Genome-wide association of carbon and nitrogen metabolism in the maize nested association mapping population.
Carbon (C) and nitrogen (N) metabolism are critical to plant growth and development and are at the basis of crop yield and adaptation. We performed high-throughput metabolite analyses on over 12,000 samples from the nested association mapping population to identify genetic variation in C and N metabolism in maize (Zea mays ssp. mays). All samples were grown in the same field and used to identify natural variation controlling the levels of 12 key C and N metabolites, namely chlorophyll a, chlorophyll b, fructose, fumarate, glucose, glutamate, malate, nitrate, starch, sucrose, total amino acids, and total protein, along with the first two principal components derived from them. Our genome-wide association results frequently identified hits with single-gene resolution. In addition to expected genes such as invertases, natural variation was identified in key C4 metabolism genes, including carbonic anhydrases and a malate transporter. Unlike several prior maize studies, extensive pleiotropy was found for C and N metabolites. This integration of field-derived metabolite data with powerful mapping and genomics resources allows for the dissection of key metabolic pathways, providing avenues for future genetic improvement.
Institute for Genomic Diversity (N.Z., J.G.W., K.K., E.S.B.), Boyce Thompson Institute for Plant Research (P.L., L.D., T.B.), Department of Plant Breeding and Genetics (C.C., K.K., E.S.B.), and Department of Plant Biology (T.B.), Cornell University, Ithaca, New York 14853;Max Planck Institute of Molecular Plant Physiology, 14476 Golm-Potsdam, Germany (Y.G., M.S.);United States Department of Agriculture-Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, New York 14853 (N.L., P.J.B., E.S.B.); andDepartment of Crop Science, North Carolina State University, Raleigh, North Carolina 27695 (Y.-S.S.).
Nengyi
N
Zhang
Institute for Genomic Diversity (N.Z., J.G.W., K.K., E.S.B.), Boyce Thompson Institute for Plant Research (P.L., L.D., T.B.), Department of Plant Breeding and Genetics (C.C., K.K., E.S.B.), and Department of Plant Biology (T.B.), Cornell University, Ithaca, New York 14853;Max Planck Institute of Molecular Plant Physiology, 14476 Golm-Potsdam, Germany (Y.G., M.S.);United States Department of Agriculture-Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, New York 14853 (N.L., P.J.B., E.S.B.); andDepartment of Crop Science, North Carolina State University, Raleigh, North Carolina 27695 (Y.-S.S.) yves.gibon@bordeaux.inra.fr mstitt@mpimp-golm.mpg.de esb33@cornell.edu.
Yves
Y
Gibon
Institute for Genomic Diversity (N.Z., J.G.W., K.K., E.S.B.), Boyce Thompson Institute for Plant Research (P.L., L.D., T.B.), Department of Plant Breeding and Genetics (C.C., K.K., E.S.B.), and Department of Plant Biology (T.B.), Cornell University, Ithaca, New York 14853;Max Planck Institute of Molecular Plant Physiology, 14476 Golm-Potsdam, Germany (Y.G., M.S.);United States Department of Agriculture-Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, New York 14853 (N.L., P.J.B., E.S.B.); andDepartment of Crop Science, North Carolina State University, Raleigh, North Carolina 27695 (Y.-S.S.).
Jason G
http://orcid.org/0000-0002-8937-6543
JG
Wallace
Institute for Genomic Diversity (N.Z., J.G.W., K.K., E.S.B.), Boyce Thompson Institute for Plant Research (P.L., L.D., T.B.), Department of Plant Breeding and Genetics (C.C., K.K., E.S.B.), and Department of Plant Biology (T.B.), Cornell University, Ithaca, New York 14853;Max Planck Institute of Molecular Plant Physiology, 14476 Golm-Potsdam, Germany (Y.G., M.S.);United States Department of Agriculture-Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, New York 14853 (N.L., P.J.B., E.S.B.); andDepartment of Crop Science, North Carolina State University, Raleigh, North Carolina 27695 (Y.-S.S.).
Nicholas
http://orcid.org/0000-0003-2653-6367
N
Lepak
Institute for Genomic Diversity (N.Z., J.G.W., K.K., E.S.B.), Boyce Thompson Institute for Plant Research (P.L., L.D., T.B.), Department of Plant Breeding and Genetics (C.C., K.K., E.S.B.), and Department of Plant Biology (T.B.), Cornell University, Ithaca, New York 14853;Max Planck Institute of Molecular Plant Physiology, 14476 Golm-Potsdam, Germany (Y.G., M.S.);United States Department of Agriculture-Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, New York 14853 (N.L., P.J.B., E.S.B.); andDepartment of Crop Science, North Carolina State University, Raleigh, North Carolina 27695 (Y.-S.S.).
Pinghua
http://orcid.org/0000-0003-4314-7400
P
Li
Institute for Genomic Diversity (N.Z., J.G.W., K.K., E.S.B.), Boyce Thompson Institute for Plant Research (P.L., L.D., T.B.), Department of Plant Breeding and Genetics (C.C., K.K., E.S.B.), and Department of Plant Biology (T.B.), Cornell University, Ithaca, New York 14853;Max Planck Institute of Molecular Plant Physiology, 14476 Golm-Potsdam, Germany (Y.G., M.S.);United States Department of Agriculture-Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, New York 14853 (N.L., P.J.B., E.S.B.); andDepartment of Crop Science, North Carolina State University, Raleigh, North Carolina 27695 (Y.-S.S.).
