Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

    Full text documents are added when available. The database is updated daily and currently holds about 240,000 items, of which 72,000 in open access.

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    Understanding plant immunity as a surveillance system to detect invasion
    Cook III, D.E. ; Mesarich, C.H. ; Thomma, B.P.H.J. - \ 2015
    Annual Review of Phytopathology 53 (2015). - ISSN 0066-4286 - p. 541 - 563.
    disease-resistance gene - bacterial elicitor flagellin - syringae effectors avrb - host-selective toxins - innate immunity - arabidopsis-thaliana - molecular-patterns - microbe interactions - durable resistance - necrotrophic pathogens
    Various conceptual models to describe the plant immune system have been presented. The most recent paradigm to gain wide acceptance in the field is often referred to as the zigzag model, which reconciles the previously formulated gene-for-gene hypothesis with the recognition of general elicitors in a single model. This review focuses on the limitations of the current paradigm of molecular plant-microbe interactions and how it too narrowly defines the plant immune system. As such, we discuss an alternative view of plant innate immunity as a system that evolves to detect invasion. This view accommodates the range from mutualistic to parasitic symbioses that plants form with diverse organisms, as well as the spectrum of ligands that the plant immune system perceives. Finally, how this view can contribute to the current practice of resistance breeding is discussed.
    DOG1-imposed dormancy mediates germination responses to temperature cues
    Murphey, M. ; Kovach, K. ; Elnacash, T. ; He, H. ; Bentsink, L. ; Donohue, K. - \ 2015
    Environmental and Experimental Botany 112 (2015). - ISSN 0098-8472 - p. 33 - 43.
    seed-maturation environment - quantitative trait locus - recent climate-change - arabidopsis-thaliana - life-history - ectopic expression - niche construction - natural-selection - dog1-like genes - dog1
    Seed dormancy and environment-dependent germination requirements interact to determine the timing of germination in natural environments. This study tested the contribution of the dormancy gene Delay Of Germination 1 (DOG1) to primary and secondary dormancy induction in response to environmental cues, and evaluated how DOG1-mediated dormancy influenced germination responses to different temperature cues. We verified that DOG1 is involved in the induction of primary dormancy in response to cool seed-maturation temperature experienced by maternal plants, and we found that it is also involved in secondary dormancy in response to warm and prolonged cold stratification experienced by seeds during imbibition. DOG1-imposed dormancy can also mediate germination responses to environmental conditions, including cold stratification and germination temperatures experienced by imbibing seeds. Specifically, germination responsiveness to temperature cues is most apparent when seeds exhibit an intermediate degree of dormancy. However, DOG1 itself does not seem to directly regulate the response to cold stratification nor does it determine the function of temperature-dependent germination, since DOG1 mutants were capable of exhibiting increased germination after cold stratification as well as temperature-dependent germination. Instead, DOG1 has major effects on germination behavior primarily by exposing or masking underlying environmental sensitivity, and thereby strongly influences how environmentally responsive germination can be, and when during a season, it is likely to exhibit environmental sensitivity.
    Organizer-Derived WOX5 Signal Maintains Root Columella Stem Cells through Chromatin-Mediated Repression of CDF4 Expression.
    Pi, L. ; Graaff, E. van der; Llavata Peris, C.I. ; Weijers, D. ; Henning, L. ; Groot, E. de; Laux, T. - \ 2015
    Developmental Cell 33 (2015)5. - ISSN 1534-5807 - p. 576 - 588.
    histone deacetylase - arabidopsis-thaliana - transcriptional repression - gene-expression - wuschel - meristem - shoot - topless - protein - fate
    Stem cells in plants and animals are maintained pluripotent by signals from adjacent niche cells. In plants, WUSCHEL HOMEOBOX (WOX) transcription factors are central regulators of stem cell maintenance in different meristem types, yet their molecular mode of action has remained elusive. Here we show that in the Arabidopsis root meristem, the WOX5 protein moves from the root niche organizer, the quiescent center, into the columella stem cells, where it directly represses the transcription factor gene CDF4. This creates a gradient of CDF4 transcription, which promotes differentiation opposite to the WOX5 gradient, allowing stem cell daughter cells to exit the stem cell state. We further show that WOX5 represses CDF4 transcription by recruiting TPL/TPR co-repressors and the histone deacetylase HDA19, which consequently induces histone deacetylation at the CDF4 regulatory region. Our results show that chromatin-mediated repression of differentiation programs is a common strategy in plant and animal stem cell niches.
    Large-Scale Phenomics Identifies Primary and Fine-Tuning Roles for CRKs in Responses Related to Oxidative Stress.
    Bourdais, G. ; Burdiak, P. ; Gauthier, A. ; Nitsch, L.M.C. ; Salojärvi, J. ; Rayapuram, C. ; Idänheimo, N. ; Hunter, K. ; Kimura, S. ; Merilo, E. ; Vaattovaara, A. ; Oracz, K. ; Kaufholdt, D. ; Pallon, A. ; Anggoro, D.T. ; Glów, D. ; Lowe, J. ; Zhou, J. ; Mohammadi, O. ; Puukko, T. ; Albert, A. ; Lang, H. ; Ernst, D. ; Kollist, H. ; Brosché, M. ; Durner, J. ; Borst, J.W. ; Collinge, D.B. ; Karpinski, S. ; Lyngkjær, M.F. ; Robatzek, S. ; Wrzaczek, M. ; Kangasjärvi, J. - \ 2015
    Plos Genetics 11 (2015)7. - ISSN 1553-7404
    receptor-like kinase - multiple sequence alignment - arabidopsis-thaliana - cell-death - protein-kinase - transcriptional regulation - pseudomonas-syringae - flagellin perception - light acclimation - stomatal immunity
    Cysteine-rich receptor-like kinases (CRKs) are transmembrane proteins characterized by the presence of two domains of unknown function 26 (DUF26) in their ectodomain. The CRKs form one of the largest groups of receptor-like protein kinases in plants, but their biological functions have so far remained largely uncharacterized. We conducted a large-scale phenotyping approach of a nearly complete crk T-DNA insertion line collection showing that CRKs control important aspects of plant development and stress adaptation in response to biotic and abiotic stimuli in a non-redundant fashion. In particular, the analysis of reactive oxygen species (ROS)-related stress responses, such as regulation of the stomatal aperture, suggests that CRKs participate in ROS/redox signalling and sensing. CRKs play general and fine-tuning roles in the regulation of stomatal closure induced by microbial and abiotic cues. Despite their great number and high similarity, large-scale phenotyping identified specific functions in diverse processes for many CRKs and indicated that CRK2 and CRK5 play predominant roles in growth regulation and stress adaptation, respectively. As a whole, the CRKs contribute to specificity in ROS signalling. Individual CRKs control distinct responses in an antagonistic fashion suggesting future potential for using CRKs in genetic approaches to improve plant performance and stress tolerance.
    Strigolactones, a Novel Carotenoid-Derived Plant Hormone
    Al-Babili, S. ; Bouwmeester, H.J. - \ 2015
    Annual Review of Plant Biology 66 (2015). - ISSN 1543-5008 - p. 161 - 186.
    arbuscular mycorrhizal symbiosis - low phosphorus availability - abscisic-acid biosynthesis - in-vitro characterization - cytochrome b(6)f complex - root-system architecture - tiller bud outgrowth - box protein max2 - germination stimulants - arabidopsis-thaliana
    Strigolactones (SLs) are carotenoid-derived plant hormones and signaling molecules. When released into the soil, SLs indicate the presence of a host to symbiotic fungi and root parasitic plants. In planta, they regulate several developmental processes that adapt plant architecture to nutrient availability. Highly branched/tillered mutants in Arabidopsis, pea, and rice have enabled the identification of four SL biosynthetic enzymes: a cis/trans-carotene isomerase, two carotenoid cleavage dioxygenases, and a cytochrome P450 (MAX1). In vitro and in vivo enzyme assays and analysis of mutants have shown that the pathway involves a combination of new reactions leading to carlactone, which is converted by a rice MAX1 homolog into an SL parent molecule with a tricyclic lactone moiety. In this review, we focus on SL biosynthesis, describe the hormonal and environmental factors that determine this process, and discuss SL transport and downstream signaling as well as the role of SLs in regulating plant development.
    Large-scale evolutionary analysis of genes and supergene clusters from terpenoid modular pathways provides insights into metabolic diversification in flowering plants.
    Hofberger, J.A. ; Ramirez, A.M. ; Bergh, E. van den; Zhu, X. ; Bouwmeester, H.J. ; Schuurink, R.C. ; Schranz, M.E. - \ 2015
    PLoS ONE 10 (2015)6. - ISSN 1932-6203 - 37 p.
    isopentenyl diphosphate isomerases - disease resistance genes - arabidopsis-thaliana - genome sequence - whole-genome - protein families - draft genome - isoprenoid biosynthesis - secondary metabolism - oxidosqualene cyclase
    An important component of plant evolution is the plethora of pathways producing more than 200,000 biochemically diverse specialized metabolites with pharmacological, nutritional and ecological significance. To unravel dynamics underlying metabolic diversification, it is critical to determine lineage-specific gene family expansion in a phylogenomics framework. However, robust functional annotation is often only available for core enzymes catalyzing committed reaction steps within few model systems. In a genome informatics approach, we extracted information from early-draft gene-space assemblies and non-redundant transcriptomes to identify protein families involved in isoprenoid biosynthesis. Isoprenoids comprise terpenoids with various roles in plant-environment interaction, such as pollinator attraction or pathogen defense. Combining lines of evidence provided by synteny, sequence homology and Hidden-Markov-Modelling, we screened 17 genomes including 12 major crops and found evidence for 1,904 proteins associated with terpenoid biosynthesis. Our terpenoid genes set contains evidence for 840 core terpene-synthases and 338 triterpene-specific synthases. We further identified 190 prenyltransferases, 39 isopentenyl-diphosphate isomerases as well as 278 and 219 proteins involved in mevalonate and methylerithrol pathways, respectively. Assessing the impact of gene and genome duplication to lineage-specific terpenoid pathway expansion, we illustrated key events underlying terpenoid metabolic diversification within 250 million years of flowering plant radiation. By quantifying Angiosperm-wide versatility and phylogenetic relationships of pleiotropic gene families in terpenoid modular pathways, our analysis offers significant insight into evolutionary dynamics underlying diversification of plant secondary metabolism. Furthermore, our data provide a blueprint for future efforts to identify and more rapidly clone terpenoid biosynthetic genes from any plant species.
