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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Greenery and Work : The positive effects of greenery in urban environments
Hiemstra, J.A. ; Vries, S. de; Spijker, J.H. - \ 2019
Wageningen : Wageningen University & Research - 6 p.
offices - work - climate - health - well-being - stress - stress tolerance - labour - kantoren - werk - klimaat - gezondheid - welzijn - stresstolerantie - arbeid (werk)
Greenery in and around offices and other working environments is good for both the indoor and outdoor climate, and has a positive effect on the health and general well-being of employees and visitors. It aids concentration, helps reduce stress and increases staff productivity. This document provides information on the benefits of greenery in relation to work and well-being, including references to scientific literature. It concludes with some tips on how to ensure the successful and beneficial inclusion of greenery.
Plant behaviour under combined stress : tomato responses to combined salinity and pathogen stress
Bai, Yuling ; Kissoudis, Christos ; Yan, Zhe ; Visser, Richard G.F. ; Linden, Gerard van der - \ 2018
The Plant Journal 93 (2018)4. - ISSN 0960-7412 - p. 781 - 793.
combined biotic and abiotic stresses - plant disease - resistance gene - salinity stress - stress interaction - stress tolerance
Crop plants are subjected to a variety of stresses during their lifecycle, including abiotic stress factors such as salinity and biotic stress factors such as pathogens. Plants have developed a multitude of defense and adaptation responses to these stress factors. In the field, different stress factors mostly occur concurrently resulting in a new state of stress, the combined stress. There is evidence that plant resistance to pathogens can be attenuated or enhanced by abiotic stress factors. With stress tolerance research being mostly focused on plant responses to individual stresses, the understanding of a plant's ability to adapt to combined stresses is limited. In the last few years, we studied powdery mildew resistance under salt stress conditions in the model crop plant tomato with the aim to understand the requirements to achieve plant resilience to a wider array of combined abiotic and biotic stress combinations. We uncovered specific responses of tomato plants to combined salinity-pathogen stress, which varied with salinity intensity and plant resistance genes. Moreover, hormones, with their complex regulation and cross-talk, were shown to play a key role in the adaptation of tomato plants to the combined stress. In this review, we attempt to understand the complexity of plant responses to abiotic and biotic stress combinations, with a focus on tomato responses (genetic control and cross-talk of signaling pathways) to combined salinity and pathogen stresses. Further, we provide recommendations on how to design novel strategies for breeding crops with a sustained performance under diverse environmental conditions.
Greenery and Work : A summary of the positive effects of greenery on well-being in working environments
Hiemstra, J.A. ; Vries, S. de; Spijker, J.H. - \ 2017
Wageningen : Wageningen University & Research - 6 p.
offices - work - climate - health - well-being - stress - stress tolerance - labour - kantoren - werk - klimaat - gezondheid - welzijn - stresstolerantie - arbeid (werk)
Greenery in and around offices and other working environments is good for both the indoor and outdoor climate, and has a positive effect on the health and general well-being of employees and visitors. It aids concentration, helps reduce stress and increases staff productivity. This document provides information on the benefits of greenery in relation to work and well-being, including references to scientific literature. It concludes with some tips on how to ensure the successful and beneficial inclusion of greenery.
Stress speelt een belangrijke rol : inzicht in koploosheid groeit door gezamenlijk onderzoek
Groot, S.P.C. ; Kierkels, T. ; Heuvelink, E. - \ 2016
Onder Glas 13 (2016)8. - p. 30 - 31.
tuinbouw - groenten - landbouwkundig onderzoek - groeistoornis - plantenontwikkeling - verlichting - tomaten - capsicum - brassica - gypsophila - stresstolerantie - temperatuur - horticulture - vegetables - agricultural research - failure to thrive - plant development - lighting - tomatoes - stress tolerance - temperature

Jonge tomaten- en paprikaplanten, maar ook een aantal andere gewassen, houden soms opeens op met groeien. Koploosheid was lange tijd een lastig maar zeer slecht begrepen fenomeen. De laatste jaren is het inzicht in een stroomversnelling gekomen. In ieder geval is het aantal mogelijke oorzaken drastisch ingeperkt.
Heat stress tolerance responses in developing tomato anthers
Bita, Elena - \ 2016
Wageningen University. Promotor(en): Gerco Angenent, co-promotor(en): Christian Bachem. - Wageningen : Wageningen University - ISBN 9789462577701 - 109
tomatoes - solanum lycopersicum - anthers - heat stress - stress tolerance - heat tolerance - heat shock - transcriptomics - reproductive performance - gene expression profiling - meiosis - tomaten - solanum lycopersicum - helmknoppen - warmtestress - stresstolerantie - hittetolerantie - hitteshock - transcriptomica - voortplantingsvermogen - genexpressieprofilering - meiose

Global warming already has and will significantly impact crop productivity and yield in the near future. In order to meet the forecasted requirements of the future agricultural production, a proper assessment of crops environmental stress tolerance needs to be designed and implemented, from the laboratory to field. Genetic variation in the ability of tomatoes to set fruit under high temperature conditions has made selection for heat tolerance possible and multiple opportunities for improvement exist, as tolerance to high temperatures is a multi-genic character involving a complex network of chaperones and other protective proteins acting together to defend the cells from heat injury. Breeding programs involved in the development of heat tolerant cultivars should identify and make use of such tolerance traits already available in collected or wild germplasm.

