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.

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    Seed dormancy back on track; its definition and regulation by DOG1
    Soppe, Wim J.J. ; Bentsink, Leónie - \ 2020
    New Phytologist (2020). - ISSN 0028-646X
    DELAY OF GERMINATION 1 - DSDS50 - germination rate - seed dormancy - T50
    Arabidopsis in the wild—the effect of seasons on seed performance
    Souza Vidigal, Deborah de; He, Hanzi ; Hilhorst, Henk W.M. ; Willems, Leo A.J. ; Bentsink, Leónie - \ 2020
    Plants 9 (2020)5. - ISSN 2223-7747
    Arabidopsis - Environmental effects - Field conditions - Seed dormancy - Seed longevity

    Climate changes play a central role in the adaptive life histories of organisms all over the world. In higher plants, these changes may impact seed performance, both during seed development and after dispersal. To examine the plasticity of seed performance as a response to environmental fluctuations, eight genotypes known to be affected in seed dormancy and longevity were grown in the field in all seasons of two years. Soil and air temperature, day length, precipitation, and sun hours per day were monitored. We show that seed performance depends on the season. Seeds produced by plants grown in the summer, when the days began to shorten and the temperature started to decrease, were smaller with deeper dormancy and lower seed longevity compared to the other seasons when seeds were matured at higher temperature over longer days. The performance of seeds developed in the different seasons was compared to seeds produced in controlled conditions. This revealed that plants grown in a controlled environment produced larger seeds with lower dormancy than those grown in the field. All together the results show that the effect of the environment largely overrules the genetic effects, and especially, differences in seed dormancy caused by the different seasons were larger than the differences between the genotypes.

