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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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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.

Experiments Are Necessary in Process-Based Tree Phenology Modelling
Hänninen, Heikki ; Kramer, Koen ; Tanino, Karen ; Zhang, Rui ; Wu, Jiasheng ; Fu, Yongshuo H. - \ 2019
Trends in Plant Science 24 (2019)3. - ISSN 1360-1385 - p. 199 - 209.
bud burst - climate change - dormancy - phenology - process-based modelling

In boreal and temperate trees, air temperature is a major environmental factor regulating the timing of spring phenological events, such as vegetative bud burst, through underlying physiological processes. This has been established by experimental research, and mathematical process-based tree phenology models have been developed based on the results. The models have often been applied when assessing the effects of climate change. Currently, there is an increasing trend to develop process-based tree phenology models using only observational phenological records from natural conditions. We point out that this method runs a high risk of producing models that do not simulate the real physiological processes in the trees and discuss experimental designs facilitating the development of biologically realistic process-based models for tree spring phenology.

The hot, the cold and the tulip : the regulation of flowering time and dormancy release
Leeggangers, Hendrika A.C.F. - \ 2017
Wageningen University. Promotor(en): Richard Immink, co-promotor(en): Henk Hilhorst. - Wageningen : Wageningen University - ISBN 9789463430289 - 244
tulipa - lilium - tulips - flowering date - flowering - dormancy - plant development - temperature - plant physiology - vegetative propagation - tulipa - lilium - tulpen - bloeidatum - bloei - slaaptoestand - plantenontwikkeling - temperatuur - plantenfysiologie - vegetatieve vermeerdering

The ornamental geophyte Tulipa gesneriana is the most cultivated bulbous species in the Netherlands. It is widely grown in the field for vegetative propagation purposes and in greenhouses for the production of high quality cut flowers. Over the last decade, the tulip bulb industry is affected by the rapid climate change the world is facing. Temperature is rising and influences the vegetative to reproductive phase change (floral induction) inside the tulip bulbs in spring and processes that are occurring during winter, such as dormancy release.

In this thesis the two temperature-dependent processes related to tulip flowering, being floral induction and dormancy release, were investigated in detail with a special focus at the molecular level. Flowering time has been studied in a broad range of species, including the model species Arabidopsis thaliana and Oryza sativa. The current understanding of this process can be translated to non-model species, such as tulip, through a ‘bottom-up’ and ‘top-down’ approach (Chapter 2). For the ‘bottom-up’ approach conservation of molecular pathways is assumed and researchers make use of sequence homology searches to identify candidate genes. The ‘top-down’ approach starts from large scale data mining, such as RNA-sequencing (RNA-seq) data or microarrays, followed by the association between phenotypes, genes and gene expression patterns. Here, a comparison with data from model plant species is made at the end of the process and this also leads to the identification of candidate genes for a particular process.

Large scale genomics data mining in tulip is only possible via transcriptome analysis with RNA-seq derived data, because no full genome-sequence is present at this moment. Genome sequencing remains a challenge for species with a large and complex genome, containing probably a large number of repetitive sequences, which is the case for tulip and lily. In chapter 3 a high quality transcriptome of tulip and lily is presented, which is derived from a collection of different tissues. In order to obtain good transcriptome coverage and to facilitate effective data mining, different filtering parameters were used. This analysis revealed the limitations of commonly applied methods used in de novo transcriptome assembly. The generated transcriptome for tulip and lily is made publicly available via a user friendly database, named the ‘Transcriptome Browser’.

The molecular regulation of the temperature-dependent floral induction was studied through the use of RNA-seq (Chapter 4). A better understanding of this process is needed to prevent floral bud blasting (dehydration of the flower) in the future. The development at the shoot apical meristem (SAM) was morphologically investigated in two contrasting temperature environments, high and low. Meristem-enriched tissues were collected before and during the start of flower development. The start of flower development is morphologically visible by rounding of the SAM and correlates with the up-regulation of TGSQA, an AP1-like gene. A ‘top-down’ approach was used to identify possible regulators of the floral induction in tulip. However, Gene ontology (GO)-enrichment analysis of the differentially expressed genes showed that the floral induction, maturation of the bulb and dormancy establishment are occurring around the same period in time. Therefore a ‘bottom-up’ approach was followed to identify specific flowering time regulators based on knowledge obtained from other species. Expression analysis in tulip, heterologous analysis in Arabidopsis and yeast two hybrid-based protein-protein interaction studies revealed that Tulipa gesneriana TERMINAL FLOWER 1 (TgTFL1) is likely a repressor of flowering, whereas Tulipa gesneriana SUPPRESSOR OF OVEREXPRESSION OF CONSTANS-LIKE2 (TgSOC1L2) acts probably as a floral activator.

