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26.  Developmental profiling of gene expression in soybean trifoliate leaves and cotyledons 
BMC Plant Biology  2015;15:169.
Background
Immediately following germination, the developing soybean seedling relies on the nutrient reserves stored in the cotyledons to sustain heterotrophic growth. During the seed filling period, developing seeds rely on the transport of nutrients from the trifoliate leaves. In soybean, both cotyledons and leaves develop the capacity for photosynthesis, and subsequently senesce and abscise once their function has ended. Before this occurs, the nutrients they contain are mobilized and transported to other parts of the plant. These processes are carefully orchestrated by genetic regulation throughout the development of the leaf or cotyledon.
Results
To identify genes involved in the processes of leaf or cotyledon development and senescence in soybean, we used RNA-seq to profile multiple stages of cotyledon and leaf tissues. Differentially expressed genes between stages of leaf or cotyledon development were determined, major patterns of gene expression were defined, and shared genes were identified. Over 38,000 transcripts were expressed during the course of leaf and cotyledon development. Of those transcripts, 5,000 were expressed in a tissue specific pattern. Of the genes that were differentially expressed between both later stage tissues, 90 % had the same direction of change, suggesting that the mechanisms of senescence are conserved between tissues. Analysis of the enrichment of biological functions within genes sharing common expression profiles highlights the main processes occurring within these defined temporal windows of leaf and cotyledon development. Over 1,000 genes were identified with predicted regulatory functions that may have a role in control of leaf or cotyledon senescence.
Conclusions
The process of leaf and cotyledon development can be divided into distinct stages characterized by the expression of specific gene sets. The importance of the WRKY, NAC, and GRAS family transcription factors as major regulators of plant senescence is confirmed for both soybean leaf and cotyledon tissues. These results help validate functional annotation for soybean genes and promoters.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0553-y) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0553-y
PMCID: PMC4492100  PMID: 26149852
Leaf senescence; Cotyledon senescence; Glycine max; Leaf development
27.  Genome-wide Identification and Expression Analysis of the CDPK Gene Family in Grape, Vitis spp 
BMC Plant Biology  2015;15:164.
Background
Calcium-dependent protein kinases (CDPKs) play vital roles in plant growth and development, biotic and abiotic stress responses, and hormone signaling. Little is known about the CDPK gene family in grapevine.
Results
In this study, we performed a genome-wide analysis of the 12X grape genome (Vitis vinifera) and identified nineteen CDPK genes. Comparison of the structures of grape CDPK genes allowed us to examine their functional conservation and differentiation. Segmentally duplicated grape CDPK genes showed high structural conservation and contributed to gene family expansion. Additional comparisons between grape and Arabidopsis thaliana demonstrated that several grape CDPK genes occured in the corresponding syntenic blocks of Arabidopsis, suggesting that these genes arose before the divergence of grapevine and Arabidopsis. Phylogenetic analysis divided the grape CDPK genes into four groups. Furthermore, we examined the expression of the corresponding nineteen homologous CDPK genes in the Chinese wild grape (Vitis pseudoreticulata) under various conditions, including biotic stress, abiotic stress, and hormone treatments. The expression profiles derived from reverse transcription and quantitative PCR suggested that a large number of VpCDPKs responded to various stimuli on the transcriptional level, indicating their versatile roles in the responses to biotic and abiotic stresses. Moreover, we examined the subcellular localization of VpCDPKs by transiently expressing six VpCDPK-GFP fusion proteins in Arabidopsis mesophyll protoplasts; this revealed high variability consistent with potential functional differences.
Conclusions
Taken as a whole, our data provide significant insights into the evolution and function of grape CDPKs and a framework for future investigation of grape CDPK genes.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0552-z) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0552-z
PMCID: PMC4485369  PMID: 26122404
Grapevine (Vitis vinifera L.) (Vitis pseudoreticulata); CDPK; Synteny analysis; Phylogenetic tree; Subcellular localization; expression profiles
28.  Isoprene emission by poplar is not important for the feeding behaviour of poplar leaf beetles 
BMC Plant Biology  2015;15:165.
Background
Chrysomela populi (poplar leaf beetle) is a common herbivore in poplar plantations whose infestation causes major economic losses. Because plant volatiles act as infochemicals, we tested whether isoprene, the main volatile organic compound (VOC) produced by poplars (Populus x canescens), affects the performance of C. populi employing isoprene emitting (IE) and transgenic isoprene non-emitting (NE) plants. Our hypothesis was that isoprene is sensed and affects beetle orientation or that the lack of isoprene affects plant VOC profiles and metabolome with consequences for C. populi feeding.
Results
Electroantennographic analysis revealed that C. populi can detect higher terpenes, but not isoprene. In accordance to the inability to detect isoprene, C. populi showed no clear preference for IE or NE poplar genotypes in the choice experiments, however, the beetles consumed a little bit less leaf mass and laid fewer eggs on NE poplar trees in field experiments. Slight differences in the profiles of volatile terpenoids between IE and NE genotypes were detected by gas chromatography - mass spectrometry. Non-targeted metabolomics analysis by Fourier Transform Ion Cyclotron Resonance Mass Spectrometer revealed genotype-, time- and herbivore feeding-dependent metabolic changes both in the infested and adjacent undamaged leaves under field conditions.
Conclusions
We show for the first time that C. populi is unable to sense isoprene. The detected minor differences in insect feeding in choice experiments and field bioassays may be related to the revealed changes in leaf volatile emission and metabolite composition between the IE and NE poplars. Overall our results indicate that lacking isoprene emission is of minor importance for C. populi herbivory under natural conditions, and that the lack of isoprene is not expected to change the economic losses in poplar plantations caused by C. populi infestation.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0542-1) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0542-1
PMCID: PMC4486431  PMID: 26122266
Chrysomela populi; Volatile organic compounds; VOC; Isoprene; Isoprenoids; Terpene; Electroantennography; Beetle behaviour; Populus x canescens; Metabolomics
29.  Genetical genomics of Populus leaf shape variation 
BMC Plant Biology  2015;15:166.