    Dormancy cycling: Translation related transcripts are the main difference between dormant and non‐dormant seeds in the field
    Buijs, G. ; Vogelzang, Afke ; Nijveen, H. ; Bentsink, L. - \ 2020
    The Plant Journal 102 (2020)2. - ISSN 0960-7412 - p. 327 - 339.
    Primary seed dormancy is a mechanism that orchestrates the timing of seed germination in order to prevent out‐of‐season germination. Secondary dormancy can be induced in imbibed seeds when they encounter prolonged unfavourable conditions. Secondary dormancy is not induced during dry storage, therefore the mechanisms underlying this process have remained largely unexplored. Here, a two‐year seed burial experiment in which dormancy cycling was studied at the physiological and transcriptional level is presented. For these analyses six different Arabidopsis thaliana genotypes were used, Landsberg erecta (Ler) and the dormancy associated DELAY OF GERMINATION (DOG) Near Isogenic Lines 1, 2, 3, 6 and 22 (NILDOG1, 2, 3, 6 and 22). The germination potential of seeds exhumed from the field showed that these seeds go through dormancy cycling and that the dynamics of this cycling is genotype‐dependent. RNA‐seq analysis revealed large transcriptional changes during dormancy cycling, especially at the time‐points preceding shifts in dormancy status. Dormancy cycling is driven by the soil temperature and the endosperm is important in perception of the environment. Genes that are upregulated in the low‐ to non‐dormant stages are enriched for genes involved in translation, indicating that the non‐dormant seeds are prepared for rapid seed germination.
    Seed stored mRNAs that are specifically associated to monosome are translationally regulated during germination
    Bai, Bing ; Horst, Sjors Van Der; Cordewener, Jan ; America, Twan ; Hanson, Johannes ; Bentsink, Leónie - \ 2020
    Plant Physiology 182 (2020)1. - ISSN 0032-0889 - p. 378 - 392.
    The life cycle of many organisms includes a quiescent stage, such as bacterial or fungal spores, insect larvae, or plant seeds. Common to these stages is their low water content and high survivability during harsh conditions. Upon rehydration, organisms need to reactivate metabolism and protein synthesis. Plant seeds contain many mRNAs that are transcribed during seed development. Translation of these mRNAs occurs during early seed germination, even before the requirement of transcription. Therefore, stored mRNAs are postulated to be important for germination. How these mRNAs are stored and protected during long-term storage is unknown. The aim of this study was to investigate how mRNAs are stored in dry seeds and whether they are indeed translated during seed germination. We investigated seed polysome profiles and the mRNAs and protein complexes that are associated with these ribosomes in seeds of the model organism Arabidopsis (Arabidopsis thaliana). We showed that most stored mRNAs are associated with monosomes in dry seeds; therefore, we focus on monosomes in this study. Seed ribosome complexes are associated with mRNA-binding proteins, stress granule (SG), and P-body proteins, which suggests regulated packing of seed mRNAs. Interestingly, approximately 17% of the mRNAs that are specifically associated with monosomes are translationally up-regulated during seed germination. These mRNAs are transcribed during seed maturation, suggesting a role for this developmental stage in determining the translational fate of mRNAs during early germination
    Transcriptome and translatome profiling and translational network analysis during seed maturation reveals conserved transcriptional and distinct translational regulatory patterns
    Bai, B. ; Horst, Sjors van der; Delhomme, Nicolas ; Robles, A.V. ; Bentsink, L. ; Hanson, Johannes - \ 2019
    BioRxiv - 40 p.
    Seed maturation is an important plant developmental process that follows embryo development. It is associated with a series of physiological changes such as the establishment of desiccation tolerance, seed longevity and seed dormancy. However, the translational dynamics associated with seed maturation, especially its connection with seed germination remains largely elusive. Here transcriptome and translatome profiling were performed during seed maturation. During seed maturation we observed a gradual disappearance of polysomes and a relative increase of monosomes, indicating a gradual reduction of global translation. Comparing the levels of polysomal associated mRNAs with total mRNA levels showed that thousands of genes are translationally regulated at early sates of maturation, as judged by dramatic changes in polysomal occupancy. By including previous published data from germination and seedling establishment, a translational regulatory network: SeedTransNet was constructed. Network analysis identified hundreds of gene modules with distinct functions and transcript sequence features indicating the existence of separate translational regulatory circuits possibly acting through specific regulatory elements. The regulatory potential of one such element was confirmed in vivo. The network identified several seed maturation associated genes as central nodes, and we could confirm the importance of many of these hub genes with a maturation associated seed phenotype by mutant analysis. One of the identified regulators an AWPM19 family protein PM19-Like1 (PM19L1) was shown to regulate seed dormancy and longevity. This putative RBP also affects the transitional regulation of one its, by the SeedTransNet identified, target mRNAs. Our data shows the usefulness of SeedTransNet in identifying regulatory pathways during seed phase transitions
    Translational dynamics during seed maturation
    Bai, B. ; Horst, Sjors van der; Hanson, Johannes ; Bentsink, L. - \ 2019
    Wageningen University & Research
    Arabidopsis thaliana - GSE127509 - PRJNA524885
    We analysed the polysomal mRNA and total mRNA during Col-0 seed maturation The aim was to investigate the translational dynamics during seed maturation
    Fate specific mRNA storage in seeds
    Bai, B. ; Horst, Sjors van der; Cordewener, J.H.G. ; America, A.H.P. ; Hanson, J. ; Bentsink, L. - \ 2019
    Wageningen University & Research
    Arabidopsis thaliana - GSE76905 - PRJNA308911
    We analyzed the monsome and polysome associated transcripts of seeds and seedlings and identify transcripts specifically associated with monosome and polysome in both tissues. The aim was to generate a global view about the state of mRNA storage in the seeds and the their fate during seed germination
    DELAY OF GERMINATION 1-LIKE 4 acts as an inducer of seed reserve accumulation
    Sall, Khadidiatou ; Dekkers, Bas J.W. ; Nonogaki, Mariko ; Katsuragawa, Yoshihiko ; Koyari, Ryosuke ; Hendrix, David ; Willems, Leo A.J. ; Bentsink, Leónie ; Nonogaki, Hiroyuki - \ 2019
    The Plant Journal 100 (2019)1. - ISSN 0960-7412 - p. 7 - 19.
    abscisic acid - dormancy - hormone - seed development - seed maturation - storage proteins