Another well-known flowering time regulator is FLOWERING LOCUS T (FT), which is a member of the PEBP gene family found in Arabidopsis and many more plant species. In tulip and lily, a total of four highly similar sequences to FT and HEADING DATA 3A (Hd3a) were identified (Chapter 5). Overexpression of Lilium longiflorum FT (LlFT) and TgFT2 in Arabidopsis resulted in an early flowering phenotype, but upon overexpression of TgFT1 and TgFT3 a late flowering phenotype was observed. The tulip PEBP genes TgFT2 and TgFT3 have a similar expression pattern during development, but show a different behaviour in Arabidopsis. Therefore the difference within the amino acid sequence was investigated, which resulted in the identification of two important amino acids for the FT function, which appeared to be mutated in TgFT3. Interchanging of these amino acids between TgFT2 and TgFT3 resulted in conversion of the phenotype, showing the potential importance of these positions in the protein and these specific amino acids for the molecular mode of action of these two proteins. Based on all the data, LlFT is considered to play a role in creating meristem competency to flowering related cues and TgFT2 to act as a florigen involved in the floral induction. The function of TgFT3 is not clear, but phylogenetic analysis suggests a bulb specific function.

After the floral induction and completion of flower development inside the tulip bulb, a period of prolonged cold is required for proper flowering in spring. Low temperature stimulates the re-mobilization of carbohydrates from the scale tissues to the sink organs, such as the floral stem, floral bud and leaves. Not many details are known about the molecular and metabolic changes during this cold period. In chapter 6, first insights are shown on the development of the different tissues inside the bulbs. The floral bud appears to be the least active tissue in comparison with the floral stem and leaves, suggesting a type of floral bud dormancy in tulip. However, metabolic changes are suggesting that the floral bud is still showing active cell division and/or preparation for elongation by turgor-driven cell wall extension. Dormancy of all tissues seems to be released ten weeks after planting and is correlated with the increase of glucose levels. In the leaves, from this same moment, photosynthesis related genes are up-regulated suggesting that the leaves are preparing for photosynthesis while still beneath the soil surface.

At the end of the thesis a glance is given at different perspectives of the tulips life cycle, categorizing tulip as a perennial, biennial or annual plant species, respectively. The perennial way of life is applicable when growing bulbs from seeds, while biennial and annual are more in relation to vegetative propagation. Also the importance of bulb size is highlighted, because it will determine if the bulbs are able to flower or not the following spring. Two scenarios are discussed related to availability of energy in the presence of carbohydrates and meristem incompetency to floral inducing signals. Throughout all research done for this thesis, it became clear that tulip bulbs and seeds have a lot in common. By combining the knowledge of processes in different plant species or developmental systems it is possible to understand how flowering and dormancy release are regulated and this provides us with novel insights how these processes are regulated in bulbous plant species, such as tulip.

Detecting QTLs and putative candidate genes involved in budbreak and flowering time in an apple multiparental population
Allard, Alix ; Bink, Marco C.A.M. ; Martinez, Sebastien ; Kelner, Jean Jacques ; Legave, Jean Michel ; Guardo, Mario Di; Pierro, Erica A. Di; Laurens, François ; De Weg, Eric W. Van; Costes, Evelyne - \ 2016
Journal of Experimental Botany 67 (2016)9. - ISSN 0022-0957 - p. 2875 - 2888.
Climate change - DAM genes - dormancy - flowering genes - Malus×domestica (Borkh) - pedigree-based analysis - phenology - QTL

In temperate trees, growth resumption in spring time results from chilling and heat requirements, and is an adaptive trait under global warming. Here, the genetic determinism of budbreak and flowering time was deciphered using five related full-sib apple families. Both traits were observed over 3 years and two sites and expressed in calendar and degree-days. Best linear unbiased predictors of genotypic effect or interaction with climatic year were extracted from mixed linear models and used for quantitative trait locus (QTL) mapping, performed with an integrated genetic map containing 6849 single nucleotide polymorphisms (SNPs), grouped into haplotypes, and with a Bayesian pedigree-based analysis. Four major regions, on linkage group (LG) 7, LG10, LG12, and LG9, the latter being the most stable across families, sites, and years, explained 5.6-21.3% of trait variance. Co-localizations for traits in calendar days or growing degree hours (GDH) suggested common genetic determinism for chilling and heating requirements. Homologs of two major flowering genes, AGL24 and FT, were predicted close to LG9 and LG12 QTLs, respectively, whereas Dormancy Associated MADs-box (DAM) genes were near additional QTLs on LG8 and LG15. This suggests that chilling perception mechanisms could be common among perennial and annual plants. Progenitors with favorable alleles depending on trait and LG were identified and could benefit new breeding strategies for apple adaptation to temperature increase.

