skip to main content


Title: Multivariate analysis reveals environmental and genetic determinants of element covariation in the maize grain ionome
Abstract

The integrated responses of biological systems to genetic and environmental variation result in substantial covariance in multiple phenotypes. The resultant pleiotropy, environmental effects, and genotype‐by‐environmental interactions (GxE) are foundational to our understanding of biology and genetics. Yet, the treatment of correlated characters, and the identification of the genes encoding functions that generate this covariance, has lagged. As a test case for analyzing the genetic basis underlying multiple correlated traits, we analyzed maize kernel ionomes from Intermated B73 x Mo17 (IBM) recombinant inbred populations grown in 10 environments. Plants obtain elements from the soil through genetic and biochemical pathways responsive to physiological state and environment. Most perturbations affect multiple elements which leads theionome, the full complement of mineral nutrients in an organism, to vary as an integrated network rather than a set of distinct single elements. We compared quantitative trait loci (QTL) determining single‐element variation toQTLthat predict variation in principal components (PCs) of multiple‐element covariance. Single‐element and multivariate approaches detected partially overlapping sets of loci.QTLinfluencing trait covariation were detected at loci that were not found by mapping single‐element traits. Moreover, this approach permitted testing environmental components of trait covariance, and identified multi‐element traits that were determined by both genetic and environmental factors as well as genotype‐by‐environment interactions. Growth environment had a profound effect on the elemental profiles and multi‐element phenotypes were significantly correlated with specific environmental variables.

 
more » « less
NSF-PAR ID:
10119998
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Plant Direct
Volume:
3
Issue:
5
ISSN:
2475-4455
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    While traits and trait plasticity are partly genetically based, investigating epigenetic mechanisms may provide more nuanced understanding of the mechanisms underlying response to environment. UsingAFLPand methylation‐sensitiveAFLP, we tested the hypothesis that differentiation to habitats along natural salt marsh environmental gradients occurs at epigenetic, but not genetic loci in two salt marsh perennials. We detected significant genetic and epigenetic structure among populations and among subpopulations, but we found multilocus patterns of differentiation to habitat type only in epigenetic variation for both species. In addition, more epigenetic than genetic loci were correlated with habitat in both species. When we analysed genetic and epigenetic variation simultaneously with partial Mantel, we found no correlation between genetic variation and habitat and a significant correlation between epigenetic variation and habitat inSpartina alterniflora. InBorrichia frutescens, we found significant correlations between epigenetic and/or genetic variation and habitat in four of five populations when populations were analysed individually, but there was no significant correlation between genetic or epigenetic variation and habitat when analysed jointly across the five populations. These analyses suggest that epigenetic mechanisms are involved in the response to salt marsh habitats, but also that the relationships among genetic and epigenetic variation and habitat vary by species. Site‐specific conditions may also cloud our ability to detect response in replicate populations with similar environmental gradients. Future studies analysing sequence data and the correlation between genetic variation andDNAmethylation will be powerful to identify the contributions of genetic and epigenetic response to environmental gradients.

     
    more » « less
  2. Abstract

    The genetic architecture of local adaptation has been of central interest to evolutionary biologists since the modern synthesis. In addition to classic theory on the effect size of adaptive mutations by Fisher, Kimura and Orr, recent theory addresses the genetic architecture of local adaptation in the face of ongoing gene flow. This theory predicts that with substantial gene flow between populations local adaptation should proceed primarily through mutations of large effect or tightly linked clusters of smaller effect loci. In this study, we investigate the genetic architecture of divergence in flowering time, mating system‐related traits, and leaf shape betweenMimulus laciniatusand a sympatric population of its close relativeM. guttatus. These three traits are probably involved inM. laciniatus’adaptation to a dry, exposed granite outcrop environment. Flowering time and mating system differences are also reproductive isolating barriers making them ‘magic traits’. Phenotypic hybrids in this population provide evidence of recent gene flow. Using next‐generation sequencing, we generate denseSNPmarkers across the genome and map quantitative trait loci (QTLs) involved in flowering time, flower size and leaf shape. We find that interspecific divergence in all three traits is due to fewQTLof large effect including a highly pleiotropicQTLon chromosome 8. ThisQTLregion contains the pleiotropic candidate gene TCP4 and is involved in ecologically important phenotypes in otherMimulusspecies. Our results are consistent with theory, indicating that local adaptation and reproductive isolation with gene flow should be due to few loci with large and pleiotropic effects.

     
    more » « less
  3. Summary

    Genetic correlations among different components of phenotypes, especially those resulting from pleiotropy, can constrain or facilitate trait evolution. These factors could especially influence the evolution of traits that are functionally integrated, such as those comprising the flower. Indeed, pleiotropy is proposed as a main driver of repeated convergent trait transitions, including the evolution of phenotypically similar pollinator syndromes.