The goal of this thesis was to characterize the response to high temperatures in meiotic tomato anthers with contrasting responses to heat and to identify genes that could be related to thermo-tolerance mechanisms during gamete development. Several molecular tools such as transcriptomic profiling by cDNA-AFLP and microarray analysis, RT-PCR or in situ RNA hybridisation were used to achieve this goal.

The second chapter reviews the effects of heat stress on reproductive flower development, candidate tolerance pathways and methods for production of heat tolerant crops.

The third chapter provides a general overview of the expression changes occurring in the developing anthers of a sensitive tomato genotype following exposure to a (short and) moderate high temperature stress (MHS). Using a combination of cDNA-AFLP, RT-PCR, and in situ RNA hybridisation, we characterized and verified the general transcriptional response to heat of tomato plants. Our results revealed that approximately 1% of the examined transcript-derived fragments exhibit alterations in expression pattern and the majority of these were down-regulated The putative functions associated with the genes identified by cDNA-AFLP indicated involvement of heat shock, metabolism, antioxidant and developmental processes. Based upon the observed transcriptional changes in response to MHS and on literature sources, we identified a number of candidate transcripts to be involved in heat-tolerance. The spatial expression of several such candidate genes was further examined using in situ RNA hybridisation and this showed that the investigated genes are expressed in the tapetum or/and in developing microspores. Furthermore, the expression of several candidate genes has been quantified by RT-PCR in additional genotypes with different degrees of heat tolerance. The results suggested a correlation between gene expression levels, pollen germination rates and tolerance to heat (Chapter 4).

In the fourth chapter we proceeded to profile the response to heat of meiotic anthers in a tolerant and a sensitive tomato genotype and investigated the expression of the identified candidate genes in several pairs of contrasting genotypes. Using microarray analysis (for an extensive overview of the meiotic response to heat) and RT-PCR, we were able to clearly distinguish differential responses of the tolerant genotype. After 2h of moderate heat stress, the heat-tolerant genotype exhibits fewer transcriptional changes than the heat-sensitive genotype. In the heat-tolerant genotype, the majority of changes in gene expression is represented by up-regulation, while in the heat-sensitive genotype there is a general trend to down-regulate gene expression soon after MHS. Moreover, the heat-tolerant genotype also shows a different level of constitutive gene expression profiles when compared to the heat-sensitive genotype indicating a difference in genetic adaptation with regards to increased temperatures. The putative functions associated with the genes identified by microarray profiling indicate involvement of heat shock, antioxidant, metabolic, and cell development pathways. Based upon the observed differences in response to MHS we selected a number of candidate transcripts involved in heat-tolerance and confirmed their expression pattern in different tomato genotypes with contrasting responses to heat. The results suggested that the candidate genes are involved in the activation of protection mechanisms in the tomato anthers during moderate heat stress and, could therefore contribute to normal growth and development of the male gametophyte and implicitly a successful fruit set under adverse temperatures.

In the fifth chapter we tested the hypothesis that heat tolerance is associated with maintenance of organ identity, fertility and lower ABA levels during heat stress (for several tomato genotypes) and analysed the dynamics of ABA accumulation under temperature stress in several tomato genotypes with contrasting responses to heat. Furthermore, pollen germination tests were performed and additional physiological aspects of anther development for each genotype were analysed as well. The general trend observed was the accumulation of lower relative levels of ABA at the end of the experimental period compared to the initial stages in more tolerant genotypes and of higher levels in the sensitive genotypes. We concluded from these results that the morphological changes in the floral tissues and the overall changes in ABA levels are correlated with the molecular responses under increased temperature in the genotypes analysed. Whether these correlations are causally related is not clear; therefore more research is needed to resolve these issues.

The sixth chapter examines our analysis of the heat stress response in meiotic tomato anthers in a broader scientific context. I discuss the different aspects of our results and present several candidate genes involved in plant thermo-tolerance. In addition, I also discuss the potential involvement of plant growth regulators in plants´ responses to heat stress and suggest various potential follow-up experimental strategies.

