbivores in Nicotiana attenuata. Plant Physiology, 152, 1731-1747.
Kim, R.J., Kim, H.J., Shim, D. & Suh, M.C. (2016) Molecular and biochemical characterizations of the monoacylglycerol lipase gene family of Arabidopsis thaliana. The Plant Journal, 85, 758-771.
Kim, S.-J., Kim, M.-R., Bedgar, D.L., Moinuddin, S.G.A., Cardenas, C.L., Davin, L.B. et al. (2004) Functional reclassification of the putative cinnamyl alcohol dehydrogenase multigene family in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 101, 1455-1460.
König, S., Feussner, K., Kaever, A., Landesfeind, M., Thurow, C., Karlovsky, P. et al. (2014) Soluble phenylpropanoids are involved in the defense response of Arabidopsis against Verticillium longisporum. New Phytologist, 202, 823-837.
Kriegshauser, L., Knosp, S., Grienenberger, E., Tatsumi, K., Gütle, D.D., Sørensen, I. et al. (2021) Function of the HYDROXYCINNAMOYL-CoA:SHIKIMATE HYDROXYCINNAMOYL TRANSFERASE is evolutionarily conserved in embryophytes. The Plant Cell, 33, 1472-1491. https://doi.org/10.1093/plcell/koab044
Labar, G., Bauvois, C., Borel, F., Ferrer, J.-L., Wouters, J. & Lambert, D.M. (2010) Crystal structure of the human Monoacylglycerol Lipase, a key actor in endocannabinoid signaling. ChemBioChem, 11, 218-227.
Labeeuw, L., Martone, P.T., Boucher, Y. & Case, R.J. (2015) Ancient origin of the biosynthesis of lignin precursors. Biology Direct, 10, 23.
Lacombe, E., Hawkins, S., Doorsselaere, J.V., Piquemal, J., Goffner, D., Poeydomenge, O. et al. (1997) Cinnamoyl CoA reductase, the first committed enzyme of the lignin branch biosynthetic pathway: cloning, expression and phylogenetic relationships. The Plant Journal, 11, 429-441.
Lamesch, P., Berardini, T.Z., Li, D., Swarbreck, D., Wilks, C., Sasidharan, R. et al. (2011) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Research, 40, D1202-D1210.
Lang, D., Ullrich, K.K., Murat, F. et al. (2018) The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution. The Plant Journal, 93, 515-533.
Le, S.Q. & Gascuel, O. (2008) An Improved General Amino Acid Replacement Matrix. Molecular Biology and Evolution, 25, 1307-1320.
Leebens-Mack, J.H., Barker, M.S., Carpenter, E.J., Deyholos, M.K., Gitzendanner, M.A., Graham, S.W. et al. (2019) One thousand plant transcriptomes and the phylogenomics of green plants. Nature, 574, 679-685.
Letunic, I. & Bork, P. (2019) Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Research, 47, W256-W259.
Li, F.-W., Brouwer, P., Carretero-Paulet, L., Cheng, S., de Vries, J., Delaux, P.-M. et al. (2018) Fern genomes elucidate land plant evolution and cyanobacterial symbioses. Nature Plants, 4, 460-472.
Li, F.-W., Nishiyama, T., Waller, M., Frangedakis, E., Keller, J., Li, Z. et al. (2020) Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts. Nature Plants, 6, 259-272.
Li, W., Zhang, F., Wu, R., Jia, R., Li, G., Guo, Y. et al. (2017) A novel N-Methyltransferase in Arabidopsis appears to feed a conserved pathway for nicotinate detoxification among land plants and is associated with lignin biosynthesis. Plant Physiology, 174, 1492-1504.
Louie, G.V., Bowman, M.E., Tu, Y., Mouradov, A., Spangenberg, G. & Noel, J.P. (2010) Structure-function analyses of a caffeic acid O-methyltransferase from perennial ryegrass reveal the molecular basis for substrate preference. The Plant Cell, 22, 4114-4127.
Maeda, H.A. & Fernie, A.R. (2021) Evolutionary history of plant metabolism. Annual Review of Plant Biology, 72, 185-216. https://doi.org/10.1146/annurev-arplant-080620-031054
Mansell, R.L.G., Gross, G.G., Stöckigt, J., Franke, H. & Zenk, M.H. (1974) Purification and properties of cinnamyl alcohol dehydrogenase from higher plants involved in lignin biosynthesis. Phytochemistry, 13, 2427-2435.
Martone, P.T., Estevez, J.M., Lu, F., Ruel, K., Denny, M.W., Somerville, C. et al. (2009) Discovery of lignin in seaweed reveals convergent evolution of cell-wall architecture. Current Biology, 19, 169-175.
