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: The persistent homology mathematical framework provides enhanced genotype-to-phenotype associations for plant morphology
Efforts to understand the genetic and environmental conditioning of plant morphology are hindered by the lack of flexible and effective tools for quantifying morphology. Here, we demonstrate that persistent-homology-based topological methods can improve measurement of variation in leaf shape, serrations, and root architecture. We apply these methods to 2D images of leaves and root systems in field-grown plants of a domesticated introgression line population of tomato (Solanum pennellii). We find that compared with some commonly used conventional traits, (1) persistent-homology-based methods can more comprehensively capture morphological variation; (2) these techniques discriminate between genotypes with a larger normalized effect size and detect a greater number of unique quantitative trait loci (QTLs); (3) multivariate traits, whether statistically derived from univariate or persistent-homology-based traits, improve our ability to understand the genetic basis of phenotype; and (4) persistent-homology-based techniques detect unique QTLs compared to conventional traits or their multivariate derivatives, indicating that previously unmeasured aspects of morphology are now detectable. The QTL results further imply that genetic contributions to morphology can affect both the shoot and root, revealing a pleiotropic basis to natural variation in tomato. Persistent homology is a versatile framework to quantify plant morphology and developmental processes that complements and extends existing methods.  more » « less
Award ID(s):
1638507
PAR ID:
10095874
Author(s) / Creator(s):
; ; ; ; ;
Date Published:
Journal Name:
Plant Physiology
ISSN:
0032-0889
Page Range / eLocation ID:
pp.00104.2018
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. SUMMARY A major challenge in global crop production is mitigating yield loss due to plant diseases. One of the best strategies to control these losses is through breeding for disease resistance. One barrier to the identification of resistance genes is the quantification of disease severity, which is typically based on the determination of a subjective score by a human observer. We hypothesized that image‐based, non‐destructive measurements of plant morphology over an extended period after pathogen infection would capture subtle quantitative differences between genotypes, and thus enable identification of new disease resistance loci. To test this, we inoculated a genetically diverse biparental mapping population of tomato (Solanum lycopersicum) withRalstonia solanacearum, a soilborne pathogen that causes bacterial wilt disease. We acquired over 40 000 time‐series images of disease progression in this population, and developed an image analysis pipeline providing a suite of 10 traits to quantify bacterial wilt disease based on plant shape and size. Quantitative trait locus (QTL) analyses using image‐based phenotyping for single and multi‐traits identified QTLs that were both unique and shared compared with those identified by human assessment of wilting, and could detect QTLs earlier than human assessment. Expanding the phenotypic space of disease with image‐based, non‐destructive phenotyping both allowed earlier detection and identified new genetic components of resistance. 
    more » « less
  2. de_Koning, D-J (Ed.)
    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
  3. Pearce, S (Ed.)
    Abstract This study investigated the genetic basis of carrot root shape traits using composite interval mapping in two biparental populations (n = 119 and n = 128). The roots of carrot F2:3 progenies were grown over 2 years and analyzed using a digital imaging pipeline to extract root phenotypes that compose market class. Broad-sense heritability on an entry-mean basis ranged from 0.46 to 0.80 for root traits. Reproducible quantitative trait loci (QTL) were identified on chromosomes 2 and 6 on both populations. Colocalization of QTLs for phenotypically correlated root traits was also observed and coincided with previously identified QTLs in published association and linkage mapping studies. Individual QTLs explained between 14 and 27% of total phenotypic variance across traits, while four QTLs for length-to-width ratio collectively accounted for up to 73% of variation. Predicted genes associated with the OFP-TRM (OVATE Family Proteins—TONNEAU1 Recruiting Motif) and IQD (IQ67 domain) pathway were identified within QTL support intervals. This observation raises the possibility of extending the current regulon model of fruit shape to include carrot storage roots. Nevertheless, the precise molecular mechanisms through which this pathway operates in roots characterized by secondary growth originating from cambium layers remain unknown. 
    more » « less
  4. Summary Pollination syndromes are a key component of flowering plant diversification, prompting questions about the architecture of single traits and genetic coordination among traits. Here, we investigate the genetics of extreme floral divergence between naturally hybridizing monkeyflowers,Mimulus parishii(self‐pollinated) andM. cardinalis(hummingbird‐pollinated).We mapped quantitative trait loci (QTLs) for 18 pigment, pollinator reward/handling, and dimensional traits in parallel sets of F2hybrids plus recombinant inbred lines and generated nearly isogenic lines (NILs) for two dimensional traits, pistil length and corolla size.Our multi‐population approach revealed a highly polygenic basis (n = 190 QTLs total) for pollination syndrome divergence, capturing minor QTLs even for pigment traits with leading major loci. There was significant QTL overlap within pigment and dimensional categories. Nectar volume QTLs clustered with those for floral dimensions, suggesting a partially shared module. The NILs refined two pistil length QTLs, only one of which has tightly correlated effects on other dimensional traits.An overall polygenic architecture of floral divergence is partially coordinated by genetic modules formed by linkage (pigments) and likely pleiotropy (dimensions plus nectar). This work illuminates pollinator syndrome diversification in a model radiation and generates a robust framework for molecular and ecological genomics. 
    more » « less
  5. null (Ed.)
    Tomato (Solanum lycopersicum L.) is a widely used model plant species for dissecting out the genomic bases of complex traits to thus provide an optimal platform for modern “-omics” studies and genome-guided breeding. Genome-wide association studies (GWAS) have become a preferred approach for screening large diverse populations and many traits. Here, we present GWAS analysis of a collection of 115 landraces and 11 vintage and modern cultivars. A total of 26 conventional descriptors, 40 traits obtained by digital phenotyping, the fruit content of six carotenoids recorded at the early ripening (breaker) and red-ripe stages and 21 climate-related variables were analyzed in the context of genetic diversity monitored in the 126 accessions. The data obtained from thorough phenotyping and the SNP diversity revealed by sequencing of ripe fruit transcripts of 120 of the tomato accessions were jointly analyzed to determine which genomic regions are implicated in the expressed phenotypic variation. This study reveals that the use of fruit RNA-Seq SNP diversity is effective not only for identification of genomic regions that underlie variation in fruit traits, but also of variation related to additional plant traits and adaptive responses to climate variation. These results allowed validation of our approach because different marker-trait associations mapped on chromosomal regions where other candidate genes for the same traits were previously reported. In addition, previously uncharacterized chromosomal regions were targeted as potentially involved in the expression of variable phenotypes, thus demonstrating that our tomato collection is a precious reservoir of diversity and an excellent tool for gene discovery. 
    more » « less