Quantitative and ecological aspects of Listeria monocytogenes population heterogeneity
Metselaar, K.I. - \ 2016
Wageningen University. Promotor(en): Marcel Zwietering; Tjakko Abee, co-promotor(en): Heidy den Besten. - Wageningen : Wageningen University - ISBN 9789462577664 - 173
listeria - listeria monocytogenes - stress - stress tolerance - ribosomes - proteins - lactobacillus plantarum - behaviour - ecological assessment - genome analysis - dna sequencing - resistance - heterogeneity - listeria - listeria monocytogenes - stress - stresstolerantie - ribosomen - eiwitten - lactobacillus plantarum - gedrag - ecologische beoordeling - genoomanalyse - dna-sequencing - weerstand - heterogeniteit

Bacterial stress response and heterogeneity therein is one of the biggest challenges posed by minimal processing. Heterogeneity and resulting tailing representing a more resistant fraction of the population, can have several causes and can be transient or stably in nature. Stable increased stress resistance is caused by alterations in the genome and therefore inheritable and is referred to as stable stress resistant variants. Also L. monocytogenes exhibits a heterogeneous response upon stress exposure which can be partially attributed to the presence of stable stress resistant variants. Adverse environments were shown to select for stable stress resistant variants. The objective of the research described in this thesis was to evaluate if L. monocytogenes population diversity and the presence of stable resistant variants is a general phenomenon that is observed upon different types of stress exposure, to get more insight in the mechanisms leading to increased resistance and to evaluate the ecological behaviour and potential impact on food safety of these stable resistant variants. Acid stress was chosen as it is an important hurdle both in food preservation, as well as in stomach survival.

First, the non-linear inactivation kinetics of L. monocytogenes upon acid exposure were quantitatively described. A commonly used biphasic inactivation model was reparameterized, which improved the statistical performance of the model and resulted in more accurate estimation of the resistant fraction within L. monocytogenes WT populations. The observed tailing suggested that stable stress resistant variants might also be found upon acid exposure. Indeed, 23 stable acid resistant variants of L. monocytogenes LO28 were isolated from the tail after exposure of late-exponential phase cells to pH 3.5 for 90 min, with different degrees of acid resistance amongst them. Increased acid resistance showed to be significantly correlated to reduced growth rate. Studying the growth boundaries of the WT and a representative set of variants indicated that the increased resistance of the variants was only related to survival of severe pH stress but did not allow for better growth or survival at mild pH stress.
A set of variants were further characterized phenotypically and cluster analysis was performed. This resulted in three clusters and four individual variants and revealed multiple-stress resistance, with both unique and overlapping features related to stress resistance, growth, motility, biofilm formation and virulence indicators. A higher glutamate decarboxylase (GAD) activity correlated with increased acid resistance. Whole genome sequencing of a set of variants was performed and revealed mutations in rpsU, encoding ribosomal protein S21. This rpsU mutation was found in all 11 variants comprising the largest phenotypic cluster, indicating a potential role of this ribosomal protein in stress resistance. Mutations in ctsR, which were previously shown to be responsible for increased resistance of heat and HHP resistant variants, were not found in the acid resistant variants. This underlined that large population diversity exists within one L. monocytogenes strain and that different adverse conditions drive selection for different variants.

Next, the performance in mixed species biofilms with Lactobacillus plantarum was evaluated, as well as their benzalkonium chloride (BAC) resistance in these biofilms. It was hypothesized that the acid resistant variants might also show better survival in biofilms with L. plantarum, which provide an acidic environment by lactose fermentation with pH values below the growth boundary of L. monocytogenes when biofilms mature. L. monocytogenes LO28 WT and eight acid resistant variants were capable of forming mixed biofilms with L. plantarum at 20°C and 30°C in BHI supplemented with manganese and glucose. Some of the variants were able to withstand the low pH in the mixed biofilms for a longer time than the WT and there were clear differences in survival between the variants which could not be correlated to (lactic) acid resistance alone. Adaptation to mild pH of liquid cultures during growth to stationary phase increased the acid resistance of some variants to a greater extent than of others, which could be correlated to increased survival in the mixed biofilms. There were no clear differences in BAC resistance between the wild type and variants in mixed biofilms.

Lastly, a set of robustness and fitness parameters of WT and variants was obtained and used to model their growth behaviour under combined mild stress conditions and to model their performance in a simulated food chain. This gave more insight in the trade-off between increased stress resistance and growth capacity. Predictions of performance were validated in single and mixed cultures by plate counts and by qPCR in which WT and an rpsU deletion variant were distinguished by specific primers. Growth predictions for WT and rpsU deletion variant were matching the experimental data generally well. Globally, the variants are more robust than the WT but the WT grows faster than most variants. Validation of performance in a simulated food chain consisting of subsequent growth and inactivation steps, confirmed the trend of higher growth fitness and lower stress robustness for the WT compared to the rpsU variant. This quantitative data set provides insights into the conditions which can select for stress resistant variants in industrial settings and their potential persistence in food processing environments.

In conclusion, the work presented in this thesis highlights the population diversity of L. monocytogenes and the impact of environmental conditions on the population composition, which is of great importance for minimal processing. The work of this thesis resulted in more insight in the mechanisms underlying increased resistance of stress resistant variants and quantitative data on the behaviour of stress resistant variants which can be implemented in predictive microbiology and quantitative risk assessments aiming at finding the balance between food safety and food quality.

