Publications (63)374.26 Total impact
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Article: A dual role of strigolactones in phosphate acquisition and utilization in plants.
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ABSTRACT: Phosphorus, acquired in the form of phosphate (Pi), is one of the primary macronutrients for plants but is least available in the soil. Pi deficiency is a major factor limiting plant growth, development and reproduction. Plants have developed a complex signaling network to respond to Pi deficiency. The recent discovery of strigolactones, a new class of plant hormones, has led to an emerging signaling module illustrating the integrated control of Pi acquisition, plant-microbe symbiotic interactions and plant architecture. This review article focuses on the recent findings of plant responses and roles of strigolactones to Pi deficiency.International Journal of Molecular Sciences 01/2013; 14(4):7681-701. · 2.60 Impact Factor -
Article: Genome Anchored QTLs for Biomass Productivity in Hybrid Populus Grown under Contrasting Environments.
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ABSTRACT: Traits related to biomass production were analyzed for the presence of quantitative trait loci (QTLs) in a Populus trichocarpa × P. deltoides F(2) population. A genetic linkage map composed of 841 SSR, AFLP, and RAPD markers and phenotypic data from 310 progeny were used to identify genomic regions harboring biomass QTLs. Twelve intervals were identified, of which BM-1, BM-2, and BM-7 were identified in all three years for both height and diameter. One putative QTL, BM-7, and one suggestive QTL exhibited significant evidence of over-dominance in all three years for both traits. Conversely, QTLs BM-4 and BM-6 exhibited evidence of under-dominance in both environments for height and diameter. Seven of the nine QTLs were successfully anchored, and QTL peak positions were estimated for each one on the P. trichocarpa genome assembly using flanking SSR markers with known physical positions. Of the 3,031 genes located in genome-anchored QTL intervals, 1,892 had PFAM annotations. Of these, 1,313, representing 255 unique annotations, had at least one duplicate copy in a QTL interval identified on a separate scaffold. This observation suggests that some QTLs identified in this study may have shared the same ancestral sequence prior to the salicoid genome duplication in Populus.PLoS ONE 01/2013; 8(1):e54468. · 4.09 Impact Factor -
Article: Populus trichocarpa cell wall chemistry and ultrastructure trait variation, genetic control and genetic correlations.
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ABSTRACT: The increasing ecological and economical importance of Populus species and hybrids has stimulated research into the investigation of the natural variation of the species and the estimation of the extent of genetic control over its wood quality traits for traditional forestry activities as well as the emerging bioenergy sector. A realized kinship matrix based on informative, high-density, biallelic single nucleotide polymorphism (SNP) genetic markers was constructed to estimate trait variance components, heritabilities, and genetic and phenotypic correlations. Seventeen traits related to wood chemistry and ultrastructure were examined in 334 9-yr-old Populus trichocarpa grown in a common-garden plot representing populations spanning the latitudinal range 44° to 58.6°. In these individuals, 9342 SNPs that conformed to Hardy-Weinberg expectations were employed to assess the genomic pair-wise kinship to estimate narrow-sense heritabilities and genetic correlations among traits. The range-wide phenotypic variation in all traits was substantial and several trait heritabilities were > 0.6. In total, 61 significant genetic and phenotypic correlations and a network of highly interrelated traits were identified. The high trait variation, the evidence for moderate to high heritabilities and the identification of advantageous trait combinations of industrially important characteristics should aid in providing the foundation for the enhancement of poplar tree breeding strategies for modern industrial use.New Phytologist 12/2012; · 6.64 Impact Factor -
Article: Evolutionary analyses of non-family genes in plants.
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ABSTRACT: There are a large number of "non-family" (NF) genes that do not cluster into families with three or more members per genome. While gene families have been extensively studied, a systematic analysis of NF genes has not been reported. We performed comparative studies on NF genes in 14 plant species. Based on the clustering of protein sequences, we identified ~94,000 NF genes across these species that were divided into five evolutionary groups: Viridiplantae-wide, angiosperm-specific, monocot-specific, dicot-specific, and those that were species-specific. Our analysis revealed that the NF genes resulted largely from less frequent gene duplications and/or a higher rate of gene loss after segmental duplication relative to genes in both low-copy-number families (LF; 3 - 10 copies per genome) and high-copy-number families (HF; >10 copies). Furthermore, we identified functions enriched in the NF gene set as compared with the HF genes. We found that NF genes were involved in essential biological processes shared by all plant lineages (e.g., photosynthesis and translation), as well as gene regulation and stress responses associated with phylogenetic diversification. In particular, our analysis of an Arabidopsis protein-protein interaction network revealed that hub proteins with the top 10% most connections were over-represented in the NF set relative to the HF set. This research highlights the roles that NF genes may play in evolutionary and functional genomics research. © 2012 The Authors. The Plant Journal © 2012 Blackwell Publishing Ltd.The Plant Journal 11/2012; · 6.16 Impact Factor -
Article: Involvement of auxin pathways in modulating root architecture during beneficial plant-microorganism interactions.
