skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Induced and natural variation affect traits independently in hybrid Populus
Abstract The genetic control of many plant traits can be highly complex. Both allelic variation (sequence change) and dosage variation (copy number change) contribute to a plant's phenotype. While numerous studies have investigated the effect of allelic or dosage variation, very few have documented both within the same system, leaving their relative contribution to phenotypic effects unclear. The Populus genome is highly polymorphic, and poplars are fairly tolerant of gene dosage variation. Here, using a previously established Populus hybrid F1 population, we assessed and compared the effect of natural allelic variation and induced dosage variation on biomass, phenology, and leaf morphology traits. We identified QTLs for many of these traits, but our results indicate limited overlap between the QTLs associated with natural allelic variation and induced dosage variation. Additionally, the integration of data from both allelic and dosage variation identifies a larger set of QTLs that together explain a larger percentage of the phenotypic variance. Finally, our results suggest that the effect of the large indels might mask that of allelic QTLs. Our study helps clarify the relationship between allelic and dosage variation and their effects on quantitative traits.  more » « less
Award ID(s):
1956429
PAR ID:
10579340
Author(s) / Creator(s):
; ; ; ;
Editor(s):
de_Koning, D-J
Publisher / Repository:
Oxford University Press / Genetics Society of America
Date Published:
Journal Name:
G3: Genes, Genomes, Genetics
Volume:
14
Issue:
11
ISSN:
2160-1836
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Cryptic genetic variants exert minimal phenotypic effects alone but are hypothesized to form a vast reservoir of genetic diversity driving trait evolvability through epistatic interactions1–3. This classical theory has been reinvigorated by pan-genomics, which is revealing pervasive variation within gene families,cis-regulatory regions and regulatory networks4–6. Testing the ability of cryptic variation to fuel phenotypic diversification has been hindered by intractable genetics, limited allelic diversity and inadequate phenotypic resolution. Here, guided by natural and engineeredcis-regulatory cryptic variants in a paralogous gene pair, we identified additional redundanttransregulators, establishing a regulatory network controlling tomato inflorescence architecture. By combining coding mutations withcis-regulatory alleles in populations segregating for all four network genes, we generated 216 genotypes spanning a wide spectrum of inflorescence complexity and quantified branching in over 35,000 inflorescences. Analysis of this high-resolution genotype–phenotype map using a hierarchical model of epistasis revealed a layer of dose-dependent interactions within paralogue pairs enhancing branching, culminating in strong, synergistic effects. However, we also identified a layer of antagonism between paralogue pairs, whereby accumulating mutations in one pair progressively diminished the effects of mutations in the other. Our results demonstrate how gene regulatory network architecture and complex dosage effects from paralogue diversification converge to shape phenotypic space, producing the potential for both strongly buffered phenotypes and sudden bursts of phenotypic change. 
    more » « less
  2. Abstract Elevated nighttime temperatures resulting from climate change significantly impact the rice crop worldwide. The rice ( Oryza sativa L.) plant is highly sensitive to high nighttime temperature (HNT) during grain-filling (reproductive stage). HNT stress negatively affects grain quality traits and has a major impact on the value of the harvested rice crop. In addition, along with grain dimensions determining rice grain market classes, the grain appearance and quality traits determine the rice grain market value. During the last few years, there has been a major concern for rice growers and the rice industry over the prevalence of rice grains opacity and the reduction of grain dimensions affected by HNT stress. Hence, the improvement of heat-stress tolerance to maintain grain quality of the rice crop under HNT stress will bolster future rice value in the market. In this study, 185 F 12 - recombinant inbred lines (RILs) derived from two US rice cultivars, Cypress (HNT-tolerant) and LaGrue (HNT-sensitive) were screened for the grain quality traits grain length (GL), grain width (GW), and percent chalkiness (%chalk) under control and HNT stress conditions and evaluated to identify the genomic regions associated with the grain quality traits. In total, there were 15 QTLs identified; 6 QTLs represented under control condition explaining 3.33% to 8.27% of the phenotypic variation, with additive effects ranging from − 0.99 to 0.0267 on six chromosomes and 9 QTLs represented under HNT stress elucidating 6.39 to 51.53% of the phenotypic variation, with additive effects ranging from − 8.8 to 0.028 on nine chromosomes for GL, GW, and % chalk. These 15 QTLs were further characterized and scanned for natural genetic variation in a japonica diversity panel (JDP) to identify candidate genes for GL, GW, and %chalk. We found 6160 high impact single nucleotide polymorphisms (SNPs) characterized as such depending on their type, region, functional class, position, and proximity to the gene and/or gene features, and 149 differentially expressed genes (DEGs) in the 51 Mbp genomic region comprising of the 15 QTLs. Out of which, 11 potential candidate genes showed high impact SNP associations. Therefore, the analysis of the mapped QTLs and their genetic dissection in the US grown Japonica rice genotypes at genomic and transcriptomic levels provide deep insights into genetic variation beneficial to rice breeders and geneticists for understanding the mechanisms related to grain quality under heat stress in rice. 
