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DOE OSTI2023

Dissection of Grass Cell Wall Lignin Formation and their Associated Dirigent Protein

This Final Report describes work underway to establish why monocot (e.g. grasses) lignins are more readily (bio)degradable than their woody gymnosperm, angiosperm, and fern counterparts. Our hypothesis is that monocot specific dirigent protein (DP) sub-families are wholly or partly involved in generating these more readily (bio)degradable lignins. Three approaches are underway: metabolomics and lignin analyses of stem and leaf tissues of the grass, Brachypodium; Crispr/Cas9 gene editing of monocot specific DP sub-families in this species, and recombinant protein expression of Brachypodium’s 44 DPs. Metabolomic and lignin analyses were completed for 6 and 8 week old Brachypodium in order to establish the molecular diversity of its largely phenolic metabolites: Crispr/Cas9 gene editing has also been done on specific DPs known to be expressed in lignifying stems, and T 2 generation plant lines are now being generated, prior to establishing the effects on lignin composition and content; in the recombinant DP work (which addresses establishing the biochemical function of the monocot specific DPs and other DPOs as needed), all 44 constructs have been generated (in collaboration with DOE JGI) and are being systematically expressed in either E. coli or yeast (Pichia sp.) for future studies. Future work will be directed towards bringing the current studies to completion, and in establishing the biochemical basis as to how these more readily (bio)degradable lignins are generated/assembled.

(bio)degradability↗

DOE OSTI2018

Secretome Analysis from the Ectomycorrhizal Ascomycete Cenococcum geophilum

Cenococcum geophilum is an ectomycorrhizal fungus with global distribution in numerous habitats and associates with a large range of host species including gymnosperm and angiosperm trees. Moreover, C. geophilum is the unique ectomycorrhizal species within the clade Dothideomycetes, the largest class of Ascomycetes containing predominantly saprotrophic and many devastating phytopathogenic fungi. Recent studies highlight that mycorrhizal fungi, as pathogenic ones, use effectors in form of Small Secreted Proteins (SSPs) as molecular keys to promote symbiosis. In order to better understand the biotic interaction of C. geophilum with its host plants, the goal of this work was to characterize mycorrhiza-induced small-secreted proteins (MiSSPs) that potentially play a role in the ectomycorrhiza formation and functioning of this ecologically very important species. We combined different approaches such as gene expression profiling, genome localization and conservation of MiSSP genes in different C. geophilum strains and closely related species as well as protein subcellular localization studies of potential targets of MiSSPs in interacting plants using in tobacco leaf cells. Gene expression analyses of C. geophilum interacting with Pinus sylvestris (pine) and Populus tremula × Populus alba (poplar) showed that similar sets of genes coding for secreted proteins were up-regulated and only few were specific to each host. Whereas pine induced more carbohydrate active enzymes (CAZymes), the interaction with poplar induced the expression of specific SSPs. We identified a set of 22 MiSSPs, which are located in both, gene-rich, repeat-poor or gene-sparse, repeat-rich regions of the C. geophilum genome, a genome showing a bipartite architecture as seen for some pathogens but not yet for an ectomycorrhizal fungus. Genome re-sequencing data of 15 C. geophilum strains and two close relatives Glonium stellatum and Lepidopterella palustris were used to study sequence conservation of MiSSP-encoding genes. The 22 MiSSPs showed a high presence-absence polymorphism among the studied C. geophilum strains suggesting an evolution through gene gain/gene loss. Finally, we showed that six CgMiSSPs target four distinct sub-cellular compartments such as endoplasmic reticulum, plasma membrane, cytosol and tonoplast. Overall, this work presents a comprehensive analysis of secreted proteins and MiSSPs in different genetic level of C. geophilum opening a valuable resource to future functional analysis.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2016

Evolution of Electrogenic Ammonium Transporters (AMTs)

