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5.  The E3 ligase OsPUB15 interacts with the receptor-like kinase PID2 and regulates plant cell death and innate immunity 
BMC Plant Biology  2015;15:49.
Background
Rice blast disease is one of the most destructive diseases of rice worldwide. We previously cloned the rice blast resistance gene Pid2, which encodes a transmembrane receptor-like kinase containing an extracellular B-lectin domain and an intracellular serine/threonine kinase domain. However, little is known about Pid2-mediated signaling.
Results
Here we report the functional characterization of the U-box/ARM repeat protein OsPUB15 as one of the PID2-binding proteins. We found that OsPUB15 physically interacted with the kinase domain of PID2 (PID2K) in vitro and in vivo and the ARM repeat domain of OsPUB15 was essential for the interaction. In vitro biochemical assays indicated that PID2K possessed kinase activity and was able to phosphorylate OsPUB15. We also found that the phosphorylated form of OsPUB15 possessed E3 ligase activity. Expression pattern analyses revealed that OsPUB15 was constitutively expressed and its encoded protein OsPUB15 was localized in cytosol. Transgenic rice plants over-expressing OsPUB15 at early stage displayed cell death lesions spontaneously in association with a constitutive activation of plant basal defense responses, including excessive accumulation of hydrogen peroxide, up-regulated expression of pathogenesis-related genes and enhanced resistance to blast strains. We also observed that, along with plant growth, the cell death lesions kept spreading over the whole seedlings quickly resulting in a seedling lethal phenotype.
Conclusions
These results reveal that the E3 ligase OsPUB15 interacts directly with the receptor-like kinase PID2 and regulates plant cell death and blast disease resistance.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0442-4) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0442-4
PMCID: PMC4330927
U-box; E3 ligase; Protein interaction; Blast resistance; Cell death; Rice
6.  Oep23 forms an ion channel in the chloroplast outer envelope 
BMC Plant Biology  2015;15:47.
Background
Metabolite, ion and protein translocation into chloroplasts occurs across two membranes, the inner and the outer envelope. Solute and metabolite channels fulfill very important functions in integrating the organelles into the metabolic network of the cell. However so far only a few have been identified. Here we describe the identification and the characterization of the outer envelope protein of 23 kDa, Oep23 from garden pea.
Results
Oep23 is found in the entire plant lineage from green algae to flowering plants. It is expressed in all organs and developmental states tested so far. The reconstituted recombinant protein Oep23 from pea forms a high conductance ion channel with a maximal conductance in the fully open state of 466 ± 14pS at a holding potential of +100 mV (in 250 mM KCl). The Oep23 channel is cation selective (PK+ : PCl- = 15 : 1) with a voltage dependent open probability of maximal Vmem = 0 mV.
Conclusion
The data indicate that the Oep23 activity represents a single channel unit and does not assemble into a multiple pore complex like bacterial type porins or mitochondrial voltage dependent anion channel. Thus, Oep23 represents a new member of ion channels in the outer envelope of chloroplasts involved in solute exchange.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0445-1) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0445-1
PMCID: PMC4331141
Chloroplasts; Organelles; Ion channel; Membrane protein; Electrophysiology
7.  The Physcomitrella patens unique alpha-dioxygenase participates in both developmental processes and defense responses 
BMC Plant Biology  2015;15:45.
Background
Plant α-dioxygenases catalyze the incorporation of molecular oxygen into polyunsaturated fatty acids leading to the formation of oxylipins. In flowering plants, two main groups of α-DOXs have been described. While the α-DOX1 isoforms are mainly involved in defense responses against microbial infection and herbivores, the α-DOX2 isoforms are mostly related to development. To gain insight into the roles played by these enzymes during land plant evolution, we performed biochemical, genetic and molecular analyses to examine the function of the single copy moss Physcomitrella patens α-DOX (Ppα-DOX) in development and defense against pathogens.
Results
Recombinant Ppα-DOX protein catalyzed the conversion of fatty acids into 2-hydroperoxy derivatives with a substrate preference for α-linolenic, linoleic and palmitic acids. Ppα-DOX is expressed during development in tips of young protonemal filaments with maximum expression levels in mitotically active undifferentiated apical cells. In leafy gametophores, Ppα-DOX is expressed in auxin producing tissues, including rhizoid and axillary hairs. Ppα-DOX transcript levels and Ppα-DOX activity increased in moss tissues infected with Botrytis cinerea or treated with Pectobacterium carotovorum elicitors. In B. cinerea infected leaves, Ppα-DOX-GUS proteins accumulated in cells surrounding infected cells, suggesting a protective mechanism. Targeted disruption of Ppα-DOX did not cause a visible developmental alteration and did not compromise the defense response. However, overexpressing Ppα-DOX, or incubating wild-type tissues with Ppα-DOX-derived oxylipins, principally the aldehyde heptadecatrienal, resulted in smaller moss colonies with less protonemal tissues, due to a reduction of caulonemal filament growth and a reduction of chloronemal cell size compared with normal tissues. In addition, Ppα-DOX overexpression and treatments with Ppα-DOX-derived oxylipins reduced cellular damage caused by elicitors of P. carotovorum.
