David Haak - Academia.edu (original) (raw)

Papers by David Haak

PeerJ, Jun 9, 2023

The gut of the European honey bee (Apis mellifera) possesses a relatively simple bacterial commun... more The gut of the European honey bee (Apis mellifera) possesses a relatively simple bacterial community, but little is known about its community of prophages (temperate bacteriophages integrated into the bacterial genome). Although prophages may eventually begin replicating and kill their bacterial hosts, they can also sometimes be beneficial for their hosts by conferring protection from other phage infections or encoding genes in metabolic pathways and for toxins. In this study, we explored prophages in 17 species of core bacteria in the honey bee gut and two honey bee pathogens. Out of the 181 genomes examined, 431 putative prophage regions were predicted. Among core gut bacteria, the number of prophages per genome ranged from zero to seven and prophage composition (the compositional percentage of each bacterial genome attributable to prophages) ranged from 0 to 7%. Snodgrassella alvi and Gilliamella apicola had the highest median prophages per genome (3.0 ± 1.46; 3.0 ± 1.59), as well as the highest prophage composition (2.58% ± 1.4; 3.0% ± 1.59). The pathogen Paenibacillus larvae had a higher median number of prophages (8.0 ± 5.33) and prophage composition (6.40% ± 3.08) than the pathogen Melissococcus plutonius or any of the core bacteria. Prophage populations were highly specific to their bacterial host species, suggesting most prophages were acquired recently relative to the divergence of these bacterial groups. Furthermore, functional annotation of the predicted genes encoded within the prophage regions indicates that some prophages in the honey bee gut encode additional benefits to their bacterial hosts, such as genes in carbohydrate metabolism. Collectively, this survey suggests that prophages within the honey bee gut may contribute to the maintenance and stability of the honey bee gut microbiome and potentially modulate specific members of the bacterial community, particularly S. alvi and G. apicola.

PLOS ONE, Jun 23, 2023

Soybean is a major source of seed protein and oil globally with an average composition of 40% pro... more Soybean is a major source of seed protein and oil globally with an average composition of 40% protein and 20% oil in the seed. The goal of this study was to identify quantitative trait loci (QTL) conferring seed protein and oil content utilizing a population constructed by crossing an above average protein content line, PI 399084 to another line that had a low protein content value, PI 507429, both from the USDA soybean germplasm collection. The recombinant inbred line (RIL) population, PI 507429 x PI 399084, was evaluated in two replications over four years (2018-2021); the seeds were analyzed for seed protein and oil content using near-infrared reflectance spectroscopy. The recombinant inbred lines and the two parents were re-sequenced using genotyping by sequencing. A total of 12,761 molecular markers, which came from genotyping by sequencing, the SoySNP6k BeadChip and selected simple sequence repeat (SSR) markers from known protein QTL chromosomal regions were used for mapping. One QTL was identified on chromosome 2 explaining up to 56.8% of the variation for seed protein content and up to 43% for seed oil content. Another QTL identified on chromosome 15 explained up to 27.2% of the variation for seed protein and up to 41% of the variation for seed oil content. The protein and oil QTLs of this study and their associated molecular markers will be useful in breeding to improve nutritional quality in soybean.

Trends in Plant Science, Oct 1, 2021

Weeds, plants that thrive in the face of disturbance, have eluded human's attempts at control... more Weeds, plants that thrive in the face of disturbance, have eluded human's attempts at control for >12 000 years, positioning them as a unique group of extreme stress tolerators. The most successful weeds have a suite of traits that enable them to rapidly adapt to environments typified by stress, growing in hostile conditions or subject to massive destruction from agricultural practices. Through their ability to persist and adapt, weeds illuminate principles of evolution and provide insights into weed management and crop improvement. Here we highlight why the time is right to move beyond traditional model systems and leverage weeds to gain a deeper understanding of the mechanisms, adaptations, and genetic and physiological bases for stress tolerance.