    The epigenetic footprint of poleward range-expanding plants in apomictic dandelions
    Preite, V. ; Snoek, L.B. ; Oplaat, C. ; Biere, A. ; Putten, W.H. van der; Verhoeven, K.J.F. - \ 2015
    Molecular Ecology 24 (2015)17. - ISSN 0962-1083 - p. 4406 - 4418.
    dna methylation polymorphism - arabidopsis-thaliana - geographic parthenogenesis - ecological epigenetics - phenotypic plasticity - cytosine methylation - population-structure - japanese knotweed - common dandelion - taraxacum
    Epigenetic modifications, such as DNA methylation variation, can generate heritable phenotypic variation independent of the underlying genetic code. However, epigenetic variation in natural plant populations is poorly documented and little understood. Here, we test if northward range expansion of obligate apomicts of the common dandelion (Taraxacum officinale) is associated with DNA methylation variation. We characterized and compared patterns of genetic and DNA-methylation variation in greenhouse-reared offspring of T. officinale that were collected along a latitudinal transect of northward range expansion in Europe. Genetic AFLP and epigenetic MS-AFLP markers revealed high levels of local diversity and modest but significant heritable differentiation between sampling locations and between the Southern, Central and Northern regions of the transect. Patterns of genetic and epigenetic variation were significantly correlated, reflecting the genetic control over epigenetic variation and/or the accumulation of lineage-specific spontaneous epimutations, which may be selectively neutral. In addition, we identified a small component of DNA methylation differentiation along the transect that is independent of genetic variation. This epigenetic differentiation might reflect environment-specific induction or, in case the DNA methylation variation affects relevant traits and fitness, selection of heritable DNA methylation variants. Such generated epigenetic variants might contribute to the adaptive capacity of individual asexual lineages under changing environments. Our results highlight the potential of heritable DNA methylation variation to contribute to population differentiation along ecological gradients. Further studies are needed using higher-resolution methods to understand the functional significance of such natural occurring epigenetic differentiation.
    Genome-Wide Mapping of Structural Variations Reveals a Copy Number Variant That Determines Reproductive Morphology in Cucumber
    Zhang, Z. ; Mao, L. ; Chen, Junshi ; Bu, F. ; Li, G. ; Sun, J. ; Li, S. ; Sun, H. ; Jiao, C. ; Blakely, R. ; Pan, J. ; Cai, R. ; Luo, R. ; Peer, Y. Van de; Jacobsen, E. ; Fei, Z. ; Huang, S. - \ 2015
    The Plant Cell 27 (2015)6. - ISSN 1040-4651 - p. 1595 - 1604.
    indel-associated mutation - tuberculate fruit gene - false discovery rate - arabidopsis-thaliana - population-scale - functional impact - sequencing data - synthase gene - paired-end - sativus l.
    Structural variations (SVs) represent a major source of genetic diversity. However, the functional impact and formation mechanisms of SVs in plant genomes remain largely unexplored. Here, we report a nucleotide-resolution SV map of cucumber (Cucumis sativas) that comprises 26,788 SVs based on deep resequencing of 115 diverse accessions. The largest proportion of cucumber SVs was formed through nonhomologous end-joining rearrangements, and the occurrence of SVs is closely associated with regions of high nucleotide diversity. These SVs affect the coding regions of 1676 genes, some of which are associated with cucumber domestication. Based on the map, we discovered a copy number variation (CNV) involving four genes that defines the Female (F) locus and gives rise to gynoecious cucumber plants, which bear only female flowers and set fruit at almost every node. The CNV arose from a recent 30.2-kb duplication at a meiotically unstable region, likely via microhomology-mediated break-induced replication. The SV set provides a snapshot of structural variations in plants and will serve as an important resource for exploring genes underlying key traits and for facilitating practical breeding in cucumber.
    Immune activation mediated by the late blight resistance protein R1 requires nuclear localization of R1 and AVR1
    Du, Y. ; Berg, J. ; Govers, F. ; Bouwmeester, K. - \ 2015
    New Phytologist 207 (2015)3. - ISSN 0028-646X - p. 735 - 747.
    disease-resistance - phytophthora-infestans - arabidopsis-thaliana - innate immunity - plant immunity - receptor - recognition - potato - gene - component
    Resistance against oomycete pathogens is mainly governed by intracellular nucleotide-binding leucine-rich repeat (NLR) receptors that recognize matching avirulence (AVR) proteins from the pathogen, RXLR effectors that are delivered inside host cells. Detailed molecular understanding of how and where NLR proteins and RXLR effectors interact is essential to inform the deployment of durable resistance (R) genes. Fluorescent tags, nuclear localization signals (NLSs) and nuclear export signals (NESs) were exploited to determine the subcellular localization of the potato late blight protein R1 and the Phytophthora infestans RXLR effector AVR1, and to target these proteins to the nucleus or cytoplasm. Microscopic imaging revealed that both R1 and AVR1 occurred in the nucleus and cytoplasm, and were in close proximity. Transient expression of NLS- or NES-tagged R1 and AVR1 in Nicotiana benthamiana showed that activation of the R1-mediated hypersensitive response and resistance required localization of the R1/AVR1 pair in the nucleus. However, AVR1-mediated suppression of cell death in the absence of R1 was dependent on localization of AVR1 in the cytoplasm. Balanced nucleocytoplasmic partitioning of AVR1 seems to be a prerequisite. Our results show that R1-mediated immunity is activated inside the nucleus with AVR1 in close proximity and suggest that nucleocytoplasmic transport of R1 and AVR1 is tightly regulated.
    Remarkably divergent regions punctuate the genome assembly of the Caenorhabditis elegans Hawaiian strain CB4856
    Thompson, O.A. ; Snoek, L.B. ; Nijveen, H. ; Sterken, M.G. ; Volkers, R.J.M. ; Brenchley, R. ; Hof, A. van 't; Bevers, R.P.J. ; Cossins, A.R. ; Yanai, I. ; Hajnal, A. ; Schmid, T. ; Perkins, J.D. ; Spencer, D. ; Kruglyak, L. ; Andersen, E.C. ; Moerman, D.G. ; Hillier, L.W. ; Kammenga, J.E. ; Waterston, R.H. - \ 2015
    Genetics 200 (2015)3. - ISSN 0016-6731 - p. 975 - 989.
    natural variation data - c. elegans - arabidopsis-thaliana - gene - polymorphism - populations - diversity - nematodes - dna - evolutionary
    The Hawaiian strain (CB4856) of Caenorhabditis elegans is one of the most divergent from the canonical laboratory strain N2 and has been widely used in developmental, population and evolutionary studies. To enhance the utility of the strain, we have generated a draft sequence of the CB4856 genome, exploiting a variety of resources and strategies. The CB4856 genome when compared against the N2 reference has 327,050 single nucleotide variants (SNVs) and 79,529 insertion-deletion events (indels) that result in a total of 3.3 megabasepairs (Mb) of N2 sequence missing from CB4856 and 1.4 Mb of sequence present in CB4856 not present in N2. As previously reported, the density of SNVs varies along the chromosomes, with the arms of chromosomes showing greater average variation than the centers. In addition, we find 61 regions totaling 2.8 Mb, distributed across all six chromosomes, that have a greatly elevated SNV density, ranging from 2% to 16% SNVs. A survey of other wild isolates show that the two alternative haplotypes for each region are widely distributed, suggesting they have been maintained by balancing selection over long evolutionary times. These divergent regions contain an abundance of genes from large rapidly evolving families encoding F-box, MATH, BATH, seven-transmembrane G-coupled receptors, and nuclear hormone receptors suggesting that they provide selective advantages in natural environments. The draft sequence makes available a comprehensive catalog of sequence differences between the CB4856 and N2 strains that will facilitate the molecular dissection of their phenotypic differences. Our work also emphasizes the importance of going beyond simple alignment of reads to a reference genome when assessing differences between genomes.
    Variation in plant-mediated interactions between rhizobacteria and caterpillars: potential role of soil composition
    Pangesti, N.P.D. ; Pineda Gomez, A.M. ; Dicke, M. ; Loon, J.J.A. van - \ 2015
    Plant Biology 17 (2015)2. - ISSN 1435-8603 - p. 474 - 483.
    induced systemic resistance - arbuscular mycorrhizal symbiosis - arabidopsis-thaliana - insect herbivores - gene-expression - jasmonic acid - pseudomonas-fluorescens - microbes - bacteria - immunity
    Selected strains of non-pathogenic rhizobacteria can trigger induced systemic resistance (ISR) in plants against aboveground insect herbivores. However, the underlying mechanisms of plant-mediated interactions between rhizobacteria and herbivorous insects are still poorly understood. Using Arabidopsis thaliana Col-0-Pseudomonas fluorescens WCS417r as a model system, we investigated the performance and the molecular mechanisms underlying plant-mediated effects of rhizobacteria on the generalist caterpillar Mamestra brassicae and the specialist Pieris brassicae. Rhizobacteria colonisation of Arabidopsis roots resulted in decreased larval weight of M. brassicae, whereas no effect was observed on larval weight of P. brassicae. Using a jasmonic acid (JA)-impaired mutant (dde2-2), we confirmed the importance of JA in rhizobacteria-mediated ISR against M. brassicae. Interestingly, in some experiments we also observed rhizobacteria-induced systemic susceptibility to M. brassicae. The role of soil composition in the variable outcomes of microbe-plant-insect interactions was then assessed by comparing M. brassicae performance and gene transcription in plants grown in potting soil or a mixture of potting soil and sand in a 1:1 ratio. In a mixture of potting soil and sand, rhizobacteria treatment had a consistent negative effect on M. brassicae, whereas the effect was more variable in potting soil. Interestingly, at 24 h post-infestation (hpi) rhizobacteria treatment primed plants grown in a mixture of potting soil and sand for stronger expression of the JA- and ethylene-regulated genes PDF1.2 and HEL, respectively. Our study shows that soil composition can modulate rhizobacteria-plant-insect interactions, and is a factor that should be considered when studying these belowground-aboveground interactions.
    Genetic basis and detection of unintended effects in genetically modified crop plants
    Ladics, G.S. ; Bartholomaeus, A. ; Bregitzer, P. ; Doerrer, N.G. ; Gray, A. ; Holzhauzer, T. ; Jordan, M. ; Keese, P. ; Kok, E.J. ; Macdonald, P. ; Parrott, W. ; Privalle, L. ; Raybould, A. ; Rhee, S.Y. ; Rice, E. ; Romeis, J. ; Vaughn, J. ; Wal, J.M. ; Glenn, K. - \ 2015
    Transgenic Research 24 (2015)4. - ISSN 0962-8819 - p. 587 - 603.
    weed risk-assessment - biochemical pathway database - engineered breeding stacks - multiple fungal pathogens - metabolic flux analysis - somaclonal variation - safety assessment - intellectual disability - arabidopsis-thaliana - transgenic barley
    In January 2014, an international meeting sponsored by the International Life Sciences Institute/Health and Environmental Sciences Institute and the Canadian Food Inspection Agency titled “Genetic Basis of Unintended Effects in Modified Plants” was held in Ottawa, Canada, bringing together over 75 scientists from academia, government, and the agro-biotech industry. The objectives of the meeting were to explore current knowledge and identify areas requiring further study on unintended effects in plants and to discuss how this information can inform and improve genetically modified (GM) crop risk assessments. The meeting featured presentations on the molecular basis of plant genome variability in general, unintended changes at the molecular and phenotypic levels, and the development and use of hypothesis-driven evaluations of unintended effects in assessing conventional and GM crops. The development and role of emerging “omics” technologies in the assessment of unintended effects was also discussed. Several themes recurred in a number of talks; for example, a common observation was that no system for genetic modification, including conventional methods of plant breeding, is without unintended effects. Another common observation was that “unintended” does not necessarily mean “harmful”. This paper summarizes key points from the information presented at the meeting to provide readers with current viewpoints on these topics.
