Phylogenomic Analysis of the Plastid Genome of the Peruvian Purple Maize Zea mays subsp. mays cv. ‘INIA 601’
Abstract
:1. Introduction
2. Results
2.1. Assembly and Identification of Heteroplasmy of cv. ‘INIA 601’ Plastid Genome
2.2. Comparison of the Plastid Genomes of Cultivated Individuals and the Teosintes
2.3. Phylogenetic Analysis
3. Discussion
3.1. Two Chloroplast Structural Isoforms Coexist in ‘INIA 601’
3.2. Phylogenetic Relationship of Zea Mays Subspecies and Origin of cv. ‘INIA 601’
4. Materials and Methods
4.1. Plant Material
4.2. DNA Extraction and Sequencing
4.3. Genome Assembly and Annotation
4.3.1. Genome Assembly
Peruvian Purple Maize (‘INIA 601’)
Zea Mays Subsp. Parviglumis and Zea Mays Subsp. Mexicana
4.3.2. Annotation
4.4. Phylogenetic Reconstruction
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- SIPAM en el mundo|Sistemas Importantes del Patrimonio Agrícola Mundial (SIPAM)|Organización de las Naciones Unidas para la Alimentación y la Agricultura|GIAHS|Food and Agriculture Organization of the United Nations. Available online: https://www.fao.org/giahs/giahsaroundtheworld/es (accessed on 4 April 2022).
- Jennings, J. La Chichera y El Patrón: Chicha and the Energetics of Feasting in the Prehistoric Andes. Archaeol. Pap. Am. Anthropol. Assoc. 2004, 14, 241–259. [Google Scholar] [CrossRef]
- Goodman, M.M.; Brown, W.L. Races of Corn. In Corn and Corn Improvement, 3rd ed.; Sprague, G., Dudley, J., Eds.; John Wiley & Sons, Ltd: New York, NY, USA, 1988; Volume 18, pp. 33–79. [Google Scholar] [CrossRef]
- Sánchez, G.; Goodman, M.; Bird, R.; Stuber, C. Isozyme and Morphological Variation in Maize of Five Andean Countries. Maydica 2006, 51, 25–42. [Google Scholar]
- Grobman, A.; Salhuana, W.; Sevilla, R.; Mangelsdorf, P. Races of Maize in Peru, 1st ed.; National Academy of Sciences-National Research Council: Washington. DC, USA, 1961; Volume 915. [Google Scholar]
- Ministerio del Ambiente. Línea de Base de la Diversidad Genética del Maíz Peruano con Fines de Bioseguridad, 1st ed.; Grupo Raso: Lima, Peru, 2018; pp. 76–144. [Google Scholar]
- Guillén-Sánchez, J.; Mori-Arismendi, S.; Paucar-Menacho, L.M. Características y Propiedades Funcionales Del Maíz Morado (Zea Mays L.) Var. Subnigroviolaceo. Sci. Agropecu. 2014, 5, 211–217. [Google Scholar] [CrossRef] [Green Version]
- Salvador-Reyes, R.; Clerici, M.T.P.S. Peruvian Andean Maize: General Characteristics, Nutritional Properties, Bioactive Compounds, and Culinary Uses. Food Res. Int. 2020, 130, 108934. [Google Scholar] [CrossRef]
- Leiva González, S.; Gayoso Bazán, G.; Chávez, L. (Zea Mays, L.) “Purple Corn” (Poaceae), a Cereal Used for Feeding in Ancient Peru. Arnaldoa 2016, 23, 295–316. [Google Scholar]
- Medina-Hoyos, A.; Narro-León, L.; Chávez-Cabrera, A. Cultivo de maíz morado (Zea mays L.) en zona altoandina de Perú: Adaptación e identificación de cultivares de alto rendimiento y contenido de antocianina. Sci. Agropecu. 2020, 11, 291–299. [Google Scholar] [CrossRef]
- Rabanal-Atalaya, M.; Medina-Hoyos, A. Evaluación del rendimiento, características morfológicas y químicas de variedades del maíz morado (Zea mays L.) en la región Cajamarca-Perú. Terra Latinoam. 2021, 39, 1–11. [Google Scholar] [CrossRef]
- Moore, M.J.; Soltis, P.S.; Bell, C.D.; Burleigh, J.G.; Soltis, D.E. Phylogenetic Analysis of 83 Plastid Genes Further Resolves the Early Diversification of Eudicots. Proc. Natl. Acad. Sci. USA 2010, 107, 4623–4628. [Google Scholar] [CrossRef] [Green Version]
- Nishiyama, T.; Kato, M. Molecular Phylogenetic Analysis among Bryophytes and Tracheophytes Based on Combined Data of Plastid Coded Genes and the 18S RRNA Gene. Mol. Biol. Evol. 1999, 16, 1027–1036. [Google Scholar] [CrossRef]
