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1.  Identification of conserved drought-adaptive genes using a cross-species meta-analysis approach 
BMC Plant Biology  2015;15:111.
Background
Drought is the major environmental stress threatening crop-plant productivity worldwide. Identification of new genes and metabolic pathways involved in plant adaptation to progressive drought stress at the reproductive stage is of great interest for agricultural research.
Results
We developed a novel Cross-Species meta-Analysis of progressive Drought stress at the reproductive stage (CSA:Drought) to identify key drought adaptive genes and mechanisms and to test their evolutionary conservation. Empirically defined filtering criteria were used to facilitate a robust integration of 17 deposited microarray experiments (148 arrays) of Arabidopsis, rice, wheat and barley. By prioritizing consistency over intensity, our approach was able to identify 225 differentially expressed genes shared across studies and taxa. Gene ontology enrichment and pathway analyses classified the shared genes into functional categories involved predominantly in metabolic processes (e.g. amino acid and carbohydrate metabolism), regulatory function (e.g. protein degradation and transcription) and response to stimulus. We further investigated drought related cis-acting elements in the shared gene promoters, and the evolutionary conservation of shared genes. The universal nature of the identified drought-adaptive genes was further validated in a fifth species, Brachypodium distachyon that was not included in the meta-analysis. qPCR analysis of 27, randomly selected, shared orthologs showed similar expression pattern as was found by the CSA:Drought.In accordance, morpho-physiological characterization of progressive drought stress, in B. distachyon, highlighted the key role of osmotic adjustment as evolutionary conserved drought-adaptive mechanism.
Conclusions
Our CSA:Drought strategy highlights major drought-adaptive genes and metabolic pathways that were only partially, if at all, reported in the original studies included in the meta-analysis. These genes include a group of unclassified genes that could be involved in novel drought adaptation mechanisms. The identified shared genes can provide a useful resource for subsequent research to better understand the mechanisms involved in drought adaptation across-species and can serve as a potential set of molecular biomarkers for progressive drought experiments.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0493-6) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0493-6
PMCID: PMC4417316  PMID: 25935420
Brachypodium distachyon; Cross-species meta-analysis; Drought stress; Evolutionary conservation; Microarray; Osmotic adjustment
2.  Repetitive sequence analysis and karyotyping reveals centromere-associated DNA sequences in radish (Raphanus sativus L.) 
BMC Plant Biology  2015;15:105.
Background
Radish (Raphanus sativus L., 2n = 2x = 18) is a major root vegetable crop especially in eastern Asia. Radish root contains various nutritions which play an important role in strengthening immunity. Repetitive elements are primary components of the genomic sequence and the most important factors in genome size variations in higher eukaryotes. To date, studies about repetitive elements of radish are still limited. To better understand genome structure of radish, we undertook a study to evaluate the proportion of repetitive elements and their distribution in radish.
Results
We conducted genome-wide characterization of repetitive elements in radish with low coverage genome sequencing followed by similarity-based cluster analysis. Results showed that about 31% of the genome was composed of repetitive sequences. Satellite repeats were the most dominating elements of the genome. The distribution pattern of three satellite repeat sequences (CL1, CL25, and CL43) on radish chromosomes was characterized using fluorescence in situ hybridization (FISH). CL1 was predominantly located at the centromeric region of all chromosomes, CL25 located at the subtelomeric region, and CL43 was a telomeric satellite. FISH signals of two satellite repeats, CL1 and CL25, together with 5S rDNA and 45S rDNA, provide useful cytogenetic markers to identify each individual somatic metaphase chromosome. The centromere-specific histone H3 (CENH3) has been used as a marker to identify centromere DNA sequences. One putative CENH3 (RsCENH3) was characterized and cloned from radish. Its deduced amino acid sequence shares high similarities to those of the CENH3s in Brassica species. An antibody against B. rapa CENH3, specifically stained radish centromeres. Immunostaining and chromatin immunoprecipitation (ChIP) tests with anti-BrCENH3 antibody demonstrated that both the centromere-specific retrotransposon (CR-Radish) and satellite repeat (CL1) are directly associated with RsCENH3 in radish.
Conclusions
Proportions of repetitive elements in radish were estimated and satellite repeats were the most dominating elements. Fine karyotyping analysis was established which allow us to easily identify each individual somatic metaphase chromosome. Immunofluorescence- and ChIP-based assays demonstrated the functional significance of satellite and centromere-specific retrotransposon at centromeres. Our study provides a valuable basis for future genomic studies in radish.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0480-y) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0480-y
PMCID: PMC4417506  PMID: 25928652
Radish; Repetitive DNA; Satellite; Karyotyping; CENH3; Centromere
7.  Genome wide comprehensive analysis and web resource development on cell wall degrading enzymes from phyto-parasitic nematodes 
BMC Plant Biology  2015;15:187.
Background
The plant cell wall serves as a primary barrier against pathogen invasion. The success of a plant pathogen largely depends on its ability to overcome this barrier. During the infection process, plant parasitic nematodes secrete cell wall degrading enzymes (CWDEs) apart from piercing with their stylet, a sharp and hard mouthpart used for successful infection. CWDEs typically consist of cellulases, hemicellulases, and pectinases, which help the nematode to infect and establish the feeding structure or form a cyst. The study of nematode cell wall degrading enzymes not only enhance our understanding of the interaction between nematodes and their host, but also provides information on a novel source of enzymes for their potential use in biomass based biofuel/bioproduct industries. Although there is comprehensive information available on genome wide analysis of CWDEs for bacteria, fungi, termites and plants, but no comprehensive information available for plant pathogenic nematodes. Herein we have performed a genome wide analysis of CWDEs from the genome sequenced phyto pathogenic nematode species and developed a comprehensive publicly available database.