    A complex interplay of tandem- and whole genome duplication drives expansion of the L-type lectin receptor kinase gene family in the brassicaceae
    Hofberger, J.A. ; Nsibo, D.L. ; Govers, F. ; Bouwmeester, K. ; Schranz, M.E. - \ 2015
    Genome Biology and Evolution 7 (2015)3. - ISSN 1759-6653 - p. 720 - 734.
    disease resistance genes - arabidopsis-thaliana - phylogenetic analysis - triggered immunity - provides insight - wide analysis - evolution - plants - diversification - expression
    The comparative analysis of plant gene families in a phylogenetic framework has greatly accelerated due to advances in next generation sequencing. In this study, we provide an evolutionary analysis of the L-type lectin receptor kinase and L-type lectin domain proteins (L-type LecRKs and LLPs) that are considered as components in plant immunity, in the plant family Brassicaceae and related outgroups. We combine several lines of evidence provided by sequence homology, HMM-driven protein domain annotation, phylogenetic analysis and gene synteny for large-scale identification of L-type LecRK and LLP genes within nine core-eudicot genomes. We show that both polyploidy and local duplication events (tandem duplication and gene transposition duplication) have played a major role in L-type LecRK and LLP gene family expansion in the Brassicaceae. We also find significant differences in rates of molecular evolution based on the mode of duplication. Additionally, we show that LLPs share a common evolutionary origin with L-type LecRKs and provide a consistent gene family nomenclature. Finally, we demonstrate that the largest and most diverse L-type LecRK clades are lineage-specific. Our evolutionary analyses of these plant immune components provide a framework to support future plant resistance breeding.
    Isolation and identification of 4-a-rhamnosyloxy benzyl glucosinolate in Noccaea caerulescens showing intraspecific variation
    Graaf, R.M. de; Krosse, S. ; Swolfs, A.E.M. ; Brinke, E. te; Prill, N. ; Leimu, R. ; Galen, P.M. van; Wang, Y. ; Aarts, M.G.M. ; Dam, N.M. van - \ 2015
    Phytochemistry 110 (2015). - ISSN 0031-9422 - p. 166 - 171.
    hyperaccumulator thlaspi-praecox - moringa-oleifera l. - mustard oil bomb - arabidopsis-thaliana - plants - isothiocyanates - stenopetala - accumulation - brassicaceae - profiles
    Glucosinolates are secondary plant compounds typically found in members of the Brassicaceae and a few other plant families. Usually each plant species contains a specific subset of the ~130 different glucosinolates identified to date. However, intraspecific variation in glucosinolate profiles is commonly found. Sinalbin (4-hydroxybenzyl glucosinolate) so far has been identified as the main glucosinolate of the heavy metal accumulating plant species Noccaea caerulescens (Brassicaceae). However, a screening of 13 N. caerulescens populations revealed that in 10 populations a structurally related glucosinolate was found as the major component. Based on nuclear magnetic resonance (NMR) and mass spectrometry analyses of the intact glucosinolate as well as of the products formed after enzymatic conversion by sulfatase or myrosinase, this compound was identified as 4-a-rhamnosyloxy benzyl glucosinolate (glucomoringin). So far, glucomoringin had only been reported as the main glucosinolate of Moringa spp. (Moringaceae) which are tropical tree species. There was no apparent relation between the level of soil pollution at the location of origin, and the presence of glucomoringin. The isothiocyanate that is formed after conversion of glucomoringin is a potent antimicrobial and antitumor agent. It has yet to be established whether glucomoringin or its breakdown product have an added benefit to the plant in its natural habitat
    AIL and HDG proteins act antagonistically to control cell proliferation
    Horstman, A. ; Fukuoka, H. ; Muino Acuna, J.M. ; Nitsch, L.M.C. ; Guo, Changhao ; Passarinho, P.A. ; Sanchez Perez, G.F. ; Immink, R.G.H. ; Angenent, G.C. ; Boutilier, K.A. - \ 2015
    Development 142 (2015). - ISSN 0950-1991 - p. 454 - 464.
    arabidopsis-thaliana - transcription factors - plant transformation - ectopic expression - quantitative pcr - chip-seq - differentiation - genes - plethora - growth
    AINTEGUMENTA-LIKE (AIL) transcription factors are key regulators of cell proliferation and meristem identity. Although AIL functions have been well described, the direct signalling components of this pathway are largely unknown.We show that BABY BOOM(BBM) and other AIL proteins physically interact with multiple members of the L1-expressed HOMEODOMAIN GLABROUS (HDG) transcription factor family, including HDG1, HDG11 and HDG12. Overexpression of HDG1, HDG11 and HDG12 restricts growth due to root and shoot meristem arrest, which is associated with reduced expression of genes involved in meristem development and cell proliferation pathways, whereas downregulation of multiple HDG genes promotes cell overproliferation. These results suggest a role for HDG proteins in promoting cell differentiation. We also reveal a transcriptional network in which BBM andHDG1regulate several common target genes, and whereBBM/AIL and HDG regulate the expression of each other. Taken together, these results suggest opposite roles for AIL and HDG proteins, with AILs promoting cell proliferation and HDGs stimulating cell differentiation, and that these functions are mediated at both the protein-protein interaction and transcriptional level.
    Marker-Based Estimation of Heritability in Immortal Populations
    Kruijer, W.T. ; Boer, M.P. ; Malosetti, M. ; Flood, P.J. ; Engel, B. ; Kooke, R. ; Keurentjes, J.J.B. ; Eeuwijk, F.A. van - \ 2015
    Genetics 199 (2015)2. - ISSN 0016-6731 - p. 379 - 398.
    genome-wide association - multi-environment trials - quantitative trait loci - plant-breeding trials - linear mixed models - arabidopsis-thaliana - missing heritability - complex traits - selection - prediction
    Heritability is a central parameter in quantitative genetics, both from an evolutionary and a breeding perspective. For plant traits heritability is traditionally estimated by comparing within and between genotype variability. This approach estimates broad-sense heritability, and does not account for different genetic relatedness. With the availability of high-density markers there is growing interest in marker based estimates of narrow-sense heritability, using mixed models in which genetic relatedness is estimated from genetic markers. Such estimates have received much attention in human genetics but are rarely reported for plant traits. A major obstacle is that current methodology and software assume a single phenotypic value per genotype, hence requiring genotypic means. An alternative that we propose here, is to use mixed models at individual plant or plot level. Using statistical arguments, simulations and real data we investigate the feasibility of both approaches, and how these affect genomic prediction with G-BLUP and genome-wide association studies. Heritability estimates obtained from genotypic means had very large standard errors and were sometimes biologically unrealistic. Mixed models at individual plant or plot level produced more realistic estimates, and for simulated traits standard errors were up to 13 times smaller. Genomic prediction was also improved by using these mixed models, with up to a 49% increase in accuracy. For GWAS on simulated traits, the use of individual plant data gave almost no increase in power. The new methodology is applicable to any complex trait where multiple replicates of individual genotypes can be scored. This includes important agronomic crops, as well as bacteria and fungi.
    Fruit illumination stimulates cell division but has no detectable effect on fruit size in tomato (Solanum lycopersicum)
    Okello, R.C. ; Heuvelink, E. ; Visser, P.H.B. de; Lammers, M. ; Maagd, R.A. de; Marcelis, L.F.M. ; Struik, P.C. - \ 2015
    Physiologia Plantarum 154 (2015)1. - ISSN 0031-9317 - p. 114 - 127.
    arabidopsis-thaliana - elongation growth - plant development - seed development - sink metabolism - cucumber fruits - gene-expression - hormone-levels - abscisic-acid - phytochrome-b
    Light affects plant growth through assimilate availability and signals regulating development. The effects of light on growth of tomato fruit were studied using cuvettes with light-emitting diodes providing white, red or blue light to individual tomato trusses for different periods during daytime. Hypotheses tested were as follows: (1) light-grown fruits have stronger assimilate sinks than dark-grown fruits, and (2) responses depend on light treatment provided, and fruit development stage. Seven light treatments [dark, 12-h white, 24-h white, 24-h red and 24-h blue light, dark in the first 24 days after anthesis (DAA) followed by 24-h white light until breaker stage, and its reverse] were applied. Observations were made between anthesis and breaker stage at fruit, cell and gene levels. Fruit size and carbohydrate content did not respond to light treatments while cell division was strongly stimulated at the expense of cell expansion by light. The effects of light on cell number and volume were independent of the combination of light color and intensity. Increased cell division and decreased cell volume when fruits were grown in the presence of light were not clearly corroborated by the expression pattern of promoters and inhibitors of cell division and expansion analyzed in this study, implying a strong effect of posttranscriptional regulation. Results suggest the existence of a complex homeostatic regulatory system for fruit growth in which reduced cell division is compensated by enhanced cell expansion.
    The Top 10 oomycete pathogens in molecular plant pathology
    Kamoun, S. ; Furzer, O. ; Jones, J.D.G. ; Judelson, H.S. ; Ali, G.S. ; Dalio, R.J.D. ; Roy, S.G. ; Schena, L. ; Zambounis, A. ; Panabières, F. ; Cahill, D. ; Ruocco, M. ; Figueiredo, A. ; Chen, X.R. ; Hulvey, J. ; Stam, R. ; Lamour, K. ; Gijzen, M. ; Tyler, B.M. ; Grünwald, N.J. ; Mukhtar, M.S. ; Tomé, D.F.A. ; Tör, M. ; Ackerveken, G. van den; McDowell, J. ; Daayf, F. ; Fry, W.E. ; Lindqvist-Kreuze, H. ; Meijer, H.J.G. ; Petre, B. ; Ristaino, J. ; Yoshida, K. ; Birch, P.R.J. ; Govers, F. - \ 2015
    Molecular Plant Pathology 16 (2015)4. - ISSN 1464-6722 - p. 413 - 434.
    grapevine downy mildew - irish potato famine - sudden oak death - blister rusts albuginaceae - eastern united-states - 3 clonal lineages - nb-lrr gene - phytophthora-infestans - plasmopara-viticola - arabidopsis-thaliana
    Oomycetes form a deep lineage of eukaryotic organisms that includes a large number of plant pathogens that threaten natural and managed ecosystems. We undertook a survey to query the community for their ranking of plant pathogenic oomycete species based on scientific and economic importance. In total, we received 263 votes from 62 scientists in 15 countries for a total of 33 species. The Top 10 species and their ranking are: (1) Phytophthora infestans; (2, tied) Hyaloperonospora arabidopsidis; (2, tied) Phytophthora ramorum; (4) Phytophthora sojae; (5) Phytophthora capsici; (6) Plasmopara viticola; (7) Phytophthora cinnamomi; (8, tied) Phytophthora parasitica; (8, tied) Pythium ultimum; and (10) Albugo candida. The article provides an introduction to these 10 taxa and a snapshot of current research. We hope that the list will serve as a benchmark for future trends in oomycete research.
    On selection for flowering time plasticity in response to density
    Vermeulen, P.J. - \ 2015
    New Phytologist 205 (2015)1. - ISSN 0028-646X - p. 429 - 439.
    arabidopsis-thaliana - phenotypic plasticity - shade-avoidance - adaptive plasticity - impatiens-capensis - dependent selection - plant-populations - genetic-variation - local adaptation - life-history
    Different genotypes often exhibit opposite plastic responses in the timing of the onset of flowering with increasing plant density. In experimental studies, selection for accelerated flowering is generally found. By contrast, game theoretical studies predict that there should be selection for delayed flowering when competition increases. Combining different optimality criteria, the conditions under which accelerated or delayed flowering in response to density would be selected for are analysed with a logistic growth simulation model. To maximize seed production at the whole-stand level (simple optimization), selection should lead to accelerated flowering at high plant density, unless very short growing seasons select for similar onset of flowering at all densities. By contrast, selection of relative individual fitness will lead to delayed flowering when season length is long and/or growth rates are high. These different results give a potential explanation for the observed differences in direction of the plastic responses within and between species, including homeostasis, as a result of the effect of the variation in season length on the benefits of delayed flowering. This suggests that limited plasticity can evolve without the costs and limits that are currently thought to constrain the evolution of plasticity.
