Connor R. Fitzpatrick

Huazhong Agricultural University

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Marc T. J. Johnson

University of Toronto

Jeffery L. Dangl

University of North Carolina at Chapel Hill

Dor Russ

Huazhong Agricultural University

Corbin D. Jones

University of North Carolina at Chapel Hill

Amy P. Hastings

Cornell University

Anurag A. Agrawal

Cornell University

David S. Guttman

University of Toronto

Isai Salas-González

Universidad Nacional Autónoma de México

Pauline W. Wang

University of Toronto

Marney E. Isaac

University of Toronto

Cooperative Institutions

University of Toronto

University of North Carolina at Chapel Hill

University of British Columbia

University of California, Berkeley

Howard Hughes Medical Institute

Ecological Society of America

John Wiley & Sons (United States)

Lawrence Berkeley National Laboratory

Universidad Nacional Autónoma de México

Cornell University

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Global urban environmental change drives adaptation in white clover

Science (2022)

James S. Santangelo Rob W. Ness Beata Cohan Connor R. Fitzpatrick Simon G. Innes

Urbanization transforms environments in ways that alter biological evolution. We examined whether urban environmental change drives parallel evolution by sampling 110,019 white clover plants from 6169 populations in 160 cities globally. Plants were assayed for a Mendelian antiherbivore defense that also affects tolerance to abiotic stressors. Urban-rural gradients were associated with the evolution of clines in defense in 47% of cities throughout the world. Variation in the strength of clines was explained by environmental changes in drought stress and vegetation cover that varied among cities. Sequencing 2074 genomes from 26 cities revealed that the evolution of urban-rural clines was best explained by adaptive evolution, but the degree of parallel adaptation varied among cities. Our results demonstrate that urbanization leads to adaptation at a global scale.

Environmental change

10.1126/science.abk0989

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Citations (110)

Soil biota composition and the performance of a noxious weed across its invaded range

Krystal Nunes Connor R. Fitzpatrick Peter M. Kotanen

<p>The success of invasive plant species is driven, in part, by feedback with soil ecosystems. Yet, how variation in belowground communities across latitudinal gradients affects invader distributions remains poorly understood. To determine the effect of soil communities on the performance of the noxious weed Cirsium arvense across its invaded range, we grew seedlings for 40 days in soils collected across a 699 km linear distance from both inside and outside established populations. We also described the mesofaunal and bacterial communities across all soil samples. We found that C. arvense typically performed better when grown in soils sourced from northern populations than from southern locations where it has a longer invasion history. We also found evidence that C. arvense performed best in soils sourced from outside invaded patches, although this was not consistent across all sites. The bacterial community showed a significant increase in the magnitude of compositional change in invaded sites at higher latitudes, while the mesofaunal community showed the opposite pattern. Bacterial community composition was significantly correlated with C. arvense performance, although mesofaunal community composition was not. Our results demonstrate that the interactions between an invasive plant and associated soil communities change across the invaded range, and the bacterial community in particular may affect variation in plant performance. Observed patterns may be caused by C.arvense presence and time since invasion allowing for an accumulation of species-specific pathogens in southern soils, while the naivete of northern soils to invasion results in a more responsive bacterial community. Although these interactions are difficult to predict, such effects could possibly facilitate the establishment of this exotic species to novel locations. </p>

Noxious weed

Biota

Cirsium arvense

10.32920/21976787.v1

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A single bacterial genus maintains root growth in a complex microbiome

Nature (2020)

Omri M. Finkel Isai Salas-González Gabriel Castrillo Jonathan M. Conway Theresa F. Law

10.1038/s41586-020-2778-7

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Citations (342)

Appendix B. Study site information including plot measures of evolutionary change in Oenothera biennis populations, soil characteristics, and plant species composition, and a photograph of the ecosystem assays.

Figshare (2016)

Connor R. Fitzpatrick Anurag A. Agrawal Nathan Basiliko Amy P. Hastings Marney E. Isaac

Study site information including plot measures of evolutionary change in Oenothera biennis populations, soil characteristics, and plant species composition, and a photograph of the ecosystem assays.