Martz, F., Maury, S., Pincon, G. & Legrand, M. (1998) cDNA cloning, substrate specificity and expression study of tobacco caffeoyl-CoA 3-O-methyltransferase, a lignin biosynthetic enzyme. Plant Molecular Biology, 36, 427-437.
Matsuno, M., Compagnon, V., Schoch, G.A., Schmitt, M., Debayle, D., Bassard, J.-E. et al. (2009) Evolution of a novel phenolic pathway for pollen development. Science, 325, 1688-1692.
Maury, S., Geoffroy, P. & Legrand, M. (1999) Tobacco O-methyltransferases involved in phenylpropanoid metabolism: the different caffeoyl-coenzyme A/5-hydroxyferuloyl-coenzyme A 3/5-O-methyltransferase and caffeic acid/5-hydroxyferulic acid 3/5-O-methyltransferase classes have distinct substrate specificities and expression patterns. Plant Physiology, 121, 215-224.
Merchant, S.S., Prochnik, S.E., Vallon, O., Harris, E.H., Karpowicz, S.J., Witman, G.B. et al. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science, 318, 245-250.
Miller, M., Owens, S.J. & Rørslett, B. (2011) Plants and colour: flowers and pollination. Optics & Laser Technology, 43, 282-294.
Moffitt, M.C., Louie, G.V., Bowman, M.E., Pence, J., Noel, J.P. & Moore, B.S. (2007) Discovery of two cyanobacterial phenylalanine ammonia lyases: kinetic and structural characterization. Biochemistry, 46, 1004-1012.
Moreau, H., Verhelst, B., Couloux, A., Derelle, E., Rombauts, S., Grimsley, N. et al. (2012) Gene functionalities and genome structure in Bathycoccus prasinos reflect cellular specializations at the base of the green lineage. Genome Biology, 13, R74.
Nagy, E.Z.A., Tork, S.D., Lang, P.A., Filip, A., Irimie, F.D., Poppe, L. et al. (2019) Mapping the hydrophobic substrate binding site of Phenylalanine Ammonia-Lyase from Petroselinum crispum. ACS Catalysis, 9, 8825-8834.
Nakatsu, T., Ichiyama, S., Hiratake, J., Saldanha, A., Kobashi, N., Sakata, K. et al. (2006) Structural basis for the spectral difference in luciferase bioluminescence. Nature, 440, 372-376.
Nelson, D. & Werck-Reichhart, D. (2011) A P450-centric view of plant evolution. The Plant Journal, 66, 194-211.
Nguyen, L.-T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQTREE: a fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular biology and evolution, 32, 268-274.
Nishiyama, T., Sakayama, H., de Vries, J., Buschmann, H., Saint-Marcoux, D., Ullrich, K.K. et al. (2018) The Chara genome: secondary complexity and implications for plant terrestrialization. Cell, 174, 448-464.
Nystedt, B., Street, N.R., Wetterbom, A., Zuccolo, A., Lin, Y.-C., Scofield, D.G. et al. (2013) The Norway spruce genome sequence and conifer genome evolution. Nature, 497, 579-584.
Oliva, J., Rommel, S., Fossdal, C.G., Hietala, A.M., Nemesio-Gorriz, M., Solheim, H. et al. (2015) Transcriptional responses of Norway spruce (Picea abies) inner sapwood against Heterobasidion parviporum. Tree Physiology, 35, 1007-1015.
Omura, T. (1999) Forty years of cytochrome P450. Biochemical and Biophysical Research Communications, 266, 690-698.
Ouyang, S., Zhu, W., Hamilton, J., Lin, H., Campbell, M., Childs, K. et al. (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Research, 35, D883-D887.
Overdijk, E.J.R., de Keijzer, J., de Groot, D., Schoina, C., Bouwmeester, K., Ketelaar, T. et al. (2016) Interaction between the moss Physcomitrella patens and Phytophthora: a novel pathosystem for live-cell imaging of subcellular defence. Journal of Microscopy, 263, 171-180.
Palenik, B., Grimwood, J., Aerts, A., Rouzé, P., Salamov, A., Putnam, N. et al. (2007) The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proceedings of the National Academy of Sciences of the United States of America, 104, 7705-7710.
Pan, H., Zhou, R., Louie, G.V., Mühlemann, J.K., Bomati, E.K., Bowman, M.E. et al. (2014) Structural Studies of Cinnamoyl-CoA Reductase and Cinnamyl-Alcohol Dehydrogenase, key enzymes of monolignol biosynthesis. The Plant Cell, 26, 3709-3727.