    The Cellulase KORRIGAN Is Part of the Cellulose Synthase Complex
    Vain, T. ; Crowell, E.F. ; Timpano, H. ; Biot, E. ; Desprez, T. ; Mansoori Zangir, N. ; Trindade, L.M. ; Pagant, S. ; Robert, S. ; Hofte, H. ; Gonneau, M. ; Vernhettes, S. - \ 2014
    Plant Physiology 165 (2014)4. - ISSN 0032-0889 - p. 1521 - 1532.
    secondary cell-wall - arabidopsis-thaliana - genetic-evidence - plasma-membrane - higher-plants - endo-1,4-beta-glucanase - microtubules - trafficking - elongation - endo-1,4-beta-d-glucanase
    Plant growth and organ formation depend on the oriented deposition of load-bearing cellulose microfibrils in the cell wall. Cellulose is synthesized by a large relative molecular weight cellulose synthase complex (CSC), which comprises at least three distinct cellulose synthases. Cellulose synthesis in plants or bacteria also requires the activity of an endo-1,4-beta-D-glucanase, the exact function of which in the synthesis process is not known. Here, we show, to our knowledge for the first time, that a leaky mutation in the Arabidopsis (Arabidopsis thaliana) membrane-bound endo-1,4-beta-D-glucanase KORRIGAN1 (KOR1) not only caused reduced CSC movement in the plasma membrane but also a reduced cellulose synthesis inhibitor-induced accumulation of CSCs in intracellular compartments. This suggests a role for KOR1 both in the synthesis of cellulose microfibrils and in the intracellular trafficking of CSCs. Next, we used a multidisciplinary approach, including live cell imaging, gel filtration chromatography analysis, split ubiquitin assays in yeast (Saccharomyces cerevisiae NMY51), and bimolecular fluorescence complementation, to show that, in contrast to previous observations, KOR1 is an integral part of the primary cell wall CSC in the plasma membrane.
    Post-transcriptional control of GRF transcription factors by microRNA miR396 and GIF co-activator affects leaf size and longevity
    Debernardi, J.M. ; Mecchia, M.A. ; Vercruyssen, L. ; Smaczniak, C. ; Kaufmann, K. ; Inze, D. ; Rodriguez, R.E. ; Palatnik, J.F. - \ 2014
    The Plant Journal 79 (2014)3. - ISSN 0960-7412 - p. 413 - 426.
    chromatin-remodeling complexes - tandem affinity purification - arabidopsis-thaliana - gene-expression - organ size - cell-division - protein complexes - shoot development - small rnas - growth
    The growth-regulating factors (GRFs) are plant-specific transcription factors. They form complexes with GRF-interacting factors (GIFs), a small family of transcriptional co-activators. In Arabidopsis thaliana, seven out of the nine GRFs are controlled by microRNA miR396. Analysis of Arabidopsis plants carrying a GRF3 allele insensitive to miR396 revealed a strong boost in the number of cells in leaves, which was further enhanced synergistically by an additional increase of GIF1 levels. Genetic experiments revealed that GRF3 can still increase cell number in gif1 mutants, albeit to a much lesser extent. Genome-wide transcript profiling indicated that the simultaneous increase of GRF3 and GIF1 levels causes additional effects in gene expression compared to either of the transgenes alone. We observed that GIF1 interacts in vivo with GRF3, as well as with chromatin-remodeling complexes, providing a mechanistic explanation for the synergistic activities of a GRF3-GIF1 complex. Interestingly, we found that, in addition to the leaf size, the GRF system also affects the organ longevity. Genetic and molecular analysis revealed that the functions of GRFs in leaf growth and senescence can be uncoupled, demonstrating that the miR396-GRF-GIF network impinges on different stages of leaf development. Our results integrate the post-transcriptional control of the GRF transcription factors with the progression of leaf development.
    Conserved histidine of metal transporter AtNRAMP1 is crucial for optimal plant growth under manganese deficiency at chilling temperatures
    Ihnatowicz, A. ; Siwinska, J. ; Meharg, A.A. ; Carey, M. ; Koornneef, M. ; Reymond, M. - \ 2014
    New Phytologist 202 (2014)4. - ISSN 0028-646X - p. 1173 - 1183.
    yeast saccharomyces-cerevisiae - barley hordeum-vulgare - arabidopsis-thaliana - drosophila-melanogaster - iron transport - ion transporters - diploid strains - calcareous soil - nramp family - environment
    Manganese (Mn) is an essential nutrient required for plant growth, in particular in the process of photosynthesis. Plant performance is influenced by various environmental stresses including contrasting temperatures, light or nutrient deficiencies. The molecular responses of plants exposed to such stress factors in combination are largely unknown. Screening of 108 Arabidopsis thaliana (Arabidopsis) accessions for reduced photosynthetic performance at chilling temperatures was performed and one accession (Hog) was isolated. Using genetic and molecular approaches, the molecular basis of this particular response to temperature (GxE interaction) was identified. Hog showed an induction of a severe leaf chlorosis and impaired growth after transfer to lower temperatures. We demonstrated that this response was dependent on the nutrient content of the soil. Genetic mapping and complementation identified NRAMP1 as the causal gene. Chlorotic phenotype was associated with a histidine to tyrosine (H239Y) substitution in the allele of Hog NRAMP1. This led to lethality when Hog seedlings were directly grown at 4 degrees C. Chemical complementation and hydroponic culture experiments showed that Mn deficiency was the major cause of this GxE interaction. For the first time, the NRAMP-specific highly conserved histidine was shown to be crucial for plant performance.
    Drought stress provokes the down-regulation of methionine and ethylene biosynthesis pathways in Medicago truncatula roots and nodules
    Larrainzar, E. ; Molenaar, J.A. ; Wienkoop, S. ; Gil-Quintana, E. ; Alibert, B. ; Limami, A.M. ; Arrese-Igor, C. ; Gonzalez, E.M. - \ 2014
    Plant, Cell & Environment 37 (2014)9. - ISSN 0140-7791 - p. 2051 - 2063.
    cystathionine gamma-synthase - signal-transduction pathway - acetylene-reduction assay - nitrogen-fixation - n-2 fixation - arabidopsis-thaliana - sucrose synthase - soybean nodules - atp sulfurylase - water-deficit
    Symbiotic nitrogen fixation is one of the first physiological processes inhibited in legume plants under water-deficit conditions. Despite the progress made in the last decades, the molecular mechanisms behind this regulation are not fully understood yet. Recent proteomic work carried out in the model legume Medicago truncatula provided the first indications of a possible involvement of nodule methionine (Met) biosynthesis and related pathways in response to water-deficit conditions. To better understand this involvement, the drought-induced changes in expression and content of enzymes involved in the biosynthesis of Met, S-adenosyl-L-methionine (SAM) and ethylene in M.truncatula root and nodules were analyzed using targeted approaches. Nitrogen-fixing plants were subjected to a progressive water deficit and a subsequent recovery period. Besides the physiological characterization of the plants, the content of total sulphur, sulphate and main S-containing metabolites was measured. Results presented here show that S availability is not a limiting factor in the drought-induced decline of nitrogen fixation rates in M.truncatula plants and provide evidences for a down-regulation of the Met and ethylene biosynthesis pathways in roots and nodules in response to water-deficit conditions.
    KORRIGAN1 Interacts Specifically with Integral Components of the Cellulose Synthase Machinery
    Mansoori Zangir, N. ; Timmers, J.F.P. ; Desprez, T. ; Lessa Alvim Kamei, C. ; Dees, D.C.T. ; Vincken, J.P. ; Visser, R.G.F. ; Höfte, H. ; Vernhettes, S. ; Trindade, L.M. - \ 2014
    PLoS ONE 9 (2014)11. - ISSN 1932-6203
    secondary cell-wall - arabidopsis-thaliana - endo-1,4-beta-glucanase - expression - membranes - protein - system - plants - gene - endo-1,4-beta-d-glucanase
    Cellulose is synthesized by the so called rosette protein complex and the catalytic subunits of this complex are the cellulose synthases (CESAs). It is thought that the rosette complexes in the primary and secondary cell walls each contains at least three different non-redundant cellulose synthases. In addition to the CESA proteins, cellulose biosynthesis almost certainly requires the action of other proteins, although few have been identified and little is known about the biochemical role of those that have been identified. One of these proteins is KORRIGAN (KOR1). Mutant analysis of this protein in Arabidopsis thaliana showed altered cellulose content in both the primary and secondary cell wall. KOR1 is thought to be required for cellulose synthesis acting as a cellulase at the plasma membrane–cell wall interface. KOR1 has recently been shown to interact with the primary cellulose synthase rosette complex however direct interaction with that of the secondary cell wall has never been demonstrated. Using various methods, both in vitro and in planta, it was shown that KOR1 interacts specifically with only two of the secondary CESA proteins. The KOR1 protein domain(s) involved in the interaction with the CESA proteins were also identified by analyzing the interaction of truncated forms of KOR1 with CESA proteins. The KOR1 transmembrane domain has shown to be required for the interaction between KOR1 and the different CESAs, as well as for higher oligomer formation of KOR1.
    Genetic dissection of leaf development in Brassica rapa using a ‘geneticalgenomics’ approach
    Xiao, D. ; Wang, H. ; Basnet, R.K. ; Jianjun Zhao, Jianjun ; Lin, K. ; Hou, X. ; Bonnema, A.B. - \ 2014
    Plant Physiology 164 (2014)3. - ISSN 0032-0889 - p. 1309 - 1325.
    quantitative trait loci - flowering time - arabidopsis-thaliana - morphological traits - functional divergence - natural variation - duplicated genes - organ growth - expression - cell
    The paleohexaploid crop Brassica rapa harbors an enormous reservoir of morphological variation, encompassing leafy vegetables, vegetable and fodder turnips (Brassica rapa, ssp. campestris), and oil crops, with different crops having very different leaf morphologies. In the triplicated B. rapa genome, many genes have multiple paralogs that may be regulated differentially and contribute to phenotypic variation. Using a genetical genomics approach, phenotypic data from a segregating doubled haploid population derived from a cross between cultivar Yellow sarson (oil type) and cultivar Pak choi (vegetable type) were used to identify loci controlling leaf development. Twenty-five colocalized phenotypic quantitative trait loci (QTLs) contributing to natural variation for leaf morphological traits, leaf number, plant architecture, and flowering time were identified. Genetic analysis showed that four colocalized phenotypic QTLs colocalized with flowering time and leaf trait candidate genes, with their cis-expression QTLs and cis- or trans-expression QTLs for homologs of genes playing a role in leaf development in Arabidopsis (Arabidopsis thaliana). The leaf gene BRASSICA RAPA KIP-RELATED PROTEIN2_A03 colocalized with QTLs for leaf shape and plant height; BRASSICA RAPA ERECTA_A09 colocalized with QTLs for leaf color and leaf shape; BRASSICA RAPA LONGIFOLIA1_A10 colocalized with QTLs for leaf size, leaf color, plant branching, and flowering time; while the major flowering time gene, BRASSICA RAPA FLOWERING LOCUS C_A02, colocalized with QTLs explaining variation in flowering time, plant architectural traits, and leaf size. Colocalization of these QTLs points to pleiotropic regulation of leaf development and plant architectural traits in B. rapa.