    More than 70% of global food supply depends on seeds. The major seed reserves, such as proteins, lipids, and polysaccharides, are produced during seed maturation. Here, we report that DELAY OF GERMINATION 1-LIKE 4 (DOGL4) is a major inducer of reserve accumulation during seed maturation. The DOGL family proteins are plant-specific proteins of largely unknown biochemical function. DOGL4 shares only limited homology in amino acid sequence with DOG1, a major regulator of seed dormancy. DOGL4 was identified as one of the outstanding abscisic acid (ABA)-induced genes in our RNA sequencing analysis, whereas DOG1 was not induced by ABA. Induction of DOGL4 caused the expression of 70 seed maturation-specific genes, even in germinating seeds, including the major seed reserves ALBUMIN, CRUCIFERIN and OLEOSIN. Although DOG1 affects the expression of many seed maturation genes, the major seed reserve genes induced by DOGL4 are not altered by the dog1 mutation. Furthermore, the reduced dormancy and longevity phenotypes observed in the dog1 seeds were not observed in the dogl4 mutants, suggesting that these two genes have limited functional overlap. Taken together, these results suggest that DOGL4 is a central factor mediating reserve accumulation in seeds, and that the two DOG1 family proteins have diverged over the course of evolution into independent regulators of seed maturation, but retain some overlapping function.

    Seed maturation and post-harvest ripening negatively affect arabidopsis somatic embryogenesis
    Wu, Han ; Chen, Baojian ; Fiers, Martijn ; Wróbel-Marek, Justyna ; Kodde, Jan ; Groot, Steven P.C. ; Angenent, Gerco ; Feng, Hui ; Bentsink, Leónie ; Boutilier, Kim - \ 2019
    Plant Cell, Tissue and Organ Culture: an international journal on in vitro culture of higher plants 139 (2019)1. - ISSN 0167-6857 - p. 17 - 27.
    ABA - Arabidopsis - Auxin - Post-harvest ripening - ROS - Seed maturation - Somatic embryogenesis

    Plant development is highly malleable, as evidenced by the ability of cultured cells, tissues and organs to regenerate into whole plants in vitro. The ability of plants to regenerate in vitro is influenced by many different factors, including the donor plant growth conditions and the type of explant. Empirical trial and error manipulation of these and other culture parameters is the basis for improving plant regeneration protocols, but the mechanisms underlying the effects of these parameters on plant regeneration are unknown. Somatic embryogenesis (SE) is a type of in vitro plant regeneration where somatic/vegetative cells are induced to form embryos. Here we show that seed maturation is one of the parameters that affects the ability of germinating embryos to undergo auxin-induced somatic embryogenesis in Arabidopsis thaliana. Late maturation stage seeds harvested from yellow siliques have a higher capacity for somatic embryogenesis than seeds harvested later from brown siliques, a process that can be mimicked by post-harvest storage. Physiological and genetic analyses suggest that an oxidizing environment and ABA metabolism enhance the rate at which germinating embryos lose capacity to reactivate embryogenic growth. Our data suggest that there is a narrow window during late seed maturation in which embryogenic competence is reduced, and that this process also takes place, albeit more slowly, during seed storage. This knowledge provides a framework for identifying new plant totipotency factors and for directing efficient SE in systems that make use of mature seed explants.

    Seeds: A Unique System to Study Translational Regulation
    Sajeev, Nikita ; Bai, Bing ; Bentsink, Leónie - \ 2019
    Trends in Plant Science 24 (2019)6. - ISSN 1360-1385 - p. 487 - 495.
    long-lived mRNA - ribosome - seed germination - translational regulation

    Seeds accumulate mRNA during their development and have the ability to store these mRNAs over extended periods of time. On imbibition, seeds transform from a quiescent dry state (no translation) to a fully active metabolic state, and selectively translate subsets of these stored mRNA. Thus, seeds provide a unique developmentally regulated ‘on/off’ switch for translation. Additionally, there is extensive translational control during seed germination. Here we discuss new findings and hypotheses linked to mRNA fate and the role of translational regulation in seeds. Translation is an understated yet important mode of gene regulation. We propose seeds as a novel system to study developmentally and physiologically regulated translation.

