Publications by authors named "Elizabeth A Kellogg"

89 Publications

The Genome and the Evolution of the Grasses.

Front Plant Sci 2021 4;12:710383. Epub 2021 Oct 4.

Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA, United States.

In this work, we sequenced and annotated the genome of , one of two genera in the grass subfamily Anomochlooideae, a lineage sister to all other grasses. The final assembly size is over 99% of the estimated genome size. We find good collinearity with the rice genome and have captured most of the gene space. is similar to other grasses in the structure of its fruit (a caryopsis or grain) but has peculiar flowers and inflorescences that are distinct from those in the outgroups and in other grasses. To provide tools for investigations of floral structure, we analyzed two large families of transcription factors, AP2-like and R2R3 MYBs, that are known to control floral and spikelet development in rice and maize among other grasses. Many of these are also regulated by small RNAs. Structure of the gene trees showed that the well documented whole genome duplication at the origin of the grasses (ρ) occurred before the divergence of the Anomochlooideae lineage from the lineage leading to the rest of the grasses (the spikelet clade) and thus that the common ancestor of all grasses probably had two copies of the developmental genes. However, (and by inference other members of Anomochlooideae) has lost one copy of many genes. The peculiar floral morphology of may thus have derived from an ancestral plant that was morphologically similar to the spikelet-bearing grasses. We further identify 114 loci producing microRNAs and 89 loci generating phased, secondary siRNAs, classes of small RNAs known to be influential in transcriptional and post-transcriptional regulation of several plant functions.
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http://dx.doi.org/10.3389/fpls.2021.710383DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8521107PMC
October 2021

Intraspecific variation in elemental accumulation and its association with salt tolerance in Paspalum vaginatum.

G3 (Bethesda) 2021 09;11(10)

Department of Biology, Washington University in St. Louis, St. Louis, MO 63130, USA.

Most plant species, including most crops, perform poorly in salt-affected soils because high sodium levels are cytotoxic and can disrupt the uptake of water and important nutrients. Halophytes are species that have evolved adaptations to overcome these challenges and may be a useful source of knowledge for salt tolerance mechanisms and genes that may be transferable to crop species. The salt content of saline habitats can vary dramatically by location, providing ample opportunity for different populations of halophytic species to adapt to their local salt concentrations; however, the extent of this variation, and the physiology and polymorphisms that drive it, remain poorly understood. Differential accumulation of inorganic elements between genotypes or populations may play an important role in local salinity adaptation. To test this, we investigated the relationships between population structure, tissue ion concentrations, and salt tolerance in 17 "fine-textured" genotypes of the halophytic turfgrass seashore paspalum (Paspalum vaginatum Swartz). A high-throughput ionomics pipeline was used to quantify the shoot concentration of 18 inorganic elements across three salinity treatments. We found a significant relationship between population structure and ion accumulation, with strong correlations between principal components derived from genetic and ionomic data. Additionally, genotypes with higher salt tolerance accumulated more K and Fe and less Ca than less tolerant genotypes. Together these results indicate that differences in ion accumulation between P. vaginatum populations may reflect locally adapted salt stress responses.
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http://dx.doi.org/10.1093/g3journal/jkab275DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8473978PMC
September 2021

Conserved noncoding sequences provide insights into regulatory sequence and loss of gene expression in maize.

Genome Res 2021 May 27. Epub 2021 May 27.

Institute for Genomic Diversity, Cornell University, Ithaca, New York 14853, USA.

Thousands of species will be sequenced in the next few years; however, understanding how their genomes work, without an unlimited budget, requires both molecular and novel evolutionary approaches. We developed a sensitive sequence alignment pipeline to identify conserved noncoding sequences (CNSs) in the Andropogoneae tribe (multiple crop species descended from a common ancestor ∼18 million years ago). The Andropogoneae share similar physiology while being tremendously genomically diverse, harboring a broad range of ploidy levels, structural variation, and transposons. These contribute to the potential of Andropogoneae as a powerful system for studying CNSs and are factors we leverage to understand the function of maize CNSs. We found that 86% of CNSs were comprised of annotated features, including introns, UTRs, putative -regulatory elements, chromatin loop anchors, noncoding RNA (ncRNA) genes, and several transposable element superfamilies. CNSs were enriched in active regions of DNA replication in the early S phase of the mitotic cell cycle and showed different DNA methylation ratios compared to the genome-wide background. More than half of putative -regulatory sequences (identified via other methods) overlapped with CNSs detected in this study. Variants in CNSs were associated with gene expression levels, and CNS absence contributed to loss of gene expression. Furthermore, the evolution of CNSs was associated with the functional diversification of duplicated genes in the context of maize subgenomes. Our results provide a quantitative understanding of the molecular processes governing the evolution of CNSs in maize.
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http://dx.doi.org/10.1101/gr.266528.120DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8256870PMC
May 2021

The Homolog in Selectively Controls Inflorescence Meristem Size.

Front Plant Sci 2021 15;12:636749. Epub 2021 Feb 15.

Donald Danforth Plant Science Center, St. Louis, MO, United States.