The ammonium transporter gene family consists of three main clades, AMT, MEP, and Rh. The evolutionary history of the AMT/MEP/Rh gene family is characterized by multiple horizontal gene transfer events, gene family expansion and contraction, and gene loss; thus the gene tree for this family of transporters is unlike the organismal tree. The genomes of angiosperms contain genes for both electrogenic and electroneutral ammonium transporters, but it is not clear how far back in the land plant lineage electrogenic ammonium transporters occur. Here, we place Marchantia polymorpha ammonium transporters in the AMT/MEP/Rh phylogeny and we show that AMTs from the liverwort M. polymorpha are electrogenic. This information suggests that electrogenic ammonium transport evolved at least as early as the divergence of bryophytes in the land plant lineage.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2019

The Plant Ontology Facilitates Comparisons of Plant Development Stages Across Species

The Plant Ontology (PO) is a community resource consisting of standardized terms, definitions, and logical relations describing plant structures and development stages, augmented by a large database of annotations from genomic and phenomic studies. This paper describes the structure of the ontology and the design principles we used in constructing PO terms for plant development stages. It also provides details of the methodology and rationale behind our revision and expansion of the PO to cover development stages for all plants, particularly the land plants (bryophytes through angiosperms). As a case study to illustrate the general approach, we examine variation in gene expression across embryo development stages in Arabidopsis and maize, demonstrating how the PO can be used to compare patterns of expression across stages and in developmentally different species. Although many genes appear to be active throughout embryo development, we identified a small set of uniquely expressed genes for each stage of embryo development and also between the two species. Evaluating the different sets of genes expressed during embryo development in Arabidopsis or maize may inform future studies of the divergent developmental pathways observed in monocotyledonous versus dicotyledonous species. The PO and its annotation database (http://www.planteome.org) make plant data for any species more discoverable and accessible through common formats, thus providing support for applications in plant pathology, image analysis, and comparative development and evolution.

Plant Sciences↗

DOE OSTI2021

Phylogenetic occurrence of the phenylpropanoid pathway and lignin biosynthesis in plants

The phenylpropanoid pathway serves as a rich source of metabolites in plants and provides precursors for lignin biosynthesis. Lignin first appeared in tracheophytes and has been hypothesized to have played pivotal roles in land plant colonization. In this review, we summarize recent progress in defining the lignin biosynthetic pathway in lycophytes, monilophytes, gymnosperms, and angiosperms. In particular, we review the key structural genes involved in p-hydroxyphenyl-, guaiacyl- and syringyl-lignin biosynthesis across plant taxa and consider and integrate new insights on major transcription factors, such as NACs and MYBs. We also review insight regarding a new transcriptional regulator, 5-enolpyruvylshikimate-3-phosphate (EPSP) synthase, canonically identified as a key enzyme in the shikimate pathway. We use several case studies, including EPSP synthase, to illustrate the evolution processes of gene duplication and neo-functionalization in lignin biosynthesis. This review provides new insights into the genetic engineering of the lignin biosynthetic pathway to overcome biomass recalcitrance in bioenergy crops.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

Functional Diversification of Populus FLOWERING LOCUS D-LIKE3 Transcription Factor and Two Paralogs in Shoot Ontogeny, Flowering, and Vegetative Phenology

Both the evolution of tree taxa and whole-genome duplication (WGD) have occurred many times during angiosperm evolution. Transcription factors are preferentially retained following WGD suggesting that functional divergence of duplicates could contribute to traits distinctive to the tree growth habit. We used gain- and loss-of-function transgenics, photoperiod treatments, and circannual expression studies in adult trees to study the diversification of three Populus FLOWERING LOCUS D-LIKE (FDL) genes encoding bZIP transcription factors. Expression patterns and transgenic studies indicate that FDL2.2 promotes flowering and that FDL1 and FDL3 function in different vegetative phenophases. Study of dominant repressor FDL versions indicates that the FDL proteins are partially equivalent in their ability to alter shoot growth. Like its paralogs, FDL3 overexpression delays short day-induced growth cessation, but also induces distinct heterochronic shifts in shoot development—more rapid phytomer initiation and coordinated delay in both leaf expansion and the transition to secondary growth in long days, but not in short days. Our results indicate that both regulatory and protein coding sequence variation contributed to diversification of FDL paralogs that has led to a degree of specialization in multiple developmental processes important for trees and their local adaptation.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2024