Supplementary data: Combined biotic and abiotic stress resistance in tomato
Kissoudis, C. ; Chowdhury, Rawnaq ; Heusden, A.W. van; Wiel, C.C.M. van de; Finkers, H.J. ; Visser, R.G.F. ; Bai, Y. ; Linden, C.G. van der - \ 2016
solanum lycopersicum - tomatoes - disease resistance - stress tolerance - defence mechanisms - plant diseases - abiotic injuries - stress response - phenotypic variation - genetic analysisplant breeding - salt tolerance
Abiotic and biotic stress factors are the major constrains for the realization of crop yield potential. As climate change progresses, the spread and intensity of abiotic as well as biotic stressors is expected to increase, with increased probability of crops being exposed to both types of stress. Shielding crops from combinatorial stress requires a better understanding of the plant’s response and its genetic architecture. In this study, we evaluated resistance to salt stress, powdery mildew and to both stresses combined in tomato, using the S. habrochaites LYC4 introgression line (IL) population. The IL population segregated for both salt stress tolerance and powdery mildew resistance. Using SNP array marker data, QTLs were identified for salt tolerance as well as Na+ and Cl- accumulation. Salt stress increased the susceptibility of the population to powdery mildew in an additive manner. Phenotypic variation for disease resistance was reduced under combined stress as indicated by the coefficient of variation (CV). No correlation was found between disease resistance and Na+ and Cl- accumulation under combined stress Most genetic loci were specific for either salt stress tolerance or powdery mildew resistance. These findings increase our understanding of the genetic regulation of responses to abiotic and biotic stress combinations and can provide leads to more efficiently breeding for tomatoes and other crops with a high level of disease resistance while maintaining their performance in combination with abiotic stress.
Supplementary data: Responses to combined abiotic and biotic stress in tomato are governed by stress intensity and mechanism of resistance
Kissoudis, C. ; Sri Sunarti, Sri ; Wiel, C.C.M. van de; Visser, R.G.F. ; Linden, C.G. van der; Bai, Y. - \ 2016
solanum lycopersicum - tomatoes - disease resistance - stress tolerance - defence mechanisms - plant diseases - abiotic injuries - stress response - phenotypic variation - genetic analysisplant breeding - salt tolerance
Stress conditions in agricultural ecosystems can occur in variable intensities. Different resistance mechanisms to abiotic stress and pathogens are deployed by plants. Thus, it is important to examine plant responses to stress combinations under different scenarios. Here, we evaluated the effect of different levels of salt stress ranging from mild to severe (50, 100 and 150mM NaCl) on powdery mildew (PM) resistance and overall performance of tomato introgression lines with contrasting levels of partial resistance, as well as isogenic lines carrying the PM resistance genes Ol-1 (associated with slow Hypersensitivity Response; HR), ol-2 (a mlo mutant associated with papilla formation) and Ol-4 (a R gene associated with fast HR). PM resistance was affected by salt stress in a genotype and stress intensity dependent manner. In susceptible and partial resistant lines, increased susceptibility was observed under mild salt stress (50mM) which was accompanied with accelerated cell death-like senescence. On the contrary, severe salt stress (150mM) reduced disease symptoms. Na+ and Cl- accumulation in the leaves was linearly related to the decreased pathogen growth under severe stress, suggesting a more direct role for the salt in suppressing PM growth. In contrast, complete resistance mediated by ol-2 and Ol-4 was unaffected under all treatment combinations, and was associated with a decreased growth penalty. Increased susceptibility and senescence under combined stress of the variety Moneymaker (MM) and the NIL Ol-1 was associated with the induction of ethylene and jasmonic acid pathway genes as well as of the cell wall invertase gene LIN6. These results highlight the significance of stress severity and resistance type on the plant’s performance under abiotic and biotic stress combination.
Supplementary data: Hormone signalling regulation of tomato response to combined biotic and abiotic stress
Kissoudis, C. ; Sri Sunarti, Sri ; Wiel, C.C.M. van de; Visser, R.G.F. ; Linden, C.G. van der; Bai, Y. - \ 2016
solanum lycopersicum - tomatoes - disease resistance - stress tolerance - defence mechanisms - plant diseases - abiotic injuries - stress response - phenotypic variation - genetic analysisplant breeding - salt tolerance
Plant hormones are paramount to plant adaptation to changing environmental conditions and interactions with microorganisms. There is currently limited knowledge on their significance in the response to stress combination. Using near isogenic lines (NILs) that carry the Ol-1, ol-2 and Ol-4 gene for resistance to tomato powdery mildew caused by Oidium neolycopersici, this study focused on the responses of these NILs to powdery mildew and salt stress combination. In these NILs, marker genes for monitoring hormonal pathways showed differential expression pattern upon powdery mildew infection. Further by crossing these NILs with tomato mutants notabilis (ABA-deficient), defenseless1 (JA-deficient) and epinastic (ET overproducer) the cross-talk among hormonal pathways was further investigated. Among the mutants, epinastic resulted in increased susceptibility of NIL-Ol-1 and breakdown of NIL-ol-2 resistance, accompanied by reduced callose deposition, effects that were more pronounced under combination with salt stress. On the other hand notabilis, resulting in H2O2 overproduction greatly reduced susceptibility of NIL-Ol-1 under combined stress accompanied however by heightened sensitivity to salt stress. Callose deposition reduction led to partial resistance breakdown in NIL-ol-2 which was reversed under combined stress. NIL-Ol-4 resistance remained robust across all mutant and treatment combinations. We discuss the critical role that hormone signalling appears to have for the outcome of combined stress and powdery mildew in terms of resistance and plant fitness integrating observations from physiological, histochemical and gene expression analyses. These significant insights obtained extend our understanding of hormonal regulation of combined stress responses and can aid in narrowing down targets for improving crop performance under stress combinations.
Supplementary data: Roles and contribution of tomato WRKY genes to salt stress and powdery mildew resistance
Kissoudis, C. ; Gao, D. ; Pramanik, Dewi ; Birhanu, Mengistu ; Wiel, C.C.M. van de; Visser, R.G.F. ; Bai, Y. ; Linden, C.G. van der - \ 2016
solanum lycopersicum - tomatoes - disease resistance - stress tolerance - defence mechanisms - plant diseases - abiotic injuries - stress response - phenotypic variation - genetic analysisplant breeding - salt tolerance
WRKY is a transcription factor family unique to plants with diverse functions in defense pathways, abiotic stress tolerance and developmental programs. Family members are characterized by the conserved WRKY domain and significant sequence variation in the remainder of the protein, which is translated into distinct functions even for closely related genes. We utilized the extensive functional characterization of the Arabidopsis thaliana WRKY family to identify tomato homologues of Arabidopsis WRKY genes that are involved in defense responses (AtWRKY 11, 29, 48, 70 and 72). In total 13 tomato WRKY homologues were identified for these genes, of which 9 were successfully over-expressed, and 12 stably silenced via RNAi in transgenic tomato lines. The transgenic lines were evaluated for their response to salt stress, powdery mildew resistance and the combination of these stresses. Lines overexpressing SlWRKY11 and SlWRKY23, and RNAi lines of SlWRKY7 and SlWRKY9 showed both increased biomass and improved salt tolerance. For SlWRKY11 and SlWRKY23 overexpression (OE) lines, this was accompanied by a moderate increase in oxidative stress tolerance. The SlWRKY6-OE line showed strongly improved salt stress tolerance, but a growth penalty under control conditions. Exceptional phenotypes were observed for the SlWRKY10-OE line (stunted growth) and the RNAi line SlWRKY23-RNAi (necrotic symptoms), but these phenotypes were partly restored to normal under salt stress. Both these lines exhibited increased resistance to powdery mildew, but this was compromised when the plants were put under salt-stress as well. Important functions for tomato WRKY genes were revealed in both the abiotic and biotic stress response and several genes should be further explored to elucidate their downstream regulatory functions that lead to increased stress tolerance.
Desiccation tolerance in seeds and plants
Dias Costa, M.C. - \ 2016
Wageningen University. Promotor(en): Harro Bouwmeester; Henk Hilhorst; Wilco Ligterink. - Wageningen : Wageningen University - ISBN 9789462576278 - 183
desiccation tolerance - tolerance - plants - seeds - plant physiology - stress tolerance - drought resistance - abscisic acid - uitdrogingstolerantie - tolerantie - planten - zaden - plantenfysiologie - stresstolerantie - droogteresistentie - abscisinezuur