    NADP-MALIC ENZYME 1 Affects Germination after Seed Storage in Arabidopsis thaliana
    Yazdanpanah, F. ; Maurino, Veronica ; Mettlet-Altmann, T. ; Buijs, G. ; Bailly, M. ; Karimi Jashni, Mansoor ; Willems, L.A.J. ; Sergeeva, L. ; Rajjou, Loïc ; Hilhorst, H.W.M. ; Bentsink, L. - \ 2019
    Plant and Cell Physiology 60 (2019)2. - ISSN 0032-0781 - p. 318 - 328.
    Aging decreases the quality of seeds and results in agricultural and economic losses. The damage that occurs at the biochemical level can alter the seed physiological status. Although loss of viability has been investigated frequently, little information exists on the molecular and biochemical factors involved in seed deterioration and loss of viability. Oxidative stress has been implicated as a major contributor to seed deterioration, and several pathways are involved in protection against this. In this study, we show that seeds of Arabidopsis thaliana lacking a functional NADP-MALIC ENZYME 1 (NADP-ME1) have reduced seed viability relative to the wild type. Seeds of the NADP-ME1 loss-of-function mutant display higher levels of protein carbonylation than those of the wild type. NADP-ME1 catalyzes the oxidative decarboxylation of malate to pyruvate with the simultaneous production of CO2 and NADPH. Upon seed imbibition, malate and amino acids accumulate in embryos of aged seeds of the NADP-ME1 loss-of-function mutant compared with those of the wild type. NADP-ME1 expression is increased in imbibed aged as compared with non-aged seeds. NADP-ME1 activity at testa rupture promotes normal germination of aged seeds. In seedlings of aged seeds, NADP-ME1 is specifically active in the root meristematic zone. We propose that NADP-ME1 activity is required for protecting seeds against oxidation during seed dry storage.
    Seed dormancy release accelerated by elevated partial pressure of oxygen is associated with DOG loci
    Buijs, G. ; Kodde, J. ; Groot, S.P.C. ; Bentsink, L. - \ 2018
    Journal of Experimental Botany 69 (2018)15. - ISSN 0022-0957 - p. 3601 - 3608.
    Seed dormancy determines the timing of seed germination and may be released by dry storage, also referred to as after-ripening. Studies on dormancy-release mechanisms are often hampered by the long after-ripening requirements of seeds. After-ripening is thought to be mainly caused by oxidative processes during seed dry storage. These processes are also the main cause of seed ageing. Increasing partial oxygen pressure through the elevated partial pressure of oxygen (EPPO) system has been shown to mimic and accelerate dry seed ageing. In this study, we investigated whether the EPPO system may also release primary seed dormancy in Arabidopsis thaliana. EPPO mimics dry after-ripening at the genetic level, as quantitative trait locus (QTL) analysis after EPPO treatment identified the DELAY OF GERMINATION loci DOG1, DOG2, and DOG6 that were first described in a study using dry after-ripening to release seed dormancy. QTL analysis also showed that dormancy release by cold stratification (another common method to break seed dormancy) partly overlaps with release by after-ripening and EPPO treatment. We conclude that EPPO is an appropriate method to mimic and accelerate dormancy release and, as such, may have applications in both research and industry.
    Combined transcriptome and translatome analyses reveal a role for tryptophan-dependent auxin biosynthesis in the control of DOG1-dependent seed dormancy
    Bai, Bing ; Novák, Ondřej ; Ljung, Karin ; Hanson, Johannes ; Bentsink, Leónie - \ 2018
    New Phytologist 217 (2018)3. - ISSN 0028-646X - p. 1077 - 1085.
    The importance of translational regulation during Arabidopsis seed germination has been shown previously. Here the role of transcriptional and translational regulation during seed imbibition of the very dormant DELAY OF GERMINATION 1 (DOG1) near-isogenic line was investigated. Polysome profiling was performed on dormant and after-ripened seeds imbibed for 6 and 24 h in water and in the transcription inhibitor cordycepin. Transcriptome and translatome changes were investigated. Ribosomal profiles of after-ripened seeds imbibed in cordycepin mimic those of dormant seeds. The polysome occupancy of mRNA species is not affected by germination inhibition, either as a result of seed dormancy or as a result of cordycepin treatment, indicating the importance of the regulation of transcript abundance. The expression of auxin metabolism genes is discriminative during the imbibition of after-ripened and dormant seeds, which is confirmed by altered concentrations of indole-3-acetic acid conjugates and precursors.
    Temperature fine-tunes Mediterranean Arabidopsis thaliana life-cycle phenology geographically
    Marcer, A. ; Souza Vidigal, Deborah de; James, P.M.A. ; Fortin, M.J. ; Méndez-Vigo, B. ; Hilhorst, H.W.M. ; Bentsink, L. ; Alonso-Blanco, C. ; Picó, F.X. - \ 2018
    Plant Biology 20 (2018)S1. - ISSN 1435-8603 - p. 148 - 156.
    Adaptive evolution - Environmental gradients - Flowering time - Geographically weighted regressions - Seed dormancy - Sliding window analysis