Piatkowski, B.T., Imwattana, K., Tripp, E.A., Weston, D.J., Healey, A., Schmutz, J. et al. (2020) Phylogenomics reveals convergent evolution of red-violet coloration in land plants and the origins of the anthocyanin biosynthetic pathway. Molecular Phylogenetics and Evolution, 151, 106904.
Ponce De León, I., Schmelz, E.A., Gaggero, C., Castro, A., Álvarez, A. & Montesano, M. (2012) Physcomitrella patens activates reinforcement of the cell wall, programmed cell death and accumulation of evolutionary conserved defence signals, such as salicylic acid and 12-oxo-phytodienoic acid, but not jasmonic acid, upon Botrytis cinerea infection. Molecular Plant Pathology, 13, 960-974.
Prochnik, S.e., Umen, J., Nedelcu, A.m., Hallmann, A., Miller, S.m., Nishii, I. et al. (2010) Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science, 329, 223-226.
Puttick, M.N., Morris, J.L., Williams, T.A., Cox, C.J., Edwards, D., Kenrick, P. et al. (2018) The interrelationships of land plants and the nature of the ancestral embryophyte. Current Biology, 28, 733-745.
Ralph, J., Lundquist, K., Brunow, G., Lu, F., Kim, H., Schatz, P.F. et al. (2004) Lignins: natural polymers from oxidative coupling of 4-hydroxyphenylpropanoids. Phytochemistry Reviews, 3, 29-60.
Renault, H., Alber, A., Horst, N.A., Basilio Lopes, A., Fich, E.A., Kriegshauser, L. et al. (2017a) A phenol-enriched cuticle is ancestral to lignin evolution in land plants. Nature Communications, 8, 14713.
Renault, H., De Marothy, M., Jonasson, G., Lara, P., Nelson, D.R., Nilsson, IngMarie et al. (2017b) Gene duplication leads to altered membrane topology of a cytochrome P450 enzyme in seed plants. Molecular Biology and Evolution, 34, 2041-2056.
Renault, H., Werck-Reichhart, D. & Weng, J.-K. (2019) Harnessing lignin evolution for biotechnological applications. Current Opinion in Biotechnology, 56, 105-111.
Rensing, S.A. (2014) Gene duplication as a driver of plant morphogenetic evolution. Current Opinion in Plant Biology, 17, 43-48.
Rensing, S.A. (2018) Great moments in evolution: the conquest of land by plants. Current Opinion in Plant Biology, 42, 49-54.
Rippin, M., Becker, B. & Holzinger, A. (2017) Enhanced desiccation tolerance in mature cultures of the streptophytic green alga Zygnema circumcarinatum revealed by transcriptomics. Plant and Cell Physiology, 58, 2067-2084.
Rippin, M., Pichrtová, M., Arc, E., Kranner, I., Becker, B. & Holzinger, A. (2019) Metatranscriptomic and metabolite profiling reveals vertical heterogeneity within a Zygnema green algal mat from Svalbard (High Arctic). Environmental Microbiology, 21, 4283-4299.
Ro, D.K., Mah, N., Ellis, B.E. & Douglas, C.J. (2001) Functional characterization and subcellular localization of poplar (Populus trichocarpa x Populus deltoides) cinnamate 4-hydroxylase. Plant Physiology, 126, 317-329.
Rupasinghe, S., Baudry, J. & Schuler, M.A. (2003) Common active site architecture and binding strategy of four phenylpropanoid P450s from Arabidopsis thaliana as revealed by molecular modeling. Protein Engineering, 16, 721-731.
Russell, D.W. & Conn, E.E. (1967) The cinnamic acid 4-hydroxylase from pea seedlings. Archives of Biochemistry and Biophysics, 122, 256-258.
Saballos, A., Ejeta, G., Sanchez, E., Kang, C. & Vermerris, W. (2009) A genomewide analysis of the cinnamyl alcohol dehydrogenase family in sorghum [Sorghum bicolor (L.) Moench] identifies SbCAD2 as the brown midrib6 gene. Genetics, 181, 783-795.
Saito, N. & Harborne, J.B. (1992) Correlations between anthocyanin type, pollinator and flower colour in the labiatae. Phytochemistry, 31, 3009-3015.
Scheres, B. & van der Putten, W.H. (2017) The plant perceptron connects environment to development. Nature, 543, 337-345.
Schoenbohm, C., Martens, S., Eder, C., Forkmann, G. & Weisshaar, B. (2000) Identification of the Arabidopsis thaliana flavonoid 3'-hydroxylase gene and functional expression of the encoded P450 enzyme. Biological Chemistry, 381, 749-753.