Background
Leaf morphology varies extensively among plant species and is under strong genetic control. Mutagenic screens in model systems have identified genes and established molecular mechanisms regulating leaf initiation, development, and shape. However, it is not known whether this diversity across plant species is related to naturally occurring variation at these genes. Quantitative trait locus (QTL) analysis has revealed a polygenic control for leaf shape variation in different species suggesting that loci discovered by mutagenesis may only explain part of the naturally occurring variation in leaf shape. Here we undertook a genetical genomics study in a poplar intersectional pseudo-backcross pedigree to identify genetic factors controlling leaf shape. The approach combined QTL discovery in a genetic linkage map anchored to the Populus trichocarpa reference genome sequence and transcriptome analysis.
Results
A major QTL for leaf lamina width and length:width ratio was identified in multiple experiments that confirmed its stability. A transcriptome analysis of expanding leaf tissue contrasted gene expression between individuals with alternative QTL alleles, and identified an ADP-ribosylation factor (ARF) GTPase (PtARF1) as a candidate gene for regulating leaf morphology in this pedigree. ARF GTPases are critical elements in the vesicular trafficking machinery. Disruption of the vesicular trafficking function of ARF by the pharmacological agent Brefeldin A (BFA) altered leaf lateral growth in the narrow-leaf P. trichocarpa suggesting a molecular mechanism of leaf shape determination. Inhibition of the vesicular trafficking processes by BFA interferes with cycling of PIN proteins and causes their accumulation in intercellular compartments abolishing polar localization and disrupting normal auxin flux with potential effects on leaf expansion.
Conclusions
In other model systems, ARF proteins have been shown to control the localization of auxin efflux carriers, which function to establish auxin gradients and apical-basal cell polarity in developing plant organs. Our results support a model where PtARF1 transcript abundance changes the dynamics of endocytosis-mediated PIN localization in leaf cells, thus affecting lateral auxin flux and subsequently lamina leaf expansion. This suggests that evolution of differential cellular polarity plays a significant role in leaf morphological variation observed in subgenera of genus Populus.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0557-7) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0557-7
PMCID: PMC4486686  PMID: 26122556
Leaf morphology; QTL analysis; Expression QTL; Genomics; Populus trichocarpa; ADP-ribosylation factor
30.  Cytoplasmic genome types of European potatoes and their effects on complex agronomic traits 
BMC Plant Biology  2015;15:162.
Background
Various wild species germplasm has been used in European potato breeding since the first introduction of potato (Solanum tuberosum L.) to Europe. As the plant cytoplasmic genome including chloroplast and mitochondrial genomes is transmitted only through the maternal parent, cytoplasmic markers are useful tools in breeding programs to determine cytoplasmic genome types and to trace maternal ancestors. The potato cytoplasmic genome can be distinguished into six distinct types (M, P, A, W, T, and D). Male sterility was found in genotypes with S. demissum-derived D-type cytoplasm and S. stoloniferum-derived W/γ-type cytoplasm. These wild species were frequently used to incorporate superior pathogen resistance genes. As a result, the percentage of these two types is increasing unintentionally in the European germplasm pool. Other than cytoplasmic male sterility, little is known about effects of the cytoplasmic genome on complex agronomic traits in potato.
Result
The cytoplasm types of 1,217 European potato cultivars and breeding clones were determined with type specific DNA markers. Most frequent were T- (59.4 %), D- (27.4 %), and W- (12.2 %) type cytoplasm, while A- (0.7 %) and M-type cytoplasm (0.3 %) was rare and P-type cytoplasm was absent. When comparing varieties with breeding clones, the former showed a relatively higher frequency of T-type and lower frequency of D- and W-type cytoplasm. Correlation analysis of cytoplasm types and agronomic data showed that W/γ-type cytoplasm was correlated with increased tuber starch content and later plant maturity. Correlation with quantitative resistance to late blight was observed for D-type and M-type cytoplasm. Both cytoplasm types had a positive effect on resistance.
Conclusion
This study revealed and quantified the cytoplasmic diversity in the European potato germplasm pool. Knowledge of cytoplasm type is important for maintaining genetic diversity and managing the male sterility problem in breeding programs. This is the first comprehensive study to show correlations of distinct cytoplasmic genomes with complex agronomic traits in potato. Correlations particularly with tuber starch content and resistance to late blight provided new knowledge on cytoplasmic effects on these important traits, which can be exploited for genetic improvement of potato.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0545-y) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0545-y
PMCID: PMC4480903  PMID: 26112802
Cytoplasmic genome; Cytoplasmic male sterility; Molecular marker-assisted selection; Late blight resistance; Agronomic trait; Potato (Solanum tuberosum L.)
31.  PlantOrDB: a genome-wide ortholog database for land plants and green algae 
BMC Plant Biology  2015;15:161.
Background
Genes with different functions are originally generated from some ancestral genes by gene duplication, mutation and functional recombination. It is widely accepted that orthologs are homologous genes evolved from speciation events while paralogs are homologous genes resulted from gene duplication events.With the rapid increase of genomic data, identifying and distinguishing these genes among different species is becoming an important part of functional genomics research.
Description
Using 35 plant and 6 green algal genomes from Phytozome v9, we clustered 1,291,670 peptide sequences into 49,355 homologous gene families in terms of sequence similarity. For each gene family, we have generated a peptide sequence alignment and phylogenetic tree, and identified the speciation/duplication events for every node within the tree. For each node, we also identified and highlighted diagnostic characters that facilitate appropriate addition of a new query sequence into the existing phylogenetic tree and sequence alignment of its best matched gene family. Based on a desired species or subgroup of all species, users can view the phylogenetic tree, sequence alignment and diagnostic characters for a given gene family selectively. PlantOrDB not only allows users to identify orthologs or paralogs from phylogenetic trees, but also provides all orthologs that are built using Reciprocal Best Hit (RBH) pairwise alignment method. Users can upload their own sequences to find the best matched gene families, and visualize their query sequences within the relevant phylogenetic trees and sequence alignments.
