New Insights Into the Evolution of C4 Photosynthesis Offered by the Tarenaya Cluster of Cleomaceae
Cleomaceae is closely related to Brassicaceae and includes C3, C3–C4, and C4 species. Thus, this family represents an interesting system for studying the evolution of the carbon concentrating mechanism. However, inadequate genetic information on Cleomaceae limits their research applications. Here, w...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-01-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2021.756505/full |
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| author | Daniele F. Parma Marcelo G. M. V. Vaz Priscilla Falquetto Jéssica C. Silva Wellington R. Clarindo Philipp Westhoff Robin van Velzen Urte Schlüter Wagner L. Araújo M. Eric Schranz Andreas P. M. Weber Adriano Nunes-Nesi |
| author_facet | Daniele F. Parma Marcelo G. M. V. Vaz Priscilla Falquetto Jéssica C. Silva Wellington R. Clarindo Philipp Westhoff Robin van Velzen Urte Schlüter Wagner L. Araújo M. Eric Schranz Andreas P. M. Weber Adriano Nunes-Nesi |
| author_sort | Daniele F. Parma |
| collection | DOAJ |
| description | Cleomaceae is closely related to Brassicaceae and includes C3, C3–C4, and C4 species. Thus, this family represents an interesting system for studying the evolution of the carbon concentrating mechanism. However, inadequate genetic information on Cleomaceae limits their research applications. Here, we characterized 22 Cleomaceae accessions [3 genera (Cleoserrata, Gynandropsis, and Tarenaya) and 11 species] in terms of genome size; molecular phylogeny; as well as anatomical, biochemical, and photosynthetic traits. We clustered the species into seven groups based on genome size. Interestingly, despite clear differences in genome size (2C, ranging from 0.55 to 1.3 pg) in Tarenaya spp., this variation was not consistent with phylogenetic grouping based on the internal transcribed spacer (ITS) marker, suggesting the occurrence of multiple polyploidy events within this genus. Moreover, only G. gynandra, which possesses a large nuclear genome, exhibited the C4 metabolism. Among the C3-like species, we observed intra- and interspecific variation in nuclear genome size as well as in biochemical, physiological, and anatomical traits. Furthermore, the C3-like species had increased venation density and bundle sheath cell size, compared to C4 species, which likely predisposed the former lineages to C4 photosynthesis. Accordingly, our findings demonstrate the potential of Cleomaceae, mainly members of Tarenaya, in offering novel insights into the evolution of C4 photosynthesis. |
| first_indexed | 2024-04-11T18:18:35Z |
| format | Article |
| id | doaj.art-2784c0d66e1e45a5a0a23feba28478e6 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-04-11T18:18:35Z |
| publishDate | 2022-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-2784c0d66e1e45a5a0a23feba28478e62022-12-22T04:09:50ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-01-011210.3389/fpls.2021.756505756505New Insights Into the Evolution of C4 Photosynthesis Offered by the Tarenaya Cluster of CleomaceaeDaniele F. Parma0Marcelo G. M. V. Vaz1Priscilla Falquetto2Jéssica C. Silva3Wellington R. Clarindo4Philipp Westhoff5Robin van Velzen6Urte Schlüter7Wagner L. Araújo8M. Eric Schranz9Andreas P. M. Weber10Adriano Nunes-Nesi11Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, BrazilDepartamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, BrazilDepartamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, BrazilDepartamento de Biologia Geral, Universidade Federal de Viçosa, Viçosa, BrazilDepartamento de Biologia Geral, Universidade Federal de Viçosa, Viçosa, BrazilPlant Metabolism and Metabolomics Laboratory, Cluster of Excellence on Plant Sciences, Heinrich Heine University Düsseldorf, Düsseldorf, GermanyBiosystematics Group, Wageningen University & Research, Wageningen, NetherlandsInstitute of Plant Biochemistry, Cluster of Excellence on Plant Science, Heinrich Heine University Düsseldorf, Düsseldorf, GermanyDepartamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, BrazilBiosystematics Group, Wageningen University & Research, Wageningen, NetherlandsInstitute of Plant Biochemistry, Cluster of Excellence on Plant Science, Heinrich Heine University Düsseldorf, Düsseldorf, GermanyDepartamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, BrazilCleomaceae is closely related to Brassicaceae and includes C3, C3–C4, and C4 species. Thus, this family represents an interesting system for studying the evolution of the carbon concentrating mechanism. However, inadequate genetic information on Cleomaceae limits their research applications. Here, we characterized 22 Cleomaceae accessions [3 genera (Cleoserrata, Gynandropsis, and Tarenaya) and 11 species] in terms of genome size; molecular phylogeny; as well as anatomical, biochemical, and photosynthetic traits. We clustered the species into seven groups based on genome size. Interestingly, despite clear differences in genome size (2C, ranging from 0.55 to 1.3 pg) in Tarenaya spp., this variation was not consistent with phylogenetic grouping based on the internal transcribed spacer (ITS) marker, suggesting the occurrence of multiple polyploidy events within this genus. Moreover, only G. gynandra, which possesses a large nuclear genome, exhibited the C4 metabolism. Among the C3-like species, we observed intra- and interspecific variation in nuclear genome size as well as in biochemical, physiological, and anatomical traits. Furthermore, the C3-like species had increased venation density and bundle sheath cell size, compared to C4 species, which likely predisposed the former lineages to C4 photosynthesis. Accordingly, our findings demonstrate the potential of Cleomaceae, mainly members of Tarenaya, in offering novel insights into the evolution of C4 photosynthesis.https://www.frontiersin.org/articles/10.3389/fpls.2021.756505/fullCleomaceaeCleoserratagenome sizeGynandropsisintermediate photosynthetic mechanismpolyploidy |
| spellingShingle | Daniele F. Parma Marcelo G. M. V. Vaz Priscilla Falquetto Jéssica C. Silva Wellington R. Clarindo Philipp Westhoff Robin van Velzen Urte Schlüter Wagner L. Araújo M. Eric Schranz Andreas P. M. Weber Adriano Nunes-Nesi New Insights Into the Evolution of C4 Photosynthesis Offered by the Tarenaya Cluster of Cleomaceae Frontiers in Plant Science Cleomaceae Cleoserrata genome size Gynandropsis intermediate photosynthetic mechanism polyploidy |
| title | New Insights Into the Evolution of C4 Photosynthesis Offered by the Tarenaya Cluster of Cleomaceae |
| title_full | New Insights Into the Evolution of C4 Photosynthesis Offered by the Tarenaya Cluster of Cleomaceae |
| title_fullStr | New Insights Into the Evolution of C4 Photosynthesis Offered by the Tarenaya Cluster of Cleomaceae |
| title_full_unstemmed | New Insights Into the Evolution of C4 Photosynthesis Offered by the Tarenaya Cluster of Cleomaceae |
| title_short | New Insights Into the Evolution of C4 Photosynthesis Offered by the Tarenaya Cluster of Cleomaceae |
| title_sort | new insights into the evolution of c4 photosynthesis offered by the tarenaya cluster of cleomaceae |
| topic | Cleomaceae Cleoserrata genome size Gynandropsis intermediate photosynthetic mechanism polyploidy |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2021.756505/full |
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