Award Abstract # 1753800
Collaborative Research: Diversity of Physcomitrium pyriforme in North America and Europe: significance of autopolyploidy within a phylogenomic and experimental framework

NSF Org: DEB
Division Of Environmental Biology
Recipient: TEXAS TECH UNIVERSITY SYSTEM
Initial Amendment Date: May 30, 2018
Latest Amendment Date: April 19, 2023
Award Number: 1753800
Award Instrument: Standard Grant
Program Manager: Maureen Kearney
mkearney@nsf.gov
 (703)292-8239
DEB
 Division Of Environmental Biology
BIO
 Directorate for Biological Sciences
Start Date: June 1, 2018
End Date: December 31, 2023 (Estimated)
Total Intended Award Amount: $417,695.00
Total Awarded Amount to Date: $417,695.00
Funds Obligated to Date: FY 2018 = $417,695.00
History of Investigator:
  • Matthew Johnson (Principal Investigator)
    matt.johnson@ttu.edu
Recipient Sponsored Research Office: Texas Tech University
2500 BROADWAY
LUBBOCK
TX  US  79409
(806)742-3884
Sponsor Congressional District: 19
Primary Place of Performance: Texas Tech University
349 Administration Bldg
Lubbock
TX  US  79409-1035
Primary Place of Performance
Congressional District:
19
Unique Entity Identifier (UEI): EGLKRQ5JBCZ7
Parent UEI:
NSF Program(s): PHYLOGENETIC SYSTEMATICS
Primary Program Source: 01001819DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s):
Program Element Code(s): 117100
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

This project will investigate the effects of genome duplication in plants. Many plant species, including some agricultural crops, have arisen as a result of genome duplication. This natural event results in offspring having genomes that are doubled in content or more as compared to their parents and may have provided opportunities for innovation during plant evolution. However, the short- and long-term consequences of genome duplication in wild plants are not well understood. This research will investigate the natural rate of genome duplication in a wild moss species distributed in North America and Europe. Researchers will create experimental, genome-duplicated offspring in the laboratory to measure how their morphology and reproduction differs from that of their parents. They will then determine if and how duplicated genomes may change over time by comparing the experimental, genome-duplicated offspring to those that occur naturally. Researchers will train undergraduate and graduate students, including members of under-represented groups, and support the professional development of early-career researchers. They will also host regional outreach lectures for K-12 teachers about best-practices in evolutionary biology education. Researchers will engage the public online using the citizen-science iNaturalist platform and will create bilingual (Spanish/English) blog posts about moss biology and polyploid evolution.

This project will expand our understanding of the consequences of autopolyploid evolution in plants. Researchers will use as an experimental model organism the moss species Physcomitrium pyriforme (Funariaceae, the Funaria moss family), which harbors a morphologically-diverse complex of seven karyotypes worldwide. The species is annual, bisexual, selfing, and is easily grown in the laboratory. Unlike most other plant model organisms, its genome content can be doubled with precision in vitro to create autopolyploid offspring. Researchers will compare reproductive barriers among naturally-occurring and artificially-induced autopolyploids as well as their homoploid progenitors. Project outcomes will include a phylogeny of the Physcomitrium pyriforme species-complex based on genome sequence data, an estimate of ploidy changes within the complex over evolutionary time and among populations today, and the description of new species. Researchers will further develop the HybPiper bioinformatics data analysis platform and train other US scientists in this method to enhance research capacity. The project will strengthen research collaborations among US institutions and build natural-history collections.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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Freyman, William A. and Johnson, Matthew G. and Rothfels, Carl J. "homologizer: Phylogenetic phasing of gene copies into polyploid subgenomes" Methods in Ecology and Evolution , v.14 , 2023 https://doi.org/10.1111/2041-210X.14072 Citation Details
Hale, Haley and Gardner, Elliot M. and Viruel, Juan and Pokorny, Lisa and Johnson, Matthew G. "Strategies for reducing persample costs in target capture sequencing for phylogenomics and population genomics in plants" Applications in Plant Sciences , v.8 , 2020 https://doi.org/10.1002/aps3.11337 Citation Details
Medina, Rafael and Johnson, Matthew G. and Liu, Yang and Wickett, Norman J. and Shaw, A. Jonathan and Goffinet, Bernard "Phylogenomic delineation of Physcomitrium (Bryophyta: Funariaceae) based on targeted sequencing of nuclear exons and their flanking regions rejects the retention of Physcomitrella , Physcomitridium and Aphanorrhegma" Journal of Systematics and Evolution , v.57 , 2019 https://doi.org/10.1111/jse.12516 Citation Details
Medina, Rafael and Johnson, Matthew G. and Patel, Nikisha and Tocci, Genevieve E. and Toren, David R. and Goffinet, Bernard "Vindication of Physcomitrium pygmaeum (Funariaceae), an elusive and endangered moss from North America's Great Basin" The Bryologist , v.125 , 2022 https://doi.org/10.1639/0007-2745-125.4.528 Citation Details
Patel, Nikisha and Medina, Rafael and Williams, Lindsay D. and Lemieux, Olivia and Goffinet, Bernard and Johnson, Matthew G. and Betancourt, ed., Andrea and Chapman, ed., Tracey "Frequent allopolyploidy with distant progenitors in the moss genera Physcomitrium and Entosthodon (Funariaceae) identified via subgenome phasing of targeted nuclear genes" Evolution , v.77 , 2023 https://doi.org/10.1093/evolut/qpad171 Citation Details
Slimp, Madeline and Williams, Lindsay D. and Hale, Haley and Johnson, Matthew G. "On the potential of Angiosperms353 for population genomic studies" Applications in Plant Sciences , 2021 https://doi.org/10.1002/aps3.11419 Citation Details
Zhang, Li and Zuo, Qin and Ma, WenZhang and Shevock, James R. and Patel, Nikisha and Johnson, Matthew and Medina, Rafael and Wilding, Nicholas and Goffinet, Bernard "Phylogenomics resolves the rediscovered Himalayan endemic <i>Brachymeniopsis gymnostoma</i> (Bryophyta, Funariaceae), as a species of <i>Entosthodon</i> , prompting also the transfer of <i>Clavitheca poeltii</i>" TAXON , v.72 , 2023 https://doi.org/10.1002/tax.13106 Citation Details