Results
In the present study, we have performed a genome wide analysis for the presence of CWDEs from five plant parasitic nematode species with fully sequenced genomes covering three genera viz. Bursaphelenchus, Glorodera and Meloidogyne. Using the Hidden Markov Models (HMM) conserved domain profiles of the respective gene families, we have identified 530 genes encoding CWDEs that are distributed among 24 gene families of glycoside hydrolases (412) and polysaccharide lyases (118). Furthermore, expression profiles of these genes were analyzed across the life cycle of a potato cyst nematode. Most genes were found to have moderate to high expression from early to late infectious stages, while some clusters were invasion stage specific, indicating the role of these enzymes in the nematode’s infection and establishment process. Additionally, we have also developed a Nematode’s Plant Cell Wall Degrading Enzyme (NCWDE) database as a platform to provide a comprehensive outcome of the present study.
Conclusions
Our study provides collective information about different families of CWDEs from five different sequenced plant pathogenic nematode species. The outcomes of this study will help in developing better strategies to curtail the nematode infection, as well as help in identification of novel cell wall degrading enzymes for biofuel/bioproduct industries.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0576-4) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0576-4
PMCID: PMC4521475  PMID: 26232118
Cell wall; Cell wall degrading enzymes; Cellulose; CWDEs; Database; Nematodes; Plant parasitic; Pectinases
8.  Sucrose accumulation in sweet sorghum stems occurs by apoplasmic phloem unloading and does not involve differential Sucrose transporter expression 
BMC Plant Biology  2015;15:186.
Background
Sorghum (Sorghum bicolor L. Moench) cultivars store non-structural carbohydrates predominantly as either starch in seeds (grain sorghums) or sugars in stems (sweet sorghums). Previous research determined that sucrose accumulation in sweet sorghum stems was not correlated with the activities of enzymes functioning in sucrose metabolism, and that an apoplasmic transport step may be involved in stem sucrose accumulation. However, the sucrose unloading pathway from stem phloem to storage parenchyma cells remains unelucidated. Sucrose transporters (SUTs) transport sucrose across membranes, and have been proposed to function in sucrose partitioning differences between sweet and grain sorghums. The purpose of this study was to characterize the key differences in carbohydrate accumulation between a sweet and a grain sorghum, to define the path sucrose may follow for accumulation in sorghum stems, and to determine the roles played by sorghum SUTs in stem sucrose accumulation.
Results
Dye tracer studies to determine the sucrose transport route revealed that, for both the sweet sorghum cultivar Wray and grain sorghum cultivar Macia, the phloem in the stem veins was symplasmically isolated from surrounding cells, suggesting sucrose was apoplasmically unloaded. Once in the phloem apoplasm, a soluble tracer diffused from the vein to stem parenchyma cell walls, indicating the lignified mestome sheath encompassing the vein did not prevent apoplasmic flux outside of the vein. To characterize carbohydrate partitioning differences between Wray and Macia, we compared the growth, stem juice volume, solute contents, SbSUTs gene expression, and additional traits. Contrary to previous findings, we detected no significant differences in SbSUTs gene expression within stem tissues.
Conclusions
Phloem sieve tubes within sweet and grain sorghum stems are symplasmically isolated from surrounding cells; hence, unloading from the phloem likely occurs apoplasmically, thereby defining the location of the previously postulated step for sucrose transport. Additionally, no changes in SbSUTs gene expression were detected in sweet vs. grain sorghum stems, suggesting alterations in SbSUT transcript levels do not account for the carbohydrate partitioning differences between cultivars. A model illustrating sucrose phloem unloading and movement to stem storage parenchyma, and highlighting roles for sucrose transport proteins in sorghum stems is discussed.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0572-8) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0572-8
PMCID: PMC4518677  PMID: 26223524
Apoplasm; Carbohydrate partitioning; Carboxyfluorescein; Parenchyma; Phloem; Sorghum; Stem; Sucrose; SUT; Symplasm
9.  The Phytoene synthase gene family of apple (Malus x domestica) and its role in controlling fruit carotenoid content 
BMC Plant Biology  2015;15:185.
Background
Carotenoid compounds play essential roles in plants such as protecting the photosynthetic apparatus and in hormone signalling. Coloured carotenoids provide yellow, orange and red colour to plant tissues, as well as offering nutritional benefit to humans and animals. The enzyme phytoene synthase (PSY) catalyses the first committed step of the carotenoid biosynthetic pathway and has been associated with control of pathway flux. We characterised four PSY genes found in the apple genome to further understand their involvement in fruit carotenoid accumulation.
Results
The apple PSY gene family, containing six members, was predicted to have three functional members, PSY1, PSY2, and PSY4, based on translation of the predicted gene sequences and/or corresponding cDNAs. However, only PSY1 and PSY2 showed activity in a complementation assay. Protein localisation experiments revealed differential localization of the PSY proteins in chloroplasts; PSY1 and PSY2 localized to the thylakoid membranes, while PSY4 localized to plastoglobuli. Transcript levels in ‘Granny Smith’ and ‘Royal Gala’ apple cultivars showed PSY2 was most highly expressed in fruit and other vegetative tissues. We tested the transient activation of the apple PSY1 and PSY2 promoters and identified potential and differential regulation by AP2/ERF transcription factors, which suggested that the PSY genes are controlled by different transcriptional mechanisms.