The interest of research groups in desiccation tolerance (DT) has increased substantially over the last decades. The emergence of germinated orthodox seeds and resurrection plants as main research models has pushed the limits of our knowledge beyond boundaries. At the same time, new questions and new challenges were posed. The work presented in this thesis aims at shedding light on some of these questions, deepening our understanding of DT and providing relevant information to improve stress resistance in crops.

Chapter 2 is a survey of the literature and discusses the ecological and evolutionary significance for seeds to be able to re-acquire DT after germination. This chapter also discusses recent progress in DT studies using developing and germinated seeds of the model plants Arabidopsis thaliana and Medicago truncatula.

In Chapter 3 I used microarray data from a time series of DT re-acquisition, together with network analysis of gene expression, to gain temporal resolution and identify relevant genes involved in the re-acquisition of DT in germinated A. thaliana seeds by incubation in abscisic acid (ABA). Overall, genes related to protection, response to stresses, seed development and seed dormancy were up-regulated, whereas genes related to cell growth and photosynthesis were down-regulated with time. Genes that respond early to exogenous ABA were related to wax biosynthetic processes, lipid storage, seed development and response to ABA stimulus. Genes that respond late to exogenous ABA were related to syncytium formation and response to abiotic stimulus (mainly light stimulus). The robustness of the network was confirmed by the projection of sets of genes – related to the acquisition of DT, seed dormancy, drought responses of adult plants and re-induction of DT by polyethylene glycol – on this network.