10.6084/m9.figshare.3563136

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Fifty years of co-evolution and beyond: integrating co-evolution from molecules to species

Molecular Ecology (2015)

Diego Carmona Connor R. Fitzpatrick Marc T. J. Johnson

Fifty years after Ehrlich and Raven's seminal paper, the idea of co-evolution continues to grow as a key concept in our understanding of organic evolution. This concept has not only provided a compelling synthesis between evolutionary biology and community ecology, but has also inspired research that extends beyond its original scope. In this article, we identify unresolved questions about the co-evolutionary process and advocate for the integration of co-evolutionary research from molecular to interspecific interactions. We address two basic questions: (i) What is co-evolution and how common is it? (ii) What is the unit of co-evolution? Both questions aim to explore the heart of the co-evolutionary process. Despite the claim that co-evolution is ubiquitous, we argue that there is in fact little evidence to support the view that reciprocal natural selection and coadaptation are common in nature. We also challenge the traditional view that co-evolution only occurs between traits of interacting species. Co-evolution has the potential to explain evolutionary processes and patterns that result from intra- and intermolecular biochemical interactions within cells, intergenomic interactions (e.g. nuclear-cytoplasmic) within species, as well as intergenomic interactions mediated by phenotypic traits between species. Research that bridges across these levels of organization will help to advance our understanding of the importance of the co-evolutionary processes in shaping the diversity of life on Earth.

Molecular evolution

10.1111/mec.13389

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Citations (41)

An efflux pump family distributed across plant commensal bacteria conditions host- and organ-specific detoxfication of a host-specific glucosinolate

Dor Russ Connor R. Fitzpatrick Chinmay Saha Theresa F. Law Corbin D. Jones

In nature, plants recruit a diverse microbial community, the plant microbiome, that is distinct from the surrounding soil community. To understand the forces that shape the plant microbiome we need to characterize the microbial traits that contribute to plant colonization. We used barcoded mutant libraries to identify bacterial genes that contribute to the colonization of a monocot and a eudicot host. We show that plant colonization is influenced by dozens of genes. While some of these colonization genes were shared between the two host plant species, most were highly specific, benefiting the colonization of a single host and organ. We characterized an efflux pump that specifically contributes to Arabidopsis shoot colonization. This efflux pump is prevalent across Pseudomonadota genomes, yet benefits the bacterial association with only a small subset of Arabidopsis thaliana accessions. Leveraging genomic diversity within Arabidopsis thaliana, we confirmed that specific glucosinolate breakdown products are detoxified by this family of efflux pumps. The broad prevalence of this efflux pump family suggests that its members contribute to protection of commensal bacteria from collateral damage of plant glucosinolate-based defense responses to herbivores and necrotrophic pathogens.

Efflux

10.1101/2024.10.18.619176

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Soil biota composition and the performance of a noxious weed across its invaded range

Ecography (2019)

Krystal Nunes Connor R. Fitzpatrick Peter M. Kotanen

The success of invasive plant species is driven, in part, by feedback with soil ecosystems. Yet, how variation in belowground communities across latitudinal gradients affects invader distributions remains poorly understood. To determine the effect of soil communities on the performance of the noxious weed Cirsium arvense across its invaded range, we grew seedlings for 40 days in soils collected across a 699 km linear distance from both inside and outside established populations. We also described the mesofaunal and bacterial communities across all soil samples. We found that C. arvense typically performed better when grown in soils sourced from northern populations than from southern locations where it has a longer invasion history. We also found evidence that C. arvense performed best in soils sourced from outside invaded patches, although this was not consistent across all sites. The bacterial community showed a significant increase in the magnitude of compositional change in invaded sites at higher latitudes, while the mesofaunal community showed the opposite pattern. Bacterial community composition was significantly correlated with C. arvense performance, although mesofaunal community composition was not. Our results demonstrate that the interactions between an invasive plant and associated soil communities change across the invaded range, and the bacterial community in particular may affect variation in plant performance. Observed patterns may be caused by C.arvense presence and time since invasion allowing for an accumulation of species‐specific pathogens in southern soils, while the naïveté of northern soils to invasion results in a more responsive bacterial community. Although these interactions are difficult to predict, such effects could possibly facilitate the establishment of this exotic species to novel locations.