Conclusion
The first committed carotenoid pathway step in apple is controlled by MdPSY1 and MdPSY2, while MdPSY4 play little or no role in this respect. This has implications for apple breeding programmes where carotenoid enhancement is a target and would allow co-segregation with phenotypes to be tested during the development of new cultivars.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0573-7) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0573-7
PMCID: PMC4517366  PMID: 26215656
Apple; Carotenoids; Fruit skin; Fruit flesh; Phytoene; Phytoene synthase; Promoter; Transient activation
10.  Comprehensive meta-analysis, co-expression, and miRNA nested network analysis identifies gene candidates in citrus against Huanglongbing disease 
BMC Plant Biology  2015;15:184.
Background
Huanglongbing (HLB), the most devastating disease of citrus, is associated with infection by Candidatus Liberibacter asiaticus (CaLas) and is vectored by the Asian citrus psyllid (ACP). Recently, the molecular basis of citrus–HLB interactions has been examined using transcriptome analyses, and these analyses have identified many probe sets and pathways modulated by CaLas infection among different citrus cultivars. However, lack of consistency among reported findings indicates that an integrative approach is needed. This study was designed to identify the candidate probe sets in citrus–HLB interactions using meta-analysis and gene co-expression network modelling.
Results
Twenty-two publically available transcriptome studies on citrus–HLB interactions, comprising 18 susceptible (S) datasets and four resistant (R) datasets, were investigated using Limma and RankProd methods of meta-analysis. A combined list of 7,412 differentially expressed probe sets was generated using a Teradata in-house Structured Query Language (SQL) script. We identified the 65 most common probe sets modulated in HLB disease among different tissues from the S and R datasets. Gene ontology analysis of these probe sets suggested that carbohydrate metabolism, nutrient transport, and biotic stress were the core pathways that were modulated in citrus by CaLas infection and HLB development. We also identified R-specific probe sets, which encoded leucine-rich repeat proteins, chitinase, constitutive disease resistance (CDR), miraculins, and lectins. Weighted gene co-expression network analysis (WGCNA) was conducted on 3,499 probe sets, and 21 modules with major hub probe sets were identified. Further, a miRNA nested network was created to examine gene regulation of the 3,499 target probe sets. Results suggest that csi-miR167 and csi-miR396 could affect ion transporters and defence response pathways, respectively.
Conclusion
Most of the potential candidate hub probe sets were co-expressed with gibberellin pathway (GA)-related probe sets, implying the role of GA signalling in HLB resistance. Our findings contribute to the integration of existing citrus–HLB transcriptome data that will help to elucidate the holistic picture of the citrus–HLB interaction. The citrus probe sets identified in this analysis signify a robust set of HLB-responsive candidates that are useful for further validation.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0568-4) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0568-4
PMCID: PMC4517500  PMID: 26215595
Citrus; Gene co-expression analysis; Gene ontology; Huanglongbing; HLB resistance; Meta-analysis; miRNA network analysis; Common and R-specific probe sets
11.  Development of transgenic wheat (Triticum aestivum L.) expressing avidin gene conferring resistance to stored product insects 
BMC Plant Biology  2015;15:183.
Background
Wheat is considered the most important cereal crop all over the world. The wheat weevil Sitophilus granarius is a serious insect pests in much of the wheat growing area worldwide and is responsible for significant loss of yield. Avidin proteins has been proposed to function as plant defense agents against insect pests.
Results
A synthetic avidin gene was introduced into spring wheat (Triticum aestivum L.) cv. Giza 168 using a biolistic bombardment protocol. The presence and expression of the transgene in six selected T0 transgenic wheat lines were confirmed at the molecular level. Accumulation of avidin protein was detected in transgenic plants compared to non-transgenic plants. Avidin transgene was stably integrated, transcribed and translated as indicated by Southern blot, ELISA, and dot blot analyses, with a high level of expression in transgenic wheat seeds. However, no expression was detected in untransformed wheat seeds. Functional integrity of avidin was confirmed by insect bioassay. The results of bioassay using transgenic wheat plants challenged with wheat weevil revealed 100 % mortality of the insects reared on transgenic plants after 21 days.
Conclusion
Transgenic wheat plants had improved resistance to Sitophilus granarius.
doi:10.1186/s12870-015-0570-x
PMCID: PMC4508906  PMID: 26194497
Stored cereals insects; post harvest loss; avidin; transgenic wheat
12.  Isolation and characterization of the C-class MADS-box gene involved in the formation of double flowers in Japanese gentian 
BMC Plant Biology  2015;15:182.
Background
Generally, double-flowered varieties are more attractive than single-flowered varieties in ornamental plants. Japanese gentian is one of the most popular floricultural plants in Japan, and it is desirable to breed elite double-flowered cultivars. In this study, we attempted to characterize a doubled-flower mutant of Japanese gentian. To identify the gene that causes the double-flowered phenotype in Japanese gentian, we isolated and characterized MADS-box genes.
Results
Fourteen MADS-box genes were isolated, and two of them were C-class MADS-box genes (GsAG1 and GsAG2). Both GsAG1 and GsAG2 were categorized into the PLE/SHP subgroup, rather than the AG/FAR subgroup. In expression analyses, GsAG1 transcripts were detected in the second to fourth floral whorls, while GsAG2 transcripts were detected in only the inner two whorls. Transgenic Arabidopsis expressing GsAG1 lacked petals and formed carpeloid organs instead of sepals. Compared with a single-flowered gentian cultivar, a double-flowered gentian mutant showed decreased expression of GsAG1 but unchanged expression of GsAG2. An analysis of the genomic structure of GsAG1 revealed that the gene had nine exons and eight introns, and that a 5,150-bp additional sequence was inserted into the sixth intron of GsAG1 in the double-flowered mutant. This insert had typical features of a Ty3/gypsy-type LTR-retrotransposon, and was designated as Tgs1. Virus-induced gene silencing of GsAG1 by the Apple latent spherical virus vector resulted in the conversion of the stamen to petaloid organs in early flowering transgenic gentian plants expressing an Arabidopsis FT gene.