Conclusion
PlantOrDB (http://bioinfolab.miamioh.edu/plantordb) is a genome-wide ortholog database for land plants and green algae. PlantOrDB offers highly interactive visualization, accurate query classification and powerful search functions useful for functional genomic research.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0531-4) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0531-4
PMCID: PMC4481079  PMID: 26112452
Homolog; Ortholog; Paralog; Database; Land plants; Green algae; Gene family; PlantOrDB
32.  A comprehensive quantitative phosphoproteome analysis of rice in response to bacterial blight 
BMC Plant Biology  2015;15:163.
Background
Rice is a major crop worldwide. Bacterial blight (BB) caused by Xanthomonas oryzae pv. oryzae (Xoo) has become one of the most devastating diseases for rice. It has been clear that phosphorylation plays essential roles in plant disease resistance. However, the role of phosphorylation is poorly understood in rice-Xoo system. Here, we report the first study on large scale enrichment of phosphopeptides and identification of phosphosites in rice before and 24 h after Xoo infection.
Results
We have successfully identified 2367 and 2223 phosphosites on 1334 and 1297 representative proteins in 0 h and 24 h after Xoo infection, respectively. A total of 762 differentially phosphorylated proteins, including transcription factors, kinases, epi-genetic controlling factors and many well-known disease resistant proteins, are identified after Xoo infection suggesting that they may be functionally relevant to Xoo resistance. In particular, we found that phosphorylation/dephosphorylation might be a key switch turning on/off many epi-genetic controlling factors, including HDT701, in response to Xoo infection, suggesting that phosphorylation switch overriding the epi-genetic regulation may be a very universal model in the plant disease resistance pathway.
Conclusions
The phosphosites identified in this study would be a big complementation to our current knowledge in the phosphorylation status and sites of rice proteins. This research represents a substantial advance in understanding the rice phosphoproteome as well as the mechanism of rice bacterial blight resistance.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0541-2) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0541-2
PMCID: PMC4482044  PMID: 26112675
Rice (Oryza sativa L.); Phosphoproteome; Bacterial blight; Post-translational modification
33.  Allelic variation at the rpv1 locus controls partial resistance to Plum pox virus infection in Arabidopsis thaliana 
BMC Plant Biology  2015;15:159.
Background
Sharka is caused by Plum pox virus (PPV) in stone fruit trees. In orchards, the virus is transmitted by aphids and by grafting. In Arabidopsis, PPV is transferred by mechanical inoculation, by biolistics and by agroinoculation with infectious cDNA clones. Partial resistance to PPV has been observed in the Cvi-1 and Col-0 Arabidopsis accessions and is characterized by a tendency to escape systemic infection. Indeed, only one third of the plants are infected following inoculation, in comparison with the susceptible Ler accession.
Results
Genetic analysis showed this partial resistance to be monogenic or digenic depending on the allelic configuration and recessive. It is detected when inoculating mechanically but is overcome when using biolistic or agroinoculation. A genome-wide association analysis was performed using multiparental lines and 147 Arabidopsis accessions. It identified a major genomic region, rpv1. Fine mapping led to the positioning of rpv1 to a 200 kb interval on the long arm of chromosome 1. A candidate gene approach identified the chloroplast phosphoglycerate kinase (cPGK2) as a potential gene underlying the resistance. A virus-induced gene silencing strategy was used to knock-down cPGK2 expression, resulting in drastically reduced PPV accumulation.
Conclusion
These results indicate that rpv1 resistance to PPV carried by the Cvi-1 and Col-0 accessions is linked to allelic variations at the Arabidopsis cPGK2 locus, leading to incomplete, compatible interaction with the virus.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0559-5) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0559-5
PMCID: PMC4479089  PMID: 26109391
Partial resistance; recessive resistance; QTL mapping; association mapping; PPV; Plum pox virus; Arabidopsis thaliana; cPGK
34.  Characterization of the cork oak transcriptome dynamics during acorn development 
BMC Plant Biology  2015;15:158.
Background
Cork oak (Quercus suber L.) has a natural distribution across western Mediterranean regions and is a keystone forest tree species in these ecosystems. The fruiting phase is especially critical for its regeneration but the molecular mechanisms underlying the biochemical and physiological changes during cork oak acorn development are poorly understood. In this study, the transcriptome of the cork oak acorn, including the seed, was characterized in five stages of development, from early development to acorn maturation, to identify the dominant processes in each stage and reveal transcripts with important functions in gene expression regulation and response to water.
Results
A total of 80,357 expressed sequence tags (ESTs) were de novo assembled from RNA-Seq libraries representative of the several acorn developmental stages. Approximately 7.6 % of the total number of transcripts present in Q. suber transcriptome was identified as acorn specific. The analysis of expression profiles during development returned 2,285 differentially expressed (DE) transcripts, which were clustered into six groups. The stage of development corresponding to the mature acorn exhibited an expression profile markedly different from other stages. Approximately 22 % of the DE transcripts putatively code for transcription factors (TF) or transcriptional regulators, and were found almost equally distributed among the several expression profile clusters, highlighting their major roles in controlling the whole developmental process. On the other hand, carbohydrate metabolism, the biological pathway most represented during acorn development, was especially prevalent in mid to late stages as evidenced by enrichment analysis. We further show that genes related to response to water, water deprivation and transport were mostly represented during the early (S2) and the last stage (S8) of acorn development, when tolerance to water desiccation is possibly critical for acorn viability.
Conclusions
To our knowledge this work represents the first report of acorn development transcriptomics in oaks. The obtained results provide novel insights into the developmental biology of cork oak acorns, highlighting transcripts putatively involved in the regulation of the gene expression program and in specific processes likely essential for adaptation. It is expected that this knowledge can be transferred to other oak species of great ecological value.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0534-1) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0534-1
PMCID: PMC4479327  PMID: 26109289
Quercus suber; Fruit; Seed; Transcriptomics; Transcription factor; Transcriptional regulators; Response to water; Carbohydrate metabolism
35.  Tc-MYBPA an Arabidopsis TT2-like transcription factor and functions in the regulation of proanthocyanidin synthesis in Theobroma cacao 
BMC Plant Biology  2015;15:160.