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

Biodiversity encompasses all life on Earth, yet our knowledge regarding the number of species composing the various branches of the tree of life varies, with tiny organisms marking the lower end of the spectrum. Bryophytes are a diverse component of most ecosystems around the globe. As land plants, their evolutionary history began some 500 million years ago, but much of the current species diversity is of rather recent origin, revealing that despite their small stature and overall low morphological complexity these organisms are evolutionarily successful. This prompts the questions, what drives their evolution, or what is natural selection acting on and what triggers innovation in the genetic toolbox of mosses? We explored these questions using a moss that is widespread in North America, and Western Europe, a moss that can be easily grown, and that may harbor several strains differing by the size of their genome. Physcomitrium pyriforme is an annual moss, growing in seasonal habitats, developing its vegetative plants in the fall, and entering dormancy following sexual reproduction and resuming growth in the spring.

 

Intellectual merits – Evolution or descent with modification refers to the passing on to the next generation of a tool kit, with some tools being potentially modified or new. New tools are thought to be developed from copies of existing tools, through modification and optimization for new functions. The two extreme mechanisms to broaden the size of the toolbox is duplicating the entire set, that is whole genome duplication, or acquiring a set from another species via genome merger. We sampled populations of P. pyriforme throughout much of its North American range. We demonstrated that the combination of traits thought to define this species, was in fact shared by seven lineages. Three of these are the outcome of interspecific hybridization, a mechanism once thought to be negligeable in mosses or bryophytes. Sorting the genes of these hybrids into two or more sets to identify the putative parental species revealed that some parents are yet unknown, pointing at even more hidden diversity with this species complex in North America. 

Whole genome duplication is likely a widely underestimated mechanism in mosses. Its consequences on gene evolution are thought to emerge after a lag period. We induced genome duplication in a moss and examined, how the expression of its genes changed in this first generation. We demonstrated for the first time in mosses that such event immediately impacts gene expression, on the scale of at least 11% of genes affected. While the mechanisms underlying these shifts are unknown for now, they do highlight the significance of whole genome duplication in altering the targets of natural selection, and hence in triggering evolution, in mosses, and plants in general. Our project produced methods advancements for the analysis of DNA sequences in species with duplicated genomes. These advancements reduce per-sample costs and make data analysis more efficient, allowing us to address research questions that were not feasible or tractable before.  

 

Broader impacts – This project provided critical professional development to one junior research associate, who now holds a tenure track position at a liberal arts college. Our former associate acquired critical skills in phylogenetic analysis, in processing data of gene expression and in assembling and annotating genomes, all skills that will support pursuing a successful career and mentoring the next generation of students in STEM. The project funded a research technician, who wrote a first-author publication on improving methods in DNA sequencing and is now managing a lab at a major genomics facility. Three undergraduate students, all of whom identify as members of underrepresented minority groups in STEM, worked on the project. The undergradautes gained skills in tissue culture, DNA extraction, and bioinformatics. The grant allowed them to travel to a national botany conference to present their biodiversity research, greatly expanding their understanding of the importance of communication in science. Finally, the project provided opportunities to engage the public through a nation-wide citizen science initiative via iNaturalist which both enhanced awareness of often-hidden moss biodiversity and allowed us to acquire samples during the pandemic.

 


Last Modified: 06/25/2024
Modified by: Matthew G Johnson

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