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

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...

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Published in:Molecular ecology 2019-03, Vol.28 (6), p.1460-1475
Main Authors: Nelson, Thomas C., Monnahan, Patrick J., McIntosh, Mariah K., Anderson, Kayli, MacArthur‐Waltz, Evan, Finseth, Findley R., Kelly, John K., Fishman, Lila
Format: Article
Language:English
Subjects:
alleles
balancing selection
Chromosome Mapping
Copy number
copy number variation
Diagnostic systems
DNA Copy Number Variations - genetics
Erythranthe guttata
Extreme values
Fitness
Flowering
flowering time
fluctuating selection
Gene amplification
Genetic diversity
Genetic Fitness
Genetics, Population
greenhouse experimentation
inbred lines
Inbreeding
life history
ligases
loci
Mimulus - genetics
Mimulus - physiology
Mimulus guttatus
Molecular modelling
phenology
Phenotype
Population
Population genetics
Populations
Progeny
Quantitative Trait Loci - genetics
Reproductive fitness
RNA Ligase (ATP) - genetics
standing variation
structural variant
transfer RNA
tRNA
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cited_by cdi_FETCH-LOGICAL-c4414-e6e8bfeb6b0ae3130a99f532a9c80fd1ca668a56311dd9554b641579666e52823
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container_issue 6
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creator Nelson, Thomas C.
Monnahan, Patrick J.
McIntosh, Mariah K.
Anderson, Kayli
MacArthur‐Waltz, Evan
Finseth, Findley R.
Kelly, John K.
Fishman, Lila
description 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 
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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 &lt; 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 &lt; 0.01), while single‐copy individuals were twice as fecund as either CNV type in a lush year (2016: p &lt; 0.005). 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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 &lt; 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 &lt; 0.01), while single‐copy individuals were twice as fecund as either CNV type in a lush year (2016: p &lt; 0.005). 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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 &lt; 0.01), while single‐copy individuals were twice as fecund as either CNV type in a lush year (2016: p &lt; 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.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>30346101</pmid><doi>10.1111/mec.14904</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-7297-9049</orcidid><orcidid>https://orcid.org/0000-0003-0627-091X</orcidid></addata></record>
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source Wiley-Blackwell Read & Publish Collection
subjects alleles
balancing selection
Chromosome Mapping
Copy number
copy number variation
Diagnostic systems
DNA Copy Number Variations - genetics
Erythranthe guttata
Extreme values
Fitness
Flowering
flowering time
fluctuating selection
Gene amplification
Genetic diversity
Genetic Fitness
Genetics, Population
greenhouse experimentation
inbred lines
Inbreeding
life history
ligases
loci
Mimulus - genetics
Mimulus - physiology
Mimulus guttatus
Molecular modelling
phenology
Phenotype
Population
Population genetics
Populations
Progeny
Quantitative Trait Loci - genetics
Reproductive fitness
RNA Ligase (ATP) - genetics
standing variation
structural variant
transfer RNA
tRNA
title Extreme copy number variation at a tRNA ligase gene affecting phenology and fitness in yellow monkeyflowers
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