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ARS Home » Northeast Area » Ithaca, New York » Robert W. Holley Center for Agriculture & Health » Plant, Soil and Nutrition Research » Research » Publications at this Location » Publication #396558

Research Project: Improving Crop Efficiency Using Genomic Diversity and Computational Modeling

Location: Plant, Soil and Nutrition Research

Title: An adaptive teosinte mexicana introgression modulates phosphatidylcholine levels and is associated with maize flowering time

Author
item BARNES, ALLISON - North Carolina State University
item RODRÍGUEZ-ZAPATA, FAUSTO - North Carolina State University
item JUÁREZ-NÚÑEZ, KARLA - National Laboratory Of Genomics And Biodiversity
item GATES, DANIEL - University Of California, Davis
item JANZEN, GARRETT - Iowa State University
item KUR, ANDI - North Carolina State University
item WANG, LI - Iowa State University
item JENSEN, SARAH - Syngenta
item ESTÉVEZ-PALMAS, JUAN - National Laboratory Of Genomics And Biodiversity
item CROW, TAYLOR - University Of California, Davis
item KAVI, HELI - North Carolina State University
item PIL, HANNAH - North Carolina State University
item STOKES, RUTHIE - North Carolina State University
item KNIZNER, KEVAN - North Carolina State University
item AGUILAR-RANGEL, MARIA - National Laboratory Of Genomics And Biodiversity
item DEMESA-ARÉVALO, EDGAR - Cold Spring Harbor Laboratory
item SKOPELITIS, TARA - Cold Spring Harbor Laboratory
item PÉREZ-LIMÓN, SERGIO - National Laboratory Of Genomics And Biodiversity
item STUTTS, WHITNEY - North Carolina State University
item THOMPSON, PETER - North Carolina State University
item CHIU, YU-CHUN - North Carolina State University
item JACKSON, DAVID - Cold Spring Harbor Laboratory
item MUDDIMAN, DAVID - North Carolina State University
item FIEHN, OLIVER - University Of California, Davis
item RUNCIE, DANIEL - University Of California, Davis
item Buckler, Edward - Ed
item ROSS-IBARRA, JEFFREY - University Of California, Davis
item HUFFORD, MATTHEW - Iowa State University
item SAWERS, RUAIRIDH - National Laboratory Of Genomics And Biodiversity
item RELLÁN-ÁLVAREZ, RUBEN - North Carolina State University

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/8/2022
Publication Date: 6/30/2022
Citation: Barnes, A.C., Rodríguez-Zapata, F., Juárez-Núñez, K.A., Gates, D.J., Janzen, G.M., Kur, A., Wang, L., Jensen, S.J., Estévez-Palmas, J.M., Crow, T.M., Kavi, H.S., Pil, H.D., Stokes, R.L., Knizner, K.T., Aguilar-Rangel, M.R., Demesa-Arévalo, E., Skopelitis, T., Pérez-Limón, S., Stutts, W.L., Thompson, P., Chiu, Y., Jackson, D., Muddiman, D.C., Fiehn, O., Runcie, D., Buckler IV, E.S., Ross-Ibarra, J., Hufford, M.B., Sawers, R.J., Rellán-Álvarez, R. 2022. An adaptive teosinte mexicana introgression modulates phosphatidylcholine levels and is associated with maize flowering time. Proceedings of the National Academy of Sciences(PNAS). 119(27)Article e2100036119. https://doi.org/10.1073/pnas.2100036119.
DOI: https://doi.org/10.1073/pnas.2100036119

Interpretive Summary: Despite more than a century of genetic research, our understanding of the genetic basis of the astounding capacity of maize to adapt to new environments is in its infancy. Recent work in many crops has pointed to the potentially important role for introgression in underpinning adaptation, but clear examples of adaptive loci arising via introgression are lacking. Here, we elucidate the evolutionary history of a major metabolic quantitative trait locus (QTL) that we mapped down to a single gene, HPC1. Alterations in highland HPC1 are the result of a teosinte mexicana introgression in maize, leading to high phosphatidylcholine levels and improving fitness by accelerating flowering.

Technical Abstract: Native Americans domesticated maize (Zea mays ssp. mays) from lowland teosinte parviglumis (Zea mays ssp. parviglumis) in the warm Mexican southwest and brought it to the highlands of Mexico and South America where it was exposed to lower temperatures that imposed strong selection on flowering time. Phospholipids are important metabolites in plant responses to low-temperature and phosphorus availability and have been suggested to influence flowering time. Here, we combined linkage mapping with genome scans to identify High PhosphatidylCholine 1 (HPC1), a gene that encodes a phospholipase A1 enzyme, as a major driver of phospholipid variation in highland maize. Common garden experiments demonstrated strong genotype-by-environment interactions associated with variation at HPC1, with the highland HPC1 allele leading to higher fitness in highlands, possibly by hastening flowering. The highland maize HPC1 variant resulted in impaired function of the encoded protein due to a polymorphism in a highly conserved sequence. A meta-analysis across HPC1 orthologs indicated a strong association between the identity of the amino acid at this position and optimal growth in prokaryotes. Mutagenesis of HPC1 via genome editing validated its role in regulating phospholipid metabolism. Finally, we showed that the highland HPC1 allele entered cultivated maize by introgression from the wild highland teosinte Zea mays ssp. mexicana and has been maintained in maize breeding lines from the Northern United States, Canada, and Europe. Thus, HPC1 introgressed from teosinte mexicana underlies a large metabolic QTL that modulates phosphatidylcholine levels and has an adaptive effect at least in part via induction of early flowering time.