The CLAVATA pathway controls meristem size during inflorescence development in both eudicots and grasses, and is initiated by peptide ligands encoded by /-related () genes. While CLV3 controls all shoot meristems in , evidence from cereal grasses indicates that different meristem types are regulated by different CLE peptides. The rice peptide FON2 primarily controls the size of the floral meristem, whereas the orthologous peptides CLE7 and CLE14 in maize have their most dramatic effects on inflorescence and branch meristems, hinting at diversification among CLE responses in the grasses. is more closely related to maize than to rice, so can be used to test whether the maize CLE network can be generalized to all members of subfamily Panicoideae. We used CRISPR-Cas9 in to knock out the gene, the closest homolog to and . mutants developed larger inflorescence meristems, as in maize, but had normal floral meristems, unlike , suggesting a panicoid-specific CLE network. Vegetative traits such as plant height, tiller number and leaf number were not significantly different between mutant and wild type plants, but time to heading was shorter in the mutants. hybridization showed strong expression of in the inflorescence and branch meristems, consistent with the mutant phenotype. Using bioinformatic analysis, we predicted the co-expression network of and its signaling components, which included genes known to control inflorescence architecture in maize as well as genes of unknown function. The similarity between SvFON2 function in Setaria and maize suggests that its developmental specialization in inflorescence meristem control may be shared among panicoid grasses.
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http://dx.doi.org/10.3389/fpls.2021.636749DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7917188PMC
February 2021

Hybridization, polyploidy and clonality influence geographic patterns of diversity and salt tolerance in the model halophyte seashore paspalum (Paspalum vaginatum).

Mol Ecol 2021 01 23;30(1):148-161. Epub 2020 Nov 23.

Department of Biology, Washington University in St. Louis, St. Louis, MO, USA.

In plant species, variation in levels of clonality, ploidy and interspecific hybridization can interact to influence geographic patterns of genetic diversity. These factors commonly vary in plants that specialize on saline habitats (halophytes) and may play a role in how they adapt to salinity variation across their range. One such halophyte is the turfgrass and emerging genomic model system seashore paspalum (Paspalum vaginatum Swartz). To investigate how clonal propagation, ploidy variation, and interspecific hybridization vary across ecotypes and local salinity levels in wild P. vaginatum, we employed genotyping-by-sequencing, cpDNA sequencing and flow cytometry in 218 accessions representing > 170 wild collections from throughout the coastal southern United States plus USDA germplasm. We found that the two morphologically distinct ecotypes of P. vaginatum differ in their adaptive strategies. The fine-textured ecotype is diploid and appears to reproduce in the wild both sexually and by clonal propagation; in contrast, the coarse-textured ecotype consists largely of clonally-propagating triploid and diploid genotypes. The coarse-textured ecotype appears to be derived from hybridization between fine-textured P. vaginatum and an unidentified Paspalum species. These clonally propagating hybrid genotypes are more broadly distributed than clonal fine-textured genotypes and may represent a transition to a more generalist adaptive strategy. Additionally, the triploid genotypes vary in whether they carry one or two copies of the P. vaginatum subgenome, indicating multiple evolutionary origins. This variation in subgenome composition shows associations with local ocean salinity levels across the sampled populations and may play a role in local adaptation.
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http://dx.doi.org/10.1111/mec.15715DOI Listing
January 2021

A genome resource for green millet Setaria viridis enables discovery of agronomically valuable loci.

Nat Biotechnol 2020 10 5;38(10):1203-1210. Epub 2020 Oct 5.

Donald Danforth Plant Science Center, St. Louis, MO, USA.

Wild and weedy relatives of domesticated crops harbor genetic variants that can advance agricultural biotechnology. Here we provide a genome resource for the wild plant green millet (Setaria viridis), a model species for studies of C grasses, and use the resource to probe domestication genes in the close crop relative foxtail millet (Setaria italica). We produced a platinum-quality genome assembly of S. viridis and de novo assemblies for 598 wild accessions and exploited these assemblies to identify loci underlying three traits: response to climate, a 'loss of shattering' trait that permits mechanical harvest and leaf angle, a predictor of yield in many grass crops. With CRISPR-Cas9 genome editing, we validated Less Shattering1 (SvLes1) as a gene whose product controls seed shattering. In S. italica, this gene was rendered nonfunctional by a retrotransposon insertion in the domesticated loss-of-shattering allele SiLes1-TE (transposable element). This resource will enhance the utility of S. viridis for dissection of complex traits and biotechnological improvement of panicoid crops.
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http://dx.doi.org/10.1038/s41587-020-0681-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7536120PMC
October 2020

Evolutionary Dynamics of Transposable Elements Following a Shared Polyploidization Event in the Tribe Andropogoneae.

G3 (Bethesda) 2020 12 3;10(12):4387-4398. Epub 2020 Dec 3.

Department of Biology, 53 Campus Drive, West Virginia University, Morgantown, WV 26506

Both polyploidization and transposable element (TE) activity are known to be major drivers of plant genome evolution. Here, we utilize the clade to investigate TE activity and accumulation after a shared polyploidization event. Comparisons of TE evolutionary dynamics in various and species, in addition to two closely related diploid species, and , revealed variation in repeat content among all taxa included in the study. The repeat composition of is more similar to that of and compared to , despite the similarity in genome size with the latter. Although LTR-retrotransposons were abundant in all species, we observed an expansion of the superfamily, specifically in and , species that have adapted to more temperate environments. Additional analyses of the genomic distribution of these retroelements provided evidence of biased insertions near genes involved in various biological processes including plant development, defense, and macromolecule biosynthesis. Specifically, insertions in and were significantly enriched near genes involved in abiotic stress response, suggesting independent evolution post divergence. The lack of insertions near the orthologous genes in suggests that duplicate gene copies generated during polyploidization may offer novel neutral sites for TEs to insert, thereby providing an avenue for subfunctionalization via TE insertional mutagenesis.
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http://dx.doi.org/10.1534/g3.120.401596DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7718754PMC
December 2020

Sterile Spikelets Contribute to Yield in Sorghum and Related Grasses.

