Common gardens in teosintes reveal the establishment of a syndrome of adaptation to altitude

PLoS Genet. 2019 Dec 20;15(12):e1008512. doi: 10.1371/journal.pgen.1008512. eCollection 2019 Dec.

Abstract

In plants, local adaptation across species range is frequent. Yet, much has to be discovered on its environmental drivers, the underlying functional traits and their molecular determinants. Genome scans are popular to uncover outlier loci potentially involved in the genetic architecture of local adaptation, however links between outliers and phenotypic variation are rarely addressed. Here we focused on adaptation of teosinte populations along two elevation gradients in Mexico that display continuous environmental changes at a short geographical scale. We used two common gardens, and phenotyped 18 traits in 1664 plants from 11 populations of annual teosintes. In parallel, we genotyped these plants for 38 microsatellite markers as well as for 171 outlier single nucleotide polymorphisms (SNPs) that displayed excess of allele differentiation between pairs of lowland and highland populations and/or correlation with environmental variables. Our results revealed that phenotypic differentiation at 10 out of the 18 traits was driven by local selection. Trait covariation along the elevation gradient indicated that adaptation to altitude results from the assembly of multiple co-adapted traits into a complex syndrome: as elevation increases, plants flower earlier, produce less tillers, display lower stomata density and carry larger, longer and heavier grains. The proportion of outlier SNPs associating with phenotypic variation, however, largely depended on whether we considered a neutral structure with 5 genetic groups (73.7%) or 11 populations (13.5%), indicating that population stratification greatly affected our results. Finally, chromosomal inversions were enriched for both SNPs whose allele frequencies shifted along elevation as well as phenotypically-associated SNPs. Altogether, our results are consistent with the establishment of an altitudinal syndrome promoted by local selective forces in teosinte populations in spite of detectable gene flow. Because elevation mimics climate change through space, SNPs that we found underlying phenotypic variation at adaptive traits may be relevant for future maize breeding.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acclimatization*
  • Gene Flow
  • Genetics, Population
  • Genotyping Techniques
  • Mexico
  • Microsatellite Repeats
  • Phenotype
  • Plant Proteins / genetics*
  • Poaceae / classification
  • Poaceae / genetics
  • Poaceae / growth & development*
  • Polymorphism, Single Nucleotide
  • Quantitative Trait Loci*
  • Selection, Genetic

Substances

  • Plant Proteins

Grants and funding

This work was supported by several grants: one from the French National Research Agency (ANR, http://www.agence-nationale-recherche.fr/) (Project ANR 12-ADAP-0002-01) to MIT and YV that also supported M-AF PhD salary; and one from ECOSNord/ANUIES/CONACYT/SEP (http://www.anuies.mx/programas-y-proyectos/cooperacion-academica-nacional-einternacional/investigacion-conjunta/acuerdo-mexico-francia-programa-ecos-sepconacyt-anuies-ecos-nord) project M12A03 to MIT and LEE. In addition, LEE research was funded by CONACYT-ANUIES 207571, and JAA-L and M-AF postdoctoral salaries were supported by CONACYT-Mexico Investigación Científica Básica (https://www.conacyt.gob.mx/index.php/sni/convocatorias-conacyt/convocatoriasfondos-sectoriales-constituidos/convocatoria-sep-conacyt/investigacion-basica-sep) CB2011/167826 awarded to LEE. NEM-A was funded by a CONACYT PhD fellowship (https://www.conacyt.gob.mx/index.php/becas-y-posgrados/becas-en-el-extranjero) grant no. 579966/410748. OO was funded by the Academy of Finland (grant 309581), the Jane and Aatos Erkko Foundation, and the Research Council of Norway (SFF-III grant 223257). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.