A gene co-expression network predicts functional genes controlling the re-establishment of desiccation tolerance in germinated Arabidopsis thaliana seeds
Dias Costa, M.C. ; Righetti, K. ; Nijveen, H. ; Yazdanpanah, F. ; Ligterink, W. ; Buitink, J. ; Hilhorst, H.W.M. - \ 2015
Planta 242 (2015)2. - ISSN 0032-0935 - p. 435 - 449.
medicago-truncatula seeds - transcription factors - expression data - abiotic stress - dormancy - drought - identification - maturation - longevity - software
Main conclusion During re-establishment of desiccation tolerance (DT), early events promote initial protection and growth arrest, while late events promote stress adaptation and contribute to survival in the dry state. Mature seeds of Arabidopsis thaliana are desiccation tolerant, but they lose desiccation tolerance (DT) while progressing to germination. Yet, there is a small developmental window during which DT can be rescued by treatment with abscisic acid (ABA). To gain temporal resolution and identify relevant genes in this process, data from a time series of microarrays were used to build a gene co-expression network. The network has two regions, namely early response (ER) and late response (LR). Genes in the ER region are related to biological processes, such as dormancy, acquisition of DT and drought, amplification of signals, growth arrest and induction of protection mechanisms (such as LEA proteins). Genes in the LR region lead to inhibition of photosynthesis and primary metabolism, promote adaptation to stress conditions and contribute to seed longevity. Phenotyping of 12 hubs in relation to re-establishment of DT with T-DNA insertion lines indicated a significant increase in the ability to re-establish DT compared with the wild-type in the lines cbsx4, at3g53040 and at4g25580, suggesting the operation of redundant and compensatory mechanisms. Moreover, we show that re-establishment of DT by polyethylene glycol and ABA occurs through partially overlapping mechanisms. Our data confirm that co-expression network analysis is a valid approach to examine data from time series of transcriptome analysis, as it provides promising insights into biologically relevant relations that help to generate new information about the roles of certain genes for DT.
Reduced seed germination in Arabidopsis over-expressing SWI/SNF2 ATPase genes
Leeggangers, H.A.C.F. ; Folta, A. ; Muras, A. ; Nap, J.P.H. ; Mlynarova, L. - \ 2015
Physiologia Plantarum 153 (2015)2. - ISSN 0031-9317 - p. 318 - 326.
thaliana - dormancy - transcription - maturation - stress - arrest - growth - rna
In the life of flowering plants, seed germination is a critical step to ensure survival into the next generation. Generally the seed prior to germination has been in a dormant state with a low rate of metabolism. In the transition from a dormant seed to a germinating seed, various epigenetic mechanisms play a regulatory role. Here, we demonstrate that the over-expression of chromatin remodeling ATPase genes (AtCHR12 or AtCHR23) reduced the frequency of seed germination in Arabidopsis thaliana up to 30% relative to the wild-type seeds. On the other hand, single loss-of-function mutations of the two genes did not affect seed germination. The reduction of germination in over-expressing mutants was more pronounced in stress conditions (salt or high temperature), showing the impact of the environment. Reduced germinations upon over-expression coincided with increased transcript levels of seed maturation genes and with reduced degradation of their mRNAs stored in dry seeds. Our results indicate that repression of AtCHR12/23 gene expression in germinating wild-type Arabidopsis seeds is required for full germination. This establishes a functional link between chromatin modifiers and regulatory networks towards seed maturation and germination.
Integration of heterogeneous molecular networks to unravel gene-regulation in Mycobacterium tuberculosis
Dam, J.C.J. van; Schaap, P.J. ; Martins dos Santos, V.A.P. ; Suarez Diez, M. - \ 2014
BMC Systems Biology 8 (2014). - ISSN 1752-0509 - 21 p.
data sets - expression profiles - microarray data - global analysis - biological data - promoter motif - inference - database - dormancy - regulon
Background: Different methods have been developed to infer regulatory networks from heterogeneous omics datasets and to construct co-expression networks. Each algorithm produces different networks and efforts have been devoted to automatically integrate them into consensus sets. However each separate set has an intrinsic value that is diluted and partly lost when building a consensus network. Here we present a methodology to generate co-expression networks and, instead of a consensus network, we propose an integration framework where the different networks are kept and analysed with additional tools to efficiently combine the information extracted from each network. Results: We developed a workflow to efficiently analyse information generated by different inference and prediction methods. Our methodology relies on providing the user the means to simultaneously visualise and analyse the coexisting networks generated by different algorithms, heterogeneous datasets, and a suite of analysis tools. As a show case, we have analysed the gene co-expression networks of Mycobacterium tuberculosis generated using over 600 expression experiments. Regarding DNA damage repair, we identified SigC as a key control element, 12 new targets for LexA, an updated LexA binding motif, and a potential mismatch repair system. We expanded the DevR regulon with 27 genes while identifying 9 targets wrongly assigned to this regulon. We discovered 10 new genes linked to zinc uptake and a new regulatory mechanism for ZuR. The use of co-expression networks to perform system level analysis allows the development of custom made methodologies. As show cases we implemented a pipeline to integrate ChIP-seq data and another method to uncover multiple regulatory layers. Conclusions: Our workflow is based on representing the multiple types of information as network representations and presenting these networks in a synchronous framework that allows their simultaneous visualization while keeping specific associations from the different networks. By simultaneously exploring these networks and metadata, we gained insights into regulatory mechanisms in M. tuberculosis that could not be obtained through the separate analysis of each data type.
Interaction between parental environment and genotype affects plant and seed performance in Arabidopsis
He, H. ; Souza Vidigal, D. De; Snoek, L.B. ; Schnabel, S.K. ; Nijveen, H. ; Hilhorst, H. ; Bentsink, L. - \ 2014
Journal of Experimental Botany 65 (2014)22. - ISSN 0022-0957 - p. 6603 - 6615.