Plant Cell 2020 11 1;32(11):3500-3518. Epub 2020 Sep 1.

Donald Danforth Plant Science Center, St. Louis, Missouri 63132

Sorghum () and its relatives in the grass tribe Andropogoneae bear their flowers in pairs of spikelets in which one spikelet (seed-bearing or sessile spikelet [SS]) of the pair produces a seed and the other is sterile or male (staminate). This division of function does not occur in other major cereals such as wheat () or rice (). Additionally, one bract of the SS spikelet often produces a long extension, the awn, that is in the same position as, but independently derived from, that of wheat and rice. The function of the sterile spikelet is unknown and that of the awn has not been tested in Andropogoneae. We used radioactive and stable isotopes of carbon, RNA sequencing of metabolically important enzymes, and immunolocalization of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) to show that the sterile spikelet assimilates carbon, which is translocated to the largely heterotrophic SS. The awn shows no evidence of photosynthesis. These results apply to distantly related species of Andropogoneae. Removal of sterile spikelets in sorghum significantly decreases seed weight (yield) by ∼9%. Thus, the sterile spikelet, but not the awn, affects yield in the cultivated species and fitness in the wild species.
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http://dx.doi.org/10.1105/tpc.20.00424DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7610286PMC
November 2020

The Genomes of the Allohexaploid Echinochloa crus-galli and Its Progenitors Provide Insights into Polyploidization-Driven Adaptation.

Mol Plant 2020 09 2;13(9):1298-1310. Epub 2020 Jul 2.

Institute of Crop Sciences & Institute of Bioinformatics, Zhejiang University, Hangzhou 310058, China. Electronic address:

The hexaploid species Echinochloa crus-galli is one of the most detrimental weeds in crop fields, especially in rice paddies. Its evolutionary history is similar to that of bread wheat, arising through polyploidization after hybridization between a tetraploid and a diploid species. In this study, we generated and analyzed high-quality genome sequences of diploid (E. haploclada), tetraploid (E. oryzicola), and hexaploid (E. crus-galli) Echinochloa species. Gene family analysis showed a significant loss of disease-resistance genes such as those encoding NB-ARC domain-containing proteins during Echinochloa polyploidization, contrary to their significant expansionduring wheat polyploidization, suggesting that natural selection might favor reduced investment in resistance in this weed to maximize its growth and reproduction. In contrast to the asymmetric patterns of genome evolution observed in wheat and other crops, no significant differences in selection pressure were detected between the subgenomes in E. oryzicola and E. crus-galli. In addition, distinctive differences in subgenome transcriptome dynamics during hexaploidization were observed between E. crus-galli and bread wheat. Collectively, our study documents genomic mechanisms underlying the adaptation of a major agricultural weed during polyploidization. The genomic and transcriptomic resources of three Echinochloa species and new insights into the polyploidization-driven adaptive evolution would be useful for future breeding cereal crops.
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http://dx.doi.org/10.1016/j.molp.2020.07.001DOI Listing
September 2020

The anatomy of abscission zones is diverse among grass species.

Am J Bot 2020 04 23;107(4):549-561. Epub 2020 Mar 23.

Donald Danforth Plant Science Center, 975 North Warson Road, St. Louis, MO, 62132, USA.

Premise: Abscission zones (AZ) are specialized cell layers that separate plant parts at the organ junction upon developmental or environmental signals. Fruit or seed abscission has been well studied in model species because of its crucial role for seed dispersal. Previous work showed that AZ localization differs among species of Poaceae and that AZ formation is histologically and genetically distinct in three distantly related grass species, refuting the idea of a broadly conserved module. However, whether AZ structure is consistent within subfamilies is unknown.

Methods: Eleven species were selected from six subfamilies of Poaceae, and their AZ was investigated using paraffin-embedded, stained material. Observations were added from the literature for an additional six species. Data were recorded on AZ location and whether cells in the AZ were distinguishable by size or lignification. Characteristics of the AZ were mapped on the phylogeny using maximum likelihood.

Results: Abscission zone anatomy and histology vary among species, and characteristics of the AZ do not correlate with phylogeny. Twelve of the seventeen studied species have an AZ in which the cells are significantly smaller than surrounding cells. Of these, eight have differential lignification. Differential lignification is often associated with differential cell size, but not vice versa.

Conclusions: Neither smaller cells in the AZ nor differential lignification between the AZ and surrounding cells is required for abscission, although differential cell size and lignification are often correlated. Abscission zone anatomy does not correlate with phylogeny, suggesting its rapid change over evolutionary time.
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http://dx.doi.org/10.1002/ajb2.1454DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7217018PMC
April 2020

Comprehensive 3D phenotyping reveals continuous morphological variation across genetically diverse sorghum inflorescences.

New Phytol 2020 06 16;226(6):1873-1885. Epub 2020 Apr 16.

Donald Danforth Plant Science Center, St Louis, MO, 63132, USA.