Plants, people, planet, Aug 19, 2019

This is an open access article under the terms of the Creative Commons Attribution License, which... more This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Phytobiomes journal, 2021

Plant microbiota play essential roles in plant health and crop productivity. Comparisons of commu... more Plant microbiota play essential roles in plant health and crop productivity. Comparisons of community composition have suggested seed, soil, and the atmosphere as reservoirs of phyllosphere microbiota. After finding that leaves of tomato (Solanum lycopersicum) plants exposed to rain carried a higher microbial population size than leaves of tomato plants not exposed to rain, we experimentally tested the hypothesis that rain is a thus-far-neglected reservoir of phyllosphere microbiota. Therefore, rain microbiota were compared with phyllosphere microbiota of tomato plants either treated with concentrated rain microbiota, filter-sterilized rain, or sterile water. Based on 16S ribosomal RNA amplicon sequencing, 104 operational taxonomic units (OTUs) significantly increased in relative abundance after inoculation with concentrated rain microbiota but no OTU significantly increased after treatment with either sterile water or filtersterilized rain. Some of the genera to which these 104 OTUs belonged were also found at higher relative abundance on tomato plants exposed to rain outdoors than on tomato plants grown protected from rain in a commercial greenhouse. Taken together, these results point to precipitation as a reservoir of phyllosphere microbiota and show the potential of controlled experiments to investigate the role of different reservoirs in the assembly of phyllosphere microbiota.

PLOS Biology, Feb 12, 2016

Speciation events often occur in rapid bursts of diversification, but the ecological and genetic ... more Speciation events often occur in rapid bursts of diversification, but the ecological and genetic factors that promote these radiations are still much debated. Using whole transcriptomes from all 13 species in the ecologically and reproductively diverse wild tomato clade (Solanum sect. Lycopersicon), we infer the species phylogeny and patterns of genetic diversity in this group. Despite widespread phylogenetic discordance due to the sorting of ancestral variation, we date the origin of this radiation to approximately 2.5 million years ago and find evidence for at least three sources of adaptive genetic variation that fuel diversification. First, we detect introgression both historically between early-branching lineages and recently between individual populations, at specific loci whose functions indicate likely adaptive benefits. Second, we find evidence of lineage-specific de novo evolution for many genes, including loci involved in the production of red fruit color. Finally, using a "PhyloG-WAS" approach, we detect environment-specific sorting of ancestral variation among populations that come from different species but share common environmental conditions. Estimated across the whole clade, small but substantial and approximately equal fractions of the euchromatic portion of the genome are inferred to contribute to each of these three sources of adaptive genetic variation. These results indicate that multiple genetic sources can promote rapid diversification and speciation in response to new ecological opportunity, in agreement with our emerging phylogenomic understanding of the complexity of both ancient and recent species radiations.

Phytopathology, Jun 14, 2023

Parastagonospora nodorum is a necrotrophic pathogen causing Stagonospora nodorum blotch (SNB) in ... more Parastagonospora nodorum is a necrotrophic pathogen causing Stagonospora nodorum blotch (SNB) in wheat. Wheat varieties grown in Virginia vary in susceptibility to SNB, and severity varies across locations and years. However, impacts of wheat genetic backgrounds and environments on SNB severity and structure of P. nodorum populations in the region has not been well studied. A population genetic study was conducted utilizing P. nodorum isolates collected from different wheat varieties and locations in Virginia. Isolates (n=320) were collected at seven locations over two years from five wheat varieties. Isolates were genotyped using multi-locus simple sequence repeat markers, and necrotrophic effector (NE) and mating type genes were amplified using gene-specific primers. Wheat varieties varied in SNB susceptibility, but site-specific environmental conditions were primary drivers of disease severity. Fungal populations were genetically diverse, but no genetic subdivision was observed among locations or varieties. Ratios of mating type idiomorphs were not significantly different from 1:1, suggesting P. nodorum is undergoing random mating. Three major NE genes were detected within the P. nodorum population but with unequal frequency. However, NE gene profiles were similar for groups of isolates originating from different varieties suggesting wheat genetic backgrounds are not differentially selecting NEs. There is no evidence of population structure in P. nodorum in Virginia and thusly, no support for wheat genetic backgrounds shaping these populations. Finally, although varieties only exhibited moderate SNB resistance, current levels are likely to be durable over time and remain a useful tool for integrated management of SNB in the region.