sativa miller brassicaceae - abscisic-acid biosynthesis - maturation environment - drought tolerance - natural variation - key enzyme - dormancy - germination - thaliana - temperature
Seed performance after dispersal is highly dependent on parental environmental cues, especially during seed formation and maturation. Here we examine which environmental factors are the most dominant in this respect and whether their effects are dependent on the genotypes under investigation. We studied the influence of light intensity, photoperiod, temperature, nitrate, and phosphate during seed development on five plant attributes and thirteen seed attributes, using 12 Arabidopsis genotypes that have been reported to be affected in seed traits. As expected, the various environments during seed development resulted in changed plant and/or seed performances. Comparative analysis clearly indicated that, overall, temperature plays the most dominant role in both plant and seed performance, whereas light has a prominent impact on plant traits. In comparison to temperature and light, nitrate mildly affected some of the plant and seed traits while phosphate had even less influence on those traits. Moreover, clear genotype-by-environment interactions were identified. This was shown by the fact that individual genotypes responded differentially to the environmental conditions. Low temperature significantly increased seed dormancy and decreased seed longevity of NILDOG1 and cyp707a1-1, whereas low light intensity increased seed dormancy and decreased seed longevity of NILDOG3 and NILDOG6. This also indicates that different genetic and molecular pathways are involved in the plant and seed responses. By identifying environmental conditions that affect the dormancy vs longevity correlation in the same way as previously identified naturally occurring loci, we have identified selective forces that probably shaped evolution for these important seed traits.
Seed washing, exogenous application of gibberellic acid, and cold stratification enhance the germination of sweet cherry (Prunus avium L.) seed
Javanmard, T. ; Zamani, Z. ; Keshavarz Afshar, R. ; Hashemi, M. ; Struik, P.C. - \ 2014
Journal of Horticultural Science and Biotechnology 89 (2014)1. - ISSN 1462-0316 - p. 74 - 78.
dormancy - release
Seed germination in sweet cherry (Prunus avium L.) is a slow and lengthy process which has delayed breeding efforts. In this study, seed from ripe fruit of the sweet cherry cultivar ‘Lambert’ were collected and, after removing the endocarp, various dormancy-breaking treatments such as seed washing, the application of exogenous gibberellic acid (GA3), or cold stratification were evaluated for their ability to enhance the percentage and rate of seed germination. The results indicated that seed washing was necessary to break dormancy in sweet cherry. The seed germination percentage and rate improved to 26.5% and 1.17 seed d–1 simply by washing the seed for 24 h. The application of up to 500 mg l–1 GA3, in addition to a seed washing treatment, further improved both the seed germination percentage and rate to 47.1% and 1.9 seed d–1, respectively. Although the seed germination percentage improved as a result of 6 weeks of cold stratification, a longer cold period (8 weeks) was required to obtain the maximum rate of germination. The application of higher concentrations of GA3 and longer periods of cold storage did not result in further improvements in the seed germination percentage or rate.The highest germination percentage (61.2%) was obtained following seed washing for 24 h, followed by 500 mg l–1 GA3 treatment, then 6 weeks of cold stratification, which was higher than the germination percentage in the control treatment (0%). The highest rate of seed germination was observed following 24 h of seed washing, then 1,000 mg l–1 GA3 treatment and 8 weeks of cold stratification (3.8 seed d–1), but this combined treatment did not differ significantly (P = 0.05) from seed washing, 1,000 mg l–1 GA3, and 6 weeks of cold stratification (3.6 seeds d–1).
Transcriptional dynamics of two seed compartments with opposing roles in Arabidopsis seed germination
Dekkers, S.J.W. ; Pearce, S. ; Bolderen-Veldkamp, R.P. ; Marshall, A. ; Widera, P. ; Gilbert, J. ; Drost, H.G. ; Bassel, G. ; Muller, K. ; King, J.R. ; Wood, A. ; Grosse, I. ; Bentsink, L. - \ 2013
Plant Physiology 163 (2013)1. - ISSN 0032-0889 - p. 205 - 215.
thaliana seeds - abscisic-acid - leaf senescence - gene activity - endosperm - reveals - dormancy - metabolism - embryo - touch
Seed germination is a critical stage in the plant life cycle and the first step toward successful plant establishment. Therefore, understanding germination is of important ecological and agronomical relevance. Previous research revealed that different seed compartments (testa, endosperm, and embryo) control germination, but little is known about the underlying spatial and temporal transcriptome changes that lead to seed germination. We analyzed genome-wide expression in germinating Arabidopsis (Arabidopsis thaliana) seeds with both temporal and spatial detail and provide Web-accessible visualizations of the data reported ( We show the potential of this high-resolution data set for the construction of meaningful coexpression networks, which provide insight into the genetic control of germination. The data set reveals two transcriptional phases during germination that are separated by testa rupture. The first phase is marked by large transcriptome changes as the seed switches from a dry, quiescent state to a hydrated and active state. At the end of this first transcriptional phase, the number of differentially expressed genes between consecutive time points drops. This increases again at testa rupture, the start of the second transcriptional phase. Transcriptome data indicate a role for mechano-induced signaling at this stage and subsequently highlight the fates of the endosperm and radicle: senescence and growth, respectively. Finally, using a phylotranscriptomic approach, we show that expression levels of evolutionarily young genes drop during the first transcriptional phase and increase during the second phase. Evolutionarily old genes show an opposite pattern, suggesting a more conserved transcriptome prior to the completion of germination.
Dormancy cycling in seeds: mechanisms and regulation
Claessens, S.M.C. - \ 2012
Wageningen University. Promotor(en): Linus van der Plas, co-promotor(en): Henk Hilhorst; P.E. Toorop. - S.l. : s.n. - ISBN 9789461731906 - 161
sisymbrium officinale - arabidopsis thaliana - kiemrust - zaden - genen - levenscyclus - slaaptoestand - membranen - metabolisme - sisymbrium officinale - arabidopsis thaliana - seed dormancy - seeds - genes - life cycle - dormancy - membranes - metabolism