    Prioritization of candidate genes in QTL regions based on associations between traits and biological processes
    Bargsten, J.W. ; Nap, J.P.H. ; Sanchez Perez, G.F. ; Dijk, A.D.J. van - \ 2014
    BMC Plant Biology 14 (2014). - ISSN 1471-2229
    genome-wide association - protein function prediction - arabidopsis-thaliana - nucleotide polymorphisms - enrichment analysis - flowering time - complex traits - oryza-sativa - rice - architecture
    Background Elucidation of genotype-to-phenotype relationships is a major challenge in biology. In plants, it is the basis for molecular breeding. Quantitative Trait Locus (QTL) mapping enables to link variation at the trait level to variation at the genomic level. However, QTL regions typically contain tens to hundreds of genes. In order to prioritize such candidate genes, we show that we can identify potentially causal genes for a trait based on overrepresentation of biological processes (gene functions) for the candidate genes in the QTL regions of that trait. Results The prioritization method was applied to rice QTL data, using gene functions predicted on the basis of sequence- and expression-information. The average reduction of the number of genes was over ten-fold. Comparison with various types of experimental datasets (including QTL fine-mapping and Genome Wide Association Study results) indicated both statistical significance and biological relevance of the obtained connections between genes and traits. A detailed analysis of flowering time QTLs illustrates that genes with completely unknown function are likely to play a role in this important trait. Conclusions Our approach can guide further experimentation and validation of causal genes for quantitative traits. This way it capitalizes on QTL data to uncover how individual genes influence trait variation.
    Regulatory Network of Secondary Metabolism in Brassica rapa: Insight into the Glucosinolate Pathway
    Pino del Carpio, D. ; Kumar, R. ; Arends, D. ; Lin, K. ; Vos, R.C.H. de; Muth, D. ; Kodde, J. ; Boutilier, K.A. ; Bucher, J. ; Wang, X. ; Jansen, R.C. ; Bonnema, G. - \ 2014
    PLoS ONE 9 (2014)9. - ISSN 1932-6203 - 11 p.
    arabidopsis-thaliana - mass-spectrometry - coexpression networks - genomics approach - genetic genomics - biosynthesis - metabolomics - identification - plants - fruit
    Brassica rapa studies towards metabolic variation have largely been focused on the profiling of the diversity of metabolic compounds in specific crop types or regional varieties, but none aimed to identify genes with regulatory function in metabolite composition. Here we followed a genetical genomics approach to identify regulatory genes for six biosynthetic pathways of health-related phytochemicals, i.e carotenoids, tocopherols, folates, glucosinolates, flavonoids and phenylpropanoids. Leaves from six weeks-old plants of a Brassica rapa doubled haploid population, consisting of 92 genotypes, were profiled for their secondary metabolite composition, using both targeted and LC-MS-based untargeted metabolomics approaches. Furthermore, the same population was profiled for transcript variation using a microarray containing EST sequences mainly derived from three Brassica species: B. napus, B. rapa and B. oleracea. The biochemical pathway analysis was based on the network analyses of both metabolite QTLs (mQTLs) and transcript QTLs (eQTLs). Colocalization of mQTLs and eQTLs lead to the identification of candidate regulatory genes involved in the biosynthesis of carotenoids, tocopherols and glucosinolates. We subsequently focused on the well-characterized glucosinolate pathway and revealed two hotspots of co-localization of eQTLs with mQTLs in linkage groups A03 and A09. Our results indicate that such a large-scale genetical genomics approach combining transcriptomics and metabolomics data can provide new insights into the genetic regulation of metabolite composition of Brassica vegetables.
    Morphology, Carbohydrate Composition and Vernalization Response in a Genetically Diverse Collection of Asian and European Turnips (Brassica rapa subsp. rapa)
    Zhang, N. ; Jianjun Zhao, Jianjun ; Lens, F. ; Visser, J. de; Menamo, T. ; Fang, W. ; Xiao, D. ; Bucher, J. ; Basnet, R.K. ; Lin, K. ; Cheng, F. ; Wang, X. ; Bonnema, A.B. - \ 2014
    PLoS ONE 9 (2014)12. - ISSN 1932-6203 - 29 p.
    storage root-formation - sucrose metabolizing enzymes - raphanus-sativus l - sugar-beet - flowering-time - gene-expression - transcriptome analysis - arabidopsis-thaliana - organ development - tuber development
    Brassica rapa displays enormous morphological diversity, with leafy vegetables, turnips and oil crops. Turnips (Brassica rapa subsp. rapa) represent one of the morphotypes, which form tubers and can be used to study the genetics underlying storage organ formation. In the present study we investigated several characteristics of an extensive turnip collection comprising 56 accessions from both Asia (mainly Japanese origin) and Europe. Population structure was calculated using data from 280 evenly distributed SNP markers over 56 turnip accessions. We studied the anatomy of turnip tubers and measured carbohydrate composition of the mature turnip tubers of a subset of the collection. The variation in 16 leaf traits, 12 tuber traits and flowering time was evaluated in five independent experiments for the entire collection. The effect of vernalization on flowering and tuber formation was also investigated. SNP marker profiling basically divided the turnip accessions into two subpopulations, with admixture, generally corresponding with geographical origin (Europe or Asia). The enlarged turnip tuber consists of both hypocotyl and root tissue, but the proportion of the two tissues differs between accessions. The ratio of sucrose to fructose and glucose differed among accessions, while generally starch content was low. The evaluated traits segregated in both subpopulations, with leaf shape, tuber colour and number of shoots per tuber explaining most variation between the two subpopulations. Vernalization resulted in reduced flowering time and smaller tubers for the Asian turnips whereas the European turnips were less affected by vernalization.
    Enhancing crop resilience to combined abiotic and biotic stress through the dissection of physiological and molecular crosstalk
    Kissoudis, C. ; Wiel, C.C.M. van de; Visser, R.G.F. ; Linden, C.G. van der - \ 2014
    Frontiers in Plant Science 5 (2014). - ISSN 1664-462X - 20 p.
    systemic acquired-resistance - activated protein-kinase - programmed cell-death - regulated gene-expression - plant immune-responses - abscisic-acid - salicylic-acid - disease resistance - arabidopsis-thaliana - transcription factor
    Plants growing in their natural habitats are often challenged simultaneously by multiple stress factors, both abiotic and biotic. Research has so far been limited to responses to individual stresses, and understanding of adaptation to combinatorial stress is limited, but indicative of non-additive interactions. Omics data analysis and functional characterization of individual genes has revealed a convergence of signaling pathways for abiotic and biotic stress adaptation. Taking into account that most data originate from imposition of individual stress factors, this review summarizes these findings in a physiological context, following the pathogenesis timeline and highlighting potential differential interactions occurring between abiotic and biotic stress signaling across the different cellular compartments and at the whole plant level. Potential effects of abiotic stress on resistance components such as extracellular receptor proteins, R-genes and systemic acquired resistance will be elaborated, as well as crosstalk at the levels of hormone, reactive oxygen species, and redox signaling. Breeding targets and strategies are proposed focusing on either manipulation and deployment of individual common regulators such as transcription factors or pyramiding of non- (negatively) interacting components such as R-genes with abiotic stress resistance genes. We propose that dissection of broad spectrum stress tolerance conferred by priming chemicals may provide an insight on stress cross regulation and additional candidate genes for improving crop performance under combined stress. Validation of the proposed strategies in lab and field experiments is a first step toward the goal of achieving tolerance to combinatorial stress in crops.
    Apoplastic Venom Allergen-like Proteins of Cyst Nematodes Modulate the Activation of Basal Plant Innate Immunity by Cell Surface Receptors
    Lozano Torres, J.L. ; Wilbers, R.H.P. ; Warmerdam, S. ; Finkers-Tomczak, A.M. ; Diaz Granados Muñoz, A. ; Schaik, C.C. van; Helder, J. ; Bakker, J. ; Goverse, A. ; Schots, A. ; Smant, G. - \ 2014
    PLoS Pathogens 10 (2014)12. - ISSN 1553-7366 - 18 p.
    root-knot nematode - cf-2-dependent disease resistance - pamp-triggered immunity - arabidopsis-thaliana - globodera-rostochiensis - heterodera-schachtii - ancylostoma-caninum - parasitic nematodes - extracellular-matrix - functional-analysis
    Despite causing considerable damage to host tissue during the onset of parasitism, nematodes establish remarkably persistent infections in both animals and plants. It is thought that an elaborate repertoire of effector proteins in nematode secretions suppresses damage-triggered immune responses of the host. However, the nature and mode of action of most immunomodulatory compounds in nematode secretions are not well understood. Here, we show that venom allergen-like proteins of plant-parasitic nematodes selectively suppress host immunity mediated by surface-localized immune receptors. Venom allergen-like proteins are uniquely conserved in secretions of all animal- and plant-parasitic nematodes studied to date, but their role during the onset of parasitism has thus far remained elusive. Knocking-down the expression of the venom allergen-like protein Gr-VAP1 severely hampered the infectivity of the potato cyst nematode Globodera rostochiensis. By contrast, heterologous expression of Gr-VAP1 and two other venom allergen-like proteins from the beet cyst nematode Heterodera schachtii in plants resulted in the loss of basal immunity to multiple unrelated pathogens. The modulation of basal immunity by ectopic venom allergen-like proteins in Arabidopsis thaliana involved extracellular protease-based host defenses and non-photochemical quenching in chloroplasts. Non-photochemical quenching regulates the initiation of the defense-related programmed cell death, the onset of which was commonly suppressed by venom allergen-like proteins from G. rostochiensis, H. schachtii, and the root-knot nematode Meloidogyne incognita. Surprisingly, these venom allergen-like proteins only affected the programmed cell death mediated by surface-localized immune receptors. Furthermore, the delivery of venom allergen-like proteins into host tissue coincides with the enzymatic breakdown of plant cell walls by migratory nematodes. We, therefore, conclude that parasitic nematodes most likely utilize venom allergen-like proteins to suppress the activation of defenses by immunogenic breakdown products in damaged host tissue.
    Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis
    Zhang, Y. ; Dijk, A.D.J. van; Scaffidi, A. ; Flematti, G.R. ; Hofmann, M. ; Charnikhova, T. ; Verstappen, F.W.A. ; Hepworth, J. ; Krol, A.R. van der; Leyser, O. - \ 2014
    Nature Chemical Biology 10 (2014). - ISSN 1552-4450 - p. 1028 - 1033.
    arbuscular mycorrhizal fungi - structural requirements - germination stimulants - biological-activities - arabidopsis-thaliana - crystal-structures - plant hormones - protein - inhibition - expression
    Strigolactones (SLs) are a class of phytohormones and rhizosphere signaling compounds with high structural diversity. Three enzymes, carotenoid isomerase DWARF27 and carotenoid cleavage dioxygenases CCD7 and CCD8, were previously shown to convert all-trans-¿-carotene to carlactone (CL), the SL precursor. However, how CL is metabolized to SLs has remained elusive. Here, by reconstituting the SL biosynthetic pathway in Nicotiana benthamiana, we show that a rice homolog of Arabidopsis MORE AXILLARY GROWTH 1 (MAX1), encodes a cytochrome P450 CYP711 subfamily member that acts as a CL oxidase to stereoselectively convert CL into ent-2'-epi-5-deoxystrigol (B-C lactone ring formation), the presumed precursor of rice SLs. A protein encoded by a second rice MAX1 homolog then catalyzes the conversion of ent-2'-epi-5-deoxystrigol to orobanchol. We therefore report that two members of CYP711 enzymes can catalyze two distinct steps in SL biosynthesis, identifying the first enzymes involved in B-C ring closure and a subsequent structural diversification step of SLs.