Schwede, T.F., Rétey, J. & Schulz, G.E. (1999) Crystal structure of Histidine Ammonia-Lyase revealing a novel polypeptide modification as the catalytic electrophile. Biochemistry, 38, 5355-5361.
Sheahan, J.J. (1996) Sinapate esters provide greater UV-B attenuation than flavonoids in Arabidopsis thaliana (Brassicaceae). American Journal of Botany, 83, 679-686.
Sheehan, H., Hermann, K. & Kuhlemeier, C. (2012) Color and scent: how single genes influence pollinator attraction. Cold Spring Harbor Symposia on Quantitative Biology, 77, 117-133.
Shockey, J.M., Fulda, M.S. & Browse, J. (2003) Arabidopsis contains a large superfamily of Acyl-Activating Enzymes. Phylogenetic and biochemical analysis reveals a new class of Acyl-Coenzyme A Synthetases. Plant Physiology, 132, 1065-1076.
Sierro, N., Battey, J., Ouadi, S., Bakaher, N., Bovet, L., Willig, A. et al. (2014) The tobacco genome sequence and its comparison with those of tomato and potato. Nature Communications, 5, 3833.
Slotte, T., Hazzouri, K.M., Ågren, J.A., Koenig, D., Maumus, F., Guo, Y.-L. et al. (2013) The Capsella rubella genome and the genomic consequences of rapid mating system evolution. Nature Genetics, 45, 831-835.
Sørensen, I., Pettolino, F.A., Bacic, A., Ralph, J., Lu, F., O’Neill, M.A. et al. (2011) The charophycean green algae provide insights into the early origins of plant cell walls. The Plant Journal, 68, 201-211.
Suzuki, S. & Umezawa, T. (2007) Biosynthesis of lignans and norlignans. Journal of Wood Science, 53, 273-284.
Sytar, O., Zivcak, M., Bruckova, K., Brestic, M., Hemmerich, I., Rauh, C. et al. (2018) Shift in accumulation of flavonoids and phenolic acids in lettuce attributable to changes in ultraviolet radiation and temperature. Scientia Horticulturae, 239, 193-204.
Szövényi, P., Frangedakis, E., Ricca, M., Quandt, D., Wicke, S. & Langdale, J.A. (2015) Establishment of Anthoceros agrestis as a model species for studying the biology of hornworts. BMC Plant Biology, 15, 1-7.
Szövényi, P., Gunadi, A. & Li, F.-W. (2021) Charting the genomic landscape of seed-free plants. Nature Plants, 7, 554-565.
Tan, D.-X., Hardeland, R., Manchester, L.C., Korkmaz, A., Ma, S., Rosales-Corral, S. et al. (2012) Functional roles of melatonin in plants, and perspectives in nutritional and agricultural science. Journal of Experimental Botany, 63, 577-597.
Tanaka, A., Shigemitsu, T., Yokota, Y. & Shika, N. (1997) A new Arabidopsis mutant induced synthesis with spotted pigmentation. Genes & Genetic Systems, 72, 141-148.
The International Brachypodium Initiative (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature, 463, 763-768.
Urban, P., Werck-Reichhart, D., Teutsch, H.G., Durst, F., Regnier, S., Kazmeier, M. et al. (1994) Characterization of recombinant plant cinnamate 4-hydroxylase produced in yeast. Kinetic and spectral properties of the major plant P450 of the phenylpropanoid pathway. European Journal of Biochemistry, 222, 843-850.
Vanholme, R., Cesarino, I., Rataj, K., Xiao, Y., Sundin, L., Goeminne, G. et al. (2013) Caffeoyl shikimate esterase (CSE) is an enzyme in the lignin biosynthetic pathway in Arabidopsis. Science, 341, 1103-1106.
Vanholme, R., De Meester, B., Ralph, J. & Boerjan, W. (2019) Lignin biosynthesis and its integration into metabolism. Current Opinion in Biotechnology, 56, 230-239.
Vanholme, R., Storme, V., Vanholme, B., Sundin, S., Christensen, J.H., Goemine, G. et al. (2012) A systems biology view of responses to lignin biosynthesis perturbations in Arabidopsis. The Plant Cell, 24, 3506-3529.
Vogt, T. (2010) Phenylpropanoid biosynthesis. Molecular Plant, 3, 2-20.