Noxious weed

Cirsium arvense

Biota

10.1111/ecog.04562

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Citations (11)

Chloroplast sequence variation and the efficacy of peptide nucleic acids for blocking host amplification in plant microbiome studies

Microbiome (2018)

Connor R. Fitzpatrick Patricia Lu‐Irving Julia K. Copeland David S. Guttman Pauline W. Wang

The ability to efficiently characterize microbial communities from host individuals can be limited by co-amplification of host organellar sequences (mitochondrial and/or plastid), which share a common ancestor and thus sequence similarity with extant bacterial lineages. One promising approach is the use of sequence-specific peptide nucleic acid (PNA) clamps, which bind to, and block amplification of, host-derived DNA. Universal PNA clamps have been proposed to block host plant-derived mitochondrial (mPNA) and plastid (pPNA) sequences at the V4 16S rRNA locus, but their efficacy across a wide range of host plant species has not been experimentally tested.Using the universal PNA clamps, we amplified and sequenced root microbial communities from replicate individuals of 32 plant species with a most recent common ancestor inferred at 140 MYA. We found the average rate of host plastid contamination across plant species was 23%, however, particular lineages exhibited much higher rates (62-94%), with the highest levels of contamination occurring in the Asteraceae. We investigated chloroplast sequence variation at the V4 locus across 500 land plant species (Embryophyta) and found six lineages with mismatches between plastid and the universal pPNA sequence, including all species within the Asteraceae. Using a modified pPNA for the Asteraceae sequence, we found (1) host contamination in Asteraceae species was reduced from 65 to 23%; and (2) host contamination in non-Asteraceae species was increased from 12 to 69%. These results demonstrate that even single nucleotide mismatches can lead to drastic reductions in pPNA efficacy in blocking host amplification. Importantly, we found that pPNA type (universal or modified) had no effect on the detection of individual bacterial taxa, or estimates of within and between sample bacterial diversity, suggesting that our modification did not introduce bias against particular bacterial lineages.When high similarity exists between host organellar DNA and PCR target sequences, PNA clamps are an important molecular tool to reduce host contamination during amplification. Here, we provide a validated framework to modify universal PNA clamps to accommodate host variation in organellar sequences.

Blocking (statistics)

10.1186/s40168-018-0534-0

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Citations (85)

Appendix C. Results from linear mixed effect modeling for each ecosystem assay, best-fitting models for each ecosystem assay using a model comparison approach, and a figure illustrating the variance explained by herbivory, plant genotype, evolution, and spatial variation for each ecosystem assay.

Figshare (2016)

Connor R. Fitzpatrick Anurag A. Agrawal Nathan Basiliko Amy P. Hastings Marney E. Isaac

Results from linear mixed effect modeling for each ecosystem assay, best-fitting models for each ecosystem assay using a model comparison approach, and a figure illustrating the variance explained by herbivory, plant genotype, evolution, and spatial variation for each ecosystem assay.

Ecosystem model

Variance components

Mixed model

10.6084/m9.figshare.3563133

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Broader functions of TIR domains in Arabidopsis immunity

bioRxiv (Cold Spring Harbor Laboratory) (2022)

Pierre Jacob Junko Hige Lijiang Song Adam M. Bayless Dor Russ

Abstract TIR domains are NAD-degrading enzymes that function during immune signaling in prokaryotes, plants, and animals. In plants, most TIR domains are incorporated into intracellular immune receptors. In Arabidopsis, TIR-derived small molecules bind and activate EDS1 heterodimers, which in turn activate RNLs, a class of cation channel-forming immune receptors. RNL activation drives cytoplasmic Ca 2+ influx, transcriptional reprogramming, pathogen resistance and host cell death. We screened for mutants that suppress an RNL activation mimic allele and identified a TIR-containing immune receptor, SADR1. Despite functioning downstream of an auto-activated RNL, SADR1 is not required for defense signaling triggered by other tested TIR-containing immune receptors. SADR1 is required for defense signaling initiated by some trans-membrane pattern recognition receptors and contributes to the unbridled spread of cell death in lesion simulating disease 1 . Together with RNLs, SADR1 regulates defense gene expression at infection site borders, likely in a non-autonomous manner. RNL mutants that cannot sustain this pattern of gene expression are unable to prevent disease spread beyond localized infection sites, suggesting that this pattern corresponds to a pathogen containment mechanism. SADR1 potentiates RNL-driven immune signaling partially through the activation of EDS1, but also partially independently of EDS1. We studied EDS1-independent TIR function using nicotinamide, an NADase inhibitor. We observed decreased defense induction from trans-membrane pattern recognition receptors and decreased calcium influx, pathogen growth restriction and host cell death following intracellular immune receptor activation. We demonstrate that TIR domains can potentiate calcium influx and defense and are thus broadly required for Arabidopsis immunity.

Immune receptor

10.1101/2022.12.23.521769

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Citations (1)