Lauren
http://orcid.org/0000-0001-8994-8508
L
Dedow
Institute for Genomic Diversity (N.Z., J.G.W., K.K., E.S.B.), Boyce Thompson Institute for Plant Research (P.L., L.D., T.B.), Department of Plant Breeding and Genetics (C.C., K.K., E.S.B.), and Department of Plant Biology (T.B.), Cornell University, Ithaca, New York 14853;Max Planck Institute of Molecular Plant Physiology, 14476 Golm-Potsdam, Germany (Y.G., M.S.);United States Department of Agriculture-Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, New York 14853 (N.L., P.J.B., E.S.B.); andDepartment of Crop Science, North Carolina State University, Raleigh, North Carolina 27695 (Y.-S.S.).
Charles
C
Chen
Institute for Genomic Diversity (N.Z., J.G.W., K.K., E.S.B.), Boyce Thompson Institute for Plant Research (P.L., L.D., T.B.), Department of Plant Breeding and Genetics (C.C., K.K., E.S.B.), and Department of Plant Biology (T.B.), Cornell University, Ithaca, New York 14853;Max Planck Institute of Molecular Plant Physiology, 14476 Golm-Potsdam, Germany (Y.G., M.S.);United States Department of Agriculture-Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, New York 14853 (N.L., P.J.B., E.S.B.); andDepartment of Crop Science, North Carolina State University, Raleigh, North Carolina 27695 (Y.-S.S.).
Yoon-Sup
YS
So
Institute for Genomic Diversity (N.Z., J.G.W., K.K., E.S.B.), Boyce Thompson Institute for Plant Research (P.L., L.D., T.B.), Department of Plant Breeding and Genetics (C.C., K.K., E.S.B.), and Department of Plant Biology (T.B.), Cornell University, Ithaca, New York 14853;Max Planck Institute of Molecular Plant Physiology, 14476 Golm-Potsdam, Germany (Y.G., M.S.);United States Department of Agriculture-Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, New York 14853 (N.L., P.J.B., E.S.B.); andDepartment of Crop Science, North Carolina State University, Raleigh, North Carolina 27695 (Y.-S.S.).
Karl
K
Kremling
Institute for Genomic Diversity (N.Z., J.G.W., K.K., E.S.B.), Boyce Thompson Institute for Plant Research (P.L., L.D., T.B.), Department of Plant Breeding and Genetics (C.C., K.K., E.S.B.), and Department of Plant Biology (T.B.), Cornell University, Ithaca, New York 14853;Max Planck Institute of Molecular Plant Physiology, 14476 Golm-Potsdam, Germany (Y.G., M.S.);United States Department of Agriculture-Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, New York 14853 (N.L., P.J.B., E.S.B.); andDepartment of Crop Science, North Carolina State University, Raleigh, North Carolina 27695 (Y.-S.S.).
Peter J
PJ
Bradbury
Institute for Genomic Diversity (N.Z., J.G.W., K.K., E.S.B.), Boyce Thompson Institute for Plant Research (P.L., L.D., T.B.), Department of Plant Breeding and Genetics (C.C., K.K., E.S.B.), and Department of Plant Biology (T.B.), Cornell University, Ithaca, New York 14853;Max Planck Institute of Molecular Plant Physiology, 14476 Golm-Potsdam, Germany (Y.G., M.S.);United States Department of Agriculture-Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, New York 14853 (N.L., P.J.B., E.S.B.); andDepartment of Crop Science, North Carolina State University, Raleigh, North Carolina 27695 (Y.-S.S.).
Thomas
T
Brutnell
Institute for Genomic Diversity (N.Z., J.G.W., K.K., E.S.B.), Boyce Thompson Institute for Plant Research (P.L., L.D., T.B.), Department of Plant Breeding and Genetics (C.C., K.K., E.S.B.), and Department of Plant Biology (T.B.), Cornell University, Ithaca, New York 14853;Max Planck Institute of Molecular Plant Physiology, 14476 Golm-Potsdam, Germany (Y.G., M.S.);United States Department of Agriculture-Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, New York 14853 (N.L., P.J.B., E.S.B.); andDepartment of Crop Science, North Carolina State University, Raleigh, North Carolina 27695 (Y.-S.S.) yves.gibon@bordeaux.inra.fr mstitt@mpimp-golm.mpg.de esb33@cornell.edu.
Mark
M
Stitt
Institute for Genomic Diversity (N.Z., J.G.W., K.K., E.S.B.), Boyce Thompson Institute for Plant Research (P.L., L.D., T.B.), Department of Plant Breeding and Genetics (C.C., K.K., E.S.B.), and Department of Plant Biology (T.B.), Cornell University, Ithaca, New York 14853;Max Planck Institute of Molecular Plant Physiology, 14476 Golm-Potsdam, Germany (Y.G., M.S.);United States Department of Agriculture-Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, New York 14853 (N.L., P.J.B., E.S.B.); andDepartment of Crop Science, North Carolina State University, Raleigh, North Carolina 27695 (Y.-S.S.) yves.gibon@bordeaux.inra.fr mstitt@mpimp-golm.mpg.de esb33@cornell.edu.
Edward S
http://orcid.org/0000-0002-3100-371X
ES
Buckler
D002244:Carbon / Q000378:metabolism*; D002256:Carbonic Anhydrases / Q000378:metabolism; D002874:Chromosome Mapping / Q000379:methods*; D016000:Cluster Analysis; D018556:Crops, Agricultural / Q000254:growth & development; D018506:Gene Expression Regulation, Plant; D008040:Genetic Linkage; D055106:Genome-Wide Association Study; D055442:Metabolome / Q000235:genetics; D009584:Nitrogen / Q000378:metabolism*; D020641:Polymorphism, Single Nucleotide / Q000235:genetics; D025341:Principal Component Analysis; D040641:Quantitative Trait Loci / Q000235:genetics; D003313:Zea mays / Q000201:enzymology / Q000235:genetics* / Q000378:metabolism*
D002244:Carbon; D002256:Carbonic Anhydrases; D009584:Nitrogen