    To understand how adaptive evolution in life-cycle phenology operates in plants, we need to unravel the effects of geographic variation in putative agents of natural selection on life-cycle phenology by considering all key developmental transitions and their co-variation patterns. We address this goal by quantifying the temperature-driven and geographically varying relationship between seed dormancy and flowering time in the annual Arabidopsis thaliana across the Iberian Peninsula. We used data on genetic variation in two major life-cycle traits, seed dormancy (DSDS50) and flowering time (FT), in a collection of 300 A. thaliana accessions from the Iberian Peninsula. The geographically varying relationship between life-cycle traits and minimum temperature, a major driver of variation in DSDS50 and FT, was explored with geographically weighted regressions (GWR). The environmentally varying correlation between DSDS50 and FT was analysed by means of sliding window analysis across a minimum temperature gradient. Maximum local adjustments between minimum temperature and life-cycle traits were obtained in the southwest Iberian Peninsula, an area with the highest minimum temperatures. In contrast, in off-southwest locations, the effects of minimum temperature on DSDS50 were rather constant across the region, whereas those of minimum temperature on FT were more variable, with peaks of strong local adjustments of GWR models in central and northwest Spain. Sliding window analysis identified a minimum temperature turning point in the relationship between DSDS50 and FT around a minimum temperature of 7.2 °C. Above this minimum temperature turning point, the variation in the FT/DSDS50 ratio became rapidly constrained and the negative correlation between FT and DSDS50 did not increase any further with increasing minimum temperatures. The southwest Iberian Peninsula emerges as an area where variation in life-cycle phenology appears to be restricted by the duration and severity of the hot summer drought. The temperature-driven varying relationship between DSDS50 and FT detected environmental boundaries for the co-evolution between FT and DSDS50 in A. thaliana. In the context of global warming, we conclude that A. thaliana phenology from the southwest Iberian Peninsula, determined by early flowering and deep seed dormancy, might become the most common life-cycle phenotype for this annual plant in the region.
    Combined transcriptome and translatome analyses reveal a role for tryptophan dependent auxin biosynthesis in the control of DOG1 dependent seed dormancy
    Bai, Bing ; Novák, Ondřej ; Ljung, Karin ; Hanson, Johannes ; Bentsink, L. - \ 2017
    Wageningen University
    Arabidopsis thaliana - GSE75368 - PRJNA304010
    Transcriptome and translatome analyses of 6 and 24 hours imbibed seeds dormant and non-dormant seeds of NILDOG1-Cvi with and without addition of the transcription inhibitor Cordycepin. NILDOG1-Cvi is the Ler WT containing an introgression of the Cvi accession on chromosome 5, which includes the DOG1 gene.
    The identification of novel genes involved in seed dormancy and after-ripening in Arabidopsis thaliana
    Yazdanpanah, F. ; Hanson, Johannes ; Hilhorst, H.W.M. ; Bentsink, L. - \ 2017
    Wageningen University
    Arabidopsis thaliana - GSE90162 - PRJNA354607
    We analysed the transcriptome of dormant and after-ripened imbibed seeds of different genotypes (Landsberg erecta and the different NILs) to identify dormancy and after-ripening genes that are absolutely required for these traits.
    Differentially expressed genes during the imbibition of dormant and after-ripened seeds - a reverse genetics approach
    Yazdanpanah, Farzaneh ; Hanson, Johannes ; Hilhorst, Henk W.M. ; Bentsink, Leónie - \ 2017
    BMC Plant Biology 17 (2017)1. - ISSN 1471-2229
    Arabidopsis thaliana - Delay of germination - Knockout lines - Seed performance - Transcriptromics
    Background: Seed dormancy, defined as the incapability of a viable seed to germinate under favourable conditions, is an important trait in nature and agriculture. Despite extensive research on dormancy and germination, many questions about the molecular mechanisms controlling these traits remain unanswered, likely due to its genetic complexity and the large environmental effects which are characteristic of these quantitative traits. To boost research towards revealing mechanisms in the control of seed dormancy and germination we depend on the identification of genes controlling those traits. Methods: We used transcriptome analysis combined with a reverse genetics approach to identify genes that are prominent for dormancy maintenance and germination in imbibed seeds of Arabidopsis thaliana. Comparative transcriptomics analysis was employed on freshly harvested (dormant) and after-ripened (AR; non-dormant) 24-h imbibed seeds of four different DELAY OF GERMINATION near isogenic lines (DOGNILs) and the Landsberg erecta (Ler) wild type with varying levels of primary dormancy. T-DNA knock-out lines of the identified genes were phenotypically investigated for their effect on dormancy and AR. Results: We identified conserved sets of 46 and 25 genes which displayed higher expression in seeds of all dormant and all after-ripened DOGNILs and Ler, respectively. Knock-out mutants in these genes showed dormancy and germination related phenotypes. Conclusions: Most of the identified genes had not been implicated in seed dormancy or germination. This research will be useful to further decipher the molecular mechanisms by which these important ecological and commercial traits are regulated.
    Extensive translational regulation during seed germination revealed by polysomal profiling
    Bai, Bing ; Peviani, Alessia ; Horst, Sjors van der; Gamm, Magdalena ; Snel, Berend ; Bentsink, Leónie ; Hanson, Johannes - \ 2017
    New Phytologist 214 (2017)1. - ISSN 0028-646X - p. 233 - 244.
    Arabidopsis - Germination - Imbibition - Polysomal profiling - Ribosome - RNA structure - Seedling establishment - Translatomics

