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.
Subject(s)
Adaptation, Physiological , Flowers , Gene-Environment Interaction , Phosphatidylcholines , Phospholipases A1 , Plant Proteins , Zea mays , Alleles , Chromosome Mapping , Flowers/genetics , Flowers/metabolism , Genes, Plant , Genetic Linkage , Phosphatidylcholines/metabolism , Phospholipases A1/classification , Phospholipases A1/genetics , Phospholipases A1/metabolism , Plant Proteins/classification , Plant Proteins/genetics , Plant Proteins/metabolism , Zea mays/genetics , Zea mays/growth & developmentABSTRACT
Plant phospholipases can be grouped into four major types, phospholipase D, phospholipase C, phospholipase A1 (PLA(1)), and phospholipase A2 (PLA(2)), that hydrolyze glycerophospholipids at different ester bonds. Within each type, there are different families or subfamilies of enzymes that can differ in substrate specificity, cofactor requirement, and/or reaction conditions. These differences provide insights into determining the cellular function of specific phospholipases in plants, and they can be explored for different industrial applications.