Conclusions
Our study shows that the unique α-DOX of the primitive land plant P. patens, although apparently not crucial, participates both in development and in the defense response against pathogens, suggesting that α-DOXs from flowering plants could have originated by duplication and successive functional diversification after the divergence from bryophytes.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0439-z) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0439-z
PMCID: PMC4334559
α-dioxygenases; Physcomitrella patens; Development; Defense; Pectobacterium; Botrytis cinerea
8.  A genome-wide analysis of MADS-box genes in peach [Prunus persica (L.) Batsch] 
BMC Plant Biology  2015;15:41.
Background
MADS-box genes encode a family of eukaryotic transcription factors distinguished by the presence of a highly-conserved ~58 amino acid DNA-binding and dimerization domain (the MADS-box). The central role played by MADS-box genes in peach endodormancy regulation led us to examine this large gene family in more detail. We identified the locations and sequences of 79 MADS-box genes in peach, separated them into established subfamilies, and broadly surveyed their tissue-specific and dormancy-induced expression patterns using next-generation sequencing. We then focused on the dormancy-related SVP/AGL24 and FLC subfamilies, comparing their numbers and phylogenetic relationships with those of other sequenced woody perennial genomes.
Results
We identified 79 MADS-box genes distributed across all eight peach chromosomes and frequently located in clusters of two or more genes. They encode proteins with a mean length of 248 ± 72 amino acids and include representatives from most of the thirteen Type II (MIKC) subfamilies, as well as members of the Type I Mα, Mβ, and Mγ subfamilies. Most Type I genes were present in species-specific monophyletic lineages, and their expression in the peach sporophyte was low or absent. Most Type II genes had Arabidopsis orthologs and were expressed at much higher levels throughout vegetative and fruit tissues. During short-day-induced growth cessation, seven Type II genes from the SVP/AGL24, AGL17, and SEP subfamilies showed significant changes in expression. Phylogenetic analyses indicated that multiple, independent expansions have taken place within the SVP/AGL24 and FLC lineages in woody perennial species.
Conclusions
Most Type I genes appear to have arisen through tandem duplications after the divergence of the Arabidopsis and peach lineages, whereas Type II genes appear to have increased following whole genome duplication events. An exception to the latter rule occurs in the FLC and SVP/AGL24 Type II subfamilies, in which species-specific tandem duplicates have been retained in a number of perennial species. These subfamilies comprise part of a genetic toolkit that regulates endodormancy transitions, but phylogenetic and expression data suggest that individual orthologs may not function identically across all species.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0436-2) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0436-2
PMCID: PMC4329201
MADS-box gene; MIKC gene; Dormancy; Peach; Prunus persica; SVP; FLC; AGL24
9.  Comparative genomics of grass EST libraries reveals previously uncharacterized splicing events in crop plants 
BMC Plant Biology  2015;15:39.
Background
Crop plants such as rice, maize and sorghum play economically-important roles as main sources of food, fuel, and animal feed. However, current genome annotations of crop plants still suffer false-positive predictions; a more comprehensive registry of alternative splicing (AS) events is also in demand. Comparative genomics of crop plants is largely unexplored.
Results
We performed a large-scale comparative analysis (ExonFinder) of the expressed sequence tag (EST) library from nine grass plants against three crop genomes (rice, maize, and sorghum) and identified 2,879 previously-unannotated exons (i.e., novel exons) in the three crops. We validated 81% of the tested exons by RT-PCR-sequencing, supporting the effectiveness of our in silico strategy. Evolutionary analysis reveals that the novel exons, comparing with their flanking annotated ones, are generally under weaker selection pressure at the protein level, but under stronger pressure at the RNA level, suggesting that most of the novel exons also represent novel alternatively spliced variants (ASVs). However, we also observed the consistency of evolutionary rates between certain novel exons and their flanking exons, which provided further evidence of their co-occurrence in the transcripts, suggesting that previously-annotated isoforms might be subject to erroneous predictions. Our validation showed that 54% of the tested genes expressed the newly-identified isoforms that contained the novel exons, rather than the previously-annotated isoforms that excluded them. The consistent results were steadily observed across cultivated (Oryza sativa and O. glaberrima) and wild (O. rufipogon and O. nivara) rice species, asserting the necessity of our curation of the crop genome annotations. Our comparative analyses also inferred the common ancestral transcriptome of grass plants and gain- and loss-of-ASV events.
Conclusions
We have reannotated the rice, maize, and sorghum genomes, and showed that evolutionary rates might serve as an indicator for determining whether the identified exons were alternatively spliced. This study not only presents an effective in silico strategy for the improvement of plant annotations, but also provides further insights into the role of AS events in the evolution and domestication of crop plants. ExonFinder and the novel exons/ASVs identified are publicly accessible at http://exonfinder.sourceforge.net/.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0431-7) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0431-7
PMCID: PMC4323234  PMID: 25652661
Crop plants; Alternative splicing; Plant transcriptome evolution; Evolutionary rate; Comparative genomics; Bioinformatics
10.  Non-targeted metabolite profiling of citrus juices as a tool for variety discrimination and metabolite flow analysis 
BMC Plant Biology  2015;15:38.