●Inflorescence architecture in plants is often complex and challenging to quantify, particularly for inflorescences of cereal grasses. Methods for capturing inflorescence architecture and for analyzing the resulting data are limited to a few easily captured parameters that may miss the rich underlying diversity. ●Here, we apply X-ray computed tomography combined with detailed morphometrics, offering new imaging and computational tools to analyze three-dimensional inflorescence architecture. To show the power of this approach, we focus on the panicles of Sorghum bicolor, which vary extensively in numbers, lengths, and angles of primary branches, as well as the three-dimensional shape, size, and distribution of the seed. ●We imaged and comprehensively evaluated the panicle morphology of 55 sorghum accessions that represent the five botanical races in the most common classification system of the species, defined by genetic data. We used our data to determine the reliability of the morphological characters for assigning specimens to race and found that seed features were particularly informative. ●However, the extensive overlap between botanical races in multivariate trait space indicates that the phenotypic range of each group extends well beyond its overall genetic background, indicating unexpectedly weak correlation between morphology, genetic identity, and domestication history.
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http://dx.doi.org/10.1111/nph.16533DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7317572PMC
June 2020

Continued Adaptation of C4 Photosynthesis After an Initial Burst of Changes in the Andropogoneae Grasses.

Syst Biol 2020 05;69(3):445-461

Laboratoire Evolution & Diversité Biologique (EDB, UMR 5174), CNRS/IRD/Université Toulouse III, 118 route de Narbonne, 31062 Toulouse, France.

C$_{4}$ photosynthesis is a complex trait that sustains fast growth and high productivity in tropical and subtropical conditions and evolved repeatedly in flowering plants. One of the major C$_{4}$ lineages is Andropogoneae, a group of $\sim $1200 grass species that includes some of the world's most important crops and species dominating tropical and some temperate grasslands. Previous efforts to understand C$_{4}$ evolution in the group have compared a few model C$_{4}$ plants to distantly related C$_{3}$ species so that changes directly responsible for the transition to C$_{4}$ could not be distinguished from those that preceded or followed it. In this study, we analyze the genomes of 66 grass species, capturing the earliest diversification within Andropogoneae as well as their C$_{3}$ relatives. Phylogenomics combined with molecular dating and analyses of protein evolution show that many changes linked to the evolution of C$_{4}$ photosynthesis in Andropogoneae happened in the Early Miocene, between 21 and 18 Ma, after the split from its C$_{3}$ sister lineage, and before the diversification of the group. This initial burst of changes was followed by an extended period of modifications to leaf anatomy and biochemistry during the diversification of Andropogoneae, so that a single C$_{4}$ origin gave birth to a diversity of C$_{4}$ phenotypes during 18 million years of speciation events and migration across geographic and ecological spaces. Our comprehensive approach and broad sampling of the diversity in the group reveals that one key transition can lead to a plethora of phenotypes following sustained adaptation of the ancestral state. [Adaptive evolution; complex traits; herbarium genomics; Jansenelleae; leaf anatomy; Poaceae; phylogenomics.].
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http://dx.doi.org/10.1093/sysbio/syz066DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7672695PMC
May 2020

Divergent gene expression networks underlie morphological diversity of abscission zones in grasses.

New Phytol 2020 02 28;225(4):1799-1815. Epub 2019 Aug 28.

Donald Danforth Plant Science Center, St Louis, MO, 63132, USA.

Abscission is a process in which plants shed their parts, and is mediated by a particular set of cells, the abscission zone (AZ). In grasses (Poaceae), the position of the AZ differs among species, raising the question of whether its anatomical structure and genetic control are conserved. The ancestral position of the AZ was reconstructed. A combination of light microscopy, transmission electron microscopy, RNA-Seq analyses and RNA in situ hybridisation were used to compare three species, two (weedy rice and Brachypodium distachyon) with the AZ in the ancestral position and one (Setaria viridis) with the AZ in a derived position below a cluster of flowers (spikelet). Rice and Brachypodium are more similar anatomically than Setaria. However, the cell wall properties and the transcriptome of rice and Brachypodium are no more similar to each other than either is to Setaria. The set of genes expressed in the studied tissues is generally conserved across species, but the precise developmental and positional patterns of expression and gene networks are almost entirely different. Transcriptional regulation of AZ development appears to be extensively rewired among the three species, leading to distinct anatomical and morphological outcomes.
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http://dx.doi.org/10.1111/nph.16087DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7003853PMC
February 2020

Different ways to be redundant.

Nat Genet 2019 05;51(5):770-771

Donald Danforth Plant Science Center, St Louis, MO, USA.

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http://dx.doi.org/10.1038/s41588-019-0406-yDOI Listing
May 2019

Specimen-based analysis of morphology and the environment in ecologically dominant grasses: the power of the herbarium.

Philos Trans R Soc Lond B Biol Sci 2018 11 19;374(1763). Epub 2018 Nov 19.

Donald Danforth Plant Science Center, 975 North Warson Road, St Louis, MO 63132, USA

Herbaria contain a cumulative sample of the world's flora, assembled by thousands of people over centuries. To capitalize on this resource, we conducted a specimen-based analysis of a major clade in the grass tribe Andropogoneae, including the dominant species of the world's grasslands in the genera , , and several others. We imaged 186 of the 250 named species of the clade, georeferenced the specimens and extracted climatic variables for each. Using semi- and fully automated image analysis techniques, we extracted spikelet morphological characters and correlated these with environmental variables. We generated chloroplast genome sequences to correct for phylogenetic covariance and here present a new phylogeny for 81 of the species. We confirm and extend earlier studies to show that and are not monophyletic. In addition, we find all morphological and ecological characters are homoplasious but variable among clades. For example, sessile spikelet length is positively correlated with awn length when all accessions are considered, but when separated by clade, the relationship is positive for three sub-clades and negative for three others. Climate variables showed no correlation with morphological variation in the spikelet pair; only very weak effects of temperature and precipitation were detected on macrohair density.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.
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http://dx.doi.org/10.1098/rstb.2017.0403DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6282083PMC
November 2018

Getting closer: vein density in C leaves.