The life cycle of most plants starts, and ends, at the seed stage. In most species mature seeds are shed and dispersed on the ground. At this stage of its life cycle the seed may be dormant and will, by definition, not germinate under favourable conditions (Bewley, 1997).

Seasonal dormancy cycling is a characteristic found in plant seeds. Being able to cycle in and out of dormancy allows the seed to survive decades or even centuries, allowing germination to be spread over time, but only when optimal conditions are available, not only for germination but especially for seedling establishment. In this thesis we have attempted to further elucidate the mechanisms behind dormancy, germination and dormancy cycling.

Sisymbrium officinale seeds need nitrate and light to start germination (Chapter 2, 3, 4, 6). Nitrate acts in part by reducing the abscisic acid (ABA) levels (a plant hormone that elevates dormancy levels). The action of light and nitrate can also be reached by applying gibberellins (GAs) to the seeds (Chapter 2, 3, 4, 6). GAs are capable of inducing enzymes that hydrolyze the ensdosperm walls (Debeaujon and Koornneef, 2000; Chen and Bradford, 2000; Nonogaki et al., 2000; Manz et al., 2005) In this way GAs could be involved in lowering the physical restrictions imposed by the resistance of the seed coat and the endosperm. On the other hand, GAs may also increase the embryo growth potential.

For successful survival of the dormant seed, metabolic activity is reduced to avoid rapid depletion of reserves. The metabolic activity of the seed was measured using electron paramagnetic resonance (EPR), with TEMPONE as a spin probe, and the respiratory activity was measured with the Q2-test (Chapter 2).We showed that primary dormancy was accompanied by hardly any metabolic or respiratory activity, and this increased considerably when dormancy was broken by nitrate. However, when the light pulse was not given and the seeds had become secondary dormant the metabolic activity slowed down.

Regulation of dormancy is tightly linked with abiotic stress factors from the environment. The regulation and survival of the seed under stress conditions is largely dependent on the composition of the cytoplasm. We tested this by EPR, using carboxyl-proxyl (CP) spin probe (Chapter 4). The primary dormant and sub-dormant seeds possessed a higher viscosity than the germinating seeds. The viscosity of secondary dormant seeds appeared intermediate; however, the ease at which the vitrified water melted was similar to that of primary dormant seeds. As a result of the differences in viscosity, the temperature of vitrified water melting differed between the different dormancy states. The changes in cytoplasmic viscosity and vitrified water melting may be linked to changes in metabolism and the content of high molecular weight compounds.

As membranes are the primary target for temperature perception, they are often implicated in regulating dormancy. Therefore, Hilhorst (1998) put forward a hypothesis in which changes in responsiveness to dormancy breaking factors like nitrate and light was a function of cellular membrane fluidity. In Chapter 3 we indeed showed that dormancy is a function of membrane fluidity. Primary dormant seeds of Sisymbrium officinale appeared to have very rigid membranes, whereas breaking dormancy increased membrane fluidity considerably. However, when sub-dormant seeds became secondary dormant membrane fluidity decreased again, but not to the rigidity seen in primary dormant seeds. One of the most common ways in which cells control membrane fluidity is by homeoviscous adaptation with the help of desaturases. Desaturase involvement in changes in membrane fluidity due to changes in dormancy was tested in Chapter 3 (using Sisymbrium officinale) and Chapter 5 (using Arabidopsis thaliana). Here we found that although desaturase activity may change the membrane fluidity or influence the germination/dormancy phenotype, the two are not linked, unless the effects of these enzymes are very local within the seed. Finally, in Chapter 7, we presented a new model in which a membrane anchored dormancy related protein/transcription factor is activated by changes in membrane fluidity. The activated form is transported to the nucleus, where it starts the germination process, which includes changes in metabolism and mobilization of storage reserves.