Background
Genetic diversity of citrus includes intrageneric hybrids, cultivars arising from cross-pollination and/or somatic mutations with particular biochemical compounds such as sugar, acids and secondary metabolite composition.
Results
Secondary metabolite profiles of juices from 12 commercial varieties grouped into blonde and navel types, mandarins, lemons and grapefruits were analyzed by LC/ESI-QTOF-MS. HCA on metabolite profiling data revealed the existence of natural groups demarcating fruit types and varieties associated to specific composition patterns. The unbiased classification provided by HCA was used for PLS-DA to find the potential variables (mass chromatographic features) responsible for the classification. Abscisic acid and derivatives, several flavonoids and limonoids were identified by analysis of mass spectra. To facilitate interpretation, metabolites were represented as flow charts depicting biosynthetic pathways. Mandarins ‘Fortune’ and ‘Hernandina’ along with oranges showed higher ABA contents and ABA degradation products were present as glycosylated forms in oranges and certain mandarins. All orange and grapefruit varieties showed high limonin contents and its glycosylated form, that was only absent in lemons. The rest of identified limonoids were highly abundant in oranges. Particularly, Sucrenya cultivar showed a specific accumulation of obacunone and limonoate A-ring lactone. Polymethoxylated flavanones (tangeritin and isomers) were absolutely absent from lemons and grapefruits whereas kaempferol deoxyhexose hexose isomer #2, naringin and neohesperidin were only present in these cultivars.
Conclusions
Analysis of relative metabolite build-up in closely-related genotypes allowed the efficient demarcation of cultivars and suggested the existence of genotype-specific regulatory mechanisms underlying the differential metabolite accumulation.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0430-8) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0430-8
PMCID: PMC4329192  PMID: 25652567
Fruit quality; Liquid chromatography; Mass spectrometry; Orange; Phenotyping; Secondary metabolites
11.  Complete plastome sequence of Thalictrum coreanum (Ranunculaceae) and transfer of the rpl32 gene to the nucleus in the ancestor of the subfamily Thalictroideae 
BMC Plant Biology  2015;15:40.
Background
Plastids originated from cyanobacteria and the majority of the ancestral genes were lost or functionally transferred to the nucleus after endosymbiosis. Comparative genomic investigations have shown that gene transfer from plastids to the nucleus is an ongoing evolutionary process but molecular evidence for recent functional gene transfers among seed plants have only been documented for the four genes accD, infA, rpl22, and rpl32.
Results
The complete plastid genome of Thalictrum coreanum, the first from the subfamily Thalictroideae (Ranunculaceae), was sequenced and revealed the losses of two genes, infA and rpl32. The functional transfer of these two genes to the nucleus in Thalictrum was verified by examination of nuclear transcriptomes. A survey of the phylogenetic distribution of the rpl32 loss was performed using 17 species of Thalictrum and representatives of related genera in the subfamily Thalictroideae. The plastid-encoded rpl32 gene is likely nonfunctional in members of the subfamily Thalictroideae (Aquilegia, Enemion, Isopyrum, Leptopyrum, Paraquilegia, and Semiaquilegia) including 17 Thalictrum species due to the presence of indels that disrupt the reading frame. A nuclear-encoded rpl32 with high sequence identity was identified in both Thalictrum and Aquilegia. The phylogenetic distribution of this gene loss/transfer and the high level of sequence similarity in transit peptides suggest a single transfer of the plastid-encoded rpl32 to the nucleus in the ancestor of the subfamily Thalictroideae approximately 20–32 Mya.
Conclusions
The genome sequence of Thalictrum coreanum provides valuable information for improving the understanding of the evolution of plastid genomes within Ranunculaceae and across angiosperms. Thalictrum is unusual among the three sequenced Ranunculaceae plastid genomes in the loss of two genes infA and rpl32, which have been functionally transferred to the nucleus. In the case of rpl32 this represents the third documented independent transfer from the plastid to the nucleus with the other two transfers occurring in the unrelated angiosperm families Rhizophoraceae and Salicaceae. Furthermore, the transfer of rpl32 provides additional molecular evidence for the monophyly of the subfamily Thalictroideae.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0432-6) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0432-6
PMCID: PMC4329224  PMID: 25652741
Gene loss; infA; Intracellular gene transfer; Meadow-rue; Plastid genome; rpl32
12.  Metabolic patterns associated with the seasonal rhythm of seed survival after dehydration in germinated seeds of Schismus arabicus 
BMC Plant Biology  2015;15:37.
Background
Seed of Shismus arabicus, a desert annual, display a seasonal tolerance to dehydration. The occurrence of a metabolic seasonal rhythm and its relation with the fluctuations in seed dehydration tolerance was investigated.