Background
The flavan-3-ols catechin and epicatechin, and their polymerized oligomers, the proanthocyanidins (PAs, also called condensed tannins), accumulate to levels of up to 15 % of the total weight of dry seeds of Theobroma cacao L. These compounds have been associated with several health benefits in humans. They also play important roles in pest and disease defense throughout the plant. In Arabidopsis, the R2R3 type MYB transcription factor TT2 regulates the major genes leading to the synthesis of PA.
Results
To explore the transcriptional regulation of the PA synthesis pathway in cacao, we isolated and characterized an R2R3 type MYB transcription factor MYBPA from cacao. We examined the spatial and temporal gene expression patterns of the Tc-MYBPA gene and found it to be developmentally expressed in a manner consistent with its involvement in PAs and anthocyanin synthesis. Functional complementation of an Arabidopsis tt2 mutant with Tc-MYBPA suggested that it can functionally substitute the Arabidopsis TT2 gene. Interestingly, in addition to PA accumulation in seeds of the Tc-MYBPA expressing plants, we also observed an obvious increase of anthocyanidin accumulation in hypocotyls. We observed that overexpression of the Tc-MYBPA gene resulted in increased expression of several key genes encoding the major structural enzymes of the PA and anthocyanidin pathway, including DFR (dihydroflavanol reductase), LDOX (leucoanthocyanidin dioxygenase) and BAN (ANR, anthocyanidin reductase).
Conclusion
We conclude that the Tc-MYBPA gene that encodes an R2R3 type MYB transcription factor is an Arabidopsis TT2 like transcription factor, and may be involved in the regulation of both anthocyanin and PA synthesis in cacao. This research may provide molecular tools for breeding of cacao varieties with improved disease resistance and enhanced flavonoid profiles for nutritional and pharmaceutical applications.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0529-y) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0529-y
PMCID: PMC4481123  PMID: 26109181
Theobroma cacao; Proanthocyanidin; Transcription factor; TT2
36.  Arabidopsis leucine-rich repeat extensin (LRX) proteins modify cell wall composition and influence plant growth 
BMC Plant Biology  2015;15:155.
Background
Leucine-rich repeat extensins (LRXs) are extracellular proteins consisting of an N-terminal leucine-rich repeat (LRR) domain and a C-terminal extensin domain containing the typical features of this class of structural hydroxyproline-rich glycoproteins (HRGPs). The LRR domain is likely to bind an interaction partner, whereas the extensin domain has an anchoring function to insolubilize the protein in the cell wall. Based on the analysis of the root hair-expressed LRX1 and LRX2 of Arabidopsis thaliana, LRX proteins are important for cell wall development. The importance of LRX proteins in non-root hair cells and on the structural changes induced by mutations in LRX genes remains elusive.
Results
The LRX gene family of Arabidopsis consists of eleven members, of which LRX3, LRX4, and LRX5 are expressed in aerial organs, such as leaves and stem. The importance of these LRX genes for plant development and particularly cell wall formation was investigated. Synergistic effects of mutations with gradually more severe growth retardation phenotypes in double and triple mutants suggest a similar function of the three genes. Analysis of cell wall composition revealed a number of changes to cell wall polysaccharides in the mutants.
Conclusions
LRX3, LRX4, and LRX5, and most likely LRX proteins in general, are important for cell wall development. Due to the complexity of changes in cell wall structures in the lrx mutants, the exact function of LRX proteins remains to be determined. The increasingly strong growth-defect phenotypes in double and triple mutants suggests that the LRX proteins have similar functions and that they are important for proper plant development.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0548-8) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0548-8
PMCID: PMC4477543  PMID: 26099801
Arabidopsis; Cell wall development; Cell wall structures; LRR-extensin; LRX
37.  The ARGOS gene family functions in a negative feedback loop to desensitize plants to ethylene 
BMC Plant Biology  2015;15:157.
Background
Ethylene plays critical roles in plant growth and development, including the regulation of cell expansion, senescence, and the response to biotic and abiotic stresses. Elements of the initial signal transduction pathway have been determined, but we are still defining regulatory mechanisms by which the sensitivity of plants to ethylene is modulated.
Results
We report here that members of the ARGOS gene family of Arabidopsis, previously implicated in the regulation of plant growth and biomass, function as negative feedback regulators of ethylene signaling. Expression of all four members of the ARGOS family is induced by ethylene, but this induction is blocked in ethylene-insensitive mutants. The dose dependence for ethylene induction varies among the ARGOS family members, suggesting that they could modulate responses across a range of ethylene concentrations. GFP-fusions of ARGOS and ARL localize to the endoplasmic reticulum, the same subcellular location as the ethylene receptors and other initial components of the ethylene signaling pathway. Seedlings with increased expression of ARGOS family members exhibit reduced ethylene sensitivity based on physiological and molecular responses.
Conclusions
These results support a model in which the ARGOS gene family functions as part of a negative feedback circuit to desensitize the plant to ethylene, thereby expanding the range of ethylene concentrations to which the plant can respond. These results also indicate that the effects of the ARGOS gene family on plant growth and biomass are mediated through effects on ethylene signal transduction.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0554-x) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0554-x
PMCID: PMC4478640  PMID: 26105742
Ethylene; Desensitization; Ethylene receptor; Endoplasmic reticulum; Auxin; Arabidopsis
38.  The additive effects of GS3 and qGL3 on rice grain length regulation revealed by genetic and transcriptome comparisons 
BMC Plant Biology  2015;15:156.
Background
Grain length, as a critical trait for rice grain size and shape, has a great effect on grain yield and appearance quality. Although several grain size/shape genes have been cloned, the genetic interaction among these genes and the molecular mechanisms of grain size/shape architecture have not yet to be explored.