    Control of anthocyanin and non-flavonoid compounds by anthocyanin-regulating MYB and bHLH transcription factors in Nicotiana benthamiana leaves
    Outchkourov, N.S. ; Carollo, C.A. ; Gomez Roldan, M.V. ; Vos, C.H. de; Bosch, H.J. ; Hall, R.D. ; Beekwilder, M.J. - \ 2014
    Frontiers in Plant Science 5 (2014). - ISSN 1664-462X - 9 p.
    r2r3-myb gene family - mass-spectrometry - tomato fruit - arabidopsis-thaliana - biosynthesis - tobacco - accumulation - metabolomics - plants - health
    Coloration of plant organs such as fruit, leaves and flowers through anthocyanin production is governed by a combination of MYB and bHLH type transcription factors (TFs). In this study we introduced Rosea1 (ROS1, a MYB type) and Delila (DEL, a bHLH type), into Nicotiana benthamiana leaves by agroinfiltration. ROS1 and DEL form a pair of well-characterized TFs from Snapdragon (Antirrhinum majus), which specifically induce anthocyanin accumulation when expressed in tomato fruit. In N. benthamiana, robust induction of a single anthocyanin, delphinidin-3-rutinoside (D3R) was observed after expression of both ROS1 and DEL. Surprisingly in addition to D3R, a range of additional metabolites were also strongly and specifically up-regulated upon expression of ROS1 and DEL. Except for the D3R, these induced compounds were not derived from the flavonoid pathway. Most notable among these are nornicotine conjugates with butanoyl, hexanoyl, and octanoyl hydrophobic moieties, and phenylpropanoid-polyamine conjugates such as caffeoyl putrescine. The defensive properties of the induced molecules were addressed in bioassays using the tobacco specialist lepidopteran insect Manduca sexta. Our study showed that the effect of ROS1 and DEL expression in N. benthamiana leaves extends beyond the flavonoid pathway. Apparently the same transcription factor may regulate different secondary metabolite pathways in different plant species.
    A novel approach for multi-domain and multi-gene famliy identification provides insights into evolutionary dynamics of disease resistance genes in core eudicot plants
    Hofberger, J.A. ; Zhou, B. ; Tang, H. ; Jones, J. ; Schranz, M.E. - \ 2014
    BMC Genomics 15 (2014). - ISSN 1471-2164
    genome-wide analysis - nb-arc domain - arabidopsis-thaliana - whole-genome - draft genome - phylogenetic analysis - triggered immunity - mildew resistance - defense responses - encoding genes
    Background Recent advances in DNA sequencing techniques resulted in more than forty sequenced plant genomes representing a diverse set of taxa of agricultural, energy, medicinal and ecological importance. However, gene family curation is often only inferred from DNA sequence homology and lacks insights into evolutionary processes contributing to gene family dynamics. In a comparative genomics framework, we integrated multiple lines of evidence provided by gene synteny, sequence homology and protein-based Hidden Markov Modelling to extract homologous super-clusters composed of multi-domain resistance (R)-proteins of the NB-LRR type (for NUCLEOTIDE BINDING/LEUCINE-RICH REPEATS), that are involved in plant innate immunity. Results To assess the diversity of R-proteins within and between species, we screened twelve eudicot plant genomes including six major crops and found a total of 2,363 NB-LRR genes. Our curated R-proteins set shows a 50% average for tandem duplicates and a 22% fraction of gene copies retained from ancient polyploidy events (ohnologs). We provide evidence for strong positive selection acting on all identified genes and show significant differences in molecular evolution rates (Ka/Ks-ratio) among tandem- (mean = 1.59), ohnolog (mean = 1.36) and singleton (mean = 1.22) R-gene duplicates. To foster the process of gene-edited plant breeding, we report species-specific presence/absence of all 140 NB-LRR genes present in the model plant Arabidopsis and describe four distinct clusters of NB-LRR "gatekeeper" loci sharing syntenic orthologs across all analyzed genomes. Conclusion By curating a near-complete set of multi-domain R-protein clusters in an eudicot-wide scale, our analysis offers significant insight into evolutionary dynamics underlying diversification of the plant innate immune system. Furthermore, our methods provide a blueprint for future efforts to identify and more rapidly clone functional NB-LRR genes from any plant species.
    A roadmap to embryo identity in plants
    Radoeva, T.M. ; Weijers, D. - \ 2014
    Trends in Plant Science 19 (2014)11. - ISSN 1360-1385 - p. 709 - 716.
    microspore-derived embryos - somatic embryogenesis - arabidopsis-thaliana - pattern-formation - transcription factor - leafy cotyledon1 - seed development - gene-expression - wuschel gene - cell
    Although plant embryogenesis is usually studied in the context of seed development, there are many alternative roads to embryo initiation. These include somatic embryogenesis in tissue culture and microspore embryogenesis, both widely used in breeding and crop propagation, but also include other modes of ectopic embryo initiation. In the past decades several genes, mostly transcription factors, were identified that can induce embryogenesis in somatic cells. Because the genetic networks in which such regulators operate to promote embryogenesis are largely unknown, a key question is how their activity relates to zygotic and alternative embryo initiation. We describe here the many roads to plant embryo initiation and discuss a framework for defining the developmental roles and mechanisms of plant embryogenesis regulators.
    Group VII Ethylene Response Factor diversification and regulation in four species from flood-prone environments.
    Veen, H. van; Akman, M. ; Jamar, D.C.L. ; Vreugdenhil, D. ; Kooiker, M. ; Tienderen, P.H. van; Voesenek, L.A.C.J. ; Schranz, M.E. ; Sasidharan, R. - \ 2014
    Plant, Cell & Environment 37 (2014)10. - ISSN 0140-7791 - p. 2421 - 2432.
    end rule pathway - submergence tolerance - transcription factors - arabidopsis-thaliana - comparative genomics - rorippa-sylvestris - gene-expression - rice - hypoxia - plants
    Flooding events negatively affect plant performance and survival. Flooding gradients thereby determine the dynamics in vegetation composition and species abundance. In adaptation to flooding, the group VII Ethylene Response Factor genes (ERF-VIIs) play pivotal roles in rice and Arabidopsis through regulation of anaerobic gene expression and antithetical survival strategies. We investigated if ERF-VIIs have a similar role in mediating survival strategies in eudicot species from flood-prone environments. Here, we studied the evolutionary origin and regulation of ERF-VII transcript abundance and the physiological responses in species from two genera of divergent taxonomic lineages (Rumex and Rorippa). Synteny analysis revealed that angiosperm ERF-VIIs arose from two ancestral loci and that subsequent diversification and duplication led to the present ERF-VII variation. We propose that subtle variation in the regulation of ERF-VII transcript abundance could explain variation in tolerance among Rorippa species. In Rumex, the main difference in flood tolerance correlated with the genetic variation in ERF-VII genes. Large transcriptional differences were found by comparing the two genera: darkness and dark submergence-induced Rumex ERF-VIIs, whereas HRE2 expression was increased in submerged Rorippa roots. We conclude that the involvement of ERF-VIIs in flooding tolerance developed in a phylogenetic-dependent manner, with subtle variations within taxonomic clades.
    Effect of sequential induction by Mamestra brassicae L. and Tetranychus urticae Koch on Lima bean plant indirect defense
    Menzel, T.R. ; Huang, T.Y. ; Weldegergis, B.T. ; Gols, R. ; Loon, J.J.A. van; Dicke, M. - \ 2014
    Journal of Chemical Ecology 40 (2014)9. - ISSN 0098-0331 - p. 977 - 985.
    induced volatile emission - host-plant - jasmonic acid - mediated interactions - arabidopsis-thaliana - methyl salicylate - induced responses - predatory mite - herbivores - prey
    Attack by multiple herbivores often leads to modification of induced plant defenses compared to single herbivory, yet little is known about the effects on induced indirect plant defense. Here, we investigated the effect of sequential induction of plant defense by Mamestra brassicae caterpillar oral secretion and an infestation by Tetranychus urticae spider mites on the expression of indirect plant defense in Lima bean plants. The effect on indirect defense was assessed using behavior assays with the specialist predatory mite Phytoseiulus persimilis in an olfactometer, headspace analysis of 11 major herbivore-induced plant volatiles (HIPVs) including (E)-ß-ocimene, and transcript levels of the corresponding gene Phaseolus lunatus (E)-ß-ocimene synthase (PlOS). Predatory mites were found to distinguish between plants induced by spider mites and caterpillar oral secretion but not between plants with single spider mite infestation and plants induced by caterpillar oral secretion prior to spider mite infestation. Indeed, the volatile blends emitted by plants induced by spider mites only and the sequential induction treatment of caterpillar oral secretion followed by spider mite infestation, were similar. Our results suggest that plant indirect defense is not affected by previous treatment with oral secretion of M. brassicae caterpillars.
    Synergism in the effect of prior jasmonic acid application on herbivore-induced volatile emission by Lima bean plants: transcription of a monoterpene synthase gene and volatile emission
    Menzel, T.R. ; Weldegergis, B.T. ; David, A. ; Boland, W. ; Gols, R. ; Loon, J.J.A. van; Dicke, M. - \ 2014
    Journal of Experimental Botany 65 (2014)17. - ISSN 0022-0957 - p. 4821 - 4831.
    induced resistance - arabidopsis-thaliana - brassica-oleracea - phytoseiulus-persimilis - attract parasitoids - signaling pathway - methyl salicylate - predatory mite - corn plants - host-plant
    Jasmonic acid (JA) plays a central role in induced plant defence e.g. by regulating the biosynthesis of herbivore-induced plant volatiles that mediate the attraction of natural enemies of herbivores. Moreover, exogenous application of JA can be used to elicit plant defence responses similar to those induced by biting-chewing herbivores and mites that pierce cells and consume their contents. In the present study, we used Lima bean (Phaseolus lunatus) plants to explore how application of a low dose of JA followed by minor herbivory by spider mites (Tetranychus urticae) affects transcript levels of P. lunatus (E)-ß-ocimene synthase (PlOS), emission of (E)-ß-ocimene and nine other plant volatiles commonly associated with herbivory. Furthermore, we investigated the plant’s phytohormonal response. Application of a low dose of JA increased PlOS transcript levels in a synergistic manner when followed by minor herbivory for both simultaneous and sequential infestation. Emission of (E)-ß-ocimene was also increased, and only JA, but not SA, levels were affected by treatments. Projection to latent structures-discriminant analysis (PLS-DA) of other volatiles showed overlap between treatments. Thus, a low-dose JA application results in a synergistic effect on gene transcription and an increased emission of a volatile compound involved in indirect defence after herbivore infestation.