Results
Dry seeds metabolism was the least affected by the season, while the metabolism of germinated and dehydrated seeds exhibit distinct seasonal patterns. Negative associations exist between amino acids, sugars and TCA cycle intermediates and seed survival, while positive relations exist with seed germination. In contrast, associations between the level of secondary metabolites identified in the dehydrated seeds and survival percentage were evenly distributed in positive and negative values, suggesting a functional role of these metabolites in the establishment of seed dehydration tolerance.
Conclusion
Our results indicate the occurrence of metabolic biorhythms in germinating and dehydrating seeds associated with seasonal changes in germination and, more pronouncedly, in seed dehydration tolerance. Increased biosynthesis of protective compounds (polyphenols) in dehydrating seeds during the winter season at the expenses of central metabolites likely contributes to the respective enhanced dehydration tolerance monitored.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0421-9) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0421-9
PMCID: PMC4330942  PMID: 25652352
Seed germination; Seed survival; Dehydration; Metabolomics; Annual rhythm
13.  Potential functions of microRNAs in starch metabolism and development revealed by miRNA transcriptome profiling of cassava cultivars and their wild progenitor 
BMC Plant Biology  2015;15:33.
Background
MicroRNAs (miRNAs) are small (approximately 21 nucleotide) non-coding RNAs that are key post-transcriptional gene regulators in eukaryotic organisms. More than 100 cassava miRNAs have been identified in a conservation analysis and a repertoire of cassava miRNAs have also been characterised by next-generation sequencing (NGS) in recent studies. Here, using NGS, we profiled small non-coding RNAs and mRNA genes in two cassava cultivars and their wild progenitor to identify and characterise miRNAs that are potentially involved in plant growth and starch biosynthesis.
Results
Six small RNA and six mRNA libraries from leaves and roots of the two cultivars, KU50 and Arg7, and their wild progenitor, W14, were subjected to NGS. Analysis of the sequencing data revealed 29 conserved miRNA families and 33 new miRNA families. Together, these miRNAs potentially targeted a total of 360 putative target genes. Whereas 16 miRNA families were highly expressed in cultivar leaves, another 13 miRNA families were highly expressed in storage roots of cultivars. Co-expression analysis revealed that the expression level of some targets had negative relationship with their corresponding miRNAs in storage roots and leaves; these targets included MYB33, ARF10, GRF1, RD19, APL2, NF-YA3 and SPL2, which are known to be involved in plant development, starch biosynthesis and response to environmental stimuli.
Conclusion
The identified miRNAs, target mRNAs and target gene ontology annotation all shed light on the possible functions of miRNAs in Manihot species. The differential expression of miRNAs between cultivars and their wild progenitor, together with our analysis of GO annotation and confirmation of miRNA: target pairs, might provide insight into know the differences between wild progenitor and cultivated cassava.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-014-0355-7) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-014-0355-7
PMCID: PMC4331152  PMID: 25648603
MicroRNA; Target Gene; Wild Progenitor; Cassava (Manihot esculenta Crantz)
14.  Transcriptomic changes due to water deficit define a general soybean response and accession-specific pathways for drought avoidance 
BMC Plant Biology  2015;15:26.
Background
Among abiotic stresses, drought is the most common reducer of crop yields. The slow-wilting soybean genotype PI 416937 is somewhat robust to water deficit and has been used previously to map the trait in a bi-parental population. Since drought stress response is a complex biological process, whole genome transcriptome analysis was performed to obtain a deeper understanding of the drought response in soybean.
Results
Contrasting data from PI 416937 and the cultivar ‘Benning’, we developed a classification system to identify genes that were either responding to water-deficit in both genotypes or that had a genotype x environment (GxE) response. In spite of very different wilting phenotypes, 90% of classifiable genes had either constant expression in both genotypes (33%) or very similar response profiles (E genes, 57%). By further classifying E genes based on expression profiles, we were able to discern the functional specificity of transcriptional responses at particular stages of water-deficit, noting both the well-known reduction in photosynthesis genes as well as the less understood up-regulation of the protein transport pathway. Two percent of classifiable genes had a well-defined GxE response, many of which are located within slow-wilting QTLs. We consider these strong candidates for possible causal genes underlying PI 416937’s unique drought avoidance strategy.
Conclusions
There is a general and functionally significant transcriptional response to water deficit that involves not only known pathways, such as down-regulation of photosynthesis, but also up-regulation of protein transport and chromatin remodeling. Genes that show a genotypic difference are more likely to show an environmental response than genes that are constant between genotypes. In this study, at least five genes that clearly exhibited a genotype x environment response fell within known QTL and are very good candidates for further research into slow-wilting.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0422-8) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0422-8
PMCID: PMC4322458  PMID: 25644024
Drought stress; Canopy-wilting; Glycine max; RNA-Sequencing; Quantitative trait loci (QTL); Genotype x environment
15.  Genome-wide SNP identification and QTL mapping for black rot resistance in cabbage 
BMC Plant Biology  2015;15:32.