    more » « less
  3. ABSTRACT Cryptic genetic variants exert minimal or no phenotypic effects alone but have long been hypothesized to form a vast, hidden reservoir of genetic diversity that drives trait evolvability through epistatic interactions. This classical theory has been reinvigorated by pan-genome sequencing, which has revealed pervasive variation within gene families and regulatory networks, including extensive cis-regulatory changes, gene duplication, and divergence between paralogs. Nevertheless, empirical testing of cryptic variation’s capacity to fuel phenotypic diversification has been hindered by intractable genetics, limited allelic diversity, and inadequate phenotypic resolution. Here, guided by natural and engineered cis-regulatory cryptic variants in a recently evolved paralogous gene pair, we identified an additional pair of redundant trans regulators, establishing a regulatory network that controls tomato inflorescence architecture. By combining coding mutations with a cis-regulatory allelic series in populations segregating for all four network genes, we systematically constructed a collection of 216 genotypes spanning the full spectrum of inflorescence complexity and quantified branching in over 27,000 inflorescences. Analysis of the resulting high-resolution genotype-phenotype map revealed a layer of dose-dependent interactions within paralog pairs that enhances branching, culminating in strong, synergistic effects. However, we also uncovered an unexpected layer of antagonism between paralog pairs, where accumulating mutations in one pair progressively diminished the effects of mutations in the other. Our results demonstrate how gene regulatory network architecture and complex dosage effects from paralog diversification converge to shape phenotypic space under a hierarchical model of epistatic interactions. Given the prevalence of paralog evolution in genomes, we propose that paralogous cryptic variation within regulatory networks elicits hierarchies of epistatic interactions, catalyzing bursts of phenotypic change. Keyword:cryptic mutations, paralogs, redundancy, cis-regulatory, tomato, inflorescence, gene regulatory network, modeling, epistasis 
    more » « less
  4. Abstract Phenotypic variation is common along environmental gradients, but it is often not known to what extent it results from genetic differentiation between populations or phenotypic plasticity. We studied populations of a livebearing fish that have colonized streams rich in toxic hydrogen sulphide (H2S). There is strong phenotypic differentiation between adjacent sulphidic and non-sulphidic populations. In this study, we varied food availability to pregnant mothers from different populations to induce maternal effects, a form of plasticity, and repeatedly measured life-history and behavioural traits throughout the ontogeny of the offspring. Genetic differentiation affected most of the traits we measured, in that sulphidic offspring tended to be born larger, mature later, have lower burst swimming performance, be more exploratory, and feed less effectively. In contrast, maternal effects impacted few traits and at a smaller magnitude, although offspring from poorly provisioned mothers tended to be born larger and be more exploratory. Population differences and maternal effects (when both were present) acted additively, and there was no evidence for population differences in plasticity. Overall, our study suggests that phenotypic divergence between these populations in nature is caused primarily by genetic differentiation and that plasticity mediated by maternal effects accentuates but does not cause differences between populations. 
    more » « less
  5. Selection on quantitative traits by heterogeneous climatic conditions can lead to substantial trait variation across a species range. In the context of rapidly changing environments, however, it is equally important to understand selection on trait plasticity. To evaluate the role of selection in driving divergences in traits and their associated plasticities within a widespread species, we compared molecular and quantitative trait variation in Populus fremontii (Fremont cottonwood), a foundation riparian distributed throughout Arizona. Using SNP data and genotypes from 16 populations reciprocally planted in three common gardens, we first performed QST-FST analyses to detect selection on traits and trait plasticity. We then explored the environmental drivers of selection using trait-climate and plasticity-climate regressions. Three major findings emerged: 1) There was significant genetic variation in traits expressed in each of the common gardens and in the phenotypic plasticity of traits across gardens, both of which were heritable. 2) Based on QST-FST comparisons, there was evidence of selection in all traits measured; however, this result varied from no effect in one garden to highly significant in another, indicating that detection of past selection is environmentally dependent. We also found strong evidence of divergent selection on plasticity across environments for two traits. 3) Traits and/or their plasticity were often correlated with population source climate (R2 up to 0.77 and 0.66, respectively). These results suggest that steep climate gradients across the Southwest have played a major role in shaping the evolution of divergent phenotypic responses in populations and genotypes now experiencing climate change. 
    more » « less