    Caterpillar-induced plant volatiles remain a reliable signal for foraging wasps during dual attack with a plant pathogen or non-host insect herbivore
    Ponzio, C.A.M. ; Gols, R. ; Weldegergis, B.T. ; Dicke, M. - \ 2014
    Plant, Cell & Environment 37 (2014)8. - ISSN 0140-7791 - p. 1924 - 1935.
    interspecific interactions - pseudomonas-syringae - arabidopsis-thaliana - phytophagous insects - multiple herbivory - cotesia-glomerata - pieris-brassicae - fungal-infection - natural enemies - damaged plants
    Plants respond to herbivory with the emission of plant volatiles, which can be used by the herbivores' natural enemies to locate their hosts or prey. In nature, plants are often simultaneously confronted with insect herbivores and phytopathogens, potentially interfering with the attraction of the herbivores' enemies as a result of modifications of the induced volatile blend. Here, we investigated parasitoid (Cotesia glomerata) attraction to volatiles of plants challenged by different attackers, either alone or in combination with Pieris brassicae caterpillars, hosts of C.¿glomerata. We used a natural system consisting of Brassica nigra plants, eggs and larvae of P.¿brassicae, Brevicoryne brassicae aphids and the bacterial phytopathogen Xanthomonas campestris pv. campestris. In all cases, parasitoids successfully located host-infested plants, and wasp foraging behaviour was unaffected by the simultaneous presence of a non-host attacker or host eggs. Analysis of the volatile emissions show that the volatile blends of caterpillar-infested treatments were different from those without caterpillars. Furthermore, dually attacked plants could not be separated from those with only caterpillars, regardless of non-host identity, supporting the behavioural data. Our results suggest that, in this system, indirect plant defences may be more resistant to interference than is generally assumed, with volatiles induced during dual attack remaining reliable indicators of host presence for parasitoids.
    Ecology of plant volatiles: taking a plant community perspective
    Pierik, R. ; Ballaré, C.L. ; Dicke, M. - \ 2014
    Plant, Cell & Environment 37 (2014)8. - ISSN 0140-7791 - p. 1845 - 1853.
    shade-avoidance - nicotiana-attenuata - neighbor detection - methyl jasmonate - associational resistance - arabidopsis-thaliana - defense responses - natural enemies - predatory mites - canopy light
    Although plants are sessile organisms, they can modulate their phenotype so as to cope with environmental stresses such as herbivore attack and competition with neighbouring plants. Plant-produced volatile compounds mediate various aspects of plant defence. The emission of volatiles has costs and benefits. Research on the role of plant volatiles in defence has focused primarily on the responses of individual plants. However, in nature, plants rarely occur as isolated individuals but are members of plant communities where they compete for resources and exchange information with other plants. In this review, we address the effects of neighbouring plants on plant volatile-mediated defences. We will outline the various roles of volatile compounds in the interactions between plants and other organisms, address the mechanisms of plant neighbour perception in plant communities, and discuss how neighbour detection and volatile signalling are interconnected. Finally, we will outline the most urgent questions to be addressed in the future.
    Identification of quantitative trait loci and a candidate locus for freezing tolerance in controlled and outdoor environments in the overwintering crucifer Boechera stricta.
    Heo, J. ; Feng, D. ; Niu, X. ; Mitchell-Olds, T. ; Tienderen, P.H. van; Tomes, D. ; Schranz, M.E. - \ 2014
    Plant, Cell & Environment 37 (2014)11. - ISSN 0140-7791 - p. 2459 - 2469.
    cold-acclimation - arabidopsis-thaliana - chlorophyll fluorescence - transcription factor - natural variation - frost tolerance - genes - temperature - wheat - expression
    Development of chilling and freezing tolerance is complex and can be affected by photoperiod, temperature and photosynthetic performance; however, there has been limited research on the interaction of these three factors. We evaluated 108 recombinant inbred lines of Boechera stricta, derived from a cross between lines originating from Montana and Colorado, under controlled long day (LD), short-day (SD) and in an outdoor environment (OE). We measured maximum quantum yield of photosystem II, lethal temperature for 50% survival and electrolyte leakage of leaves. Our results revealed significant variation for chilling and freezing tolerance and photosynthetic performance in different environments. Using both single- and multi-trait analyses, three main-effect quantitative trait loci (QTL) were identified. QTL on linkage group (LG)3 were SD specific, whereas QTL on LG4 were found under both LD and SD. Under all conditions, QTL on LG7 were identified, but were particularly predictive for the outdoor experiment. The co-localization of photosynthetic performance and freezing tolerance effects supports these traits being co-regulated. Finally, the major QTL on LG7 is syntenic to the Arabidopsis C-repeat binding factor locus, known regulators of chilling and freezing responses in Arabidopsis thaliana and other species.
    The tomato phosphatidylinositol-phospholipase C2 (SlPLC2) is required for defense gene induction by the fungal elicitor xylanase
    Gonorazky, G. ; Ramirez, L. ; Abd-El-Haliem, A. ; Vossen, J.H. ; Lamattina, L. ; Have, A. ten; Joosten, M.H.A.J. ; Laxalt, A.M. - \ 2014
    Journal of Plant Physiology 171 (2014)11. - ISSN 0176-1617 - p. 959 - 965.
    phosphatidic-acid accumulation - cultured rice cells - nitric-oxide - disease resistance - c/diacylglycerol kinase - arabidopsis-thaliana - signaling pathways - activation - responses - plants
    The tomato [Solanum lycopersicum (Sl)] phosphatidylinositol-phospholipase C (PI-PLC) gene family is composed of six members, named SlPLC1 to SlPLC6, differentially regulated upon pathogen attack. We have previously shown that the fungal elicitor xylanase rapidly induces nitric oxide (NO), which is required for PI-PLCs activity and downstream defense responses in tomato cell suspensions. Here, we show that all six SlPLC genes are expressed in tomato cell suspensions. Treatment of the cells with xylanase induces an early increase in SlPLC5 transcript levels, followed by a raise of the amount of SlPLC2 transcripts. The production of NO is required to augment SlPLC5 transcript levels in xylanase-treated tomato cells. Xylanase also induces SlPLC2 and SlPLC5 transcript levels in planta. We knocked-down the expression of SlPLC2 and SlPLC5 by virus-induced gene silencing. We found that SlPLC2 is required for xylanase-induced expression of the defense-related genes PR1 and HSR203J.
    Functional analysis of the tomato immune receptor Ve1 through domain swaps with Its non-functional homolog Ve2
    Fradin, E.F. ; Zhang, Z. ; Rövenich, H. ; Song, Y. ; Liebrand, T.W.H. ; Masini, L. ; Berg, G.C.M. van den; Joosten, M.H.A.J. ; Thomma, B.P.H.J. - \ 2014
    PLoS ONE 9 (2014)2. - ISSN 1932-6203 - 14 p.
    leucine-rich repeat - disease resistance protein - cladosporium-fulvum - arabidopsis-thaliana - endoplasmic-reticulum - hypersensitive response - verticillium resistance - plasma-membrane - innate immunity - kinase bri1
    Resistance in tomato against race 1 strains of the fungal vascular wilt pathogens Verticillium dahliae and V. albo-atrum is mediated by the Ve locus. This locus comprises two closely linked inversely oriented genes, Ve1 and Ve2, which encode cell surface receptors of the extracellular leucine-rich repeat receptor-like protein (eLRR-RLP) type. While Ve1 mediates Verticillium resistance through monitoring the presence of the recently identified V. dahliae Ave1 effector, no functionality for Ve2 has been demonstrated in tomato. Ve1 and Ve2 contain 37 eLRRs and share 84% amino acid identity, facilitating investigation of Ve protein functionality through domain swapping. In this study it is shown that Ve chimeras in which the first thirty eLRRs of Ve1 were replaced by those of Ve2 remain able to induce HR and activate Verticillium resistance, and that deletion of these thirty eLRRs from Ve1 resulted in loss of functionality. Also the region between eLRR30 and eLRR35 is required for Ve1-mediated resistance, and cannot be replaced by the region between eLRR30 and eLRR35 of Ve2. We furthermore show that the cytoplasmic tail of Ve1 is required for functionality, as truncation of this tail results in loss of functionality. Moreover, the C-terminus of Ve2 fails to activate immune signaling as chimeras containing the C-terminus of Ve2 do not provide Verticillium resistance. Furthermore, Ve1 was found to interact through its C-terminus with the eLRR-containing receptor-like kinase (eLRR-RLK) interactor SOBIR1 that was recently identified as an interactor of eLRR-RLP (immune) receptors. Intriguingly, also Ve2 was found to interact with SOBIR1.
    Quantitative label-free phosphoproteomics of six different life stages of the late blight pathogen Phytophthora infestans reveals abundant phosphorylation of members of the CRN effector family
    Resjö, S. ; Ali, A. ; Meijer, H.J.G. ; Seidl, M.F. ; Snel, B. ; Sandin, M. ; Levander, F. ; Govers, F. ; Andreasson, E. - \ 2014
    Journal of Proteome Research 13 (2014)4. - ISSN 1535-3893 - p. 1848 - 1859.
    tandem mass-spectrometry - protein-kinases - arabidopsis-thaliana - in-vitro - proteomics - identification - expression - potato - organization - specificity
    The oomycete Phytophthora infestans is the causal agent of late blight in potato and tomato. Since the underlying processes that govern pathogenicity and development in P. infestans are largely unknown, we have performed a large-scale phosphoproteomics study of six different P. infestans life stages. We have obtained quantitative data for 2922 phosphopeptides and compared their abundance. Life-stage-specific phosphopeptides include ATP-binding cassette transporters and a kinase that only occurs in appressoria. In an extended data set, we identified 2179 phosphorylation sites and deduced 22 phosphomotifs. Several of the phosphomotifs matched consensus sequences of kinases that occur in P. infestans but not Arabidopsis. In addition, we detected tyrosine phosphopeptides that are potential targets of kinases resembling mammalian tyrosine kinases. Among the phosphorylated proteins are members of the RXLR and Crinkler effector families. The latter are phosphorylated in several life stages and at multiple positions, in sites that are conserved between different members of the Crinkler family. This indicates that proteins in the Crinkler family have functions beyond their putative role as (necrosis-inducing) effectors. This phosphoproteomics data will be instrumental for studies on oomycetes and host–oomycete interactions. The data sets have been deposited to ProteomeXchange (identifier PXD000433).
    The Brassicaceae-Specific EWR1 Gene Provides Resistance to Vascular Wilt Pathogens
    Yadeta, K.A. ; Valkenburg, D.J. ; Hanemian, M. ; Marco, Y. ; Thomma, B.P.H.J. - \ 2014
    PLoS ONE 9 (2014)2. - ISSN 1932-6203 - 11 p.
    asymmetric interlaced pcr - arabidopsis-thaliana - verticillium wilt - antimicrobial peptides - defense peptides - tomato ve1 - plant - dahliae - disease - proteins
    Soil-borne vascular wilt diseases caused by Verticillium spp. are among the most destructive diseases worldwide in a wide range of plant species. The most effective means of controlling Verticillium wilt diseases is the use of genetic resistance. We have previously reported the identification of four activation-tagged Arabidopsis mutants which showed enhanced resistance to Verticillium wilt. Among these, one mutant also showed enhanced resistance to Ralstonia solanacearum, a bacterial vascular wilt pathogen. Cloning of the activation tag revealed an insertion upstream of gene At3g13437, which we designated as EWR1 (for Enhancer of vascular Wilt Resistance 1) that encodes a putatively secreted protein of unknown function. The search for homologs of Arabidopsis EWR1 (AtEWR1) in public databases only identified homologs within the Brassicaceae family. We subsequently cloned the EWR1 homolog from Brassica oleracea (BoEWR1) and show that over-expression in Arabidopsis results in V. dahliae resistance. Moreover, over-expression of AtEWR1 and BoEWR1 in N. benthamiana, a member of the Solanaceae family, results in V. dahliae resistance, suggesting that EWR1 homologs can be used to engineer Verticillium wilt resistance in non-Brassicaceae crops as well.
