Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis
Yerba mate (YM, Ilex paraguariensis) is an economically important crop marketed for the elaboration of mate, the third-most widely consumed caffeine-containing infusion worldwide. Here, we report the first genome assembly of this species, which has a total length of 1.06 Gb and contains 53,390 prote...
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eLife Sciences Publications Ltd
2025-01-01
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| Online Access: | https://elifesciences.org/articles/104759 |
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| author | Federico A Vignale Andrea Hernandez Garcia Carlos P Modenutti Ezequiel J Sosa Lucas A Defelipe Renato Oliveira Gisele L Nunes Raúl M Acevedo German F Burguener Sebastian M Rossi Pedro D Zapata Dardo A Marti Pedro Sansberro Guilherme Oliveira Emily M Catania Madeline N Smith Nicole M Dubs Satish Nair Todd J Barkman Adrian G Turjanski |
| author_facet | Federico A Vignale Andrea Hernandez Garcia Carlos P Modenutti Ezequiel J Sosa Lucas A Defelipe Renato Oliveira Gisele L Nunes Raúl M Acevedo German F Burguener Sebastian M Rossi Pedro D Zapata Dardo A Marti Pedro Sansberro Guilherme Oliveira Emily M Catania Madeline N Smith Nicole M Dubs Satish Nair Todd J Barkman Adrian G Turjanski |
| author_sort | Federico A Vignale |
| collection | DOAJ |
| description | Yerba mate (YM, Ilex paraguariensis) is an economically important crop marketed for the elaboration of mate, the third-most widely consumed caffeine-containing infusion worldwide. Here, we report the first genome assembly of this species, which has a total length of 1.06 Gb and contains 53,390 protein-coding genes. Comparative analyses revealed that the large YM genome size is partly due to a whole-genome duplication (Ip-α) during the early evolutionary history of Ilex, in addition to the hexaploidization event (γ) shared by core eudicots. Characterization of the genome allowed us to clone the genes encoding methyltransferase enzymes that catalyse multiple reactions required for caffeine production. To our surprise, this species has converged upon a different biochemical pathway compared to that of coffee and tea. In order to gain insight into the structural basis for the convergent enzyme activities, we obtained a crystal structure for the terminal enzyme in the pathway that forms caffeine. The structure reveals that convergent solutions have evolved for substrate positioning because different amino acid residues facilitate a different substrate orientation such that efficient methylation occurs in the independently evolved enzymes in YM and coffee. While our results show phylogenomic constraint limits the genes coopted for convergence of caffeine biosynthesis, the X-ray diffraction data suggest structural constraints are minimal for the convergent evolution of individual reactions. |
| format | Article |
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| institution | Kabale University |
| issn | 2050-084X |
| language | English |
| publishDate | 2025-01-01 |
| publisher | eLife Sciences Publications Ltd |
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| series | eLife |
| spelling | doaj-art-ec1bc2f305ce428aae7a47345a15f9e52025-01-08T14:00:41ZengeLife Sciences Publications LtdeLife2050-084X2025-01-011410.7554/eLife.104759Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesisFederico A Vignale0https://orcid.org/0000-0003-0849-0916Andrea Hernandez Garcia1Carlos P Modenutti2Ezequiel J Sosa3Lucas A Defelipe4https://orcid.org/0000-0001-7859-7300Renato Oliveira5Gisele L Nunes6Raúl M Acevedo7https://orcid.org/0000-0001-7582-3018German F Burguener8https://orcid.org/0000-0002-8600-7136Sebastian M Rossi9https://orcid.org/0000-0002-6694-0076Pedro D Zapata10https://orcid.org/0000-0001-6476-8324Dardo A Marti11Pedro Sansberro12https://orcid.org/0000-0002-6540-3666Guilherme Oliveira13Emily M Catania14Madeline N Smith15Nicole M Dubs16https://orcid.org/0009-0006-0695-398XSatish Nair17Todd J Barkman18https://orcid.org/0000-0003-2259-2345Adrian G Turjanski19https://orcid.org/0000-0003-2190-137XEuropean Molecular Biology Laboratory - Hamburg Unit, Hamburg, GermanyDepartment of Biochemistry, University of Illinois at Urbana-Champaign, Urbana, United StatesIQUIBICEN-CONICET, Ciudad Universitaria, Pabellón 2, Ciudad Autonoma de Buenos Aires, Argentina; Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 2, Ciudad Autónoma de Buenos Aires, ArgentinaIQUIBICEN-CONICET, Ciudad Universitaria, Pabellón 2, Ciudad Autonoma de Buenos Aires, Argentina; Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 2, Ciudad Autónoma de Buenos Aires, ArgentinaEuropean