Journal of Plant Ecology, Mar 9, 2021

Aims Within-species genetic and phenotypic variation have well-known effects on evolutionary proc... more Aims Within-species genetic and phenotypic variation have well-known effects on evolutionary processes, but less is known about how within-species variation may influence community-level processes. Ecologically meaningful intraspecific variation might be particularly important in the context of anthropogenic impacts on natural systems, such as agriculture and species invasion, because human actions can cause strong selection pressures. Methods In a greenhouse study, we explored intraspecific (30 accessions) and ecotypic variation (representing agricultural and nonagricultural habitats) in biomass and rhizome production in response to inter- and intraspecific competition and soil fertility of Johnsongrass (Sorghum halepense), a widespread invasive species and agricultural weed. Important Findings Contrary to our expectations and previous results, we did not find variation in biomass production among Johnsongrass ecotypes at this early life stage. However, we did find that Johnsongrass biomass varied substantially depending on competitor identity, soil fertility treatments and among accessions. Rhizomes were 11% larger in the agricultural ecotype and up to 3-fold larger in fertilized treatment; while rhizome biomass increased by ~50% when fertilized, but did not differ among ecotypes. Interestingly, in competition, Johnsongrass produced 32% less biomass and 20% less rhizome mass with a conspecific than when competing interspecifically with corn. Our results indicate species-specific competitive responses and changes in rhizome allocation in response to neighbor identity; suggesting the possibility of adaptation by Johnsongrass to shift allocation under competition.

CABI eBooks, 2007

This chapter synthesizes ongoing and past work on two prominent secondary metabolites in ripe fru... more This chapter synthesizes ongoing and past work on two prominent secondary metabolites in ripe fruits, emodin and capsaicinoids, to illustrate the importance of adopting an integrative approach in deciphering the ecological role and evolutionary context of these compounds. First, a short critique of how secondary compounds have been viewed by plant ecologists, is given. Thereafter, the biosynthesis pathways of emodin and capsaicinoids where they occur in plant tissue and how their occurrence is linked to abiotic conditions are described. Biotic interactions, particularly, pre-dispersal, dispersal and post-dispersal phases of plant life history are discussed, as well as the similarities and differences between secondary compounds in fruits and in other plant tissues. A unifying theme is that an unusually wide array of selection pressure on fruits and seeds has led to an unusually diverse set of functions for secondary compounds in ripe fruits.

PeerJ, Nov 8, 2021

Fruit house microbial communities that are unique from the rest of the plant. While symbiotic mic... more Fruit house microbial communities that are unique from the rest of the plant. While symbiotic microbial communities complete important functions for their hosts, the fruit microbiome is often understudied compared to other plant organs. Fruits are reproductive tissues that house, protect, and facilitate the dispersal of seeds, and thus they are directly tied to plant fitness. Fruit microbial communities may, therefore, also impact plant fitness. In this study, we assessed how bacterial communities associated with fruit of Solanum carolinense, a native herbaceous perennial weed, vary at fine spatial scales (<0.5 km). A majority of the studies conducted on plant microbial communities have been done at large spatial scales and have observed microbial community variation across these large spatial scales. However, both the environment and pollinators play a role in shaping plant microbial communities and likely have impacts on the plant microbiome at fine scales. We collected fruit samples from eight sampling locations, ranging from 2 to 450 m apart, and assessed the fruit bacterial communities using 16S rRNA gene amplicon sequencing. Overall, we found no differences in observed richness or microbial community composition among sampling locations. Bacterial community structure of fruits collected near one another were not more different than those that were farther apart at the scales we examined. These fine spatial scales are important to obligate out-crossing plant species such as S. carolinense because they are ecologically relevant to pollinators. Thus, our results could imply that pollinators serve to homogenize fruit bacterial communities across these smaller scales.

Molecular Biology and Evolution, Mar 26, 2021

Dissecting the genetic mechanisms underlying dioecy (i.e., separate female and male individuals) ... more Dissecting the genetic mechanisms underlying dioecy (i.e., separate female and male individuals) is critical for understanding the evolution of this pervasive reproductive strategy. Nonetheless, the genetic basis of sex determination remains unclear in many cases, especially in systems where dioecy has arisen recently. Within the economically important plant genus Solanum ($2,000 species), dioecy is thought to have evolved independently at least 4 times across roughly 20 species. Here, we generate the first genome sequence of a dioecious Solanum and use it to ascertain the genetic basis of sex determination in this species. We de novo assembled and annotated the genome of Solanum appendiculatum (assembly size: 750MbscaffoldN50:0.92Mb;750 Mb scaffold N50: 0.92 Mb; 750MbscaffoldN50:0.92Mb;35,000 genes), identified sex-specific sequences and their locations in the genome, and inferred that males in this species are the heterogametic sex. We also analyzed gene expression patterns in floral tissues of males and females, finding approximately 100 genes that are differentially expressed between the sexes. These analyses, together with observed patterns of gene-family evolution specific to S. appendiculatum, consistently implicate a suite of genes from the regulatory network controlling pectin degradation and modification in the expression of sex. Furthermore, the genome of a species with a relatively young sex-determination system provides the foundational resources for future studies on the independent evolution of dioecy in this clade.