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ABSTRACT: A wide variety of microorganisms known to produce auxin and auxin precursors form beneficial relationships with plants and alter host root development. Moreover other signals produced by microorganisms affect auxin pathways in host plants. The precise role of auxin and auxin signaling pathways in modulating plant-microbe interactions, however, is unknown. Dissecting out the auxin synthesis, transport and signaling pathways resulting in the characteristic molecular, physiological and developmental response in plants will further illuminate upon how these intriguing inter-species interactions, of environmental, ecological and economic significance, occur. The present review seeks to survey and summarize the scattered evidences in support of known host root modifications brought about by beneficial microorganisms and implicate the role of auxin synthesis, transport and signal transduction in modulating beneficial effects in plants. Finally, through a synthesis of the current body of work we present outstanding challenges and potential future research directions on studies related to auxin signaling in plant-microbe interactions. © 2012 Blackwell Publishing Ltd.Plant Cell and Environment 11/2012; · 5.22 Impact Factor -
Article: 3D Chemical Image using TOF-SIMS Revealing the Biopolymer Component Spatial and Lateral Distributions in Biomass.
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ABSTRACT: Show me inside: 3D time-of-flight secondary-ion mass spectrometry (TOF-SIMS) with a dual-beam mode allows detecting the characteristic biopolymers from surface to subsurface in plant cell walls. Lateral and vertical distribution of major components can thereby be mapped to understand the structural architecture of plant cell walls at under sub-micrometer scales (see picture: green=cellulose, red=lignin).Angewandte Chemie International Edition 10/2012; · 13.45 Impact Factor -
Article: Putting the Pieces Together: High-performance LC-MS/MS Provides Network-, Pathway-, and Protein-level Perspectives in Populus.
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ABSTRACT: High-performance mass spectrometry (MS)-based proteomics enabled the construction of a detailed proteome atlas for Populus, a woody perennial plant model organism. Optimization of experimental procedures and implementation of current state-of-the-art instrumentation afforded the most detailed look into the predicted proteome space of Populus, offering varying proteome perspectives: 1) network-wide, 2) pathway-specific, and 3) protein-level viewpoints. Together, enhanced protein retrieval through a detergent-based lysis approach and maximized peptide sampling via the dual-pressure linear ion trap mass spectrometer (LTQ Velos), have resulted in the identification of 63,056 tryptic peptides. The technological advancements, specifically spectral-acquisition and sequencing speed, afforded the deepest look into the Populus proteome, with peptide abundances spanning 6 orders of magnitude and mapping to ~25% of the predicted proteome space. In total, tryptic peptides mapped to 13,574 protein assignments across four organ-types: mature (fully expanded, leaf plastichronic index (LPI) 10-12) leaf, young (juvenile, LPI 4-6) leaf, root, and stem. To resolve protein ambiguity, identified proteins were grouped by sequence similarity (≥ 90%), thereby reducing the protein assignments into 7,538 protein groups. In addition, this large-scale data set features the first systems-wide survey of protein expression across different Populus organs. As a demonstration of the precision and comprehensiveness of the semi-quantitative analysis, we were able to contrast two stages of leaf development, mature versus young leaf. Statistical comparison through ANOVA analysis revealed 1,432 protein groups that exhibited statistically significant (p≤0.01) differences in protein abundance. Experimental validation of the metabolic circuitry expected in mature leaf (characterized by photosynthesis and carbon fixation) compared to young leaf (characterized by rapid growth and moderate photosynthetic activities) strongly testifies to the credibility of the approach. Instead of quantitatively comparing a few proteins, a systems view of all the changes associated with a given cellular perturbation could be made.Molecular & Cellular Proteomics 10/2012; · 7.40 Impact Factor -
Article: Highly Efficient Isolation of Populus Mesophyll Protoplasts and Its Application in Transient Expression Assays
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ABSTRACT: Background: Populus is a model woody plant and a promising feedstock for lignocellulosic biofuel production. However, its lengthy life cycle impedes rapid characterization of gene function.PLoS ONE 09/2012; · 4.09 Impact Factor -
Article: Initial characterization of shade avoidance response suggests functional diversity between Populus phytochrome B genes.