Molecular Biology Laboratory - Hamburg Unit, Hamburg, GermanyInstituto Tecnológico Vale, Belém, BrazilInstituto Tecnológico Vale, Belém, BrazilLaboratorio de Biotecnología Aplicada y Genómica Funcional, Instituto de Botánica del Nordeste (IBONE-CONICET), Facultad de Ciencias Agrarias, Universidad Nacional del Nordeste, Corrientes, ArgentinaDepartment of Plant Sciences, University of California, Davis, Davis, United StatesInstituto de Biotecnología de Misiones, Facultad de Ciencias Exactas, Químicas y Naturales, Universidad Nacional de Misiones (INBIOMIS-FCEQyN-UNaM), Misiones, ArgentinaInstituto de Biotecnología de Misiones, Facultad de Ciencias Exactas, Químicas y Naturales, Universidad Nacional de Misiones (INBIOMIS-FCEQyN-UNaM), Misiones, ArgentinaInstituto de Biología Subtropical, Universidad Nacional de Misiones (IBS-UNaM-CONICET), Posadas, ArgentinaLaboratorio de Biotecnología Aplicada y Genómica Funcional, Instituto de Botánica del Nordeste (IBONE-CONICET), Facultad de Ciencias Agrarias, Universidad Nacional del Nordeste, Corrientes, ArgentinaInstituto Tecnológico Vale, Belém, BrazilDepartment of Biological Sciences, Western Michigan University, Kalamazoo, United StatesDepartment of Biological Sciences, Western Michigan University, Kalamazoo, United StatesDepartment of Biological Sciences, Western Michigan University, Kalamazoo, United StatesCarl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, United States; Center for Biophysics and Quantitative Biology, University of Illinois at Urbana Champaign, Urbana, United StatesDepartment of Biological Sciences, Western Michigan University, Kalamazoo, United StatesIQUIBICEN-CONICET, Ciudad Universitaria, Pabellón 2, Ciudad Autonoma de Buenos Aires, Argentina; Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 2, Ciudad Autónoma de Buenos Aires, ArgentinaYerba mate (YM, Ilex paraguariensis) is an economically important crop marketed for the elaboration of mate, the third-most widely consumed caffeine-containing infusion worldwide. Here, we report the first genome assembly of this species, which has a total length of 1.06 Gb and contains 53,390 protein-coding genes. Comparative analyses revealed that the large YM genome size is partly due to a whole-genome duplication (Ip-α) during the early evolutionary history of Ilex, in addition to the hexaploidization event (γ) shared by core eudicots. Characterization of the genome allowed us to clone the genes encoding methyltransferase enzymes that catalyse multiple reactions required for caffeine production. To our surprise, this species has converged upon a different biochemical pathway compared to that of coffee and tea. In order to gain insight into the structural basis for the convergent enzyme activities, we obtained a crystal structure for the terminal enzyme in the pathway that forms caffeine. The structure reveals that convergent solutions have evolved for substrate positioning because different amino acid residues facilitate a different substrate orientation such that efficient methylation occurs in the independently evolved enzymes in YM and coffee. While our results show phylogenomic constraint limits the genes coopted for convergence of caffeine biosynthesis, the X-ray diffraction data suggest structural constraints are minimal for the convergent evolution of individual reactions.https://elifesciences.org/articles/104759Ilex paraguariensisyerba mategenomecaffeineconvergent evolutionwhole-genome duplication |
| spellingShingle | Federico A Vignale Andrea Hernandez Garcia Carlos P Modenutti Ezequiel J Sosa Lucas A Defelipe Renato Oliveira Gisele L Nunes Raúl M Acevedo German F Burguener Sebastian M Rossi Pedro D Zapata Dardo A Marti Pedro Sansberro Guilherme Oliveira Emily M Catania Madeline N Smith Nicole M Dubs Satish Nair Todd J Barkman Adrian G Turjanski Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis eLife Ilex paraguariensis yerba mate genome caffeine convergent evolution whole-genome duplication |
| title | Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis |
| title_full | Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis |
| title_fullStr | Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis |
| title_full_unstemmed | Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis |
| title_short | Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis |
| title_sort | yerba mate ilex paraguariensis genome provides new insights into convergent evolution of caffeine biosynthesis |
| topic | Ilex paraguariensis yerba mate genome caffeine convergent evolution whole-genome duplication |
| url | https://elifesciences.org/articles/104759 |
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