In Chapter 4 the relation between DT in germinated seeds and drought resistance in adult plants is analysed, using rice (Oryza sativa) as experimental model. Considering the predictions of a future with lower availability of fresh water, efforts to increase rice drought tolerance without reducing yield are increasingly important. The results presented in this chapter suggest that the intrinsic mechanisms of drought tolerance in adult plants are part of the mechanisms used by seeds to tolerate desiccation, but the molecular nature of these mechanisms remains elusive.

Chapter 5 explores the relation between DT and longevity in germinated seeds of the Brazilian tree species Sesbania virgata as experimental model. DT and longevity are acquired by orthodox seeds during the maturation phase of development and lost upon germination. DT can be re-induced in germinated seeds by an osmotic and/or ABA treatment, but there is no information on how these treatments affect seed longevity. S. virgata seeds lose DT slowly upon radicle growth. The radicle appeared to be the most sensitive organ and the cotyledons the most resistant. The ability to produce lateral roots was key for whole seedling survival. An osmotic treatment improved DT in germinated S. virgata seeds, but not longevity. This implies that DT and seed longevity can be uncoupled.

Xerophyta viscosa is one of the best studied resurrection species. Despite the fact that adult plants and mature seeds display DT, young X. viscosa seedlings are sensitive to fast drying. A treatment with ABA can induce DT early in shoots of these seedlings, but not in roots. Chapter 6 addresses the changes in the transcriptome and proteome of X. viscosa seedlings during induction of DT. A draft genome sequence of X. viscosa was used to improve transcript and protein identification and annotation. Differences in ABA signalling and the cross talk between ABA and ethylene were presented as determinant for shoot and root responses. Moreover, differences in the accumulation of late embryogenesis abundant proteins were also shown as being key for DT in shoots and roots.

In Chapter 7, DT-transcriptomes of distantly related organisms are compared and surveyed for a core set of genes representing the signatures of critical adaptive DT mechanisms. A shortlist of 260 genes emerged, with a significant number of genes under the control of ABI3 and related to dormancy. The results reinforced the idea that core mechanisms and key regulators involved in DT developed early in the history of life and were carried forward by diverse species and life forms in a conserved manner and in conjunction with dormancy.

In Chapter 8, the findings of this thesis are integrated, showing how they can contribute to future improvement of stress tolerance in crops. The ability of germinated seeds to re-acquire DT is discussed in combination with dormancy and longevity and related to seed survival under unfavourable environmental conditions. The relationship between drought- and desiccation tolerance and the role of ABA are presented briefly. Possible approaches to mine for new genes for crop improvement, such as searching for conserved genes and analysing new genome sequences, are addressed. Finally, a new perspective of the way to consider the evolution of DT is proposed.

Genetics and regulation of combined abiotic and biotic stress tolerance in tomato
Kissoudis, C. - \ 2016
Wageningen University. Promotor(en): Richard Visser, co-promotor(en): Gerard van der Linden; Yuling Bai. - Wageningen : Wageningen University - ISBN 9789462576568 - 212
solanum lycopersicum - tomatoes - disease resistance - stress tolerance - defence mechanisms - plant diseases - abiotic injuries - stress response - phenotypic variation - genetic analysis - plant breeding - salt tolerance - solanum lycopersicum - tomaten - ziekteresistentie - stresstolerantie - verdedigingsmechanismen - plantenziekten - abiotische beschadigingen - stressreactie - fenotypische variatie - genetische analyse - plantenveredeling - zouttolerantie

Projections on the impact of climate change on agricultural productivity foresee prolonged and/or increased stress intensities and enlargement of a significant number of pathogens habitats. This significantly raises the occurrence probability of (new) abiotic and biotic stress combinations. With stress tolerance research being mostly focused on responses to individual stresses, our understanding of plants’ ability to adapt to combined stresses is limited.

In an attempt to bridge this knowledge gap, we hierarchized in chapter 1 existing information on individual abiotic or biotic stress adaptation mechanisms taking into consideration different anatomical, physiological and molecular layers of plant stress tolerance and defense. We identified potentially crucial regulatory intersections between abiotic and biotic stress signalling pathways following the pathogenesis timeline, and emphasized the importance of subcellular to whole plant level interactions by successfully dissecting the phenotypic response to combined stress. We considered both explicit and shared adaptive responses to abiotic and biotic stress, which included amongst others R-gene and systemic acquired resistance as well as reactive oxygen species (ROS), redox and hormone signalling, and proposed breeding targets and strategies.

In chapter 3 we focused on salt stress and powdery mildew combination in tomato, a vegetable crop with a wealth of genetic resources, and started with a genetic study. S. habrochaites LYC4 was found to exhibit resistance to both salt stress and powdery mildew. A LYC4 introgression line (IL) population segregated for both salt stress tolerance and powdery mildew resistance. Introgressions contributing to salt tolerance, including Na+ and Cl- accumulation, and powdery mildew resistance were precisely pinpointed with the aid of SNP marker genotyping. Salt stress (100mM NaCl) combined with powdery mildew infection increased the susceptibility of the population to powdery mildew in an additive manner, while decreasing the phenotypic variation for this trait. Only a few overlapping QTLs for disease resistance and salt stress tolerance were identified (one on a short region at the top of Chromosome 9 where numerous receptor-like kinases reside). Most genetic loci were specific for either salt stress tolerance or powdery mildew resistance indicating distinct genetic architectures. This enables genetic pyramiding approaches to build up combined stress tolerance.