Conclusions
These results revealed that GsAG1 plays a key role as a C-functional gene in stamen organ identity. The identification of the gene responsible for the double-flowered phenotype will be useful in further research on the floral morphogenesis of Japanese gentian.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0569-3) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0569-3
PMCID: PMC4504037  PMID: 26183329
AGAMOUS; Apple latent spherical virus vector; Double-flowers; Japanese gentian; LTR-type retrotransposon; MADS-box genes
13.  Temporal patterns of gene expression associated with tuberous root formation and development in sweetpotato (Ipomoea batatas) 
BMC Plant Biology  2015;15:180.
Background
The tuberous root of sweetpotato is undisputedly an important organ from agronomic and biological perspectives. Little is known regarding the regulatory networks programming tuberous root formation and development.
Results
Here, as a first step toward understanding these networks, we analyzed and characterized the genome-wide transcriptional profiling and dynamics of sweetpotato root in seven distinct developmental stages using a customized microarray containing 39,724 genes. Analysis of these genes identified temporal programs of gene expression, including hundreds of transcription factor (TF) genes. We found that most genes active in roots were shared across all developmental stages, although significant quantitative changes in gene abundance were observed for 5,368 (including 435 TFs) genes. Clustering analysis of these differentially expressed genes pointed out six distinct expression patterns during root development. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis revealed that genes involved in different processes were enriched at specific stages of root development. In contrast with the large number of shared expressed genes in root development, each stage or period of root development has only a small number of specific genes. In total, 712 (including 27 TFs) and 1,840 (including 115 TFs) genes were identified as root-stage and root-period specific, respectively at the level of microarray. Several of the specific TF genes are known regulators of root development, including DA1-related protein, SHORT-ROOT and BEL1-like. The remaining TFs with unknown roles would also play critical regulatory roles during sweetpotato tuberous root formation and development.
Conclusions
The results generated in this study provided spatiotemporal patterns of root gene expression in support of future efforts for understanding the underlying molecular mechanism that control sweetpotato yield and quality.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0567-5) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0567-5
PMCID: PMC4502468  PMID: 26174091
Sweetpotato; Tuberous root; Transcriptome; Expression patterns
14.  MicroRNAs and targets in senescent litchi fruit during ambient storage and post-cold storage shelf life 
BMC Plant Biology  2015;15:181.
Background
Litchi has a high commercial value due to its bright color and rich nutrients. However, it deteriorates with the pericarp turning brown within 1–2 days after harvest. The factors that mediate litchi fruit senescence are complicated. MicroRNAs act as negative regulators involved in almost every physiological process. To understand the mechanism of litchi fruit senescence and pericarp browning at the miRNA level, five small RNA libraries and a degradome library prepared from the pericarp of litchi fruit subjected to ambient storage and post-cold storage shelf life were sequenced.
Results
By aligning the sRNA reads onto the litchi unigene assembly, 296 miRNAs belonging to 49 known miRNA families were first identified from litchi. In addition, 11 litchi-specific miRNAs were identified. Among these, 167 known miRNAs were identified to cleave 197 targets, and three litchi-specific miRNAs were found to have five targets. Through combined analysis of stem-loop quantitative real-time polymerase chain reaction (qRT-PCR) and transcriptome profiling, 14 miRNA-target pairs were found to be actively involved in litchi fruit senescence-related processes, including energy regulation, anthocyanin metabolism, hormone signaling, and pathogen-infection defense.
Conclusions
A network of miRNA-targets that regulate litchi fruit senescence has been proposed, revealing the miRNA-mediated regulation in senescent litchi fruit. This will aid in developing new strategies to postpone the senescence of litchi fruit and other horticultural products.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0509-2) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0509-2
PMCID: PMC4504174  PMID: 26179282
Litchi chinensis; MicroRNAs; Targets; Senescence; Storage
15.  Phylogeny and differentiation of the St genome in Elymus L. sensu lato (Triticeae; Poaceae) based on one nuclear DNA and two chloroplast genes 
BMC Plant Biology  2015;15:179.
Background
Hybridization and polyploidization can be major mechanisms for plant evolution and speciation. Thus, the process of polyploidization and evolutionary history of polyploids is of widespread interest. The species in Elymus L. sensu lato are allopolyploids that share a common St genome from Pseudoroegneria in different combinations with H, Y, P, and W genomes. But how the St genome evolved in the Elymus s. l. during the hybridization and polyploidization events remains unclear. We used nuclear and chloroplast DNA-based phylogenetic analyses to shed some light on this process.
Results
The Maximum likelihood (ML) tree based on nuclear ribosomal internal transcribed spacer region (nrITS) data showed that the Pseudoroegneria, Hordeum and Agropyron species served as the St, H and P genome diploid ancestors, respectively, for the Elymus s. l. polyploids. The ML tree for the chloroplast genes (matK and the intergenic region of trnH-psbA) suggests that the Pseudoroegneria served as the maternal donor of the St genome for Elymus s. l. Furthermore, it suggested that Pseudoroegneria species from Central Asia and Europe were more ancient than those from North America. The molecular evolution in the St genome appeared to be non-random following the polyploidy event with a departure from the equilibrium neutral model due to a genetic bottleneck caused by recent polyploidization.