New Phytol 2019 02 18;221(3):1260-1267. Epub 2018 Oct 18.

Donald Danforth Plant Science Center, St Louis, MO, 63132, USA.

Contents Summary 1260 I. Introduction 1260 II. Molecular and genetic mechanisms of C leaf venation 1262 III. Conclusions and future perspectives 1266 Acknowledgements 1266 References 1266 SUMMARY: C grasses are major contributors to the world's food supply. Their highly efficient method of carbon fixation is a unique adaptation that combines close vein spacing and distinct photosynthetic cell types. Despite its importance, the molecular genetic basis of C leaf development is still poorly understood. Here we summarize current knowledge of leaf venation and review recent progress in understanding molecular and genetic regulation of vascular patterning events in C plants. Evidence points to the interplay of auxin, brassinosteroids, SHORTROOT/SCARECROW and INDETERMINATE DOMAIN transcription factors. Identification and functional characterization of candidate regulators acting early in vascular development will be essential for further progress in understanding the precise regulation of these processes.
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http://dx.doi.org/10.1111/nph.15491DOI Listing
February 2019

A Dynamic Co-expression Map of Early Inflorescence Development in Provides a Resource for Gene Discovery and Comparative Genomics.

Front Plant Sci 2018 12;9:1309. Epub 2018 Sep 12.

Donald Danforth Plant Science Center, St. Louis, MO, United States.

The morphological and functional diversity of plant form is governed by dynamic gene regulatory networks. In cereal crops, grain and/or pollen-bearing inflorescences exhibit vast architectural diversity and developmental complexity, yet the underlying genetic framework is only partly known. s is a small, rapidly growing grass species in the subfamily Panicoideae, a group that includes economically important cereal crops such as maize and sorghum. The inflorescence displays complex branching patterns, but its early development is similar to that of other panicoid grasses, and thus is an ideal model for studying inflorescence architecture. Here we report a detailed transcriptional resource that captures dynamic transitions across six sequential stages of inflorescence development, from reproductive onset to floral organ differentiation. Co-expression analyses identified stage-specific signatures of development, which include homologs of previously known developmental genes from maize and rice, suites of transcription factors and gene family members, and genes of unknown function. This spatiotemporal co-expression map and associated analyses provide a foundation for gene discovery in inflorescence development, and a comparative model for exploring related architectural features in agronomically important cereals.
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http://dx.doi.org/10.3389/fpls.2018.01309DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6143762PMC
September 2018

Robust DNA Isolation and High-throughput Sequencing Library Construction for Herbarium Specimens.

J Vis Exp 2018 03 8(133). Epub 2018 Mar 8.

Donald Danforth Plant Science Center;

Herbaria are an invaluable source of plant material that can be used in a variety of biological studies. The use of herbarium specimens is associated with a number of challenges including sample preservation quality, degraded DNA, and destructive sampling of rare specimens. In order to more effectively use herbarium material in large sequencing projects, a dependable and scalable method of DNA isolation and library preparation is needed. This paper demonstrates a robust, beginning-to-end protocol for DNA isolation and high-throughput library construction from herbarium specimens that does not require modification for individual samples. This protocol is tailored for low quality dried plant material and takes advantage of existing methods by optimizing tissue grinding, modifying library size selection, and introducing an optional reamplification step for low yield libraries. Reamplification of low yield DNA libraries can rescue samples derived from irreplaceable and potentially valuable herbarium specimens, negating the need for additional destructive sampling and without introducing discernible sequencing bias for common phylogenetic applications. The protocol has been tested on hundreds of grass species, but is expected to be adaptable for use in other plant lineages after verification. This protocol can be limited by extremely degraded DNA, where fragments do not exist in the desired size range, and by secondary metabolites present in some plant material that inhibit clean DNA isolation. Overall, this protocol introduces a fast and comprehensive method that allows for DNA isolation and library preparation of 24 samples in less than 13 h, with only 8 h of active hands-on time with minimal modifications.
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http://dx.doi.org/10.3791/56837DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5946958PMC
March 2018

Sparse panicle1 is required for inflorescence development in Setaria viridis and maize.

Nat Plants 2017 04 18;3:17054. Epub 2017 Apr 18.

Donald Danforth Plant Science Center, 975 N Warson Road, St. Louis, Missouri 63132, USA.