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ABSTRACT: Shade avoidance signaling involves perception of incident red/far-red (R/FR) light by phytochromes (PHYs) and modulation of downstream transcriptional networks. Although these responses are well studied in Arabidopsis, little is known about the role of PHYs and the transcriptional responses to shade in the woody perennial Populus. Tissue expression and subcellular localization of Populus PHYs was studied by quantitative real-time PCR (qRT-PCR) and protoplast transient assay. Transgenic lines with altered PHYB1 and/or PHYB2 expression were used in phenotypic assays and transcript profiling with qRT-PCR. RNA-Seq was used to identify transcriptional responses to enriched FR light. All three PHYs were differentially expressed among tissue types and PHYBs were targeted to the nucleus under white light. Populus PHYB1 rescued Arabidopsis phyB mutant phenotypes. Phenotypes of Populus transgenic lines and the expression of candidate shade response genes suggested that PHYB1 and PHYB2 have distinct yet overlapping functions. RNA-Seq analysis indicated that genes associated with cell wall modification and brassinosteroid signaling were induced under enriched FR light in Populus. This study is an initial attempt at deciphering the role of Populus PHYs by evaluating transcriptional reprogramming to enriched FR and demonstrates functional diversity and overlap of the Populus PHYB1 and PHYB2 in regulating shade responses.New Phytologist 09/2012; 196(3):726-37. · 6.64 Impact Factor -
Article: Characterization of Transposable Elements in the Ectomycorrhizal Fungus Laccaria bicolor
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ABSTRACT: Background The publicly available Laccaria bicolor genome sequence has provided a considerable genomic resource allowing systematic identification of transposable elements (TEs) in this symbiotic ectomycorrhizal fungus. Using a TE-specific annotation pipeline we have characterized and analyzed TEs in the L. bicolor S238N-H82 genome. Methodology/Principal Findings TEs occupy 24% of the 60 Mb L. bicolor genome and represent 25,787 full-length and partial copy elements distributed within 171 families. The most abundant elements were the Copia-like. TEs are not randomly distributed across the genome, but are tightly nested or clustered. The majority of TEs exhibits signs of ancient transposition except some intact copies of terminal inverted repeats (TIRS), long terminal repeats (LTRs) and a large retrotransposon derivative (LARD) element. There were three main periods of TE expansion in L. bicolor: the first from 57 to 10 Mya, the second from 5 to 1 Mya and the most recent from 0.5 Mya ago until now. LTR retrotransposons are closely related to retrotransposons found in another basidiomycete, Coprinopsis cinerea. Conclusions This analysis 1) represents an initial characterization of TEs in the L. bicolor genome, 2) contributes to improve genome annotation and a greater understanding of the role TEs played in genome organization and evolution and 3) provides a valuable resource for future research on the genome evolution within the Laccaria genus.PLoS ONE 08/2012; · 4.09 Impact Factor -
Article: Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa.
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ABSTRACT: • Plant population genomics informs evolutionary biology, breeding, conservation and bioenergy feedstock development. For example, the detection of reliable phenotype-genotype associations and molecular signatures of selection requires a detailed knowledge about genome-wide patterns of allele frequency variation, linkage disequilibrium and recombination. • We resequenced 16 genomes of the model tree Populus trichocarpa and genotyped 120 trees from 10 subpopulations using 29 213 single-nucleotide polymorphisms. • Significant geographic differentiation was present at multiple spatial scales, and range-wide latitudinal allele frequency gradients were strikingly common across the genome. The decay of linkage disequilibrium with physical distance was slower than expected from previous studies in Populus, with r(2) dropping below 0.2 within 3-6 kb. Consistent with this, estimates of recent effective population size from linkage disequilibrium (N(e) ≈ 4000-6000) were remarkably low relative to the large census sizes of P. trichocarpa stands. Fine-scale rates of recombination varied widely across the genome, but were largely predictable on the basis of DNA sequence and methylation features. • Our results suggest that genetic drift has played a significant role in the recent evolutionary history of P. trichocarpa. Most importantly, the extensive linkage disequilibrium detected suggests that genome-wide association studies and genomic selection in undomesticated populations may be more feasible in Populus than previously assumed.New Phytologist 08/2012; 196(3):713-725. · 6.64 Impact Factor -
Article: Reference genome sequence of the model plant Setaria.