Results
To investigate the genetic interaction between two major grain length loci of rice, GS3 and qGL3, we developed two near-isogenic lines (NILs), NIL-GS3 (GS3/qGL3) and NIL-qgl3 (gs3/qgl3), in the genetic background of 93–11 (gs3/qGL3) by conventional backcrossing and marker-assisted selection (MAS). Another NIL-GS3/qgl3 (GS3/qgl3) was developed by crossing NIL-GS3 with NIL-qgl3 and using MAS. By comparing the grain lengths of 93–11, NIL-GS3, NIL-qgl3 and NIL-GS3/qgl3, we investigated the effects of GS3, qGL3 and GS3 × qGL3 interaction on grain length based on two-way ANOVA. We found that GS3 and qGL3 had additive effects on rice grain length regulation. Comparative analysis of primary panicle transcriptomes in the four NILs revealed that the genes affected by GS3 and qGL3 partially overlapped, and both loci might be involved in brassinosteroid signaling.
Conclusion
Our data provide new information to better understand the rice grain length regulation mechanism and help rice breeders improve rice yield and appearance quality by molecular design breeding.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0515-4) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0515-4
PMCID: PMC4479070  PMID: 26105598
Additive effect; Grain length; GS3; qGL3; Rice; Transcriptome; Brassinosteroid
39.  Study of genetic variability in Vitis vinifera L. germplasm by high-throughput Vitis18kSNP array: the case of Georgian genetic resources 
BMC Plant Biology  2015;15:154.
Background
Georgia, in the Caucasian region, is considered the first domestication centre of grapevine. This country is characterized by high morphological variability of cultivated (Vitis vinifera L. subsp. sativa (DC.) Hegi) and wild (Vitis vinifera L. subsp. sylvestris (Gmel.) Hegi) compartments. The main objective of this study was to investigate the level of genetic diversity obtained by the novel custom Vitis18kSNP array, in order to analyse 71 grapevine accessions representative of wild and cultivated Georgian germplasms.
Results
The number of loci successfully amplified was 15,317 out of 18,775 SNP and 79 % of loci resulted polymorphic. Sixty-eight unique profiles were identified, 42 for the sativa and 26 for the sylvestris compartment. Cluster analysis highlighted two main groups, one for cultivars and another for wild individuals, while a genetic structure according to accession taxonomic status and cultivar geographical origin was revealed by multivariate analysis, differentiating clearly the genotypes into 3 main groups, two groups including cultivars and one for wild individuals, even though a considerable overlapping area was observed.
Conclusions
Pattern of genetic diversity structure presented an additional proof that grapevine domestication events took place in the Caucasian region contributing to the crop evolution. Our results demonstrated a moderate differentiation between sativa and sylvestris compartments, even though a connection between several samples of both subspecies may be assumed for the occurrence of cross hybridization events among native wild populations and the cultivated accessions. Nevertheless, first degree relationships have not been discovered between wild and cultivated individuals.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0510-9) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0510-9
PMCID: PMC4477415  PMID: 26099513
Domestication; Molecular markers; SNP; V. vinifera subsp. sativa; V. vinifera subsp. sylvestris
40.  Diffraction evidence for the structure of cellulose microfibrils in bamboo, a model for grass and cereal celluloses 
BMC Plant Biology  2015;15:153.
Background
Cellulose from grasses and cereals makes up much of the potential raw material for biofuel production. It is not clear if cellulose microfibrils from grasses and cereals differ in structure from those of other plants. The structures of the highly oriented cellulose microfibrils in the cell walls of the internodes of the bamboo Pseudosasa amabilis are reported. Strong orientation facilitated the use of a range of scattering techniques.
Results
Small-angle neutron scattering provided evidence of extensive aggregation by hydrogen bonding through the hydrophilic edges of the sheets of chains. The microfibrils had a mean centre-to-centre distance of 3.0 nm in the dry state, expanding on hydration. The expansion on hydration suggests that this distance between centres was through the hydrophilic faces of adjacent microfibrils. However in the other direction, perpendicular to the sheets of chains, the mean, disorder-corrected Scherrer dimension from wide-angle X-ray scattering was 3.8 nm. It is possible that this dimension is increased by twinning (crystallographic coalescence) of thinner microfibrils over part of their length, through the hydrophobic faces. The wide-angle scattering data also showed that the microfibrils had a relatively large intersheet d-spacing and small monoclinic angle, features normally considered characteristic of primary-wall cellulose.
Conclusions
Bamboo microfibrils have features found in both primary-wall and secondary-wall cellulose, but are crystallographically coalescent to a greater extent than is common in celluloses from other plants. The extensive aggregation and local coalescence of the microfibrils are likely to have parallels in other grass and cereal species and to influence the accessibility of cellulose to degradative enzymes during conversion to liquid biofuels
doi:10.1186/s12870-015-0538-x
PMCID: PMC4477487  PMID: 26099632
WAXS; WANS; SANS; Crystallinity; Aggregation; Cellulase
41.  Temporal transcriptome profiling reveals expression partitioning of homeologous genes contributing to heat and drought acclimation in wheat (Triticum aestivum L.) 
BMC Plant Biology  2015;15:152.
Background
Hexaploid wheat (Triticum aestivum) is a globally important crop. Heat, drought and their combination dramatically reduce wheat yield and quality, but the molecular mechanisms underlying wheat tolerance to extreme environments, especially stress combination, are largely unknown. As an allohexaploid, wheat consists of three closely related subgenomes (A, B, and D), and was reported to show improved tolerance to stress conditions compared to tetraploid. But so far very little is known about how wheat coordinates the expression of homeologous genes to cope with various environmental constraints on the whole-genome level.