Setaria viridis is a rapid-life-cycle model panicoid grass. To identify genes that may contribute to inflorescence architecture and thus have the potential to influence grain yield in related crops such as maize, we conducted an N-nitroso-N-methylurea (NMU) mutagenesis of S. viridis and screened for visible inflorescence mutant phenotypes. Of the approximately 2,700 M families screened, we identified four recessive sparse panicle mutants (spp1-spp4) characterized by reduced and uneven branching of the inflorescence. To identify the gene underlying the sparse panicle1 (spp1) phenotype, we performed bulked segregant analysis and deep sequencing to fine map it to an approximately 1 Mb interval. Within this interval, we identified disruptive mutations in two genes. Complementation tests between spp1 and spp3 revealed they were allelic, and deep sequencing of spp3 identified an independent disruptive mutation in SvAUX1 (AUXIN1), one of the two genes in the ∼1 Mb interval and the only gene disruption shared between spp1 and spp3. SvAUX1 was found to affect both inflorescence development and root gravitropism in S. viridis. A search for orthologous mutant alleles in maize confirmed a very similar role of ZmAUX1 in maize, which highlights the utility of S. viridis in accelerating functional genomic studies in maize.
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http://dx.doi.org/10.1038/nplants.2017.54DOI Listing
April 2017

High-throughput phenotyping.

Am J Bot 2017 04 11;104(4):505-508. Epub 2017 Apr 11.

Donald Danforth Plant Science Center, 975 North Warson Road, St. Louis, Missouri 63132 USA

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http://dx.doi.org/10.3732/ajb.1700044DOI Listing
April 2017

Repeated and diverse losses of corolla bilateral symmetry in the Lamiaceae.

Ann Bot 2017 05;119(7):1211-1223

Department of Biology, The University of Missouri-St. Louis, One University Blvd, St. Louis, MO 63121, USA.

Background And Aims: Independent evolution of derived complex characters provides a unique opportunity to assess whether and how similar genetic changes correlate with morphological convergence. Bilaterally symmetrical corollas have evolved multiple times independently from radially symmetrical ancestors and likely represent adaptations to attract specific pollinators. On the other hand, losses of bilateral corolla symmetry have occurred sporadically in various groups, due to either modification of bilaterally symmetrical corollas in late development or early establishment of radial symmetry.

Methods: This study integrated phylogenetic, scanning electron microscopy (SEM)-based morphological, and gene expression approaches to assess the possible mechanisms underlying independent evolutionary losses of corolla bilateral symmetry.

Key Results: This work compared three species of Lamiaceae having radially symmetrical mature corollas with a representative sister taxon having bilaterally symmetrical corollas and found that each reaches radial symmetry in a different way. Higher core Lamiales share a common duplication in the CYCLOIDEA (CYC ) 2 gene lineage and show conserved and asymmetrical expression of CYC2 clade and RAD genes along the adaxial-abaxial floral axis in species having bilateral corolla symmetry. In Lycopus americanus , the development and expression pattern of La-CYC2A and La-CYC2B are similar to those of their bilaterally symmetrical relatives, whereas the loss of La-RAD expression correlates with a late switch to radial corolla symmetry. In Mentha longifolia , late radial symmetry may be explained by the loss of Ml-CYC2A , and by altered expression of two Ml-CYC2B and Ml-RAD genes . Finally, expanded expression of Cc-CYC2A and Cc-RAD strongly correlates with the early development of radially symmetrical corollas in Callicarpa cathayana .

Conclusions: Repeated losses of mature corolla bilateral symmetry in Lamiaceae are not uncommon, and may be achieved by distinct mechanisms and various changes to symmetry genes, including the loss of a CYC2 clade gene from the genome, and/or contraction, expansion or alteration of CYC2 clade and RAD -like gene expression.
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http://dx.doi.org/10.1093/aob/mcx012DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5604593PMC
May 2017

Comprehensive identification and clustering of CLV3/ESR-related (CLE) genes in plants finds groups with potentially shared function.

New Phytol 2017 Oct 1;216(2):605-616. Epub 2016 Dec 1.

Donald Danforth Plant Science Center, 975 North Warson Rd, St Louis, MO, 63132, USA.

CLV3/ESR (CLE) proteins are important signaling peptides in plants. The short CLE peptide (12-13 amino acids) is cleaved from a larger pre-propeptide and functions as an extracellular ligand. The CLE family is large and has resisted attempts at classification because the CLE domain is too short for reliable phylogenetic analysis and the pre-propeptide is too variable. We used a model-based search for CLE domains from 57 plant genomes and used the entire pre-propeptide for comprehensive clustering analysis. In total, 1628 CLE genes were identified in land plants, with none recognizable from green algae. These CLEs form 12 groups within which CLE domains are largely conserved and pre-propeptides can be aligned. Most clusters contain sequences from monocots, eudicots and Amborella trichopoda, with sequences from Picea abies, Selaginella moellendorffii and Physcomitrella patens scattered in some clusters. We easily identified previously known clusters involved in vascular differentiation and nodulation. In addition, we found a number of discrete groups whose function remains poorly characterized. Available data indicate that CLE proteins within a cluster are likely to share function, whereas those from different clusters play at least partially different roles. Our analysis provides a foundation for future evolutionary and functional studies.
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http://dx.doi.org/10.1111/nph.14348DOI Listing
October 2017

The draft genome of the C panicoid grass species Dichanthelium oligosanthes.

Genome Biol 2016 10 28;17(1):223. Epub 2016 Oct 28.

Donald Danforth Plant Science Center, St. Louis, MO, 63132, USA.

Background: Comparisons between C and C grasses often utilize C species from the subfamilies Ehrhartoideae or Pooideae and C species from the subfamily Panicoideae, two clades that diverged over 50 million years ago. The divergence of the C panicoid grass Dichanthelium oligosanthes from the independent C lineages represented by Setaria viridis and Sorghum bicolor occurred approximately 15 million years ago, which is significantly more recent than members of the Bambusoideae, Ehrhartoideae, and Pooideae subfamilies. D. oligosanthes is ideally placed within the panicoid clade for comparative studies of C and C grasses.