A systems genetic analysis identifies putative mechanisms and candidate genes regulating vessel traits in poplar wood

Wood is the water conducting tissue of tree stems. Like most angiosperm trees, poplar wood contains water-conducting vessel elements whose functional properties affect water transport and growth rates, as well as susceptibility to embolism and hydraulic failure during water stress and drought. Here we used a unique hybrid poplar pedigree carrying genomically characterized chromosomal insertions and deletions to undertake a systems genomics analysis of vessel traits. We assayed gene expression in wood forming tissues from clonal replicates of genotypes covering dosage quantitative trait loci with insertions and deletions, genotypes with extreme vessel trait phenotypes, and control genotypes. A gene co-expression analysis was used to assign genes to modules, which were then used in integrative analyses to identify modules associated with traits, to identify putative molecular and cellular processes associated with each module, and finally to identify candidate genes using multiple criteria including dosage responsiveness. These analyses identified known processes associated with vessel traits including stress response, abscisic acid and cell wall biosynthesis, and in addition identified previously unexplored processes including cell cycle and protein ubiquitination. We discuss our findings relative to component processes contributing to vessel trait variation including signaling, cell cycle, cell expansion, and cell differentiation.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

Transcriptome Sequencing of Agave angustifolia Reveals Conservation and Diversification in the Expression of Cinnamyl Alcohol Dehydrogenase Genes in Agave Species

Agave angustifolia is an important crassulacean acid metabolism plant species, with wide applications in beverage and sisal fiber production. In this study, we carried out a transcriptome analysis of A. angustifolia leaves, generating a total of 58,482,436 clean reads through Illumina paired-end sequencing. De novo transcriptome assembly generated 67,314 unigenes, with about half of them having homologs in four public databases. In the Nr database, Asparagus officinalis was shown to be most closely related to agave, and the early angiosperm Amborella trichopoda was selected as an outgroup species. We further identified five, two, seven, seven, seven, six and six CAD genes in asparagus, amborella, A. deserti, A. tequilana, A. americana, A. hybrid H11648 and A. angustifolia, respectively. The maximum likelihood phylogenetic tree revealed the species-specific expansion of CAD genes in arabidopsis, rice and agave. The expression analysis indicated the conservatively expressed CAD1/2/4/6, providing candidate targets for manipulation to improve lignin traits. The species-specific expression of CAD3/5/7 indicates the existence of different regulatory mechanisms controlling the expression of these genes in agave species. This study presents the first transcriptome dataset of A. angustifolia, facilitating future studies on lignin biosynthesis in agave.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

Do Genetic Drift and Gene Flow Affect the Geographic Distribution of Female Plants in Gynodioecious Lobelia siphilitica?

Variation in population sex ratio is particularly pronounced in gynodioecious angiosperms. Extremely high female frequencies in gynodioecious populations cannot be readily explained by selective forces alone. To assess the contributions of drift and gene flow to extreme sex-ratio variation, we documented sex ratio and population size in 92 populations of Lobelia siphilitica across its range and genotyped plants using plastid and nuclear genetic markers. Similarity in spatial patterns of genetic and demographic variables may suggest that drift and/or gene flow have contributed to population sex-ratio variation in L. siphilitica. We found strong spatial structuring of extremely high female frequencies: populations with >50% female plants are restricted to the south–central portion of the range. However, we did not detect any spatial structuring in population size nor metrics of genetic diversity, suggesting that extreme variation in female frequency is not strongly affected by drift or gene flow. Extreme sex-ratio variation is frequently observed in gynodioecious plants, but its causes are difficult to identify. Further investigation into mechanisms that create or maintain the spatial structure of sex ratios in gynodioecious species will provide much needed insight.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2025

