Extreme copy number variation at a tRNA ligase gene affecting phenology and fitness in yellow monkeyflowers

Thomas C. Nelson, Patrick J. Monnahan, Mariah K. McIntosh, Kayli Anderson, Evan MacArthur-Waltz, Findley R. Finseth, John K. Kelly, Lila Fishman

Research output: Contribution to journalArticlepeer-review

11 Scopus citations

Abstract

Copy number variation (CNV) is a major part of the genetic diversity segregating within populations, but remains poorly understood relative to single nucleotide variation. Here, we report on a tRNA ligase gene (Migut.N02091; RLG1a) exhibiting unprecedented, and fitness-relevant, CNV within an annual population of the yellow monkeyflower Mimulus guttatus. RLG1a variation was associated with multiple traits in pooled population sequencing (PoolSeq) scans of phenotypic and phenological cohorts. Resequencing of inbred lines revealed intermediate-frequency three-copy variants of RLG1a (trip+; 5/35 = 14%), and trip+ lines exhibited elevated RLG1a expression under multiple conditions. trip+ carriers, in addition to being over-represented in late-flowering and large-flowered PoolSeq populations, flowered later under stressful conditions in a greenhouse experiment (p < 0.05). In wild population samples, we discovered an additional rare RLG1a variant (high+) that carries 250–300 copies of RLG1a totalling ~5.7 Mb (20–40% of a chromosome). In the progeny of a high+ carrier, Mendelian segregation of diagnostic alleles and qPCR-based copy counts indicate that high+ is a single tandem array unlinked to the single-copy RLG1a locus. In the wild, high+ carriers had highest fitness in two particularly dry and/or hot years (2015 and 2017; both p < 0.01), while single-copy individuals were twice as fecund as either CNV type in a lush year (2016: p < 0.005). Our results demonstrate fluctuating selection on CNVs affecting phenological traits in a wild population, suggest that plant tRNA ligases mediate stress-responsive life-history traits, and introduce a novel system for investigating the molecular mechanisms of gene amplification.

Original languageEnglish (US)
Pages (from-to)1460-1475
Number of pages16
JournalMolecular ecology
Volume28
Issue number6
DOIs
StatePublished - Mar 2019
Externally publishedYes

Bibliographical note

Funding Information:
National Science Foundation, Grant/Award Number: DEB-0846089, DEB-1457763 and OIA-1736249; National Institute of General Medical Sciences, Grant/Award Number: R01 GM073990

Funding Information:
We thank Gloria Goni-McAteer, Hanna McIntosh, John Crandall and Emily Beck for assistance with the field plant collections, and Aurora Bayless, Daniel Crowser, and Katie Zarn for laboratory and greenhouse help. We appreciate the logistical support for library preparation, qPCR and marker genotyping provided by Tamara Max and Denghui (David) Xing in the University of Montana Genomics Core. This work was supported by NSF DEB-0846089, DEB-1457763, and OIA-1736249 to L.F. and by NIH R01-GM073990 to J.K.K.

Publisher Copyright:
© 2018 John Wiley & Sons Ltd

Keywords

  • balancing selection
  • flowering time
  • fluctuating selection
  • life history
  • standing variation
  • structural variant

Fingerprint

Dive into the research topics of 'Extreme copy number variation at a tRNA ligase gene affecting phenology and fitness in yellow monkeyflowers'. Together they form a unique fingerprint.

Cite this