Background
Black rot is a destructive bacterial disease causing large yield and quality losses in Brassica oleracea. To detect quantitative trait loci (QTL) for black rot resistance, we performed whole-genome resequencing of two cabbage parental lines and genome-wide SNP identification using the recently published B. oleracea genome sequences as reference.
Results
Approximately 11.5 Gb of sequencing data was produced from each parental line. Reference genome-guided mapping and SNP calling revealed 674,521 SNPs between the two cabbage lines, with an average of one SNP per 662.5 bp. Among 167 dCAPS markers derived from candidate SNPs, 117 (70.1%) were validated as bona fide SNPs showing polymorphism between the parental lines. We then improved the resolution of a previous genetic map by adding 103 markers including 87 SNP-based dCAPS markers. The new map composed of 368 markers and covers 1467.3 cM with an average interval of 3.88 cM between adjacent markers. We evaluated black rot resistance in the mapping population in three independent inoculation tests using F2:3 progenies and identified one major QTL and three minor QTLs.
Conclusion
We report successful utilization of whole-genome resequencing for large-scale SNP identification and development of molecular markers for genetic map construction. In addition, we identified novel QTLs for black rot resistance. The high-density genetic map will promote QTL analysis for other important agricultural traits and marker-assisted breeding of B. oleracea.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0424-6) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0424-6
PMCID: PMC4323122  PMID: 25644124
Cabbage; Whole-genome resequencing; Genetic linkage map; Black rot; QTL
16.  Carotenoid accumulation affects redox status, starch metabolism, and flavonoid/anthocyanin accumulation in citrus 
BMC Plant Biology  2015;15:27.
Background
Carotenoids are indispensable plant secondary metabolites that are involved in photosynthesis, antioxidation, and phytohormone biosynthesis. Carotenoids are likely involved in other biological functions that have yet to be discovered. In this study, we integrated genomic, biochemical, and cellular studies to gain deep insight into carotenoid-related biological processes in citrus calli overexpressing CrtB (phytoene synthase from Pantoea agglomerans). Fortunella hindsii Swingle (a citrus relative) and Malus hupehensis (a wild apple) calli were also utilized as supporting systems to investigate the effect of altered carotenoid accumulation on carotenoid-related biological processes.
Results
Transcriptomic analysis provided deep insight into the carotenoid-related biological processes of redox status, starch metabolism, and flavonoid/anthocyanin accumulation. By applying biochemical and cytological analyses, we determined that the altered redox status was associated with variations in O2- and H2O2 levels. We also ascertained a decline in starch accumulation in carotenoid-rich calli. Furthermore, via an extensive cellular investigation of the newly constructed CrtB overexpressing Fortunella hindsii Swingle, we demonstrated that starch level reducation occurred in parallel with significant carotenoid accumulation. Moreover, studying anthocyanin-rich Malus hupehensis calli showed a negative effect of carotenoids on anthocyanin accumulation.
Conclusions
In citrus, altered carotenoid accumulation resulted in dramatic effects on metabolic processes involved in redox modification, starch degradation, and flavonoid/anthocyanin biosynthesis. These findings provided new perspectives to understand the biological importance of carotenogenesis and of the developmental processes associated with the nutritional and sensory qualities of agricultural products that accumulate carotenoids.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0426-4) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0426-4
PMCID: PMC4323224  PMID: 25644332
Carotenogenesis; Citrus; Redox status; Starch; Chromoplast; Anthocyanin
17.  Linkage mapping of Barley yellow dwarf virus resistance in connected populations of maize 
BMC Plant Biology  2015;15:29.
Background
With increasing winter temperatures, Barley yellow dwarf virus (BYDV) is expected to become an increasing problem in maize cultivation in Germany. Earlier studies revealed that BYDV has a negative impact on maize performance. Molecular markers would accelerate the development of BYDV resistant maize. Therefore, the objectives of this study were (i) the identification of quantitative trait loci (QTL) for BYDV resistance in five connected segregating maize populations in a field experiment and (ii) their comparison with the QTL detected under greenhouse conditions.
Results
In linkage analyses of the traits virus extinction, infection rate, and the symptom red edges, a highly associated major QTL was identified on chromosome 10. This QTL explained 45% of the phenotypic variance for the traits virus extinction and infection rate and 30% for the symptom red edges.
Conclusion
We could show that BYDV resistance traits are oligogenically inherited. The QTL on chromosome 10 could be observed in the connected linkage analyses and in the single population analyses. Furthermore, this QTL could also be confirmed in the greenhouse experiment. Our results let suggest that this QTL is involved in multiple virus resistance and the markers are promising for marker assisted selection.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0420-x) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0420-x
PMCID: PMC4329211  PMID: 25643896
QTL analysis; BYDV; Connected populations; Zea mays L.
18.  Construction of a high-density genetic map and QTLs mapping for sugars and acids in grape berries 
BMC Plant Biology  2015;15:28.