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ABSTRACT: We generated a high-quality reference genome sequence for foxtail millet (Setaria italica). The ∼400-Mb assembly covers ∼80% of the genome and >95% of the gene space. The assembly was anchored to a 992-locus genetic map and was annotated by comparison with >1.3 million expressed sequence tag reads. We produced more than 580 million RNA-Seq reads to facilitate expression analyses. We also sequenced Setaria viridis, the ancestral wild relative of S. italica, and identified regions of differential single-nucleotide polymorphism density, distribution of transposable elements, small RNA content, chromosomal rearrangement and segregation distortion. The genus Setaria includes natural and cultivated species that demonstrate a wide capacity for adaptation. The genetic basis of this adaptation was investigated by comparing five sequenced grass genomes. We also used the diploid Setaria genome to evaluate the ongoing genome assembly of a related polyploid, switchgrass (Panicum virgatum).Nature Biotechnology 05/2012; 30(6):555-61. · 29.50 Impact Factor -
Article: Genomic aspects of research involving polyploid plants
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ABSTRACT: Almost all extant plant species have doubled their genomes at least once in their evolutionary histories, resulting in polyploidy which provided a rich genomic resource for evolutionary processes. Moreover, superior polyploid clones have been developed during the process of crop domestication. Polyploid plants generated by evolutionary processes and/or crop domestication have been the intentional or serendipitous focus of research dealing with the dynamics and consequences of genome evolution. One of the new trends in genomics research is to create synthetic polyploid plants which provide materials for studying the initial genomic changes/responses immediately after polyploid formation. Polyploid plants are also used in functional genomics research to study gene expression in a complex genomic background. In this review, we summarize recent progress in genomics research involving ancient, young, and synthetic polyploid plants, with a focus on genome size evolution, genomic diversity, genomic rearrangement, genetic and epigenetic changes in duplicated genes, gene discovery, and comparative genomics. Implications on plant sciences including evolution, functional genomics, and plant breeding are presented. Polyploids will be a focus of genomic research in the future as rapid advances in DNA sequencing technology create unprecedented opportunities for discovering and monitoring genomic and transcriptomic changes. The accumulation of knowledge on polyploid formation, maintenance, and divergence at whole-genome and subgenome levels will not only help plant biologists understand how plants have evolved and diversified, but also assist plant breeders in designing new strategies for crop improvement. KeywordsEvolution–Genetics–EpigeneticsPlant Cell Tissue and Organ Culture 04/2012; 104(3):387-397. · 3.09 Impact Factor -
Article: Characterization of microsatellites in the coding regions of the Populus genome
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ABSTRACT: With the development of high-throughput sequencing techniques, transcriptome sequencing projects which provide valuable resources for designing simple sequence repeat (SSR) primers have been carried out for many plants. However, the utility of SSRs for molecular breeding depends on genome-wide distribution and coverage, as well as moderately high allelic variability, in the available SSR library. In this study, we characterized the exonic SSRs developed from the publicly available Populus genome as a case study to determine their value for molecular breeding. As expected, our results confirmed that microsatellites occurred approximately three times less often in coding regions than in non-coding regions. Mutability test also showed that exonic SSRs contained less allelic variability than intronic SSRs. More importantly, exonic SSRs were unevenly distributed both among and within chromosomes. Large exonic SSRs deserts were observed on several chromosomes. Differential selection between paralogous chromosomes, at the gene level, appears to be responsible for these SSR deserts, though the mechanisms that cause chromosome-specific SSR deserts are not known. This work provides ample evidence that the candidate gene approach based on unigenes identified from transcribed sequences may not be the best strategy to identify highly polymorphic SSRs. KeywordsExonic SSRs–Allelic variability–Polymorphism information content–Molecular breeding– PopulusMolecular Breeding 04/2012; 27(1):59-66. · 2.85 Impact Factor -
Article: Identification of quantitative trait loci and candidate genes for cadmium tolerance in Populus.