Conclusion
Our results suggest the ancient common maternal ancestral genome in Elymus s. l. is the St genome from Pseudoroegneria. The evolutionary differentiation of the St genome in Elymus s. l. after rise of this group may have multiple causes, including hybridization and polyploidization. They also suggest that E. tangutorum should be treated as C. dahurica var. tangutorum, and E. breviaristatus should be transferred into Campeiostachys. We hypothesized that the Elymus s. l. species origined in Central Asia and Europe, then spread to North America. Further study of intraspecific variation may help us evaluate our phylogenetic results in greater detail and with more certainty.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0517-2) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0517-2
PMCID: PMC4499217  PMID: 26164196
Elymus s. l.; St genome; nr DNA; Chloroplast gene; Phylogeny; Molecular evolution
16.  Towards a comprehensive phylogeny of the large temperate genus Pedicularis (Orobanchaceae), with an emphasis on species from the Himalaya-Hengduan Mountains 
BMC Plant Biology  2015;15:176.
Background
Striking interspecific variations in floral traits of the large temperate genus Pedicularis have given rise to controversies concerning infra-generic classifications. To date, phylogenetic relationships within the genus have not been well resolved. The main goal of this study is to construct a backbone phylogeny of Pedicularis, with extensive sampling of species from the Himalaya-Hengduan Mountains. Phylogenetic analyses included 257 species, representing all 13 informal groups and 104 out of 130 series in the classification system of Tsoong, using sequences of the nuclear ribosomal internal transcribed spacer (nrITS) and three plastid regions (matK, rbcL and trnL-F). Bayesian inference and maximum likelihood methods were applied in separate and combined analyses of these datasets.
Results
Thirteen major clades are resolved with strong support, although the backbone of the tree is poorly resolved. There is little consensus between the phylogenetic tree and Tsoong’s classification of Pedicularis. Only two of the 13 groups (15.4 %), and 19 of the 56 series (33.9 %) with more than one sampled species were found to be strictly monophyletic. Most opposite-/whorled-leaved species fall into a single clade, i.e. clade 1, while alternate leaves species occur in the remaining 12 clades. Excluding the widespread P. verticillata in clade 1, species from Europe and North America fall into clades 6–8.
Conclusions
Our results suggest that combinations of morphological and geographic characters associated with strongly supported clades are needed to elucidate a comprehensive global phylogeny of Pedicularis. Alternate leaves are inferred to be plesiomorphic in Pedicularis, with multiple transitions to opposite/whorled phyllotaxy. Alternate-leaved species show high diversity in plant habit and floral forms. In the Himalaya-Hengduan Mountains, geographical barriers may have facilitated diversification of species with long corolla tubes, and the reproductive advantages of beakless galeas in opposite-/whorled-leaved species may boost speciation at high altitude.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0547-9) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0547-9
PMCID: PMC4498522  PMID: 26159907
Adaptive radiation; Floral diversity; Phyllotaxy; Himalaya-Hengduan Mountains; Orobanchaceae; Pedicularis; Phylogenetic analysis
17.  Resolving deep relationships of PACMAD grasses: a phylogenomic approach 
BMC Plant Biology  2015;15:178.
Background
Plastome sequences for 18 species of the PACMAD grasses (subfamilies Panicoideae, Aristidoideae, Chloridoideae, Micrairoideae, Arundinoideae, Danthonioideae) were analyzed phylogenomically. Next generation sequencing methods were used to provide complete plastome sequences for 12 species. Sanger sequencing was performed to determine the plastome of one species, Hakonechloa macra, to provide a reference for annotation. These analyses were conducted to resolve deep subfamilial relationships within the clade. Divergence estimates were assessed to determine potential factors that led to the rapid radiation of this lineage and its dominance of warmer open habitats.
Results
New plastomes were completely sequenced and characterized for 13 PACMAD species. An autapomorphic ~1140 bp deletion was found in Hakonechloa macra putatively pseudogenizing rpl14 and eliminating rpl16 from this plastome. Phylogenomic analyses support Panicoideae as the sister group to the ACMAD clade. Complete plastome sequences provide greater support at deep nodes within the PACMAD clade. The initial diversification of PACMAD subfamilies was estimated to occur at 32.4 mya.
Conclusions
Phylogenomic analyses of complete plastomes provides resolution for deep relationships of PACMAD grasses. The divergence estimate of 32.4 mya at the crown node of the PACMAD clade coincides with the Eocene-Oligocene Transition (EOT). The Eocene was a period of global cooling and drying, which led to forest fragmentation and the expansion of open habitats now dominated by these grasses. Understanding how these grasses are related and determining a cause for their rapid radiation allows for future predictions of grassland distribution in the face of a changing global climate.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0563-9) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0563-9
PMCID: PMC4498559  PMID: 26160195
Complete plastome; Divergence estimates; PACMAD Clade; Panicoideae; Phylogenomics; Rapid radiation
18.  Proteomic analysis of Artemisia annua – towards elucidating the biosynthetic pathways of the antimalarial pro-drug artemisinin 
BMC Plant Biology  2015;15:175.
Background
MS-based proteomics was applied to the analysis of the medicinal plant Artemisia annua, exploiting a recently published contig sequence database (Graham et al. (2010) Science 327, 328–331) and other genomic and proteomic sequence databases for comparison. A. annua is the predominant natural source of artemisinin, the precursor for artemisinin-based combination therapies (ACTs), which are the WHO-recommended treatment for P. falciparum malaria.