Identification and Characterization of Lipid Droplet-Associated Protein (LDAP) Isoforms from Tung Tree (Vernicia fordii)

Lipid droplets (LDs) are cytoplasmic organelles responsible primarily for the storage of neutral lipids, such as triacyclglycerols (TAGs). Derived from the endoplasmic reticulum bilayer, LDs are composed of a hydrophobic lipid core encased by a phospholipid monolayer and surface-associated proteins. To date, only a relatively few LD ‘coat’ proteins in plants have been identified and characterized, most of which come from studies of the model plant Arabidopsis thaliana. To expand our knowledge of the plant LD proteome, the LD-associated protein (LDAP) family from the tung tree (Vernicia fordii), whose seeds are rich in a commercially valuable TAG containing the conjugated fatty acid α-eleostearic acid (C18:3Δ9cis,11trans,13trans [α-ESA]), was identified and characterized. Based on the tung tree transcriptome, three LDAP isoforms (VfLDAP1-3) were elucidated and the encoded proteins distinctly clustered into three clades along with their respective isoforms from other angiosperm species. Ectopic expression of the VfLDAPs in Nicotiana benthamiana leaves revealed that they localized specifically to LDs and influenced LD numbers and sizes, as well as increasing TAG content and altering TAG fatty acid composition. Interestingly, in a partially reconstructed TAG-ESA biosynthetic pathway, the co-expression of VfLDAP3 and, to a lesser degree, VfLDAP2, significantly increased the content of α-ESA stored within the LDs. These results suggest that the VfLDAPs can influence the steady-state content and composition of TAG in plant cells and that certain LDAP isoforms may have evolved to more efficiently package TAGs into LDs containing unusual fatty acids, such as α-ESA.

Plant Sciences↗

NASA NTRS1974

Release of volatile mercury from vascular plants

Volatile, organic solvent soluble mercury has been found in leaves and seeds of several angiosperms. Leaves of garlic vine, avocado, and haole-koa release mercury in volatile form rapidly at room temperature. In garlic vine, the most active release is temperature dependent, but does not parallel the vapor-pressure temperature relationship for mercury. Mercury can be trapped in nitric-perchloric acid digestion fluid, or n-hexane, but is lost from the hexane unless the acid mixture is present. Seeds of haole-koa also contain extractable mercury but volatility declines in the series n-hexane (90%), methanol (50%), water (10%). This suggests that reduced volatility may accompany solvolysis in the more polar media.

Siegel, S. M.↗

NASA NTRS1983

Prochloron-ascidian symbioses: Photosynthetic potential and productivity

The chlorophyll content of didemnid asidians with symbiotic algae (Prochloron) from oligotropic tropical marine waters around Palau, Western Carolin Islands is discussed. Several species contain as much chlorophyll per unit dry weight as many herbaceous crop plants and more than do other symbiotic associations such as lichens, green Hydra, etc. Their chlorphyllA/B ratios (3-9) were generally much lighter than those of angiosperms (2-4). Where they abound, Prochloron - ascidian symbiosis could make a major contribution to the productivity, especially in localized areas of tropical marine waters characterized by low nutrient levels and high irradiance.

Lewin, R. A.↗

NASA NTRS1993

Cellular polarity and interactions in plant graviperception

Presented are results of studies on the mechanisms of gravitropic sensing in higher and lower plants. Gravitropic roots of the aquatic angiosperm, Limnobium, were found to have sedimented amyloplasts in their elongation zone but not in their rootcap; nuclei were found to sediment in the elongation zone as well. Another study attempted to understand how plastid sedimentation occurs in vertical Ceratodon cells and how this sedimentation is regulated. To determine whether the cytoskeleton restricts plastid sedimentation, the effects of amiprophos-methyl (APM) and cytochalasin (CD) on plastid position were qualified. Results suggest that microtubules restrict the sedimentation of plastids along the length of the cell and that microtubules are load-bearing for all the plastids in the apical cell, demonstrating the importance of the cytoskeleton in maintaining organelle position and cell organization against the force of gravity. Physcomitrella and Funaria were also studied. Results suggest that gravitropism may be relatively common in moss protonemata and reinforce the idea that amyloplast mass functions in gravitropic sensing.