Considering that abiotic stress in nature can be of variable intensities, we evaluated selected ILs under combined stress with salinity ranging from mild to severe (50, 100 and 150mM NaCl) in chapter 4. Mild salt stress (50mM) increased powdery mildew susceptibility and was accompanied by accelerated cell death-like senescence. On the contrary, severe salt stress (150mM) reduced the disease symptoms and this correlated with leaf Na+ and Cl- content in the leaves. The effects of salt stress on powdery mildew resistance may be dependent on resistance type and mechanisms. Near Isogenic Lines (NILs) that carry different PM resistance genes (Ol-1 (associated with slow hypersensitivity response, HR), ol-2 (an mlo mutant associated with papilla formation) and Ol-4 (an R gene associated with fast HR) indeed exhibited differential responses to combined stress. NIL-Ol-1 resembled the LYC4 ILs response, while NIL-ol-2 and NIL-Ol-4 maintained robust resistance and exhibited no senescence symptoms across all combinations, despite the observed reduction in callose deposition in NIL-ol-2. Increased susceptibility, senescence and fitness cost of NIL-Ol-1 under combined stress coincided with high induction of ethylene and jasmonate biosynthesis and response pathways, highly induced expression of cell wall invertase LsLIN6, and a reduction in the expression of genes encoding for antioxidant enzymes. These observations underlined the significance of stress intensity and mechanism of resistance to the outcome of salt stress and powdery mildew combination, underscoring the involvement of ethylene signalling to the susceptibility response under combined stress.

To examine the significance of hormone signalling in combined stress responses we evaluated crosses of tomato hormone mutants notabilis (ABA-deficient), defenseless1 (JA-deficient) and epinastic (ET overproducer) with NIL-Ol-1, NIL-ol-2 and NIL-Ol-4 in chapter 5. The highly pleiotropic epinastic mutant increased susceptibility of NIL-Ol-1, but decreased the senescence response under combined stress, and resulted in partial breakdown of NIL-ol-2 resistance, accompanied by reduced callose deposition. The effects of ET overproduction on susceptibility were more pronounced under combined stress. ABA deficiency in notabilis on the other hand greatly reduced susceptibility of NIL-Ol-1under combined stress at the expense of stronger growth reduction, and induced ROS overproduction. Partial resistance breakdown in the ol-2xnotabilis mutant accompanied by reduced callose deposition was observed, and this was restored under combined stress. Jasmonic acid deficiency phenotypic effects in defenseless mutants were subtle with modest increase in susceptibility for NIL-Ol-1 and NIL-ol-2. For NIL-ol-2 this increased susceptibility was reverted under combined stress. NIL-Ol-4 resistance remained robust across all mutant and treatment combinations. These results highlight the catalytic role of ET and ABA signalling on susceptibility and senescence under combined stress, accentuating concomitantly the importance of signalling fine tuning to minimize pleiotropic effects.

The potential of exploiting transcription factors to enhance tolerance to multiple stress factors and their combination was investigated in chapter 6 through the identification and functional characterization of tomato homologues of AtWRKYs 11, 29, 48, 70 and 72. Thirteen tomato WRKY homologues were identified, of which 9 were overexpressed (using transformation with A. tumefaciens) and 12 stably silenced via RNAi in tomato cultivar Money Maker (MM). SlWRKY11-OE and SlWRKY23-OE overexpressors and RNAi lines of SlWRKY7 and SlWRKY9 showed both increased biomass and relative salt tolerance. SlWRKY6-OE exhibited the highest relative salt stress tolerance, but had strongly decreased growth under control conditions. Exceptional phenotypes under control conditions were observed for SlWRKY10-OE (stunted growth) and SlWRKY23-RNAi (necrotic symptoms). These phenotypes were significantly restored under salt stress, and accompanied by decreased ROS production. Both lines exhibited increased resistance to powdery mildew, but this resistance was compromised under salt stress combination, indicating that these genes have important functions at the intersection of abiotic and biotic stress adaptation. SlWRKY23 appears to have a key regulatory role in the control of abiotic stress/defense and cell death control.

Experimental observations are critically discussed in the General Discussion with emphasis on potential distinctive responses in different pathosystems and abiotic and biotic stress resistance mechanisms as well as genetic manipulations for effectively achieving combined stress tolerance. This includes deployment of individual common regulators as well as pyramiding of non-(negatively) interacting components such as R-genes with abiotic stress resistance genes, and their translation potential for other abiotic and biotic stress combinations. Understanding and improving plant tolerance to stress combinations can greatly contribute to accelerating crop improvement towards sustained or even increased productivity under stress.