Seed maturation in Arabidopsis is characterised by nuclear size reduction and increased chromatin condensation
Zanten, M. van; Koini, M.A. ; Geyer, R. ; Liu, Y. ; Brambilla, V. ; Bartels, D. ; Koornneef, M. ; Fransz, P. ; Soppe, W.J.J. - \ 2011
Proceedings of the National Academy of Sciences of the United States of America 108 (2011)50. - ISSN 0027-8424 - p. 20219 - 20224.
plant craterostigma-plantagineum - desiccation tolerance - gene-regulation - dormancy - germination - heterochromatin - mutants - establishment - transcription - organization
Most plant species rely on seeds for their dispersal and survival under unfavorable environmental conditions. Seeds are characterized by their low moisture content and significantly reduced metabolic activities. During the maturation phase, seeds accumulate storage reserves and become desiccation-tolerant and dormant. Growth is resumed after release of dormancy and the occurrence of favorable environmental conditions. Here we show that embryonic cotyledon nuclei of Arabidopsis thaliana seeds have a significantly reduced nuclear size, which is established at the beginning of seed maturation. In addition, the chromatin of embryonic cotyledon nuclei from mature seeds is highly condensed. Nuclei regain their size and chromatin condensation level during germination. The reduction in nuclear size is controlled by the seed maturation regulator ABSCISIC ACID-INSENSITIVE 3, and the increase during germination requires two predicted nuclear matrix proteins, LITTLE NUCLEI 1 and LITTLE NUCLEI 2. Our results suggest that the specific properties of nuclei in ripe seeds are an adaptation to desiccation, independent of dormancy. We conclude that the changes in nuclear size and chromatin condensation in seeds are independent, developmentally controlled processes
DOG1 expression is predicted by the seed-maturation envornment and contributes to geographical variation in germination in Arabidopsis thaliana
Chiang, G.C.K. ; Bartsch, M. ; Barua, D. ; Nakabayashi, K. ; Debieu, M. ; Kronholm, I. ; Koornneef, M. ; Soppe, W.J.J. ; Donohue, K. ; Meaux, J. De - \ 2011
Molecular Ecology 20 (2011)16. - ISSN 0962-1083 - p. 3336 - 3349.
flowering time gene - natural-selection - dormancy - brassicaceae - evolution - field - diversification - adaptation - characters - plasticity
Seasonal germination timing of Arabidopsis thaliana strongly influences overall life history expression and is the target of intense natural selection. This seasonal germination timing depends strongly on the interaction between genetics and seasonal environments both before and after seed dispersal. DELAY OF GERMINATION 1 (DOG1) is the first gene that has been identified to be associated with natural variation in primary dormancy in A. thaliana. Here, we report interaccession variation in DOG1 expression and document that DOG1 expression is associated with seed-maturation temperature effects on germination; DOG1 expression increased when seeds were matured at low temperature, and this increased expression was associated with increased dormancy of those seeds. Variation in DOG1 expression suggests a geographical structure such that southern accessions, which are more dormant, tend to initiate DOG1 expression earlier during seed maturation and achieved higher expression levels at the end of silique development than did northern accessions. Although elimination of the synthesis of phytohormone abscisic acid (ABA) results in the elimination of maternal temperature effects on dormancy, DOG1 expression predicted dormancy better than expression of genes involved in ABA metabolism
Carbon disulphide promotes sprouting of potato minitubers
Salimi, Kh. ; Hosseini, M.B. ; Struik, P.C. ; Tavakkol Afshari, R. - \ 2010
Australian Journal of Crop Science 4 (2010)3. - ISSN 1835-2693 - p. 163 - 168.
dormancy - microtubers - growth
We investigated the effects of postharvest application of carbon disulphide (CS2) in various concentrations (0, 15, 25, 35, 45 and 55 ml m-3) and with different exposure duration (24, 48, 72 and 96 h) on breaking of dormancy and sprouting of potato (Solanum tuberosum L., cv. Marfona) minitubers of two ages (freshly harvested and one week after harvest) and two weight classes (1.5 and 12 g). In comparison with the control minitubers, CS2 treated minitubers showed significantly shorter dormancy and better sprouting. More rotting and weaker responses were observed in freshly harvested treated minitubers compared with minitubers treated one week after harvest. The number of sprouts per minituber and their length were significantly enhanced by treating minitubers with CS2 compared with the untreated control minitubers, but there were strong interactions with minituber weight. Results showed that duration of CS2 treatment was more important than concentration and longer duration of CS2 treatment exhibited a stronger action on breaking dormancy and sprouting of potato minitubers than shorter treatments. But, when longer duration was accompanied with higher concentration, treatment with CS2 led to formation of needle sprouts, which are undesirable as they do not produce vigorous stems
Effects of gibberellic acid and carbon disulphide on sprouting of potato minitubers
Salimi, Kh. ; Tavakkol Afshari, R. ; Hosseini, M.B. ; Struik, P.C. - \ 2010
Scientia Horticulturae 124 (2010)1. - ISSN 0304-4238 - p. 14 - 18.
dormancy - microtubers - growth - plant