Background
QTLs controlling individual sugars and acids (fructose, glucose, malic acid and tartaric acid) in grape berries have not yet been identified. The present study aimed to construct a high-density, high-quality genetic map of a winemaking grape cross with a complex parentage (V. vinifera × V. amurensis) × ((V. labrusca × V. riparia) × V. vinifera), using next-generation restriction site-associated DNA sequencing, and then to identify loci related to phenotypic variability over three years.
Results
In total, 1 826 SNP-based markers were developed. Of these, 621 markers were assembled into 19 linkage groups (LGs) for the maternal map, 696 for the paternal map, and 1 254 for the integrated map. Markers showed good linear agreement on most chromosomes between our genetic maps and the previously published V. vinifera reference sequence. However marker order was different in some chromosome regions, indicating both conservation and variation within the genome. Despite the identification of a range of QTLs controlling the traits of interest, these QTLs explained a relatively small percentage of the observed phenotypic variance. Although they exhibited a large degree of instability from year to year, QTLs were identified for all traits but tartaric acid and titratable acidity in the three years of the study; however only the QTLs for malic acid and β ratio (tartaric acid-to-malic acid ratio) were stable in two years. QTLs related to sugars were located within ten LGs (01, 02, 03, 04, 07, 09, 11, 14, 17, 18), and those related to acids within three LGs (06, 13, 18). Overlapping QTLs in LG14 were observed for fructose, glucose and total sugar. Malic acid, total acid and β ratio each had several QTLs in LG18, and malic acid also had a QTL in LG06. A set of 10 genes underlying these QTLs may be involved in determining the malic acid content of berries.
Conclusion
The genetic map constructed in this study is potentially a high-density, high-quality map, which could be used for QTL detection, genome comparison, and sequence assembly. It may also serve to broaden our understanding of the grape genome.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0428-2) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0428-2
PMCID: PMC4329212  PMID: 25644551
Berry quality; Genetic map; Next-generation sequencing (NGS); QTL analysis; Quantitative trait loci; Restriction-site associated DNA (RAD); Vitis
19.  Transcriptome analysis of nitrogen-starvation-responsive genes in rice 
BMC Plant Biology  2015;15:31.
Background
Nitrogen (N), a critical macronutrient for plant growth and development, is a major limiting factor in most agricultural systems. Microarray analyses have been conducted to investigate genome-wide gene expression in response to changes in N concentrations. Although RNA-Seq analysis can provide a more precise determination of transcript levels, it has not previously been employed to investigate the expression of N-starvation-induced genes.
Results
We constructed cDNA libraries from leaf sheaths and roots of rice plants grown under N-deficient or -sufficient conditions for 12 h. Sequencing the libraries resulted in identification of 33,782 annotated genes. A comparison of abundances revealed 1,650 transcripts that were differentially expressed (fold-change ≥ 2) due to an N-deficiency. Among them, 1,158 were differentially expressed in the leaf sheaths (548 up-regulated and 610 down-regulated) and 492 in the roots (276 up, 216 down). Among the 36 deficiency-induced genes first identified via RNA-Seq analyses, 34 were subsequently confirmed by qRT-PCR. Our RNA-Seq data identified 8,509 multi-exonic genes with 19,628 alternative splicing events. However, we saw no significant difference in alternative splicing between N-sufficient and -deficient conditions. We found 2,986 novel transcripts, of which 192 were regulated under the N-deficiency.
Conclusion
We identified 1,650 genes that were differentially expressed after 12 h of N-starvation. Responses by those genes to a limited supply of N were confirmed by RT-PCR and GUS assays. Our results provide valuable information about N-starvation-responsive genes and will be useful when investigating the signal transduction pathway of N-utilization.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0425-5) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0425-5
PMCID: PMC4333837  PMID: 25644226
N-starvation; Oryza sativa; Transcription factors; Transcriptome sequencing
20.  Molecular evolution and diversification of the Argonaute family of proteins in plants 
BMC Plant Biology  2015;15:23.
Background
Argonaute (AGO) proteins form the core of the RNA-induced silencing complex, a central component of the smRNA machinery. Although reported from several plant species, little is known about their evolution. Moreover, these genes have not yet been cloned from the ecological model plant, Nicotiana attenuata, in which the smRNA machinery is known to mediate important ecological traits.
Results
Here, we not only identify 11 AGOs in N. attenuata, we further annotate 133 genes in 17 plant species, previously not annotated in the Phytozome database, to increase the number of plant AGOs to 263 genes from 37 plant species. We report the phylogenetic classification, expansion, and diversification of AGOs in the plant kingdom, which resulted in the following hypothesis about their evolutionary history: an ancestral AGO underwent duplication events after the divergence of unicellular green algae, giving rise to four major classes with subsequent gains/losses during the radiation of higher plants, resulting in the large number of extant AGOs. Class-specific signatures in the RNA-binding and catalytic domains, which may contribute to the functional diversity of plant AGOs, as well as context-dependent changes in sequence and domain architecture that may have consequences for gene function were found.