Results
The comparison of various databases containing A. annua sequences (NCBInr/viridiplantae, UniProt/viridiplantae, UniProt/A. annua, an A. annua trichome Trinity contig database, the above contig database and another A. annua EST database) revealed significant differences in respect of their suitability for proteomic analysis, showing that an organism-specific database that has undergone extensive curation, leading to longer contig sequences, can greatly increase the number of true positive protein identifications, while reducing the number of false positives. Compared to previously published data an order-of-magnitude more proteins have been identified from trichome-enriched A. annua samples, including proteins which are known to be involved in the biosynthesis of artemisinin, as well as other highly abundant proteins, which suggest additional enzymatic processes occurring within the trichomes that are important for the biosynthesis of artemisinin.
Conclusions
The newly gained information allows for the possibility of an enzymatic pathway, utilizing peroxidases, for the less well understood final stages of artemisinin’s biosynthesis, as an alternative to the known non-enzymatic in vitro conversion of dihydroartemisinic acid to artemisinin. Data are available via ProteomeXchange with identifier PXD000703.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0565-7) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0565-7
PMCID: PMC4496932  PMID: 26156581
Artemisia annua; Artemisinin; Malaria; Mass spectrometry; Plant proteomics; Proteogenomics; Trichomes
19.  Microspore culture reveals complex meiotic behaviour in a trigenomic Brassica hybrid 
BMC Plant Biology  2015;15:173.
Background
Development of synthetic allohexaploid Brassica (2n = AABBCC) would be beneficial for agriculture, as allelic contributions from three genomes could increase hybrid vigour and broaden adaptation. Microspore culture of a near-allohexaploid hybrid derived from the cross (B. napus × B. carinata) × B. juncea was undertaken in order to assess the frequency and distribution of homologous and homoeologous crossovers in this trigenomic hybrid. SNP and SSR molecular markers were used to detect inheritance of A, B and C genome alleles in microspore-derived (MD) progeny. SNP allele copy number was also assessed. The MD progeny were also compared to progeny derived by self-pollination and open-pollination for fertility (estimated by self-pollinated seed set and pollen viability) and DNA ploidy (measured by flow cytometry).
Results
In the trigenomic hybrid, homologous chromosome pairs Aj-An, Bj-Bc and Cn-Cc had similar meiotic crossover frequencies and segregation to that previously observed in established Brassica species, as demonstrated by marker haplotype analysis of the MD population. Homoeologous pairing between chromosomes A1-C1, A2-C2 and A7-C6 was detected at frequencies of 12–18 %, with other homoeologous chromosome regions associating from 8 % (A3-C3) to 0–1 % (A8-C8, A8-C9) of the time. Copy number analysis revealed eight instances of additional chromosomes and 20 instances of chromosomes present in one copy in somatically doubled MD progeny. Presence of chromosome A6 was positively correlated with self-pollinated seed set and pollen viability in the MD population. Many MD progeny were unable to produce self-pollinated seed (76 %) or viable pollen (53 %), although one MD plant produced 198 self-pollinated seeds. Average fertility was significantly lower in progeny obtained by microspore culture than progeny obtained by self-pollination or open-pollination, after excluding MD progeny which had not undergone chromosome doubling.
Conclusions
Based on SNP data analysis of the microspore-derived progeny, crossover frequency per chromosome in the allohexaploid hybrid was found to be similar to that in established Brassica species, suggesting that the higher chromosome number did not significantly disrupt cellular regulation of meiosis. SNP allele copy number analysis revealed the occurrence not only of homoeologous duplication/deletion events but also other cryptic duplications and deletions that may have been the result of mitotic instability. Microspore culture simplified the assessment of chromosome behaviour in the allohexaploid hybrid but yielded progeny with lower fertility and a greater range of ploidy levels compared to progeny obtained by self- or open-pollination.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0555-9) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0555-9
PMCID: PMC4493989  PMID: 26152188
Allohexaploid; Brassica; SNP chip; Chromosome behaviour; Allele copy number analysis; Interspecific hybrids
20.  The striking and unexpected cytogenetic diversity of genus Tanacetum L. (Asteraceae): a cytometric and fluorescent in situ hybridisation study of Iranian taxa 
BMC Plant Biology  2015;15:174.
Background
Although karyologically well studied, the genus Tanacetum (Asteraceae) is poorly known from the perspective of molecular cytogenetics. The prevalence of polyploidy, including odd ploidy warranted an extensive cytogenetic study. We studied several species native to Iran, one of the most important centres of diversity of the genus. We aimed to characterise Tanacetum genomes through fluorochrome banding, fluorescent in situ hybridisation (FISH) of rRNA genes and the assessment of genome size by flow cytometry. We appraise the effect of polyploidy and evaluate the existence of intraspecific variation based on the number and distribution of GC-rich bands and rDNA loci. Finally, we infer ancestral genome size and other cytogenetic traits considering phylogenetic relationships within the genus.
Results
We report first genome size (2C) estimates ranging from 3.84 to 24.87 pg representing about 11 % of those recognised for the genus. We found striking cytogenetic diversity both in the number of GC-rich bands and rDNA loci. There is variation even at the population level and some species have undergone massive heterochromatic or rDNA amplification. Certain morphometric data, such as pollen size or inflorescence architecture, bear some relationship with genome size. Reconstruction of ancestral genome size, number of CMA+ bands and number of rDNA loci show that ups and downs have occurred during the evolution of these traits, although genome size has mostly increased and the number of CMA+ bands and rDNA loci have decreased in present-day taxa compared with ancestral values.