Results: We report the assembly of the nuclear and chloroplast genomes of D. oligosanthes, from high-throughput short read sequencing data and a comparative transcriptomics analysis of the developing leaf of D. oligosanthes, S. viridis, and S. bicolor. Physiological and anatomical characterizations verified that D. oligosanthes utilizes the C pathway for carbon fixation and lacks Kranz anatomy. Expression profiles of transcription factors along developing leaves of D. oligosanthes and S. viridis were compared with previously published data from S. bicolor, Zea mays, and Oryza sativa to identify a small suite of transcription factors that likely acquired functions specifically related to C photosynthesis.

Conclusions: The phylogenetic location of D. oligosanthes makes it an ideal C plant for comparative analysis of C evolution in the panicoid grasses. This genome will not only provide a better C species for comparisons with C panicoid grasses, but also highlights the power of using high-throughput sequencing to address questions in evolutionary biology.
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http://dx.doi.org/10.1186/s13059-016-1080-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5084476PMC
October 2016

Verdant: automated annotation, alignment and phylogenetic analysis of whole chloroplast genomes.

Bioinformatics 2017 01 14;33(1):130-132. Epub 2016 Sep 14.

Donald Danforth Plant Science Center, St. Louis, MO 63132, USA.

Motivation: Chloroplast genomes are now produced in the hundreds for angiosperm phylogenetics projects, but current methods for annotation, alignment and tree estimation still require some manual intervention reducing throughput and increasing analysis time for large chloroplast systematics projects.

Results: Verdant is a web-based software suite and database built to take advantage a novel annotation program, annoBTD. Using annoBTD, Verdant provides accurate annotation of chloroplast genomes without manual intervention. Subsequent alignment and tree estimation can incorporate newly annotated and publically available plastomes and can accommodate a large number of taxa. Verdant sharply reduces the time required for analysis of assembled chloroplast genomes and removes the need for pipelines and software on personal hardware.

Availability And Implementation: Verdant is available at: http://verdant.iplantcollaborative.org/plastidDB/ It is implemented in PHP, Perl, MySQL, Javascript, HTML and CSS with all major browsers supported.

Contact: [email protected] information: Supplementary data are available at Bioinformatics online.
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http://dx.doi.org/10.1093/bioinformatics/btw583DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5408774PMC
January 2017

Gα and regulator of G-protein signaling (RGS) protein pairs maintain functional compatibility and conserved interaction interfaces throughout evolution despite frequent loss of RGS proteins in plants.

New Phytol 2017 Oct 16;216(2):562-575. Epub 2016 Sep 16.

Donald Danforth Plant Science Center, 975 North Warson Road, St Louis, MO, 63132, USA.

Signaling pathways regulated by heterotrimeric G-proteins exist in all eukaryotes. The regulator of G-protein signaling (RGS) proteins are key interactors and critical modulators of the Gα protein of the heterotrimer. However, while G-proteins are widespread in plants, RGS proteins have been reported to be missing from the entire monocot lineage, with two exceptions. A single amino acid substitution-based adaptive coevolution of the Gα:RGS proteins was proposed to enable the loss of RGS in monocots. We used a combination of evolutionary and biochemical analyses and homology modeling of the Gα and RGS proteins to address their expansion and its potential effects on the G-protein cycle in plants. Our results show that RGS proteins are widely distributed in the monocot lineage, despite their frequent loss. There is no support for the adaptive coevolution of the Gα:RGS protein pair based on single amino acid substitutions. RGS proteins interact with, and affect the activity of, Gα proteins from species with or without endogenous RGS. This cross-functional compatibility expands between the metazoan and plant kingdoms, illustrating striking conservation of their interaction interface. We propose that additional proteins or alternative mechanisms may exist which compensate for the loss of RGS in certain plant species.
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http://dx.doi.org/10.1111/nph.14180DOI Listing
October 2017

Cross species selection scans identify components of C4 photosynthesis in the grasses.

J Exp Bot 2017 01 19;68(2):127-135. Epub 2016 Jul 19.

Donald Danforth Plant Science Center, 975 N Warson Rd, St Louis, MO 63132, USA

C photosynthesis is perhaps one of the best examples of convergent adaptive evolution with over 25 independent origins in the grasses (Poaceae) alone. The availability of high quality grass genome sequences presents new opportunities to explore the mechanisms underlying this complex trait using evolutionary biology-based approaches. In this study, we performed genome-wide cross-species selection scans in C lineages to facilitate discovery of C genes. The study was enabled by the well conserved collinearity of grass genomes and the recently sequenced genome of a C panicoid grass, Dichanthelium oligosanthes This method, in contrast to previous studies, does not rely on any a priori knowledge of the genes that contribute to biochemical or anatomical innovations associated with C photosynthesis. We identified a list of 88 candidate genes that include both known and potentially novel components of the C pathway. This set includes the carbon shuttle enzymes pyruvate, phosphate dikinase, phosphoenolpyruvate carboxylase and NADP malic enzyme as well as several predicted transporter proteins that likely play an essential role in promoting the flux of metabolites between the bundle sheath and mesophyll cells. Importantly, this approach demonstrates the application of fundamental molecular evolution principles to dissect the genetic basis of a complex photosynthetic adaptation in plants. Furthermore, we demonstrate how the output of the selection scans can be combined with expression data to provide additional power to prioritize candidate gene lists and suggest novel opportunities for pathway engineering.
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http://dx.doi.org/10.1093/jxb/erw256DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5429014PMC
January 2017

Abscission zone development in Setaria viridis and its domesticated relative, Setaria italica.

