Teosinte introgression modulates phosphatidylcholine levels and induces early maize flowering time

Authors: RODRIGUEZ-ZAPATA, FAUSTO - North Carolina State University; BARNES, ALLISON - North Carolina State University; BLOCKER-JUAREZ, KARLA - National Laboratory Of Genomics And Biodiversity; GATES, DAN - University Of California, Davis; KUR, ANDI - North Carolina State University; WANG, LI - Iowa State University; JANZEN, GARRETT - Iowa State University; JENSEN, SARAH - Cornell University; ESTEVEZ-PALMAS, JUAN - National Laboratory Of Genomics And Biodiversity; CROW, TAYLOR - University Of California, Davis; AGUILAR-RANGEL, ROCIO - National Laboratory Of Genomics And Biodiversity; DEMESA-AREVALO, EDGAR - Cold Spring Harbor Laboratory; SKOPELITIS, TARA - Cold Spring Harbor Laboratory; PEREZ-LIMON, SERGIO - National Laboratory Of Genomics And Biodiversity; STUTTS, WHITNEY - North Carolina State University; THOMPSON, PETER - North Carolina State University; CHIU, YU-CHUN - North Carolina State University; JACKSON, DAVID - Cold Spring Harbor Laboratory; FIEHN, OLIVER - University Of California, Davis; RUNCIE, DANIEL - University Of California, Davis; Buckler, Edward - Ed; ROSS-IBARRA, JEFFREY - University Of California, Davis; HUFFORD, MATTHEW - Iowa State University; SAWERS, RUAIRIDH - National Laboratory Of Genomics And Biodiversity; RELLAN-ALVAREZ, RUBEN - National Laboratory Of Genomics And Biodiversity

Submitted to: bioRxiv
Publication Type: Pre-print Publication
Publication Acceptance Date: 1/26/2021
Publication Date: 1/26/2021
Citation: Rodriguez-Zapata, F., Barnes, A.C., Blocker-Juarez, K.A., Gates, D., Kur, A., Wang, L., Janzen, G.M., Jensen, S., Estevez-Palmas, J.M., Crow, T., Aguilar-Rangel, R., Demesa-Arevalo, E., Skopelitis, T., Perez-Limon, S., Stutts, W., Thompson, P., Chiu, Y., Jackson, D., Fiehn, O., Runcie, D., Buckler IV, E.S., Ross-Ibarra, J., Hufford, M.B., Sawers, R., Rellan-Alvarez, R. 2021. Teosinte introgression modulates phosphatidylcholine levels and induces early maize flowering time. bioRxiv. https://doi.org/10.1101/2021.01.25.426574.
DOI: https://doi.org/10.1101/2021.01.25.426574

Interpretive Summary: Maize has evolved and adapted to different environmental conditions. Today it inhabits both the warm Mexican southwest and the cool Mexican and South American highlands. Phospholipid metabolism has been linked to low-temperature stress in maize and other species, but the mechanisms driving maize adaptation are still poorly understood. This project identified a mutation that causes a single amino acid change in the phospholipase A1 enzyme of modern maize. The amino acid change identified was associated with improved plant growth in cold, high-altitude environments. Comparing maize to related species indicated that this amino acid change likely comes from Zea mays ssp. mexicana, which is a close relative of modern maize. Looking at the conservation of this amino acid across all of life showed that bacterial proteins with the low-temperature amino acid came from species with lower optimal growth temperatures than bacterial proteins with the high-temperature amino acid, suggesting conservation over a long evolutionary time period. The effect of the mutation in modern maize was validated with genome editing. Phospholipids are important membrane components and signaling molecules, and this study investigates natural mutations that affect phospholipid composition and environmental adaptation in maize. It uses genetic, molecular, and physiological approaches to understand maize adaptation to cold, high altitude environments. The results from this study can be used to inform modern crop improvement efforts and understanding of how maize adapts to cold temperatures.

Technical Abstract: After domestication from lowland teosinte parviglumis (Zea mays ssp.parviglumis) in the warm Mexican southwest, maize (Zea mays ssp. mays) colonized the highlands of México and South America. In the highlands, maize was exposed to lower temperatures that imposed strong selection on flowering time. Previous work in maize and other has linked variation in phospholipid metabolism to low temperature stress as well as changes in flowering time. Here, we combined linkage mapping analysis with genome scans to identify High PhosphatidylCholine 1 (HPC1), a gene which 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 results in impaired function of the encoded protein due to a polymorphism in a highly conserved sequence. A meta-analysis indicated a strong association between the identity of the amino acid at this position in a prokaryotic protein harboring this conserved sequence and optimal growth temperature of the organism. 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 Northern US, 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.