Conclusions
Tanacetum genomes are highly unstable in the number of GC-rich bands and rDNA loci, although some patterns can be established at the diploid and tetraploid levels. In particular, aneuploid taxa and some odd ploidy species show greater cytogenetic instability than the rest of the genus. We have also confirmed a linked rDNA arrangement for all the studied Tanacetum species. The labile scenario found in Tanacetum proves that some cytogenetic features previously regarded as relatively constant, or even diagnostic, can display high variability, which is better interpreted within a phylogenetic context.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0564-8) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0564-8
PMCID: PMC4494159  PMID: 26152193
5S; 35S; Aneuploidy; Evolutionary cytogenetics; Genomic instability; L-type arrangement; Polyploidy; Odd ploidy; Ribosomal DNA
21.  Comparative metabolic responses and adaptive strategies of wheat (Triticum aestivum) to salt and alkali stress 
BMC Plant Biology  2015;15:170.
Background
It is well known that salinization (high-pH) has been considered as a major environmental threat to agricultural systems. The aim of this study was to investigate the differences between salt stress and alkali stress in metabolic profiles and nutrient accumulation of wheat; these parameters were also evaluated to determine the physiological adaptive mechanisms by which wheat tolerates alkali stress.
Results
The harmful effect of alkali stress on the growth and photosynthesis of wheat were stronger than those of salt stress. High-pH of alkali stress induced the most of phosphate and metal ions to precipitate; as a result, the availability of nutrients significantly declined. Under alkali stress, Ca sharply increased in roots, however, it decreased under salt stress. In addition, we detected the 75 metabolites that were different among the treatments according to GC-MS analysis, including organic acids, amino acids, sugars/polyols and others. The metabolic data showed salt stress and alkali stress caused different metabolic shifts; alkali stress has a stronger injurious effect on the distribution and accumulation of metabolites than salt stress. These outcomes correspond to specific detrimental effects of a highly pH environment.
Conclusions
Ca had a significant positive correlation with alkali tolerates, and increasing Ca concentration can immediately trigger SOS Na exclusion system and reduce the Na injury. Salt stress caused metabolic shifts toward gluconeogenesis with increased sugars to avoid osmotic stress; energy in roots and active synthesis in leaves were needed by wheat to develop salt tolerance. Alkali stress (at high pH) significantly inhibited photosynthetic rate; thus, sugar production was reduced, N metabolism was limited, amino acid production was reduced, and glycolysis was inhibited.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0546-x) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0546-x
PMCID: PMC4492011  PMID: 26149720
Wheat; Salt stress; Alkali stress; Growth; Photosynthesis; Metal elements; Free ions; Metabolites
22.  Ectopic shoot meristem generation in monocotyledonous rpk1 mutants is linked to SAM loss and altered seedling morphology 
BMC Plant Biology  2015;15:171.
Background
In dicot Arabidopsis thaliana embryos two cotyledons develop largely autonomously from the shoot apical meristem (SAM). Recessive mutations in the Arabidopsis receptor-like kinase RPK1 lead to monocotyledonous seedlings, with low (10 %) penetrance due to complex functional redundancy. In strong rpk1 alleles, about 10 % of these (i. e. 1 % of all homozygotes) did not develop a SAM. We wondered whether RPK1 might also control SAM gene expression and SAM generation in addition to its known stochastic impact on cell division and PINFORMED1 (PIN1) polarity in the epidermis.
Results
SAM-less seedlings developed a simple morphology with a straight and continuous hypocotyl-cotyledon structure lacking a recognizable epicotyl. According to rpk1’s auxin-related PIN1 defect, the seedlings displayed defects in the vascular tissue. Surprisingly, SAM-less seedlings variably expressed essential SAM specific genes along the hypocotyl-cotyledon structure up into the cotyledon lamina. Few were even capable of developing an ectopic shoot meristem (eSM) on top of the cotyledon.
Conclusions
The results highlight the developmental autonomy of the SAM vs. cotyledons and suggest that the primary rpk1 defect does not lie in the seedling’s ability to express SAM genes or to develop a shoot meristem. Rather, rpk1’s known defects in cell division and auxin homeostasis, by disturbed PIN1 polarity, impact on SAM and organ generation. In early embryo stages this failure generates a simplified monocotyledonous morphology. Once generated, this likely entails a loss of positional information that in turn affects the spatiotemporal development of the SAM. SAM-bearing and SAM-less monocotyledonous phenotypes show morphological similarities either to real monocots or to dicot species, which only develop one cotyledon. The specific cotyledon defect in rpk1 mutants thus sheds light upon the developmental implications of the transition from two cotyledons to one.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0556-8) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0556-8
PMCID: PMC4492102  PMID: 26150008
RPK1; Arabidopsis; Shoot meristem; SAM; Cotyledon; Monocot; Dicot; Plant embryo; Angiosperm evolution
23.  Multiple interval QTL mapping and searching for PSTOL1 homologs associated with root morphology, biomass accumulation and phosphorus content in maize seedlings under low-P 
BMC Plant Biology  2015;15:172.
Background
Modifications in root morphology are important strategies to maximize soil exploitation under phosphorus starvation in plants. Here, we used two multiple interval models to map QTLs related to root traits, biomass accumulation and P content in a maize RIL population cultivated in nutrient solution. In addition, we searched for putative maize homologs to PSTOL1, a gene responsible to enhance early root growth, P uptake and grain yield in rice and sorghum.