Am J Bot 2016 06 1;103(6):998-1005. Epub 2016 Jun 1.

Donald Danforth Plant Science Center, 975 North Warson Road, St. Louis, Missouri 63132 USA

Premise Of The Study: Development of an abscission zone (AZ) is needed for dispersal of seeds, and AZ loss was a critical early step in plant domestication. The AZ forms in different tissues in different species of plants, but whether the AZ is developmentally similar wherever it occurs is unknown. AZ development in Setaria viridis was studied as a representative of the previously uncharacterized subfamily Panicoideae.

Methods: One accession of the wild species S. viridis and two of its domesticate, S. italica, were studied. Strength of the AZ was measured with a force gauge. Anatomy of the AZ was studied throughout development using bright field and confocal microscopy.

Key Results: The force required to remove a spikelet of S. viridis from the parent plant dropped steadily during development, whereas that required to remove spikelets of S. italica increased initially before stabilizing at a high level. Despite the clear difference in tensile strength of the AZ, anatomical differences between S. viridis and S. italica were subtle, and the position of the AZ was not easy to determine in cross sections of pedicel apices. Staining with DAPI showed that nuclei were present up to and presumably through abscission in S. viridis, and acridine orange staining showed much less lignification than in other cereals.

Conclusions: The AZ in Setaria is developmentally and anatomically different from that characterized in rice, barley, and many eudicots. In particular, no set of small, densely cytoplasmic cells is obvious. This difference in anatomy could point to differential genetic control of the structure.
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http://dx.doi.org/10.3732/ajb.1500499DOI Listing
June 2016

Multilocus phylogeny and phylogenomics of Eriochrysis P. Beauv. (Poaceae-Andropogoneae): Taxonomic implications and evidence of interspecific hybridization.

Mol Phylogenet Evol 2016 06 3;99:155-167. Epub 2016 Mar 3.

Donald Danforth Plant Science Center, 975 North Warson Road, St. Louis, MO 63132, USA. Electronic address:

Species delimitation is a vital issue concerning evolutionary biology and conservation of biodiversity. However, it is a challenging task for several reasons, including the low interspecies variability of markers currently used in phylogenetic reconstructions and the occurrence of reticulate evolution and polyploidy in many lineages of flowering plants. The first phylogeny of the grass genus Eriochrysis is presented here, focusing on the New World species, in order to examine its relationships to other genera of the subtribe Saccharinae/tribe Andropogoneae and to define the circumscriptions of its taxonomically complicated species. Molecular cloning and sequencing of five regions of four low-copy nuclear genes (apo1, d8, ep2-ex7 and ep2-ex8, kn1) were performed, as well as complete plastome sequencing. Trees were reconstructed using maximum parsimony, maximum likelihood, and Bayesian inference analyses. The present phylogenetic analyses indicate that Eriochrysis is monophyletic and the Old World E. pallida is sister to the New World species. Subtribe Saccharinae is polyphyletic, as is the genus Eulalia. Based on nuclear and plastome sequences plus morphology, we define the circumscriptions of the New World species of Eriochrysis: E. laxa is distinct from E. warmingiana, and E. villosa is distinct from E. cayennensis. Natural hybrids occur between E. laxa and E. villosa. The hybrids are probably tetraploids, based on the number of paralogues in the nuclear gene trees. This is the first record of a polyploid taxon in the genus Eriochrysis. Some incongruities between nuclear genes and plastome analyses were detected and are potentially caused by incomplete lineage sorting and/or ancient hybridization. The set of low-copy nuclear genes used in this study seems to be sufficient to resolve phylogenetic relationships and define the circumscriptions of other species complexes in the grass family and relatives, even in the presence of polyploidy and reticulate evolution. Complete plastome sequencing is also a promising tool for phylogenetic inference.
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http://dx.doi.org/10.1016/j.ympev.2016.02.022DOI Listing
June 2016

Has the connection between polyploidy and diversification actually been tested?

Curr Opin Plant Biol 2016 04 8;30:25-32. Epub 2016 Feb 8.

Donald Danforth Plant Science Center, 975 North Warson Rd., St. Louis, MO 63132, USA. Electronic address:

Many major clades of angiosperms have several whole genome duplications (polyploidization events) in their distant past, suggesting that polyploidy drives or at least permits diversification. However, data on recently diverged groups are more equivocal, finding little evidence of elevated diversification following polyploidy. The discrepancy may be attributable at least in part to methodology. Many studies use indirect methods, such as chromosome numbers, genome size, and Ks plots, to test polyploidy, although these approaches can be misleading, and often lack sufficient resolution. A direct test of diversification following polyploidy requires a sequence-based approach that traces the history of nuclear genomes rather than species. These methods identify the point of coalescence of ancestral genomes, but may be misleading about the time and thus the extent of diversification. Limitations of existing methods mean that the connection between polyploidy and diversification has not been rigorously tested and remains unknown.
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http://dx.doi.org/10.1016/j.pbi.2016.01.002DOI Listing
April 2016
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