Results
To explore the transcriptional response of wheat to the individual and combined stress, we performed high-throughput transcriptome sequencing of seedlings under normal condition and subjected to drought stress (DS), heat stress (HS) and their combination (HD) for 1 h and 6 h, and presented global gene expression reprograms in response to these three stresses. Gene Ontology (GO) enrichment analysis of DS, HS and HD responsive genes revealed an overlap and complexity of functional pathways between each other. Moreover, 4,375 wheat transcription factors were identified on a whole-genome scale based on the released scaffold information by IWGSC, and 1,328 were responsive to stress treatments. Then, the regulatory network analysis of HSFs and DREBs implicated they were both involved in the regulation of DS, HS and HD response and indicated a cross-talk between heat and drought stress. Finally, approximately 68.4 % of homeologous genes were found to exhibit expression partitioning in response to DS, HS or HD, which was further confirmed by using quantitative RT-PCR and Nullisomic-Tetrasomic lines.
Conclusions
A large proportion of wheat homeologs exhibited expression partitioning under normal and abiotic stresses, which possibly contributes to the wide adaptability and distribution of hexaploid wheat in response to various environmental constraints.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0511-8) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0511-8
PMCID: PMC4474349  PMID: 26092253
Wheat; Heat; Drought; Transcriptome; Homeologous genes
42.  Widespread and evolutionary analysis of a MITE family Monkey King in Brassicaceae 
BMC Plant Biology  2015;15:149.
Background
Miniature inverted repeat transposable elements (MITEs) are important components of eukaryotic genomes, with hundreds of families and many copies, which may play important roles in gene regulation and genome evolution. However, few studies have investigated the molecular mechanisms involved. In our previous study, a Tourist-like MITE, Monkey King, was identified from the promoter region of a flowering time gene, BnFLC.A10, in Brassica napus. Based on this MITE, the characteristics and potential roles on gene regulation of the MITE family were analyzed in Brassicaceae.
Results
The characteristics of the Tourist-like MITE family Monkey King in Brassicaceae, including its distribution, copies and insertion sites in the genomes of major Brassicaceae species were analyzed in this study. Monkey King was actively amplified in Brassica after divergence from Arabidopsis, which was indicated by the prompt increase in copy number and by phylogenetic analysis. The genomic variations caused by Monkey King insertions, both intra- and inter-species in Brassica, were traced by PCR amplification. Genomic sequence analysis showed that most complete Monkey King elements are located in gene-rich regions, less than 3kb from genes, in both the B. rapa and A. thaliana genomes. Sixty-seven Brassica expressed sequence tags carrying Monkey King fragments were also identified from the NCBI database. Bisulfite sequencing identified specific DNA methylation of cytosine residues in the Monkey King sequence. A fragment containing putative TATA-box motifs in the MITE sequence could bind with nuclear protein(s) extracted from leaves of B. napus plants. A Monkey King-related microRNA, bna-miR6031, was identified in the microRNA database. In transgenic A. thaliana, when the Monkey King element was inserted upstream of 35S promoter, the promoter activity was weakened.
Conclusion
Monkey King, a Brassicaceae Tourist-like MITE family, has amplified relatively recently and has induced intra- and inter-species genomic variations in Brassica. Monkey King elements are most abundant in the vicinity of genes and may have a substantial effect on genome-wide gene regulation in Brassicaceae. Monkey King insertions potentially regulate gene expression and genome evolution through epigenetic modification and new regulatory motif production.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0490-9) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0490-9
PMCID: PMC4471910  PMID: 26084405
Brassicaceae; Brassica; Miniature inverted repeat transposable elements; Monkey King; Tourist-like MITE; DNA methylation; bna-miR6031
43.  Genome-wide analysis of the gene families of resistance gene analogues in cotton and their response to Verticillium wilt 
BMC Plant Biology  2015;15:148.
Background
Gossypium raimondii is a Verticillium wilt-resistant cotton species whose genome encodes numerous disease resistance genes that play important roles in the defence against pathogens. However, the characteristics of resistance gene analogues (RGAs) and Verticillium dahliae response loci (VdRLs) have not been investigated on a global scale. In this study, the characteristics of RGA genes were systematically analysed using bioinformatics-driven methods. Moreover, the potential VdRLs involved in the defence response to Verticillium wilt were identified by RNA-seq and correlations with known resistance QTLs.
Results
The G. raimondii genome encodes 1004 RGA genes, and most of these genes cluster in homology groups based on high levels of similarity. Interestingly, nearly half of the RGA genes occurred in 26 RGA-gene-rich clusters (Rgrcs). The homology analysis showed that sequence exchanges and tandem duplications frequently occurred within Rgrcs, and segmental duplications took place among the different Rgrcs. An RNA-seq analysis showed that the RGA genes play roles in cotton defence responses, forming 26 VdRLs inside in the Rgrcs after being inoculated with V. dahliae. A correlation analysis found that 12 VdRLs were adjacent to the known Verticillium wilt resistance QTLs, and that 5 were rich in NB-ARC domain-containing disease resistance genes.
Conclusions
The cotton genome contains numerous RGA genes, and nearly half of them are located in clusters, which evolved by sequence exchanges, tandem duplications and segmental duplications. In the Rgrcs, 26 loci were induced by the V. dahliae inoculation, and 12 are in the vicinity of known Verticillium wilt resistance QTLs.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0508-3) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0508-3
PMCID: PMC4471920  PMID: 26084488
Cotton; Verticillium wilt-resistant; Resistance gene analogues; RGA-gene-rich clusters; Verticillium dahliae response loci
44.  Genome-wide analysis, expression profile of heat shock factor gene family (CaHsfs) and characterisation of CaHsfA2 in pepper (Capsicum annuum L.) 
BMC Plant Biology  2015;15:151.
Background
Heat shock factors (Hsfs) play crucial roles in plant developmental and defence processes. The production and quality of pepper (Capsicum annuum L.), an economically important vegetable crop, are severely reduced by adverse environmental stress conditions, such as heat, salt and osmotic stress. Although the pepper genome has been fully sequenced, the characterization of the Hsf gene family under abiotic stress conditions remains incomplete.