Effects of treatments with gibberellic acid (GA(3), 50 mg L-1 for 2 h) or carbon disulphide (CS2, 25 ml m(-3) for four days) on breaking of dormancy and sprouting of potato (Solanum tuberosum L., cvs Agria and Marfona) minitubers of different weight classes (0.3, 0.7 and 1.5 g) were investigated. The dormancy period tended to decrease with an increase in the weight of minitubers, whereas the number of sprouts per minituber, their length and fresh weight and the sprout mass per unit of sprout length of the longest sprout tended to increase with an increase in minituber weight. In both cultivars, applying GA(3) or CS2 advanced breaking of dormancy, but GA(3) was less effective in Marfona than in Agria. Advancing breaking of dormancy was associated with removal of apical dominance and therefore applying GA(3) or CS2 also increased the number of sprouts per minituber, especially in Agria. In Agria, the dry matter content of sprouts from the CS2 treatment was higher than in the GA(3) or control treatments, whereas in Marfona dry matter content of sprouts was highest in the GA(3) treatment. The length of sprouts, fresh weight of sprouts and the sprout mass per unit of sprout length of the longest sprout were significantly enhanced by treating minitubers with GA(3) or CS2 compared with the untreated control minitubers, but there were strong interactions with cultivar and minituber weight. These interactions are important in practical use of dormancy breaking methods. (C) 2009 Elsevier B.V. All rights reserved.
Germinator: A software package for high-throughput scoring and curve fitting of Arabidopsis seed germination
Joosen, R.V.L. ; Kodde, J. ; Willems, L.A.J. ; Ligterink, W. ; Plas, L.H.W. van der; Hilhorst, H.W.M. - \ 2010
The Plant Journal 62 (2010)1. - ISSN 0960-7412 - p. 148 - 159.
quantitative trait loci - inbred line population - image-analysis - thaliana - tolerance - dormancy - mutants - stress - biosynthesis - expression
Over the past few decades seed physiology research has contributed to many important scientific discoveries and has provided valuable tools for the production of high quality seeds. An important instrument for this type of research is the accurate quantification of germination; however gathering cumulative germination data is a very laborious task which is often prohibitive to the execution of large experiments. In this paper we present the Germinator package: a simple, highly cost efficient and flexible procedure for high-throughput automatic scoring and evaluation of germination that can be implemented without the use of complex robotics. The Germinator package contains three modules; 1) design of experimental setup with various options to replicate and randomize samples; 2) automatic scoring of germination based on the color contrast between the protruding radicle and seed coat on a single image; 3) curve fitting of cumulative germination data and the extraction, recap and visualization of the various germination parameters. The curve fitting module enables analysis of general cumulative germination data and can be used for all plant species. We show that the automatic scoring system works for Arabidopsis thaliana and Brassica spp. seeds, but is likely to be applicable to other species, as well. In this paper we show the accuracy, reproducibility and flexibility of the Germinator package. We have successfully applied it to evaluate natural variation for salt tolerance in a large population of Recombinant Inbred Lines (RIL) and were able to identify several QTL for salt tolerance. Germinator is a low-cost package that allows the monitoring of several thousands of germination tests, several times a day by a single person.
ABA Inhibits Embryo Cell Expansion and Early Cell Division Events During Coffee (Coffea arabica 'Rubi') Seed Germination
Silva, E.A.A. da; Toorop, P.E. ; Lammeren, A.A.M. van; Hilhorst, H.W.M. - \ 2008
Annals of Botany 102 (2008)3. - ISSN 0305-7364 - p. 425 - 433.
abscisic-acid - tomato seeds - endosperm development - arabidopsis-thaliana - replication - gibberellin - cytoskeleton - deficient - dormancy
Background and Aims: Coffee seed germination represents an interplay between the embryo and the surrounding endosperm. A sequence of events in both parts of the seed determines whether germination will be successful or not. Following previous studies, the aim here was to further characterize the morphology of endosperm degradation and embryo growth with respect to morphology and cell cycle, and the influence of abscisic acid on these processes. Methods: Growth of cells in a fixed region of the axis was quantified from light micrographs. Cell cycle events were measured by flow cytometry and by immunocytochemistry, using antibodies against ß-tubulin. Aspects of the endosperm were visualized by light and scanning electron microscopy. Key Results: The embryonic axis cells grew initially by isodiametric expansion. This event coincided with reorientation and increase in abundance of microtubules and with accumulation of ß-tubulin. Radicle protrusion was characterized by a shift from isodiametric expansion to elongation of radicle cells and further accumulation of ß-tubulin. Early cell division events started prior to radicle protrusion. Abscisic acid decreased the abundance of microtubules and inhibited the growth of the embryo cells, the reorganization of the microtubules, DNA replication in the embryonic axis, the formation of a protuberance and the completion of germination. The endosperm cap cells had smaller and thinner cell walls than the rest of the endosperm. Cells in the endosperm cap displayed compression followed by loss of cell integrity and the appearance of a protuberance prior to radicle protrusion. Conclusions: Coffee seed germination is the result of isodiametric growth of the embryo followed by elongation, at the expense of integrity of endosperm cap cells. The cell cycle, including cell division, is initiated prior to radicle protrusion. ABA inhibits expansion of the embryo, and hence subsequent events, including germination. Key words: Abscisic acid, ß-tubulin, Coffea arabica, coffee seed, cell morphology, germination, microtubules
The SWI/SNF chromatin-remodeling gene AtCHR12 mediates temporary growth arrest in Arabidopsis thaliana upon perceiving environmental stress
Mlynarova, L. ; Nap, J.P.H. ; Bisseling, T. - \ 2007
The Plant Journal 51 (2007)5. - ISSN 0960-7412 - p. 874 - 885.
pea axillary buds - transcriptional regulation - expression - complexes - proteins - plants - identification - activation - dormancy - tobacco