Conclusions
Together, the results demonstrate that the evolution of AGOs has been a dynamic process producing the signatures of functional diversification in the smRNA pathways of higher plants.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-014-0364-6) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-014-0364-6
PMCID: PMC4318128  PMID: 25626325
Argonaute; miRNA; Plants; Nicotiana attenuata; Herbivory; Evolution; Small-RNA
21.  Identification and comparative analysis of differentially expressed miRNAs in leaves of two wheat (Triticum aestivum L.) genotypes during dehydration stress 
BMC Plant Biology  2015;15:21.
Background
MicroRNAs (miRNAs) play critical roles in the processes of plant growth and development, but little is known of their functions during dehydration stress in wheat. Moreover, the mechanisms by which miRNAs confer different levels of dehydration stress tolerance in different wheat genotypes are unclear.
Results
We examined miRNA expressions in two different wheat genotypes, Hanxuan10, which is drought-tolerant, and Zhengyin1, which is drought-susceptible. Using a deep-sequencing method, we identified 367 differentially expressed miRNAs (including 46 conserved miRNAs and 321 novel miRNAs) and compared their expression levels in the two genotypes. Among them, 233 miRNAs were upregulated and 10 were downregulated in both wheat genotypes after dehydration stress. Interestingly, 13 miRNAs exhibited opposite patterns of expression in the two wheat genotypes, downregulation in the drought-tolerant cultivar and upregulation in the drought-susceptible cultivar. We also identified 111 miRNAs that were expressed predominantly in only one or the other genotype after dehydration stress. We verified the expression patterns of a number of representative miRNAs using qPCR analysis and northern blot, which produced results consistent with those of the deep-sequencing method. Moreover, monitoring the expression levels of 10 target genes by qPCR analysis revealed negative correlations with the levels of their corresponding miRNAs.
Conclusions
These results indicate that differentially expressed patterns of miRNAs between these two genotypes may play important roles in dehydration stress tolerance in wheat and may be a key factor in determining the levels of stress tolerance in different wheat genotypes.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0413-9) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0413-9
PMCID: PMC4312605  PMID: 25623724
Dehydration stress; Triticum aestivum L; Differentially expressed miRNAs; Comparative analysis
22.  Digital gene expression analysis of gene expression differences within Brassica diploids and allopolyploids 
BMC Plant Biology  2015;15:22.
Background
Brassica includes many successfully cultivated crop species of polyploid origin, either by ancestral genome triplication or by hybridization between two diploid progenitors, displaying complex repetitive sequences and transposons. The U’s triangle, which consists of three diploids and three amphidiploids, is optimal for the analysis of complicated genomes after polyploidization. Next-generation sequencing enables the transcriptome profiling of polyploids on a global scale.
Results
We examined the gene expression patterns of three diploids (Brassica rapa, B. nigra, and B. oleracea) and three amphidiploids (B. napus, B. juncea, and B. carinata) via digital gene expression analysis. In total, the libraries generated between 5.7 and 6.1 million raw reads, and the clean tags of each library were mapped to 18547–21995 genes of B. rapa genome. The unambiguous tag-mapped genes in the libraries were compared. Moreover, the majority of differentially expressed genes (DEGs) were explored among diploids as well as between diploids and amphidiploids. Gene ontological analysis was performed to functionally categorize these DEGs into different classes. The Kyoto Encyclopedia of Genes and Genomes analysis was performed to assign these DEGs into approximately 120 pathways, among which the metabolic pathway, biosynthesis of secondary metabolites, and peroxisomal pathway were enriched. The non-additive genes in Brassica amphidiploids were analyzed, and the results indicated that orthologous genes in polyploids are frequently expressed in a non-additive pattern. Methyltransferase genes showed differential expression pattern in Brassica species.
Conclusion
Our results provided an understanding of the transcriptome complexity of natural Brassica species. The gene expression changes in diploids and allopolyploids may help elucidate the morphological and physiological differences among Brassica species.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0417-5) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0417-5
PMCID: PMC4312607  PMID: 25623840
Brassica spp; Polyploidization; Sequencing; Digital gene expression (DGE)
23.  Redundancy and metabolic function of the glutamine synthetase gene family in poplar 
BMC Plant Biology  2015;15:20.
Background
Glutamine synthetase (GS; EC: 6.3.1.2, L-glutamate: ammonia ligase ADP-forming) is a key enzyme in ammonium assimilation and metabolism in higher plants. In poplar, the GS family is organized in 4 groups of duplicated genes, 3 of which code for cytosolic GS isoforms (GS1.1, GS1.2 and GS1.3) and one group that codes for the choroplastic GS isoform (GS2). Our previous work suggested that GS duplicates may have been retained to increase the amount of enzyme in a particular cell type.