Results
A total of 25 CaHsf members were identified in the pepper genome by bioinformatics analysis and PCR assays. They were grouped into three classes, CaHsfA, B and C, based on highly conserved Hsf domains, were distributed over 11 of 12 chromosomes, with none found on chromosome 11, and all of them, except CaHsfA5, formed a protein–protein interaction network. According to the RNA-seq data of pepper cultivar CM334, most CaHsf members were expressed in at least one tissue among root, stem, leaf, pericarp and placenta. Quantitative real-time PCR assays showed that all of the CaHsfs responded to heat stress (40 °C for 2 h), except CaHsfC1 in thermotolerant line R9 leaves, and that the expression patterns were different from those in thermosensitive line B6. Many CaHsfs were also regulated by salt and osmotic stresses, as well as exogenous Ca2+, putrescine, abscisic acid and methyl jasmonate. Additionally, CaHsfA2 was located in the nucleus and had transcriptional activity, consistent with the typical features of Hsfs. Time-course expression profiling of CaHsfA2 in response to heat stress revealed differences in its expression level and pattern between the pepper thermosensitive line B6 and thermotolerant line R9.
Conclusions
Twenty-five Hsf genes were identified in the pepper genome and most of them responded to heat, salt, osmotic stress, and exogenous substances, which provided potential clues for further analyses of CaHsfs functions in various kinds of abiotic stresses and of corresponding signal transduction pathways in pepper.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0512-7) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0512-7
PMCID: PMC4472255  PMID: 26088319
Pepper; Identification of CaHsfs family; Abiotic stress; CaHsfA2; Gene expression
45.  A major QTL controlling apple skin russeting maps on the linkage group 12 of ‘Renetta Grigia di Torriana’ 
BMC Plant Biology  2015;15:150.
Background
Russeting is a disorder developed by apple fruits that consists of cuticle cracking followed by the replacement of the epidermis by a corky layer that protects the fruit surface from water loss and pathogens. Although influenced by many environmental conditions and orchard management practices, russeting is under genetic control. The difficulty in classifying offspring and consequent variable segregation ratios have led several authors to conclude that more than one genetic determinant could be involved, although some evidence favours a major gene (Ru).
Results
In this study we report the mapping of a major genetic russeting determinant on linkage group 12 of apple as inferred from the phenotypic observation in a segregating progeny derived from ‘Renetta Grigia di Torriana’, the construction of a 20 K Illumina SNP chip based genetic map, and QTL analysis. Recombination analysis in two mapping populations restricted the region of interest to approximately 400 Kb. Of the 58 genes predicted from the Golden Delicious sequence, a putative ABCG family transporter has been identified. Within a small set of russeted cultivars tested with markers of the region, only six showed the same haplotype of ‘Renetta Grigia di Torriana’.
Conclusions
A major determinant (Ru_RGT) for russeting development putatively involved in cuticle organization is proposed as a candidate for controlling the trait. SNP and SSR markers tightly co-segregating with the Ru_RGT locus may assist the breeder selection. The observed segregations and the analysis of the ‘Renetta Grigia di Torriana’ haplotypic region in a panel of russeted and non-russeted cultivars may suggest the presence of other determinants for russeting in apple.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0507-4) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0507-4
PMCID: PMC4472412  PMID: 26084469
Malus x domestica; Russet; Mapping; Quantitative Trait Locus (QTL); Single Nucleotide Polymorphism (SNP); Infinium® Illumina SNP chip
46.  Mining and identification of polyunsaturated fatty acid synthesis genes active during camelina seed development using 454 pyrosequencing 
BMC Plant Biology  2015;15:147.
Background
Camelina (Camelina sativa L.) is well known for its high unsaturated fatty acid content and great resistance to environmental stress. However, little is known about the molecular mechanisms of unsaturated fatty acid biosynthesis in this annual oilseed crop. To gain greater insight into this mechanism, the transcriptome profiles of seeds at different developmental stages were analyzed by 454 pyrosequencing.
Results
Sequencing of two normalized 454 libraries produced 831,632 clean reads. A total of 32,759 unigenes with an average length of 642 bp were obtained by de novo assembly, and 12,476 up-regulated and 12,390 down-regulated unigenes were identified in the 20 DAF (days after flowering) library compared with the 10 DAF library. Functional annotations showed that 220 genes annotated as fatty acid biosynthesis genes were up-regulated in 20 DAF sample. Among them, 47 candidate unigenes were characterized as responsible for polyunsaturated fatty acid synthesis. To verify unigene expression levels calculated from the transcriptome analysis results, quantitative real-time PCR was performed on 11 randomly selected genes from the 220 up-regulated genes; 10 showed consistency between qRT-PCR and 454 pyrosequencing results.
Conclusions
Investigation of gene expression levels revealed 32,759 genes involved in seed development, many of which showed significant changes in the 20 DAF sample compared with the 10 DAF sample. Our 454 pyrosequencing data for the camelina transcriptome provide an insight into the molecular mechanisms and regulatory pathways of polyunsaturated fatty acid biosynthesis in camelina. The genes characterized in our research will provide candidate genes for the genetic modification of crops.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0513-6) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0513-6
PMCID: PMC4470060  PMID: 26084534
Camelina sativa; Oil crop; Polyunsaturated fatty acid; Transcriptome; Gene expression; qRT-PCR
47.  Natural hybridization and asymmetric introgression at the distribution margin of two Buddleja species with a large overlap 
BMC Plant Biology  2015;15:146.
Background
Natural hybridization in plants is universal and plays an important role in evolution. Based on morphology it has been presumed that hybridization occurred in the genus Buddleja, though genetic studies confirming this assumption have not been conducted to date. The two species B. crispa and B. officinalis overlap in their distributions over a wide range in South-West China, and we aimed to provide genetic evidence for ongoing hybridization in this study.