Oecologia, Mar 25, 2016

birds. Pungency had little influence on total short-term seed removal by animals, although prior ... more birds. Pungency had little influence on total short-term seed removal by animals, although prior work on this species indicates that capsaicin reduces mortality caused by fungi at longer time scales. Gut passage strongly reduced removal by insects, altering the relative impact of the three predator types. The weak impact of pungency on shortterm predation contrasts with previous studies, highlighting the context dependence of secondary metabolites. The strong impact of gut passage demonstrates that this mechanism alone can influence which seed predators consume seeds, and that impacts of gut passage can be larger than those of secondary metabolites, which are more commonly acknowledged as a defense mechanism.

Ecology, 2008

JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, a... more JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact

BioScience, Aug 26, 2020

Weedy and invasive plants threaten our food supply, native biodiversity, and the structure and fu... more Weedy and invasive plants threaten our food supply, native biodiversity, and the structure and function of ecosystems. The number and impact of these damaging plants are expected to continue to grow with ongoing global change. Some of the most common policy tools to help mitigate this threat are regulatory weed lists, which limit the importation and movement of listed plant species, but there has never been a comprehensive analysis of plants regulated in the United States. We analyzed US state regulatory lists (e.g., noxious, invasive, prohibited) to evaluate their composition, patterns of listing, congruities with weed distributions, and limitations. In total, 46 states maintain regulatory weed lists that include 3210 total listings of 1249 unique species; 48% of them are introduced, 40% are native, and 12% are not yet found in the United States. Overall, the listed species are not a good reflection of the weeds in each state, and listing appears largely reactive, regulating species after they become widespread. We highlight patterns and incongruities among lists and discuss their implications, especially the large number of regulated species native to the United States.

Frontiers in agronomy, Jan 28, 2021

As resistance to herbicides limits growers' weed management options, integrated weed management (... more As resistance to herbicides limits growers' weed management options, integrated weed management (IWM) systems that combine non-chemical tactics with herbicides are becoming critical. A 2 year integrated weed management (IWM) study was conducted at three locations in VA, USA. The factorial study evaluated: (1) soybean planting date (early or late planted) (2) with or without winter cover (cereal rye/wheat or no cover), and (3) with or without harvest weed seed control (HWSC). Prior to soybean planting in the first year, winter cover resulted in a 22% reduction in common ragweed density compared to no cover. At soybean harvest in the first year, the lowest common ragweed densities were in the late planted plots following winter wheat, and common ragweed aboveground biomass was reduced by 46 and 22% at two locations in late planted compared to early planted soybean. To evaluate the impact of the first year's treatments and HWSC, full season soybeans were planted across the trial in the second year. Prior to soybean planting in the second year, late planting in the first year common ragweed density was reduced by 83% at one location, but significant reductions were not observed elsewhere. When comparing winter cover to no cover, common ragweed densities were reduced by 31 and 49% at two locations and densities were similar at the third location. Harvest weed seed control reduced common ragweed density by 43% at one location compared to the conventional harvest plots but no significant reductions were observed at the other locations or at other rating timings. However, there was a significant location by planting date by winter cover interaction and the overall lowest common ragweed densities (4.1 to 10.3 plants m −2) were in the late planted plots with winter cover. This research indicated that winter cover, late planting, and HWSC can reduce common ragweed populations with late planting being the most influential. Therefore, double-cropping soybean after wheat is likely the most viable means to better control common ragweed using IWM as it combines both winter cover and late planting date.

Population genomics, 2018

Genotypes are the central data to any population genetic and genomic study, and genotyping method... more Genotypes are the central data to any population genetic and genomic study, and genotyping methods have steadily evolved since the first direct glimpses of genetic variation were enabled through enzyme protein electrophoresis. Following the development of the polymerase chain reaction, allozymes were supplanted by methods that directly measured allelic variation in nuclear and organellar DNA, most notably through the use of restriction fragment length polymorphisms (RFLPs), amplified fragment length polymorphisms (AFLPs), and microsatellites. At the turn of the millennium, genome-scale polymorphism detection and scoring still was hampered by the low-throughput nature of Sanger sequencing. This limitation changed with the advent of genotyping microarrays that at first yielded hundreds of data points per sample – a revolution at the time – and that subsequently improved to the point where hundreds of thousands of genetic variants could be scored simultaneously. These methods suffered a major flaw, however, in that their cost put them out of reach for studies of most ecologically important but economically unimportant species. The democratization of population genomics arrived with the advent of high-throughput, short-read sequencers and subsequent development of DNA library techniques to subsample the genome in a large number of individuals. Today, such methods – genotyping-by-sequencing, restriction site-associated DNA sequencing, RNA sequencing, and sequence capture – have become mainstays of the population geneticist’s toolkit. Refinements to existing library and sequencing methods continue to emerge at a rapid pace, and novel sequencing platforms may soon put the gold standard of long-read, genome-wide coverage within a broader reach. In this chapter, we comprehensively review genotyping methods used in population genetics, beginning with allozymes and progressing through AFLPs, microsatellites, and SNP arrays. We subsequently turn to a detailed discussion of methods that leverage next-generation technologies to enable truly genome-scale genotyping. Finally, we discuss recent developments and emerging technologies that constitute the “third wave” of sequencing and genotyping methods. Throughout, our aim is to provide methodological details that will be of use to population geneticists.