Results
The current study was conducted to test this hypothesis by developing a more comprehensive understanding of the molecular and biochemical characteristics of the poplar GS isoenzymes and by determinating their kinetic parameters. To obtain further insights into the function of the poplar GS genes, in situ hybridization and laser capture microdissections were conducted in different tissues, and the precise GS gene spatial expression patterns were determined in specific cell/tissue types of the leaves, stems and roots. The molecular and functional analysis of the poplar GS family and the precise localization of the corresponding mRNA in different cell types strongly suggest that the GS isoforms play non-redundant roles in poplar tree biology. Furthermore, our results support the proposal that a function of the duplicated genes in specific cell/tissue types is to increase the abundance of the enzymes.
Conclusion
Taken together, our results reveal that there is no redundancy in the poplar GS family at the whole plant level but it exists in specific cell types where the two duplicated genes are expressed and their gene expression products have similar metabolic roles. Gene redundancy may contribute to the homeostasis of nitrogen metabolism in functions associated with changes in environmental conditions and developmental stages.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-014-0365-5) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-014-0365-5
PMCID: PMC4329200  PMID: 25608602
Populus; Gene family; Gene duplication; Glutamine; Ammonium assimilation
24.  Global analysis of gene expression profiles in physic nut (Jatropha curcas L.) seedlings exposed to drought stress 
BMC Plant Biology  2015;15:17.
Background
Physic nut (Jatropha curcas L.) is a small perennial tree or large shrub, which is well-adapted to semi-arid regions and is considered to have potential as a crop for biofuel production. It is now regarded as an excellent model for studying biofuel plants. However, our knowledge about the molecular responses of this species to drought stress is currently limited.
Results
In this study, genome-wide transcriptional profiles of roots and leaves of 8-week old physic nut seedlings were analyzed 1, 4 and 7 days after withholding irrigation. We observed a total of 1533 and 2900 differentially expressed genes (DEGs) in roots and leaves, respectively. Gene Ontology analysis showed that the biological processes enriched in droughted plants relative to unstressed plants were related to biosynthesis, transport, nucleobase-containing compounds, and cellular protein modification. The genes found to be up-regulated in roots were related to abscisic acid (ABA) synthesis and ABA signal transduction, and to the synthesis of raffinose. Genes related to ABA signal transduction, and to trehalose and raffinose synthesis, were up-regulated in leaves. Endoplasmic reticulum (ER) stress response genes were significantly up-regulated in leaves under drought stress, while a number of genes related to wax biosynthesis were also up-regulated in leaves. Genes related to unsaturated fatty acid biosynthesis were down-regulated and polyunsaturated fatty acids were significantly reduced in leaves 7 days after withholding irrigation. As drought stress increased, genes related to ethylene synthesis, ethylene signal transduction and chlorophyll degradation were up-regulated, and the chlorophyll content of leaves was significantly reduced by 7 days after withholding irrigation.
Conclusions
This study provides us with new insights to increase our understanding of the response mechanisms deployed by physic nut seedlings under drought stress. The genes and pathways identified in this study also provide much information of potential value for germplasm improvement and breeding for drought resistance.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-014-0397-x) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-014-0397-x
PMCID: PMC4307156  PMID: 25604012
Physic nut (Jatropha curcas L.); drought stress; gene expression profiles; abscisic acid; waxes and fatty acids; endoplasmic reticulum stress response; senescence
25.  Genome-wide transcriptomic and phylogenetic analyses reveal distinct aluminum-tolerance mechanisms in the aluminum-accumulating species buckwheat (Fagopyrum tataricum) 
BMC Plant Biology  2015;15:16.
Background
Similar to common buckwheat (Fagopyrum esculentum), tartary buckwheat (Fagopyrum tataricum) shows a high level of aluminum (Al) tolerance and accumulation. However, the molecular mechanisms for Al detoxification and accumulation are still poorly understood. To begin to elucidate the molecular basis of Al tolerance and accumulation, we used the Illumina high-throughput mRNA sequencing (RNA-seq) technology to conduct a genome-wide transcriptome analysis on both tip and basal segments of the roots exposed to Al.
Results
By using the Trinity method for the de novo assembly and cap3 software to reduce the redundancy and chimeras of the transcripts, we constructed 39,815 transcripts with an average length of 1184 bp, among which 20,605 transcripts were annotated by BLAST searches in the NCBI non-redundant protein database. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis showed that expression of genes involved in the defense of cell wall toxicity and oxidative stress was preferentially induced by Al stress. Our RNA-seq data also revealed that organic acid metabolism was unlikely to be a rate-limiting step for the Al-induced secretion of organic acids in buckwheat. We identified two citrate transporter genes that were highly induced by Al and potentially involved in the release of citrate into the xylem. In addition, three of four conserved Al-tolerance genes were found to be duplicated in tartary buckwheat and display diverse expression patterns.
Conclusions
Nearly 40,000 high quality transcript contigs were de novo assembled for tartary buckwheat, providing a reference platform for future research work in this plant species. Our differential expression and phylogenetic analysis revealed novel aspects of Al-tolerant mechanisms in buckwheat.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-014-0395-z) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-014-0395-z
PMCID: PMC4307214  PMID: 25603892
Aluminum tolerance; Al-tolerance genes; Buckwheat; Homolog; Organic acid; Transcriptome

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