Wagner, A., Tobimatsu, Y., Phillips, L., Flint, H., Geddes, B., Lu, F. et al. (2015) Syringyl lignin production in conifers: Proof of concept in a Pine tracheary element system. Proceedings of the National Academy of Sciences of the United States of America, 112, 6218-6223.
Wan, T., Liu, Z.-M., Li, L.-F., Leitch, A.R., Leitch, I.J., Lohaus, R. et al. (2018) A genome for gnetophytes and early evolution of seed plants. Nature Plants, 4, 82-89.
Wang, S., Li, L., Li, H., Sahu, S.K., Wang, H., Xu, Y. et al. (2020) Genomes of early-diverging streptophyte algae shed light on plant terrestrialization. Nature Plants, 6, 95-106.
Weng, J.K. (2013) The evolutionary paths towards complexity: a metabolic perspective. New Phytologist, 201, 1141-1149.
Weng, J.-K., Akiyama, T., Ralph, J. & Chapple, C. (2011) Independent recruitment of an O-methyltransferase for syringyl lignin biosynthesis in Selaginella moellendorffii. The Plant Cell, 23, 2708-2724.
Weng, J.-K. & Chapple, C. (2010) The origin and evolution of lignin biosynthesis. New Phytologist, 187, 273-285.
Weng, J.-K., Li, X., Stout, J. & Chapple, C. (2008) Independent origins of syringyl lignin in vascular plants. Proceedings of the National Academy of Sciences of the United States of America, 105, 7887-7892.
Whelan, S. & Goldman, N. (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Molecular Biology and Evolution, 18, 691-699.
Wickett, N.J., Mirarab, S., Nguyen, N., Warnow, T., Carpenter, E., Matasci, N. et al. (2014) Phylotranscriptomic analysis of the origin and early diversification of land plants. Proceedings of the National Academy of Sciences of the United States of America, 111, E4859-E4868.
Wodniok, S., Brinkmann, H., Glöckner, G., Heidel, A.J., Philippe, H., Melkonian, M. et al. (2011) Origin of land plants: do conjugating green algae hold the key? BMC Evolutionary Biology, 11, 104.
Wohl, J. & Petersen, M. (2020) Functional expression and characterization of cinnamic acid 4-hydroxylase from the hornwort Anthoceros agrestis in Physcomitrella patens. Plant Cell Reports, 39, 597-607.
Wolf, L., Rizzini, L., Stracke, R., Ulm, R. & Rensing, S.A. (2010) The molecular and physiological responses of Physcomitrella patens to ultraviolet-B radiation. Plant Physiology, 153, 1123-1134.
Worden, A.z., Lee, J.-h., Mock, T., Rouze, P., Simmons, M.p., Aerts, A.l. et al. (2009) Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science, 324, 268-272.
Xu, Z., Zhang, D., Hu, J., Zhou, X., Ye, X., Reichel, K.L. et al. (2009) Comparative genome analysis of lignin biosynthesis gene families across the plant kingdom. BMC Bioinformatics, 10, S3.
Xue, J.-S., Zhang, B., Zhan, H., Lv, Y.-L., Jia, X.-L., Wang, T. et al. (2020) Phenylpropanoid derivatives are essential components of sporopollenin in vascular plants. Molecular Plant, 13, 1644-1653.
Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J. & Zhang, Y. (2015) The I-TASSER suite: protein structure and function prediction. Nature Methods, 12, 7-8.
Ye, Z.-H., Kneusel, R.E., Matern, U. & Varner, J.E. (1994) An alternative methylation pathway in lignin biosynthesis in Zinnia. The Plant Cell, 6, 1427-1439.
Ye, Z.-H. & Varner, J.E. (1995) Differential expression of two O-methyltransferases in lignin biosynthesis in Zinnia elegans. Plant Physiology, 108, 459-467.
Youn, B., Camacho, R., Moinuddin, S.G.A., Lee, C., Davin, L.B., Lewis, N.G. et al. (2006) Crystal structures and catalytic mechanism of the Arabidopsis cinnamyl alcohol dehydrogenases AtCAD5 and AtCAD4. Organic & Biomolecular Chemistry, 4, 1687-1697.
Zhang, J., Fu, X.-X., Li, R.-Q., Zhao, X., Liu, Y., Li, M.-H. et al. (2020) The hornwort genome and early land plant evolution. Nature Plants, 6, 107-118.
Zhang, Y. (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics, 9, 40.
Zubieta, C., Kota, P., Ferrer, J.L., Dixon, R.A. & Noel, J.P. (2002) Structural basis for the modulation of lignin monomer methylation by caffeic acid/5-hydroxyferulic acid 3/5-O-methyltransferase. The Plant Cell, 14, 1265-1277.