One of the earliest responses of plants to environmental stress is establishing a temporary growth arrest that allows adaptation to adverse conditions. The response to abiotic stress requires the modulation of gene expression, which may be mediated by the alteration of chromatin structures. This alteration can be accomplished with the help of chromatin-remodeling enzymes, such as the various SWI/SNF classes of ATPases. Here, we investigate the role of the Arabidopsis SNF2/Brahma-type AtCHR12 chromatin-remodeling gene in plant growth and development in reaction to adverse environmental conditions. We show that the AtCHR12 chromatin-remodeling gene plays a vital role in mediating the temporary growth arrest of Arabidopsis that is induced upon perception of stress. Exposing an AtCHR12 overexpressing mutant to stress conditions leads to growth arrest of normally active primary buds, as well as to reduced growth of the primary stem. In contrast, the AtCHR12 knockout mutant shows less growth arrest than the wild-type when exposed to moderate stress. Without stress, mutant plants are indistinguishable from the wild-type, and the growth arrest response seems to depend on the severity of the stress applied. Modulation of AtCHR12 expression correlates with changes in expression of dormancy-associated genes. This is in agreement with the concept of AtCHR12 participation in priming the plants for the growth arrest response. Our data indicate that AtCHR12-associated growth arrest differs from DELLA-mediated growth restraint. This establishes AtCHR12 as a novel gene involved in the response repertoire of plants that permits flexible modulation of growth in adverse and/or otherwise limiting environments.
Germination ecophysiology of Annona crassiflora Mart. seeds
Silva, E.A.A. da; Melo, D.L.B. de; Davide, A.C. ; Bode, N. ; Abreu, G.B. ; Faria, J.M.R. ; Hilhorst, H.W.M. - \ 2007
Annals of Botany 99 (2007)5. - ISSN 0305-7364 - p. 823 - 830.
arabidopsis-thaliana - endosperm - dormancy - embryo - light
Background and Aims Little is known about environmental factors that break morphophysiological dormancy in seeds of the Annonaceae and the mechanisms involved. The aim of this study was to characterize the morphological and physiological components of dormancy of Annona crassiflora, a tree species native to the Cerrado of Brazil, in an ecophysiological context. Methods Morphological and biochemical characteristics of both embryo and endosperm were monitored during dormancy break and germination at field conditions. Seeds were buried in the field and exhumed monthly for 2 years. Germination, embryo length and endosperm digestion, with endo-beta-mannanase activity as a marker, were measured in exhumed seeds, and scanning electron microscopy was used to detect cell division. The effect of constant low and high temperatures and exogenous gibberellins on dormancy break and germination was also tested under laboratory conditions. Key Results After burial in April, A. crassiflora seeds lost their physiological dormancy in the winter months with lowest monthly average minimum temperatures (May-August) prior to the first rainfall of the wet season. The loss of physiological dormancy enabled initiation of embryo growth within the seed during the first 2 months of the rainy season (September-October), resulting in a germination peak in November. Embryo growth occurred mainly through cell expansion but some dividing cells were also observed. Endosperm digestion started at the micropylar side around the embryo and diffused to the rest of the endosperm. Exogenous gibberellins induced both embryo growth and endo-beta-mannanase activity in dormant seeds. Conclusions The physiological dormancy component is broken by low temperature and/or temperature fluctuations preceding the rainy season. Subsequent embryo growth and digestion of the endosperm are both likely to be controlled by gibberellins synthesized during the breaking of physiological dormancy. Radicle protrusion thus occurred at the beginning of the rainy season, thereby maximizing the opportunity for seedlings to emerge and establish.
Effect of stale seedbed preparations and subsequent weed control in lettuce (cv. Iceboll) on weed densities
Riemens, M.M. ; Weide, R.Y. van der; Bleeker, P.O. ; Lotz, L.A.P. - \ 2007
Weed Research 47 (2007)2. - ISSN 0043-1737 - p. 149 - 156.
onkruidbestrijding - zaaibedbereiding - zaaibedden - onkruidwieders - eggen - schoffels - glyfosaat - rotatiewieders - lactuca sativa - slasoorten - weed control - seedbed preparation - seedbeds - weeders - harrows - hoes - glyphosate - rotary weeders - lactuca sativa - lettuces - soybean glycine-max - light environment - short-duration - germination - soil - dormancy - induction - tillage - photocontrol - sensitivity
The effects of stale seedbed preparations and several weed control methods on the emergence of weeds in lettuce were studied. The specific goal was to evaluate the use of a stale seedbed in combination with chemical or mechanical weed control methods in the field. Depending on location and year, stale seedbed preparations followed by weed control prior to planting reduced the amount of weeds during crop growth by 43¿83%. Control of the emerged seedlings after a stale seedbed preparation was more effective with glyphosate than with a rotary harrow. Covering the rotary harrow during control to prevent light reaching the soil improved its effect on the weed density during crop growth in two of 3 years. Radiation with far red light (FR) did not reduce the number of emerging weeds in this study. Mechanical control by finger weeder, torsion weeder and hoe was applied without stale seedbed preparations. These measures reduced the weed densities by 88¿99%, compared with the untreated control and were more effective than chemical weed control with carbetamide and chlorpropham. The results show that the stale seedbed technique in combination with mechanical control of emerging weeds can reduce the weed population during crop growth as effectively as chemical control. The technique may therefore help reduce the use of herbicides in lettuce crops in the future.
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