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ABSTRACT: Understanding genetic variation for the response of Populus to heavy metals like cadmium (Cd) is an important step in elucidating the underlying mechanisms of tolerance. In this study, a pseudo-backcross pedigree of Populus trichocarpa Torr. & Gray and Populus deltoides Bart. was characterized for growth and performance traits after Cd exposure. A total of 16 quantitative trait loci (QTL) at logarithm of odds (LOD) ratio ≥ 2.5 were detected for total dry weight, its components and root volume. Major QTL for Cd responses were mapped to two different linkage groups and the relative allelic effects were in opposing directions on the two chromosomes, suggesting differential mechanisms at these two loci. The phenotypic variance explained by Cd QTL ranged from 5.9 to 11.6% and averaged 8.2% across all QTL. A whole-genome microarray study led to the identification of nine Cd-responsive genes from these QTL. Promising candidates for Cd tolerance include an NHL repeat membrane-spanning protein, a metal transporter and a putative transcription factor. Additional candidates in the QTL intervals include a putative homolog of a glutamate cysteine ligase, and a glutathione-S-transferase. Functional characterization of these candidate genes should enhance our understanding of Cd metabolism and transport and phytoremediation capabilities of Populus.Tree Physiology 04/2012; 32(5):626-38. · 2.88 Impact Factor -
Article: Micropropagation of Populus trichocarpa ‘Nisqually-1’: the genotype deriving the Populus reference genome
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ABSTRACT: Populus serves as a model tree for biotechnology and molecular biology research due to the availability of the reference genome sequence of Populus trichocarpa (Torr. & Gray) genotype ‘Nisqually-1’. However, ‘Nisqually-1’ has been shown to be very recalcitrant to micropropagation, regeneration and transformation. In this study, a highly efficient micropropagation protocol from greenhouse-grown shoot tips of ‘Nisqually-1’ was established. The optimal micropropagation protocol involves growing in vitro shoots in plant growth regulator-free Murashige and Skoog (MS) basal medium supplemented with 3% sucrose, 0.3% Gelrite® and 5–10gL−1 of activated charcoal. Plants grown on this medium were significantly longer, and contained significantly higher concentrations of chlorophyll. This highly effective protocol provides a consistent supply of quality leaf and stem materials throughout the year for transformation experiments and other in vitro manipulations, therefore eliminating inconsistency due to seasonal and greenhouse environmental variations and the need for repetitive tissue sterilization.Plant Cell Tissue and Organ Culture 04/2012; 99(3):251-257. · 3.09 Impact Factor -
Article: Identification of quantitative trait loci affecting ectomycorrhizal symbiosis in an interspecific F1 poplar cross and differential expression of genes in ectomycorrhizas of the two parents: Populus deltoides and Populus trichocarpa
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ABSTRACT: A Populus deltoides × Populus trichocarpa F1 pedigree was analyzed for quantitative trait loci (QTLs) affecting ectomycorrhizal development and for microarray characterization of gene networks involved in this symbiosis. A 300 genotype progeny set was evaluated for its ability to form ectomycorrhiza with the basidiomycete Laccaria bicolor. The percentage of mycorrhizal root tips was determined on the root systems of all 300 progeny and their two parents. QTL analysis identified four significant QTLs, one on the P. deltoides and three on the P. trichocarpa genetic maps. These QTLs were aligned to the P. trichocarpa genome and each contained several megabases and encompass numerous genes. NimbleGen whole-genome microarray, using cDNA from RNA extracts of ectomycorrhizal root tips from the parental genotypes P. trichocarpa and P. deltoides, was used to narrow the candidate gene list. Among the 1,543 differentially expressed genes (p value ≤ 0.05; ≥5.0-fold change in transcript level) having different transcript levels in mycorrhiza of the two parents, 41 transcripts were located in the QTL intervals: 20 in Myc_d1, 14 in Myc_t1, and seven in Myc_t2, while no significant differences among transcripts were found in Myc_t3. Among these 41 transcripts, 25 were overrepresented in P. deltoides relative to P. trichocarpa; 16 were overrepresented in P. trichocarpa. The transcript showing the highest overrepresentation in P. trichocarpa mycorrhiza libraries compared to P. deltoides mycorrhiza codes for an ethylene-sensitive EREBP-4 protein which may repress defense mechanisms in P. trichocarpa while the highest overrepresented transcripts in P. deltoides code for proteins/genes typically associated with pathogen resistance. KeywordsQuantitative trait loci–Poplar–Symbiosis–Ectomycorrhiza– LaccariaTree Genetics & Genomes 04/2012; 7(3):617-627. · 2.34 Impact Factor -
Article: Bioinformatics-Based Identification of Candidate Genes from QTLs Associated with Cell Wall Traits in Populus