    A comprehensive set of transcript sequences of the heavy metal hyperaccumulator Noccaea caerulescens
    Lin, Y.F. ; Severing, E.I. ; Lintel Hekkert, B. te; Schijlen, E.G.W.M. ; Aarts, M.G.M. - \ 2014
    Frontiers in Plant Science 5 (2014). - ISSN 1664-462X - 15 p.
    gene copy number - thlaspi-caerulescens - arabidopsis-thaliana - expression differences - glucosinolate biosynthesis - elevated expression - zinc accumulation - stress-response - cd tolerance - plants
    Noccaea caerulescens is an extremophile plant species belonging to the Brassicaceae family. It has adapted to grow on soils containing high, normally toxic, concentrations of metals such as nickel, zinc, and cadmium. Next to being extremely tolerant to these metals, it is one of the few species known to hyperaccumulate these metals to extremely high concentrations in their aboveground biomass. In order to provide additional molecular resources for this model metal hyperaccumulator species to study and understand the mechanism of adaptation to heavy metal exposure, we aimed to provide a comprehensive database of transcript sequences for N. caerulescens. In this study, 23,830 transcript sequences (isotigs) with an average length of 1025 bp were determined for roots, shoots and inflorescences of N. caerulescens accession “Ganges” by Roche GS-FLEX 454 pyrosequencing. These isotigs were grouped into 20,378 isogroups, representing potential genes. This is a large expansion of the existing N. caerulescens transcriptome set consisting of 3705 unigenes. When translated and compared to a Brassicaceae proteome set, 22,232 (93.2%) of the N. caerulescens isotigs (corresponding to 19,191 isogroups) had a significant match and could be annotated accordingly. Of the remaining sequences, 98 isotigs resembled non-plant sequences and 1386 had no significant similarity to any sequence in the GenBank database. Among the annotated set there were many isotigs with similarity to metal homeostasis genes or genes for glucosinolate biosynthesis. Only for transcripts similar to Metallothionein3 (MT3), clear evidence for an additional copy was found. This comprehensive set of transcripts is expected to further contribute to the discovery of mechanisms used by N. caerulescens to adapt to heavy metal exposure
    Competing neighbors: light perception and root function
    Gundel, P.E. ; Pierik, R. ; Mommer, L. ; Ballare, L. - \ 2014
    Oecologia 176 (2014)1. - ISSN 0029-8549 - p. 1 - 10.
    far-red light - self/non-self discrimination - shade-avoidance responses - below-ground competition - scots pine-seedlings - blue-light - arabidopsis-thaliana - kin recognition - regulated gravitropism - environmental-control
    Plant responses to competition have often been described as passive consequences of reduced resource availability. However, plants have mechanisms to forage for favorable conditions and anticipate competition scenarios. Despite the progresses made in understanding the role of light signaling in modulating plant–plant interactions, little is known about how plants use and integrate information gathered by their photoreceptors aboveground to regulate performance belowground. Given that the phytochrome family of photoreceptors plays a key role in the acquisition of information about the proximity of neighbors and canopy cover, it is tempting to speculate that changes in the red:far-red (R:FR) ratio perceived by aboveground plant parts have important implications shaping plant behavior belowground. Exploring data from published experiments, we assess the neglected role of light signaling in the control of root function. The available evidence indicates that plant exposure to low R:FR ratios affects root growth and morphology, root exudate profiles, and interactions with beneficial soil microorganisms. Although dependent on species identity, signals perceived aboveground are likely to affect root-to-root interactions. Root systems could also be guided to deploy new growth predominantly in open areas by light signals perceived by the shoots. Studying interactions between above- and belowground plant–plant signaling is expected to improve our understanding of the mechanisms of plant competition.
    Genomic characterisation of the effector complement of the potato cyst nematode Globodera pallida
    Thorpe, P. ; Mantelin, S. ; Cock, P.J.A. ; Blok, V.C. ; Coke, M.C. ; Evers-van den Akker, S. ; Guzeeva, E. ; Lilley, C.J. ; Smant, G. ; Reid, A.J. ; Wright, K.M. ; Urwin, P.E. ; Jones, J.T. - \ 2014
    BMC Genomics 15 (2014). - ISSN 1471-2164 - 15 p.
    plant-parasitic nematodes - esophageal gland-cells - heterodera-glycines - meloidogyne-incognita - phytophthora-infestans - arabidopsis-thaliana - chorismate mutase - giant-cells - protein - sequence
    Background The potato cyst nematode Globodera pallida has biotrophic interactions with its host. The nematode induces a feeding structure – the syncytium – which it keeps alive for the duration of the life cycle and on which it depends for all nutrients required to develop to the adult stage. Interactions of G. pallida with the host are mediated by effectors, which are produced in two sets of gland cells. These effectors suppress host defences, facilitate migration and induce the formation of the syncytium. Results The recent completion of the G. pallida genome sequence has allowed us to identify the effector complement from this species. We identify 128 orthologues of effectors from other nematodes as well as 117 novel effector candidates. We have used in situ hybridisation to confirm gland cell expression of a subset of these effectors, demonstrating the validity of our effector identification approach. We have examined the expression profiles of all effector candidates using RNAseq; this analysis shows that the majority of effectors fall into one of three clusters of sequences showing conserved expression characteristics (invasive stage nematode only, parasitic stage only or invasive stage and adult male only). We demonstrate that further diversity in the effector pool is generated by alternative splicing. In addition, we show that effectors target a diverse range of structures in plant cells, including the peroxisome. This is the first identification of effectors from any plant pathogen that target this structure. Conclusion This is the first genome scale search for effectors, combined to a life-cycle expression analysis, for any plant-parasitic nematode. We show that, like other phylogenetically unrelated plant pathogens, plant parasitic nematodes deploy hundreds of effectors in order to parasitise plants, with different effectors required for different phases of the infection process.
    Comparative transcriptome analysis of the metal hyperaccumulator Noccaea caerulescens
    Halimaa, P. ; Blande, D. ; Aarts, M.G.M. ; Tuomainen, M. ; Tervahauta, A. ; Karenlampi, S. - \ 2014
    Frontiers in Plant Science 5 (2014). - ISSN 1664-462X
    gene copy number - thlaspi-caerulescens - arabidopsis-thaliana - expression differences - zinc accumulation - topology prediction - tobacco plants - cadmium - tolerance - populations
    The metal hyperaccumulator Noccaea caerulescens is an established model to study the adaptation of plants to metalliferous soils. Various comparators have been used in these studies. The choice of suitable comparators is important and depends on the hypothesis to be tested and methods to be used. In high-throughput analyses such as microarray, N. caerulescens has been compared to non-tolerant, non-accumulator plants like Arabidopsis thaliana or Thlaspi arvense rather than to the related hypertolerant or hyperaccumulator plants. An underutilized source is N. caerulescens populations with considerable variation in their capacity to accumulate and tolerate metals. Whole transcriptome sequencing (RNA-Seq) is revealing interesting variation in their gene expression profiles. Combining physiological characteristics of N. caerulescens accessions with their RNA-Seq has a great potential to provide detailed insight into the underlying molecular mechanisms, including entirely new gene products. In this review we will critically consider comparative transcriptome analyses carried out to explore metal hyperaccumulation and hypertolerance of N. caerulescens, and demonstrate the potential of RNA-Seq analysis as a tool in evolutionary genomics
    Expression profiling reveals functionally redundant multiple-copy genes related to zinc, iron and cadmium responses in Brassica rapa
    Li, J. ; Liu, B. ; Cheng, F. ; Wang, X. ; Aarts, M.G.M. ; Wu, J. - \ 2014
    New Phytologist 203 (2014)1. - ISSN 0028-646X - p. 182 - 194.
    hyperaccumulator thlaspi-caerulescens - ferric-chelate reductase - arabidopsis-thaliana - metal homeostasis - human-nutrition - deficiency - tolerance - plants - toxicity - protein
    Genes underlying environmental adaptability tend to be over-retained in polyploid plant species. Zinc deficiency (ZnD) and iron deficiency (FeD), excess Zn (ZnE) and cadmium exposure (CdE) are major environmental problems for crop cultivation, but little is known about the differential expression of duplicated genes upon these stress conditions. Applying Tag-Seq technology to leaves of Brassica rapa grown under FeD, ZnD, ZnE or CdE conditions, with normal conditions as a control, we examined global gene expression changes and compared the expression patterns of multiple paralogs. We identified 812, 543, 331 and 447 differentially expressed genes under FeD, ZnD, ZnE and CdE conditions, respectively, in B. rapa leaves. Genes involved in regulatory networks centered on the transcription factors bHLH038 or bHLH100 were differentially expressed under (ZnE-induced) FeD. Further analysis revealed that genes associated with Zn, Fe and Cd responses tended to be over-retained in the B. rapa genome. Most of these multiple-copy genes showed the same direction of expression change under stress conditions. We conclude that the duplicated genes involved in trace element responses in B. rapa are functionally redundant, making the regulatory network more complex in B. rapa than in Arabidopsis thaliana
    Soybean SAT1 (Symbiotic Ammonium Transporter 1) encodes a bHLH transcription factor involved in nodule growth and NH4+ transport
    Chiasson, D.M. ; Loughlin, P.C. ; Mazurkiewicz, D. ; Mohammadidehcheshmeh, M. ; Fedorova, E.E. ; Okamoto, M. ; McLean, E. ; Glass, A.D.M. ; Smith, S.E. ; Bisseling, T. ; Tyerman, S.D. ; Day, D.A. ; Kaiser, B.N. - \ 2014
    Proceedings of the National Academy of Sciences of the United States of America 111 (2014)13. - ISSN 0027-8424 - p. 4814 - 4819.
    arabidopsis-thaliana - circadian clock - lotus-japonicus - stress-response - er stress - membrane - protein - expression - domain - gene
    Glycine max symbiotic ammonium transporter 1 was first documented as a putative ammonium (NH4+) channel localized to the symbiosome membrane of soybean root nodules. We show that Glycine max symbiotic ammonium transporter 1 is actually a membrane-localized basic helix–loop–helix (bHLH) DNA-binding transcription factor now renamed Glycine max bHLH membrane 1 (GmbHLHm1). In yeast, GmbHLHm1 enters the nucleus and transcriptionally activates a unique plasma membrane NH4+ channel Saccharomyces cerevisiae ammonium facilitator 1. Ammonium facilitator 1 homologs are present in soybean and other plant species, where they often share chromosomal microsynteny with bHLHm1 loci. GmbHLHm1 is important to the soybean rhizobium symbiosis because loss of activity results in a reduction of nodule fitness and growth. Transcriptional changes in nodules highlight downstream signaling pathways involving circadian clock regulation, nutrient transport, hormone signaling, and cell wall modification. Collectively, these results show that GmbHLHm1 influences nodule development and activity and is linked to a novel mechanism for NH4+ transport common to both yeast and plants.
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