    We assessed the role of pleiotropy in the differentiation of floral and other reproductive traits between two species –Jaltomata sinuosaandJ. umbellata(Solanaceae) – that have divergent suites of floral traits consistent with bee and hummingbird pollination, respectively. To do so, we generated a hybrid population and examined the genetic architecture (trait segregation and quantitative trait locus (QTL) distribution) underlying 25 floral and fertility traits.

    We found that most floral traits had a relatively simple genetic basis (few, predominantly additive,QTLs of moderate to large effect), as well as little evidence of antagonistic pleiotropy (few trait correlations andQTLcolocalization, particularly between traits of different classes). However, we did detect a potential case of adaptive pleiotropy among floral size and nectar traits.

    These mechanisms may have facilitated the rapid floral trait evolution observed withinJaltomata, and may be a common component of rapid phenotypic change more broadly.

     
    more » « less
  4. Abstract

    Phenotypic plasticity allows organisms to change their phenotype in response to shifts in the environment. While a central topic in current discussions of evolutionary potential, a comprehensive understanding of the genetic underpinnings of plasticity is lacking in systems undergoing adaptive diversification. Here, we investigate the genetic basis of phenotypic plasticity in a textbook adaptive radiation, Lake Malawi cichlid fishes. Specifically, we crossed two divergent species to generate an F3hybrid mapping population. At early juvenile stages, hybrid families were split and reared in alternate foraging environments that mimicked benthic/scraping or limnetic/sucking modes of feeding. These alternate treatments produced a variation in morphology that was broadly similar to the major axis of divergence among Malawi cichlids, providing support for the flexible stem theory of adaptive radiation. Next, we found that the genetic architecture of several morphological traits was highly sensitive to the environment. In particular, of 22 significant quantitative trait loci (QTL), only one was shared between the environments. In addition, we identifiedQTLacting across environments with alternate alleles being differentially sensitive to the environment. Thus, our data suggest that while plasticity is largely determined by loci specific to a given environment, it may also be influenced by loci operating across environments. Finally, our mapping data provide evidence for the evolution of plasticity via genetic assimilation at an important regulatory locus,ptch1. In all, our data address long‐standing discussions about the genetic basis and evolution of plasticity. They also underscore the importance of the environment in affecting developmental outcomes, genetic architectures, morphological diversity and evolutionary potential.

     
    more » « less
  5. Abstract

    Floral attraction traits can significantly affect pollinator visitation patterns, but adaptive evolution of these traits may be constrained by correlations with other traits. In some cases, molecular pathways contributing to floral attraction are well characterized, offering the opportunity to explore loci potentially underlying variation among individuals. Here, we quantify the range of variation in floralUVpatterning (i.e.UV‘bulls‐eye nectar guides) among crop and wild accessions ofBrassica rapa. We then use experimental crosses to examine the genetic architecture, candidate loci and biochemical underpinnings of this patterning as well as phenotypic manipulations to test the ecological impact. We find qualitative variation inUVpatterning between wild (commonly lackingUVpatterns) and crop (commonly exhibitingUVpatterns) accessions. Similar to the majority of crops, recombinant inbred lines (RILs) derived from an oilseed crop × WIfast‐plant®cross exhibitUVpatterns, the size of which varies extensively among genotypes. InRILs, we further observe strong statistical‐genetic andQTLcorrelations within petal morphological traits and within measurements of petalUVpatterning; however, correlations between morphology andUVpatterning are weak or nonsignificant, suggesting thatUVpatterning is regulated and may evolve independently of overall petal size.HPLCanalyses reveal a high concentration of sinapoyl glucose inUV‐absorbing petal regions, which, in concert with physical locations ofUV‐traitQTLs, suggest a regulatory and structural gene as candidates underlying observed quantitative variation. Finally, insects prefer flowers withUVbulls‐eye patterns over those that lack patterns, validating the importance ofUVpatterning in pollen‐limited populations ofB. rapa.

     
    more » « less