    This work investigates the extent of translational regulation during seed germination. The polysome occupancy of each gene is determined by genome-wide profiling of total mRNA and polysome-associated mRNA. This reveals extensive translational regulation during Arabidopsis thaliana seed germination. The polysome occupancy of thousands of individual mRNAs changes to a large extent during the germination process. Intriguingly, these changes are restricted to two temporal phases (shifts) during germination, seed hydration and germination. Sequence features, such as upstream open reading frame number, transcript length, mRNA stability, secondary structures, and the presence and location of specific motifs correlated with this translational regulation. These features differed significantly between the two shifts, indicating that independent mechanisms regulate translation during seed germination. This study reveals substantial translational dynamics during seed germination and identifies development-dependent sequence features and cis elements that correlate with the translation control, uncovering a novel and important layer of gene regulation during seed germination.

    Parental Effects on Seed Transcriptome-Metabolome
    He, Hanzi ; Willems, Leo ; Batushansky, Albert ; Fait, Aaron ; Hanson, Johannes ; Nijveen, Harm ; Hilhorst, Henk ; Bentsink, Leonie - \ 2016
    Wageningen University
    GSE75837 - Arabidopsis thaliana - GSE75837 - Arabidopsis thaliana - PRJNA305511
    Transcriptome analyses on seeds developed in different parental conditions
    DELAY OF GERMINATION 1 plays a role in Arabidopsis seed maturation
    Dekkers, Bas ; He, Hanzi ; Hanson, Johannes ; Willems, Leo ; Cueff, Gwendal ; Rajjou, Loïc ; Hilhorst, Henk ; Bentsink, Leonie - \ 2016
    Wageningen University
    GSE65471 - Arabidopsis thaliana - GSE65471 - Arabidopsis thaliana - PRJNA274129
    We analysed the transcriptome of dry seeds (the end product of seed maturation) of three genotypes with different DOG1 expression levels. These included the WT Ler (low DOG1 expression), the near isogenic line NILDOG1-Cvi (strong DOG1 expression) and the non-dormant dog1-1 mutant (absence of DOG1 expression). NILDOG1-Cvi is the Ler WT containing an introgression of the Cvi accession on chromosome 5, which includes the DOG1 gene (Bentsink et al., 2006). The dog1-1 mutant is in the NILDOG1-Cvi genetic background.
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