Results
Based on path analysis, root surface area was the root morphology component that most strongly contributed to total dry weight and to P content in maize seedling under low-P availability. Multiple interval mapping models for single (MIM) and multiple traits (MT-MIM) were combined and revealed 13 genomic regions significantly associated with the target traits in a complementary way. The phenotypic variances explained by all QTLs and their epistatic interactions using MT-MIM (23.4 to 35.5 %) were higher than in previous studies, and presented superior statistical power. Some of these QTLs were coincident with QTLs for root morphology traits and grain yield previously mapped, whereas others harbored ZmPSTOL candidate genes, which shared more than 55 % of amino acid sequence identity and a conserved serine/threonine kinase domain with OsPSTOL1. Additionally, four ZmPSTOL candidate genes co-localized with QTLs for root morphology, biomass accumulation and/or P content were preferentially expressed in roots of the parental lines that contributed the alleles enhancing the respective phenotypes.
Conclusions
QTL mapping strategies adopted in this study revealed complementary results for single and multiple traits with high accuracy. Some QTLs, mainly the ones that were also associated with yield performance in other studies, can be good targets for marker-assisted selection to improve P-use efficiency in maize. Based on the co-localization with QTLs, the protein domain conservation and the coincidence of gene expression, we selected novel maize genes as putative homologs to PSTOL1 that will require further validation studies.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0561-y) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0561-y
PMCID: PMC4492167  PMID: 26148492
Phosphorus acquisition; Protein kinase; SNP marker; OsPSTOL1; Zea mays
24.  Origin and evolution of Petrocosmea (Gesneriaceae) inferred from both DNA sequence and novel findings in morphology with a test of morphology-based hypotheses 
BMC Plant Biology  2015;15:167.
Background
Petrocosmea Oliver (Gesneriaceae) currently comprises 38 species with four non-nominate varieties, nearly all of which have been described solely from herbarium specimens. However, the dried specimens have obscured the full range of extremely diverse morphological variation that exists in the genus and has resulted in a poor subgeneric classification system that does not reflect the evolutionary history of this group. It is important to develop innovative methods to find new morphological traits and reexamine and reevaluate the traditionally used morphological data based on new hypothesis. In addition, Petrocosmea is a mid-sized genus but exhibits extreme diverse floral variants. This makes the genus of particular interest in addressing the question whether there are any key factors that is specifically associated with their evolution and diversification.
Results
Here we present the first phylogenetic analyses of the genus based on dense taxonomic sampling and multiple genes combined with a comprehensive morphological investigation. Maximum-parsimony, maximum likelihood and Bayesian analyses of molecular data from two nuclear DNA and six cpDNA regions support the monophyly of Petrocosmea and recover five major clades within the genus, which is strongly corroborated by the reconstruction of ancestral states for twelve new morphological characters directly observed from living material. Ancestral area reconstruction shows that its most common ancestor was likely located east and southeast of the Himalaya-Tibetan plateau. The origin of Petrocosmea from a potentially Raphiocarpus-like ancestor might have involved a series of morphological modifications from caulescent to acaulescent habit as well as from a tetrandrous flower with a long corolla-tube to a diandrous flower with a short corolla-tube, also evident in the vestigial caulescent habit and transitional floral form in clade A that is sister to the remainder of the genus. Among the five clades in Petrocosmea, the patterns of floral morphological differentiation are consistent with discontinuous lineage-associated morphotypes as a repeated adaptive response to alternative environments.
Conclusion
Our results suggest that the lineage-specific morphological differentiations reflected in the upper lip, a functional organ for insect pollination, are likely adaptive responses to pollinator shifts. We further recognize that the floral morphological diversification in Petrocosmea involves several evolutionary phenomena, i.e. evolutionary successive specialization, reversals, parallel evolution, and convergent evolution, which are probably associated with adaptation to pollination against the background of heterogeneous abiotic and biotic environments in the eastern wing regions of Himalaya-Tibetan plateau.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0540-3) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0540-3
PMCID: PMC4489212  PMID: 26135135
DNA sequence; Evolution; Floral morphology; Gesneriaceae; Himalaya-Tibetan plateau; Petrocosmea
25.  Transposable elements, mRNA expression level and strand-specificity of small RNAs are associated with non-additive inheritance of gene expression in hybrid plants 
BMC Plant Biology  2015;15:168.
Background
Gene expression inheritance patterns in Arabidopsis hybrid plants were investigated for correlation with the presence of transposable elements (TEs) and small RNA profile.
Results
The presence of TEs in a gene and the expression of small RNA matching a gene were both found to be associated with non-additive mRNA inheritance patterns in hybrids. Expression levels below mid-parent values in the hybrids were associated with low mRNA expression in parents, with the presence of small RNA from both strands, and with the presence of TEs. High-parent dominance of mRNA levels was found to be associated with high parental mRNA expression levels, the absence of TEs, and for some genes, with small RNA fragments that are predominantly from the sense strand. These small RNAs exhibit a broader size distribution than siRNA and reduced nucleotide end bias, which are consistent with an origin from degraded mRNA. Thus, increased as well as decreased gene expression in hybrids relative to the parental mean is associated with gene expression levels, TE presence and small RNA fragments with differing characteristics.
Conclusions
The data presented here is consistent with a role for differential mRNA decay kinetics as one mechanism contributing to high-parent dominance in gene expression. Our evidence is also consistent with trans repression by siRNA and TEs as the cause of low-parent dominance.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0549-7) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0549-7
PMCID: PMC4490736  PMID: 26139102
Hybrid; Gene expression inheritance; Small RNA; Transposon

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