Sack, Fred D.↗

NASA NTRS1993

Did surface temperatures constrain microbial evolution?

The proposition that glaciation may not have occurred before the Cenozoic--albeit not yet a consensus position--nevertheless raises for reconsideration the surface temperature history of the earth. Glacial episodes, from the Huronian (2.3 billion years ago; BYA) through the late Paleozoic (320 to 250 million years ago; MYA) have been critical constraints on estimation of the upper bounds of temperature (Crowley 1983, Kasting and Toon 1989). Once removed, few if any constraints on the upper temperature limit other than life remain. Walker (1982) recognized that life provides an upper limit to temperature in the Precambrian. We propose a more radical concept: the upper temperature limit for viable growth of a given microbial group corresponds to the actual surface temperature at the time of the group's first appearance. In particular, we propose here that two major evolutionary developments--the emergence of cyanobacteria and aerobic eukaryotes--can be used to determine surface temperature in the Precambrian, and that only subsequent cooling mediated by higher plants and then angiosperms permitted what may possibly be the earth's first glaciation in the late Cenozoic.

NASA Program Exobiology↗

NASA NTRS1998

Analysis of xylem formation in pine by cDNA sequencing

Secondary xylem (wood) formation is likely to involve some genes expressed rarely or not at all in herbaceous plants. Moreover, environmental and developmental stimuli influence secondary xylem differentiation, producing morphological and chemical changes in wood. To increase our understanding of xylem formation, and to provide material for comparative analysis of gymnosperm and angiosperm sequences, ESTs were obtained from immature xylem of loblolly pine (Pinus taeda L.). A total of 1,097 single-pass sequences were obtained from 5' ends of cDNAs made from gravistimulated tissue from bent trees. Cluster analysis detected 107 groups of similar sequences, ranging in size from 2 to 20 sequences. A total of 361 sequences fell into these groups, whereas 736 sequences were unique. About 55% of the pine EST sequences show similarity to previously described sequences in public databases. About 10% of the recognized genes encode factors involved in cell wall formation. Sequences similar to cell wall proteins, most known lignin biosynthetic enzymes, and several enzymes of carbohydrate metabolism were found. A number of putative regulatory proteins also are represented. Expression patterns of several of these genes were studied in various tissues and organs of pine. Sequencing novel genes expressed during xylem formation will provide a powerful means of identifying mechanisms controlling this important differentiation pathway.

Non-NASA Center↗

DOE OSTI2017

Two early eudicot fossil flowers from the Kamikitaba assemblage (Coniacian, Late Cretaceous) in northeastern Japan