- Chase, M.W.; Soltis, D.E.; Olmstead, R.G.; Morgan, D.; Les, D.H.; Mishler, B.D.; Duvall, M.R.; Price, R.A.; Hills, H.G.; Qiu, Y.-L.; et al. Phylogenetics of Seed Plants: An Analysis of Nucleotide Sequences from the Plastid Gene RbcL. Ann. Mo. Bot. Gard. 1993, 80, 528–580. [Google Scholar] [CrossRef] [Green Version]
- Savolainen, V.; Chase, M.W.; Hoot, S.B.; Morton, C.M.; Soltis, D.E.; Bayer, C.; Fay, M.F.; de Bruijn, A.Y.; Sullivan, S.; Qiu, Y.L. Phylogenetics of Flowering Plants Based on Combined Analysis of Plastid AtpB and RbcL Gene Sequences. Syst. Biol. 2000, 49, 306–362. [Google Scholar] [CrossRef] [PubMed]
- Maier, R.M.; Neckermann, K.; Igloi, G.L.; Kössel, H. Complete Sequence of the Maize Chloroplast Genome: Gene Content, Hotspots of Divergence and Fine Tuning of Genetic Information by Transcript Editing. J. Mol. Biol. 1995, 251, 614–628. [Google Scholar] [CrossRef] [PubMed]
- Saski, C.; Lee, S.-B.; Fjellheim, S.; Guda, C.; Jansen, R.K.; Luo, H.; Tomkins, J.; Rognli, O.A.; Daniell, H.; Clarke, J.L. Complete Chloroplast Genome Sequences of Hordeum Vulgare, Sorghum Bicolor and Agrostis Stolonifera, and Comparative Analyses with Other Grass Genomes. TAG Theor. Appl. Genet. Theor. Angew. Genet. 2007, 115, 571–590. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huang, Y.; Li, X.; Yang, Z.; Yang, C.; Yang, J.; Ji, Y. Analysis of Complete Chloroplast Genome Sequences Improves Phylogenetic Resolution in Paris (Melanthiaceae). Front. Plant Sci. 2016, 7, 1797. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pérez-Zamorano, B.; Vallebueno-Estrada, M.; Martínez González, J.; García Cook, A.; Montiel, R.; Vielle-Calzada, J.-P.; Delaye, L. Organellar Genomes from a ∼5000-Year-Old Archaeological Maize Sample Are Closely Related to NB Genotype. Genome Biol. Evol. 2017, 9, 904–915. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Orton, L.M.; Burke, S.V.; Wysocki, W.P.; Duvall, M.R. Plastid Phylogenomic Study of Species within the Genus Zea: Rates and Patterns of Three Classes of Microstructural Changes. Curr. Genet. 2017, 63, 311–323. [Google Scholar] [CrossRef]
- Schnable, P.S.; Ware, D.; Fulton, R.S.; Stein, J.C.; Wei, F.; Pasternak, S.; Liang, C.; Zhang, J.; Fulton, L.; Graves, T.A.; et al. The B73 Maize Genome: Complexity, Diversity, and Dynamics. Science 2009, 326, 1112–1115. [Google Scholar] [CrossRef] [Green Version]
- Bosacchi, M.; Gurdon, C.; Maliga, P. Plastid Genotyping Reveals Uniformity of Cms-T Maize Cytoplasms. Plant Physiol. 2015, 169, 2129–2137. [Google Scholar] [CrossRef] [Green Version]
- Liu, D.; Cui, Y.; Li, S.; Bai, G.; Li, Q.; Zhao, Z.; Liang, D.; Wang, C.; Wang, J.; Shi, X.; et al. A New Chloroplast DNA Extraction Protocol Significantly Improves the Chloroplast Genome Sequence Quality of Foxtail Millet (Setaria Italica (L.) P. Beauv.). Sci. Rep. 2019, 9, 16227. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.; Zhao, M.; Li, L.; Wang, K. Characterization of the Complete Chloroplast Genome of the Eastern Gamagrass, Tripsacum Dactyloides. Mitochondrial. DNA Part B Resour. 2017, 2, 910–912. [Google Scholar] [CrossRef] [Green Version]
- Warburton, M.L.; Wilkes, G.; Taba, S.; Charcosset, A.; Mir, C.; Dumas, F.; Madur, D.; Dreisigacker, S.; Bedoya, C.; Prasanna, B.M.; et al. Gene Flow among Different Teosinte Taxa and into the Domesticated Maize Gene Pool. Genet. Resour. Crop. Evol. 2011, 58, 1243–1261. [Google Scholar] [CrossRef]
- Altschul, S.F.; Gish, W.; Miller, W.; Myers, E.W.; Lipman, D.J. Basic Local Alignment Search Tool. J. Mol. Biol. 1990, 215, 403–410. [Google Scholar] [CrossRef]
- Katoh, K.; Standley, D.M. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Mol. Biol. Evol. 2013, 30, 772–780. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- López, M.G.; Fass, M.; Rivas, J.G.; Carbonell-Caballero, J.; Vera, P.; Puebla, A.; Defacio, R.; Dopazo, J.; Paniego, N.; Hopp, H.E.; et al. Plastome Genomics in South American Maize Landraces: Chloroplast Lineages Parallel the Geographical Structuring of Nuclear Gene Pools. Ann. Bot. 2021, 128, 115–125. [Google Scholar] [CrossRef]
