The effect of artificial selection on phenotypic plasticity in maize

Authors: GAGE, JOSEPH - University Of Wisconsin; JARQUIN, DIEGO - University Of Nebraska; ROMAY, MARIA CINTA - Cornell University; LORENZ, AARON - University Of Minnesota; Buckler, Edward - Ed; KAEPPLER, SHAWN - University Of Wisconsin; ALKHALIFAH, NASER - Iowa State University; BOHN, MARTIN - University Of Illinois; CAMPBELL, DARWIN - Iowa State University; Edwards, Jode; ERTL, DAVID - Iowa Corn Promotion Board; Flint-Garcia, Sherry; GARDINER, JACK - University Of Missouri; GOOD, BYRON - University Of Guelph; HIRSCH, CANDICE - University Of Minnesota; Holland, Jim - Jim; HOOKER, DAVID - University Of Guelph; Knoll, Joseph - Joe; KOLKMAN, JUDITH - Cornell University; KRUGER, GREG - University Of Nebraska; Lauter, Nicholas; LAWRENCE-DILL, CAROLYN - Iowa State University; LEE, ELIZABETH - University Of Guelph; LYNCH, JONATHAN - Pennsylvania State University; MURRAY, SETH - Texas A&M University; NELSON, REBECCA - Cornell University; PETZOLDT, JANE - University Of Wisconsin; ROCHEFORD, TORBERT - Purdue University; SCHNABLE, JAMES - University Of Nebraska; SCHNABLE, PATRICK - Iowa State University; Scully, Brian; SMITH, MARGARET - Cornell University; SPRINGER, NATHAN - University Of Minnesota; SRINIVASAN, SRIKANT - Iowa State University; WALTON, RENEE - Iowa State University; WELDEKIDAN, TECLEMARIAM - University Of Delaware; WISSER, RANDELL - University Of Delaware; XU, WENWEI - Texas A&M University; YU, JIANMING - Iowa State University; DE LEON, NATALIA - University Of Wisconsin

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/18/2017
Publication Date: 11/7/2017
Citation: Gage, J., Jarquin, D., Romay, M., Lorenz, A., Buckler IV, E.S., Kaeppler, S., Alkhalifah, N., Bohn, M., Campbell, D., Edwards, J.W., Ertl, D., Flint Garcia, S.A., Gardiner, J., Good, B., Hirsch, C., Holland, J.B., Hooker, D., Knoll, J.E., Kolkman, J., Kruger, G., Lauter, N.C., Lawrence-Dill, C., Lee, E., Lynch, J., Murray, S., Nelson, R., Petzoldt, J., Rocheford, T., Schnable, J., Schnable, P., Scully, B.T., Smith, M., Springer, N., Srinivasan, S., Walton, R., Weldekidan, T., Wisser, R., Xu, W., Yu, J., De Leon, N. 2017. The effect of artificial selection on phenotypic plasticity in maize. Nature Communications. 8:1348. https://doi.org/10.1038/S41467-017-01450-2.
DOI: https://doi.org/10.1038/S41467-017-01450-2

Interpretive Summary: The expression of an individual’s phenotype is a function of its genotype (G), the environment experienced during its lifetime (E), and the complex relationship established by certain genotypes to specific environmental influences. This variable plastic response is referred to as genotype-by-environment interaction (G×E). In this study, leveraging resources from the Maize G×E project, we tested the following hypotheses: 1) loci that have experienced changes in allele frequency due to selection for high productivity explain less G×E variation than regions that did not undergo selection; and 2) G×E variation is disproportionately controlled by regulatory mechanisms. To test the first hypothesis, we identified SNPs that show high divergence in allele frequency between temperate improved and tropical improved maize lines. We then tested how much G×E variation those SNPs explained relative to a set of SNPs that show little to no divergence. To address the second postulation, we examined the location of polymorphisms associated with G×E in relation to nearby genes to search for enrichment of associations in regulatory, as opposed to genic regions.

Technical Abstract: Remarkable productivity levels have been achieved in crop species through artificial selection and adaptation to modern agronomic practices around the world. The question remains as to whether this intensive selection has also changed the ability of improved cultivars to consistently maintain high productivity across variable environmental conditions. A deeper understanding of the types of genetic architecture and modulation mechanisms controlling phenotypic plasticity and genotype by environment (G×E) interaction will enhance the ability to predict performance of crop varieties grown in diverse environmental conditions. We used the framework of the Genomes to Fields (G2F) G×E Maize project to assess the effect of selection on G×E variation and to characterize polymorphisms associated with plastic response. The G×E Maize project evaluated a collection of over 800 diverse maize hybrids across 21 sites in North America in 2014. Genotypes were evaluated for relevant phenological and agronomic characteristics such as flowering time, plant and ear height, and grain yield. Genomic regions displaying evidence of selection during modern temperate maize breeding were identified by evaluating Fst between pools of temperate and tropical inbred lines. Selected genomic regions explained less of the variability for yield G×E than regions that do not show evidence of selection, indicating that improvement due to breeding efforts may have reduced G×E of modern cultivars. A Finlay-Wilkinson regression was used to quantify and subsequently map hybrid stability. Loci associated with stability were evaluated for distance from the closest annotated gene model to identify trends in genomic position of variants controlling stability. We observed an enrichment of variants 0-5,000 base pairs upstream of genes and a corresponding decrease in genic associations, hypothetically due to control of plasticity by short-range regulatory elements.