Two new fossil taxa referable to the basal eudicot grade are described from the Kamikitaba locality (ca. 89 MYBP, early Coniacian: Late Cretaceous) in the Ashizawa Formation (Asamigawa Member) of Futaba Group in northeastern Japan. These charcoalified mesofossils exhibit well-preserved three-dimensional structure and were analyzed using synchrotron-radiation X-ray microtomography (SRXTM) at the Advanced Photon Source (APS) to document the composition and internal structure. Cathiaria japonica sp. nov. is represented by infructescence segments that consist of an axis bearing three to four fruits. The capsular fruits are sessile and dehiscent and consist of a gynoecium subtended by a bract. No perianth parts are present. The gynoecium is monocarpellate containing two pendulous seeds. The carpel is ascidiate in the lower half and conduplicate in the upper part, style is deflected abaxially with a dorsiventral suture and a large, obliquely decurrent stigma. Pollen grains are tricolpate with a reticulate exine. The morphological features of Cathiaria are consistent with an assignment to the Buxaceae s. l. (including Didymelaceae). Archaeostella verticillata gen. et sp. nov. is represented by flowers that are small, actinomorphic, pedicellate, bisexual, semi-inferior, and multicarpellate. The floral receptacle is cup shaped with a perigynous perianth consisting of several tepals inserted around the rim. The androecium comprises ca. 120 stamens with clear differentiation into anther and filament. The anthers are basifixed and tetrasporangiate. The gynoecium consists of a whorl of ten conduplicate, laterally connate but distally distinct carpels with a conspicuous dorsal bulge, including a central cavity. The styles are short, becoming recurved with a ventrally decurrent stigma. The fruit type is a follicle. Seeds are ca. 10 per carpel, marginal, pendulous from the broad, oblique summit of the locule. Seeds are small, spindle-shaped, with a chalazal extension, Pollen grains are tricolpate with a reticulate exine pattern, suggesting a relationship to eudicots. The morphological features of Archaeostella indicate a possible relationship to Trochodendraceae in the basal grade of eudicots, although it is uncertain if the anther thecae open by longitudinal slits as in extant Trochodendron. The fossil currently provides the earliest record of the family and documents the presence of Trochodendraceae in eastern Eurasia during the middle part of the Late Cretaceous. Furthermore, the recovery of Cathiaria japonica and Archaeostella verticillata from the Kamikitaba locality suggests that the basal eudicot families Trochodendraceae and Buxaceae s. l. (including Didymelaceae) were differentiated and distributed in eastern Eurasia area during the Late Cretaceous.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2019

Methane and CO2 chamber fluxes and porewater concentrations US-OWC Ameriflux wetland site, 2015-2018

The data measurements of CH4 and CO2 at different patch types (classified by dominant macrophyte vegetation or hydrological state). CH4 and CO2 data include 3 types of measurements: 1) Surface flux measurements from chamber measurements. 2) Leaf flux measurements from plant chambers, providing the rate per leaf area of methane flow through three species of macropyte aerenchemous plants (Water Lily, American Lotus, and Cattail) with the corresponding flux of CO2 at the same leaves. 3) Pore water concentrations of dissolved CO2 and CH4 concentrations. These are measured along vertical profiles at varying depths from the soil-water interface using in-situ porewater dialysis profiles (peepers). Observations of 1 and 3 are available monthly for most months of the growing season (May-September) of 2015, 2016 and 2018. Leaf flux measurements (plant chambers) are available only in June, July and August of 2018. We also included the patch type classification maps during 2015, 2017 and 2018 the relative water elevation map (bathymetry) for the site.In 8/23/2020 we added the data file ChamberFluxes_2018_Separated_Diffusive_Ebullitive_Fluxes.xlsx with observation related to chamber measurements in OWC during September 2018. In these observations, we partitioned the methane flux to its diffusive and ebullitive components, using an analysis approach we describe in section 5 of the methods "Ebullition and diffusion partitioning".

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2022

Raw seedling and sapling census data collected from June 2015 - April 2019 within a tropical wet forest in Puerto Rico

This data package contains data used to evaluate the effects of experimental warming (4˚C above ambient), drought, and hurricane disturbance on species richness, diversity, and composition of understory plant communities across ontogeny at the Tropical Responses to Altered Climate Experiment (TRACE) in Luquillo, Puerto Rico. The raw data in this package include a file for the species composition matrix of woody seedlings (>10 cm and <20 cm height; TRACE_composition_seedling.csv) and saplings (>20 cm height; TRACE_composition_sapling.csv) within the six TRACE plots, collected during six census dates from June 2015 to April 2019. Also included is also a file with the species names associated with the species codes found in the composition files (TRACE_species_codes.csv), and a data dictionary file describing the columns in the composition files (data_dictionary_composition_files.csv). All data files are in csv format, with the exception of the metadata which is in xml format.

54 ENVIRONMENTAL SCIENCES↗