Advances in Experimental Medicine and Biology, Oct 20, 2013

To understand the origin, history, and function, of natural biological variation, from nucleotide... more To understand the origin, history, and function, of natural biological variation, from nucleotide to community levels, is a fundamental promise of ecological genomics. The most fruitful systems for this work are those that possess both ecological and genomic resources. Such systems provide an opportunity to precisely dissect genetic and developmental mechanisms, and to connect genotypes to phenotypes, as well as to directly demonstrate the ecological and evolutionary relevance of this phenotypic variation. Here we synthesize findings emerging from our efforts to understand two fundamental evolutionary processes - speciation and adaptation - using ecological genomics approaches. Many of these studies have been in the wild tomato clade (Solanum section Lycopersicon), a group that has both exceptional diversity and genomic tools. We also highlight the expanding taxonomic reach of this work, especially in two genera - Capsicum and Jaltomata - that are closely related to Solanum. Parallel approaches in these ecologically and reproductively diverse clades enable us to examine novel questions and traits that are not captured within Solanum, while leveraging the power of comparative studies to understand shared ecological and evolutionary patterns. By synthesizing findings from phenotypic, ecophysiological, genetic, and comparative perspectives, our ultimate goal is to understand the complex mechanistic and evolutionary contributions to the formation of new traits and species diversity.

Ecology, Jun 1, 2014

Plant defense traits can be shaped by evolutionary and physiological constraints, as well as loca... more Plant defense traits can be shaped by evolutionary and physiological constraints, as well as local ecological selection. We assessed the relative importance of these factors in shaping defense trait variation across the wild tomato clade (a group of 13 closely related species) using an herbivore bioassay (Manduca sexta). With phylogenetic comparative methods, we evaluated patterns of constitutive and induced defense variation, and the extent of coupling between alternative defense strategies. We detected substantial variation among species and found no evidence for phylogenetic conservatism among defensive traits, unlike for two other ecologically relevant (reproductive) traits. In addition, constitutive and induced defense syndromes were unassociated. These data indicate that, in this group, there is no evidence for either phylogenetic conservatism of shared consumer guilds that shape defense traits, or for constraints on defense trait evolution, including mechanistic trade-offs between defense strategies. Our data suggest that defense trait variation in this clade instead results from rapid responses to local ecological conditions.

BMC Genomics, Jan 7, 2017

Background: The development of long-read sequencing technologies, such as single-molecule real-ti... more Background: The development of long-read sequencing technologies, such as single-molecule real-time (SMRT) sequencing by PacBio, has produced a revolution in the sequencing of small genomes. Sequencing organelle genomes using PacBio long-read data is a cost effective, straightforward approach. Nevertheless, the availability of simple-to-use software to perform the assembly from raw reads is limited at present. Results: We present Organelle-PBA, a Perl program designed specifically for the assembly of chloroplast and mitochondrial genomes. For chloroplast genomes, the program selects the chloroplast reads from a whole genome sequencing pool, maps the reads to a reference sequence from a closely related species, and then performs read correction and de novo assembly using Sprai. Organelle-PBA completes the assembly process with the additional step of scaffolding by SSPACE-LongRead. The program then detects the chloroplast inverted repeats and reassembles and reorients the assembly based on the organelle origin of the reference. We have evaluated the performance of the software using PacBio reads from different species, read coverage, and reference genomes. Finally, we present the assembly of two novel chloroplast genomes from the species Picea glauca (Pinaceae) and Sinningia speciosa (Gesneriaceae). Conclusion: Organelle-PBA is an easy-to-use Perl-based software pipeline that was written specifically to assemble mitochondrial and chloroplast genomes from whole genome PacBio reads.

Trends in Ecology and Evolution, Jun 1, 2023