- Kistler, L.; Maezumi, S.Y.; Gregorio de Souza, J.; Przelomska, N.A.S.; Malaquias Costa, F.; Smith, O.; Loiselle, H.; Ramos-Madrigal, J.; Wales, N.; Ribeiro, E.R.; et al. Multiproxy Evidence Highlights a Complex Evolutionary Legacy of Maize in South America. Science 2018, 362, 1309–1313. [Google Scholar] [CrossRef] [Green Version]
- Palmer, J.D. Chloroplast DNA Exists in Two Orientations. Nat. Lond. 1983, 301, 92–93. [Google Scholar] [CrossRef]
- Aldrich, J.; Cherney, B.; Merlin, E.; Williams, C.; Mets, L. Recombination within the Inverted Repeat Sequences of the Chlamydomonas Reinhardii Chloroplast Genome Produces Two Orientation Isomers. Curr. Genet. 1985, 9, 233–238. [Google Scholar] [CrossRef]
- Wang, W.; Lanfear, R. Long-Reads Reveal That the Chloroplast Genome Exists in Two Distinct Versions in Most Plants. Genome Biol. Evol. 2019, 11, 3372–3381. [Google Scholar] [CrossRef]
- Syme, A.E.; McLay, T.G.B.; Udovicic, F.; Cantrill, D.J.; Murphy, D.J.; McLay, T.G.B.; Udovicic, F.; Cantrill, D.J.; Murphy, D.J. Long-Read Assemblies Reveal Structural Diversity in Genomes of Organelles–an Example with Acacia Pycnantha. Gigabyte 2021, 2021, 1–23. [Google Scholar] [CrossRef]
- Stein, D.B.; Palmer, J.D.; Thompson, W.F. Structural Evolution and Flip-Flop Recombination of Chloroplast DNA in the Fern Genus Osmunda. Curr. Genet. 1986, 10, 835–841. [Google Scholar] [CrossRef]
- Kavanagh, T.A.; Thanh, N.D.; Lao, N.T.; McGrath, N.; Peter, S.O.; Horváth, E.M.; Dix, P.J.; Medgyesy, P. Homeologous Plastid DNA Transformation in Tobacco Is Mediated by Multiple Recombination Events. Genetics 1999, 152, 1111–1122. [Google Scholar] [CrossRef] [PubMed]
- Vigouroux, Y.; Glaubitz, J.C.; Matsuoka, Y.; Goodman, M.M.; Sánchez, G.J.; Doebley, J. Population Structure and Genetic Diversity of New World Maize Races Assessed by DNA Microsatellites. Am. J. Bot. 2008, 95, 1240–1253. [Google Scholar] [CrossRef] [PubMed]
- Matsuoka, Y.; Vigouroux, Y.; Goodman, M.M.; Sanchez, G.J.; Buckler, E.; Doebley, J. A Single Domestication for Maize Shown by Multilocus Microsatellite Genotyping. Proc. Natl. Acad. Sci. USA 2002, 99, 6080–6084. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moreno-Letelier, A.; Aguirre-Liguori, J.A.; Piñero, D.; Vázquez-Lobo, A.; Eguiarte, L.E. The Relevance of Gene Flow with Wild Relatives in Understanding the Domestication Process. R. Soc. Open Sci. 2020, 7, 191545. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Costa, F.M.; Silva, N.C. de A.; Vidal, R.; Clement, C.R.; Freitas, F. de O.; Alves-Pereira, A.; Petroli, C.D.; Zucchi, M.I.; Veasey, E.A. Maize Dispersal Patterns Associated with Different Types of Endosperm and Migration of Indigenous Groups in Lowland South America. Ann. Bot. 2022, 129, 737–751. [Google Scholar] [CrossRef]
- Inglis, P.W.; Pappas, M.C.R.; Resende, L.V.; Grattapaglia, D. Fast and Inexpensive Protocols for Consistent Extraction of High Quality DNA and RNA from Challenging Plant and Fungal Samples for High-Throughput SNP Genotyping and Sequencing Applications. PLoS ONE 2018, 13, e0206085. [Google Scholar] [CrossRef]
- Li, H. Minimap2: Pairwise Alignment for Nucleotide Sequences. Bioinforma. Oxf. Engl. 2018, 34, 3094–3100. [Google Scholar] [CrossRef] [Green Version]
- Kolmogorov, M.; Yuan, J.; Lin, Y.; Pevzner, P.A. Assembly of Long, Error-Prone Reads Using Repeat Graphs. Nat. Biotechnol. 2019, 37, 540–546. [Google Scholar] [CrossRef]
- Wick, R.R.; Schultz, M.B.; Zobel, J.; Holt, K.E. Bandage: Interactive Visualization of de Novo Genome Assemblies. Bioinforma. Oxf. Engl. 2015, 31, 3350–3352. [Google Scholar] [CrossRef] [Green Version]
- Li, H. lh3/minigraph. Available online: https://github.com/lh3/minigraph (accessed on 9 May 2022).