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ABSTRACT: Quantitative trait locus (QTL) studies are an integral part of plant research and are used to characterize the genetic basis of phenotypic variation observed in structured populations and inform marker-assisted breeding efforts. These QTL intervals can span large physical regions on a chromosome comprising hundreds of genes, thereby hampering candidate gene identification. Genome history, evolution, and expression evidence can be used to narrow the genes in the interval to a smaller list that is manageable for detailed downstream functional genomics characterization. Our primary motivation for the present study was to address the need for a research methodology that identifies candidate genes within a broad QTL interval. Here we present a bioinformatics-based approach for subdividing candidate genes within QTL intervals into alternate groups of high probability candidates. Application of this approach in the context of studying cell wall traits, specifically lignin content and S/G ratios of stem and root in Populus plants, resulted in manageable sets of genes of both known and putative cell wall biosynthetic function. These results provide a roadmap for future experimental work leading to identification of new genes controlling cell wall recalcitrance and, ultimately, in the utility of plant biomass as an energy feedstock. Keywords Populus -Whole-genome duplication-Quantitative trait loci-Wood chemistry-Syringyl lignin-Guaiacyl lignin-BiofuelsBioEnergy Research 04/2012; 3(2):172-182. · 3.56 Impact Factor -
Article: From systems biology to photosynthesis and whole-plant physiology: a conceptual model for integrating multi-scale networks.
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ABSTRACT: Network analysis is now a common statistical tool for molecular biologists. Network algorithms are readily used to model gene, protein and metabolic correlations providing insight into pathways driving biological phenomenon. One output from such an analysis is a candidate gene list that can be responsible, in part, for the biological process of interest. The question remains, however, as to whether molecular network analysis can be used to inform process models at higher levels of biological organization. In our previous work, transcriptional networks derived from three plant species were constructed, interrogated for orthology and then correlated with photosynthetic inhibition at elevated temperature. One unique aspect of that study was the link from co-expression networks to net photosynthesis. In this addendum, we propose a conceptual model where traditional network analysis can be linked to whole-plant models thereby informing predictions on key processes such as photosynthesis, nutrient uptake and assimilation, and C partitioning.Plant signaling & behavior 02/2012; 7(2):260-2. -
Article: Defining the boundaries and characterizing the landscape of functional genome expression in vascular tissues of Populus using shotgun proteomics.
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ABSTRACT: Current state-of-the-art experimental and computational proteomic approaches were integrated to obtain a comprehensive protein profile of Populus vascular tissue. This featured: (1) a large sample set consisting of two genotypes grown under normal and tension stress conditions, (2) bioinformatics clustering to effectively handle gene duplication, and (3) an informatics approach to track and identify single amino acid polymorphisms (SAAPs). By applying a clustering algorithm to the Populus database, the number of protein entries decreased from 64,689 proteins to a total of 43,069 protein groups, thereby reducing 7505 identified proteins to a total of 4226 protein groups, in which 2016 were singletons. This reduction implies that ∼50% of the measured proteins shared extensive sequence homology. Using conservative search criteria, we were able to identify 1354 peptides containing a SAAP and 201 peptides that become tryptic due to a K or R substitution. These newly identified peptides correspond to 502 proteins, including 97 previously unidentified proteins. In total, the integration of deep proteome measurements on an extensive sample set with protein clustering and peptide sequence variants provided an exceptional level of proteome characterization for Populus, allowing us to spatially resolve the vascular tissue proteome.Journal of Proteome Research 01/2012; 11(1):449-60. · 5.11 Impact Factor
Top co-authors
Top Journals
Institutions
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2008–2012
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University of Tennessee
Knoxville, TN, USA
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2007–2012
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Oak Ridge National Laboratory
- • Environmental Sciences Division
- • Biosciences Division
Oak Ridge, FL, USA
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2011
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U.S. Department of Energy
Washington, D. C., DC, USA
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