Results
We investigated the occurrence of hybrids between the two species at the southern-most edge of the distribution of B. crispa using five nuclear loci and pollination experiments. The genetic data suggest substantial differentiation between the two species as species-specific alleles are separated by at least 7–28 mutations. The natural hybrids found were nearly all F1s (21 of 23), but backcrosses were detected, and some individuals, morphologically indistinguishable from the parental species, showed introgression. Pollen viability test shows that the percentage of viable pollen grains was 50 ± 4 % for B. crispa, and 81 ± 2 % for B. officinalis. This difference is highly significant (t = 7.382, p < 0.0001). Hand cross-pollination experiments showed that B. crispa is not successful as pollen-parent, but B. officinalis is able to pollinate B. crispa to produce viable hybrid seed. Inter-specific seed-set is low (8 seeds per fruit, as opposed to about 65 for intra-specific pollinations), suggesting post-zygotic reproductive barriers. In addition, one of the reference populations also suggests a history of introgression at other localities.
Conclusions
The occurrence of morphologically intermediate individuals between B. crispa and B. officinalis at Xishan Mountain is unequivocally linked to hybridization and almost all examined individuals of the putative hybrids were likely F1s. Despite pollination experiments indicating higher chances for introgression into B. officinalis (hybrids only produced viable seed when crossed with B. officinalis), observed introgression was asymmetrical into B. crispa. This could be due to seeds produced by hybrids not contributing to seedlings, or other factors favoring the establishment of backcrosses towards B. crispa. However, further research will be needed to confirm these observations, as the small number of plants used for the pollination experiments could have introduced an artifact, for example if used individuals were more or less compatible than the species average, and also the small number of loci used could convey a picture of introgression that is not representative for the whole genome.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0539-9) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0539-9
PMCID: PMC4470074  PMID: 26081944
Asymmetric introgression; Buddleja; Hybridization; Nuclear genes; Reproductive isolation
48.  Effect of temperature stress on the early vegetative development of Brassica oleracea L. 
BMC Plant Biology  2015;15:145.
Background
Due to its biennual life cycle Brassica oleracea is especially exposed to seasonal changes in temperature that could limit its growth and fitness. Thermal stress could limit plant growth, leaf development and photosynthesis. We evaluated the performance of two local populations of B. oleracea: one population of cabbage (B. oleracea capitata group) and one population of kale (B. oleracea acephala group) under limiting low and high temperatures.
Results
There were differences between crops and how they responded to high and low temperature stress. Low temperatures especially affect photosynthesis and fresh weight. Stomatal conductance and the leaf water content were dramatically reduced and plants produce smaller and thicker leaves. Under high temperatures there was a reduction of the weight that could be associated to a general impairment of the photosynthetic activity.
Conclusions
Although high temperatures significantly reduced the dry weight of seedlings, in general terms, low temperature had a higher impact in B. oleracea physiology than high temperature. Interestingly, our results suggest that the capitata population is less sensitive to changes in air temperature than the acephala population.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0535-0) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0535-0
PMCID: PMC4467057  PMID: 26077340
Brassica; Physiology; Photosynthesis; Thermal stress
49.  mirEX 2.0 - an integrated environment for expression profiling of plant microRNAs 
BMC Plant Biology  2015;15:144.
Background
MicroRNAs are the key post-transcriptional regulators of gene expression in development and stress responses. Thus, precisely quantifying the level of each particular microRNA is of utmost importance when studying the biology of any organism.
Description
The mirEX 2.0 web portal (http://www.combio.pl/mirex) provides a comprehensive platform for the exploration of microRNA expression data based on quantitative Real Time PCR and NGS sequencing experiments, covering various developmental stages, from wild-type to mutant plants. The portal includes mature and pri-miRNA expression levels detected in three plant species (Arabidopsis thaliana, Hordeum vulgare and Pellia endiviifolia), and in A. thaliana miRNA biogenesis pathway mutants. In total, the database contains information about the expression of 461 miRNAs representing 268 families. The data can be explored through the use of advanced web tools, including (i) a graphical query builder system allowing a combination of any given species, developmental stages and tissues, (ii) a modular presentation of the results in the form of thematic windows, and (iii) a number of user-friendly utilities such as a community-building discussion system and extensive tutorial documentation (e.g., tooltips, exemplary videos and presentations). All data contained within the mirEX 2.0 database can be downloaded for use in further applications in a context-based way from the result windows or from a dedicated web page.
Conclusions
The mirEX 2.0 portal provides the plant research community with easily accessible data and powerful tools for application in multi-conditioned analyses of miRNA expression from important plant species in different biological and developmental backgrounds.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0533-2) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0533-2
PMCID: PMC4490709  PMID: 26141515
microRNA; Gene expression; Database; Arabidopsis thaliana; Hordeum vulgare; Pellia endiviifolia
50.  Fungal endophytes of Vanilla planifolia across Réunion Island: isolation, distribution and biotransformation 
BMC Plant Biology  2015;15:142.
Background
The objective of the work was to characterize fungal endophytes from aerial parts of Vanilla planifolia. Also, to establish their biotransformation abilities of flavor-related metabolites. This was done in order to find a potential role of endophytes on vanilla flavors.
Results
Twenty three MOTUs were obtained, representing 6 fungal classes. Fungi from green pods were cultured on mature green pod based media for 30 days followed by 1H NMR and HPLC-DAD analysis. All fungi from pods consumed metabolized vanilla flavor phenolics. Though Fusarium proliferatum was recovered more often (37.6 % of the isolates), it is Pestalotiopsis microspora (3.0 %) that increased the absolute amounts (quantified by 1H NMR in μmol/g DW green pods) of vanillin (37.0 × 10−3), vanillyl alcohol (100.0 × 10−3), vanillic acid (9.2 × 10−3) and p-hydroxybenzoic acid (87.9 × 10−3) by significant amounts.
Conclusions
All plants studied contained endophytic fungi and the isolation of the endophytes was conducted from plant organs at nine sites in Réunion Island including under shade house and undergrowth conditions. Endophytic variation occured between cultivation practices and the type of organ. Given the physical proximity of fungi inside pods, endophytic biotransformation may contribute to the complexity of vanilla flavors.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-015-0522-5) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-015-0522-5
PMCID: PMC4465486  PMID: 26070309
Endophytes; Distribution; Diversity; Biotransformation; Vanilla; Interaction

Results 26-50 (2173)