- Jin, J.-J.; Yu, W.-B.; Yang, J.-B.; Song, Y.; de Pamphilis, C.W.; Yi, T.-S.; Li, D.-Z. GetOrganelle: A Fast and Versatile Toolkit for Accurate de Novo Assembly of Organelle Genomes. Genome Biol. 2020, 21, 241. [Google Scholar] [CrossRef]
- Marçais, G.; Delcher, A.L.; Phillippy, A.M.; Coston, R.; Salzberg, S.L.; Zimin, A. MUMmer4: A Fast and Versatile Genome Alignment System. PLOS Comput. Biol. 2018, 14, e1005944. [Google Scholar] [CrossRef] [PubMed]
- Tillich, M.; Lehwark, P.; Pellizzer, T.; Ulbricht-Jones, E.S.; Fischer, A.; Bock, R.; Greiner, S. GeSeq–Versatile and Accurate Annotation of Organelle Genomes. Nucleic Acids Res. 2017, 45, W6–W11. [Google Scholar] [CrossRef] [Green Version]
- Chan, P.P.; Lowe, T.M. TRNAscan-SE: Searching for TRNA Genes in Genomic Sequences. In Gene Prediction: Methods and Protocols; Kollmar, M., Ed.; Methods in Molecular Biology; Springer: New York, NY, USA, 2019; pp. 1–14. [Google Scholar] [CrossRef]
- Greiner, S.; Lehwark, P.; Bock, R. OrganellarGenomeDRAW (OGDRAW) Version 1.3.1: Expanded Toolkit for the Graphical Visualization of Organellar Genomes. Nucleic Acids Res. 2019, 47, W59–W64. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stamatakis, A. RAxML Version 8: A Tool for Phylogenetic Analysis and Post-Analysis of Large Phylogenies. Bioinformatics 2014, 30, 1312–1313. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huerta-Cepas, J.; Serra, F.; Bork, P. ETE 3: Reconstruction, Analysis, and Visualization of Phylogenomic Data. Mol. Biol. Evol. 2016, 33, 1635–1638. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Waskom, M. Seaborn: Statistical Data Visualization. J. Open Source Softw. 2021, 6, 3021. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Montenegro, J.D.; Julca, I.; Chumbe-Nolasco, L.D.; Rodríguez-Pérez, L.M.; Sevilla Panizo, R.; Medina-Hoyos, A.; Gutiérrez-Reynoso, D.L.; Guerrero-Abad, J.C.; Amasifuen Guerra, C.A.; García-Serquén, A.L. Phylogenomic Analysis of the Plastid Genome of the Peruvian Purple Maize Zea mays subsp. mays cv. ‘INIA 601’. Plants 2022, 11, 2727. https://doi.org/10.3390/plants11202727
Montenegro JD, Julca I, Chumbe-Nolasco LD, Rodríguez-Pérez LM, Sevilla Panizo R, Medina-Hoyos A, Gutiérrez-Reynoso DL, Guerrero-Abad JC, Amasifuen Guerra CA, García-Serquén AL. Phylogenomic Analysis of the Plastid Genome of the Peruvian Purple Maize Zea mays subsp. mays cv. ‘INIA 601’. Plants. 2022; 11(20):2727. https://doi.org/10.3390/plants11202727
Chicago/Turabian StyleMontenegro, Juan D., Irene Julca, Lenin D. Chumbe-Nolasco, Lila M. Rodríguez-Pérez, Ricardo Sevilla Panizo, Alicia Medina-Hoyos, Dina L. Gutiérrez-Reynoso, Juan Carlos Guerrero-Abad, Carlos A. Amasifuen Guerra, and Aura L. García-Serquén. 2022. "Phylogenomic Analysis of the Plastid Genome of the Peruvian Purple Maize Zea mays subsp. mays cv. ‘INIA 601’" Plants 11, no. 20: 2727. https://doi.org/10.3390/plants11202727