Determinants of barley grain yield in a wide range of Mediterranean environments
Francia, E. ; Tondelli, A. ; Rizza, F. ; Badeck, F.W. ; Li Destri Nicosia, O. ; Akar, T. ; Grando, S. ; Al-Yassin, A. ; Benkelkacim, A. ; Thomas, W.T.B. ; Eeuwijk, F.A. van; Romagosa, I. ; Stanca, A.M. ; Pechionni, N. - \ 2011
Field Crops Research 120 (2011)1. - ISSN 0378-4290 - p. 169 - 178.
carbon-isotope discrimination - drought tolerance - stress tolerance - number - genes - wheat - improvement - adaptation - temperature - photoperiod
Barley grain yield in rainfed Mediterranean regions can be largely influenced by terminal drought events. In this study the ecophysiological performance of the ‘Nure’ (winter) × ‘Tremois’ (spring) barley mapping population (118 Doubled Haploids, DHs) was evaluated in a multi-environment trial of eighteen site–year combinations across the Mediterranean Basin during two consecutive harvest years (2004 and 2005). Mean grain yield of sites ranged from 0.07 to 5.43 t ha-1, clearly dependent upon both the total water input (rainfall plus irrigation) and the water stress index (WSI) accumulated during the growing season. All DHs were characterized for possessing molecular marker alleles tagging four genes that regulate barley cycle, i.e. Vrn-H1, Vrn-H2, Ppd-H2 and Eam6. Grain yield differences were initially interpreted in terms of mean differences between genotypes (G), environments (E), and for each combination of genotype and environment (GE) through a “full interaction” ANOVA model. Variance components estimates clearly showed the greater importance of GE over G, although both were much lower than E. Alternative linear and bilinear models of increasing complexity were used to describe GE. A linear model fitting allelic variation at the four genes explained genotype main effect and genotype × environment interaction much better than growth habit itself. Adaptation was primarily driven by the allelic constitution at three out of the four segregating major genes, i.e. Vrn-H1, Ppd-H2 and Eam6. In fact, the three genes together explained 47.2% of G and 26.3% of GE sum of squares. Grain yield performance was more determined by the number of grains per unit area than by the grain weight (phenotypic correlation across all genotypic values: r = 0.948 and 0.559, respectively). The inter-relationships among a series of characters defining grain yield and its components were also explored as a function of the length of the different barley developmental phases, i.e. vegetative, reproductive, and grain filling stages. In most environments, the best performing (adapted) genotypes were those with faster development until early occurrence of anthesis. This confirmed the crucial role of the period defining the number of grains per unit area in grain yield determination under Mediterranean environments
Verbetering acclimatisatie geënt uitgangsmateriaal : inventarisatie van stress bij enten van glasgroenten met MIPS en vermindering uitval tijdens acclimatisatie door Graft Promotors
Snel, J. ; Stevens, L.H. ; Schoor, R. van der; Davelaar, E. ; Dijkhuis, P. ; Jalink, H. ; Krieken, W.M. van der - \ 2010
Wageningen : Plant Research International (Rapport / Plant Research International 363) - 22
tuinbouw - glastuinbouw - glasgroenten - acclimatisatie - conditionering - enten - uitselecteren - stresstolerantie - het enten (grafting) - toegepast onderzoek - horticulture - greenhouse horticulture - greenhouse vegetables - acclimatization - conditioning - scions - culling - stress tolerance - grafting - applied research
In dit project zullen met MIPS nieuwe procedures ontwikkeld worden voor het conditioneren en acclimatiseren van enten van groentengewassen. Met MIPS kunnen de effecten van conditionering en acclimatisering op groei, stress en stressgevoeligheid van de enten in de kas nauwkeurig en snel gemeten worden. Op deze wijze wordt een flink aantal conditionering/acclimatisering combinaties in relatief korte tijd geanalyseerd. Uiteindelijk zal uit deze combinaties een aantal geselecteerd worden voor evaluatie en validatie onder praktijkcondities.
Quantification of Bacillus cereus stress responses
Besten, H.M.W. den - \ 2010
Wageningen University. Promotor(en): Marcel Zwietering; Tjakko Abee, co-promotor(en): Roy Moezelaar. - [S.l. : S.n. - ISBN 9789085857143 - 216
bacillus cereus - stressreactie - zoutgehalte - zouttolerantie - hittetolerantie - adaptatie - weerstand - stresstolerantie - bacillus cereus - stress response - salinity - salt tolerance - heat tolerance - adaptation - resistance - stress tolerance
The microbial stability and safety of minimally processed foods is controlled by a deliberate combination of preservation hurdles. However, this preservation strategy is challenged by the ability of spoilage bacteria and food-borne pathogens to adapt to stressing environments providing cell robustness. Bacillus cereus is a toxin-producing, spore-forming bacterium, and is able to survive minimal processing conditions. A quantitative approach was followed to gain insight in B. cereus’ stress adaptive behavior at population, individual cell and molecular level.
B. cereus’ ability to adapt to salt stress and gain robustness towards subsequent heat challenge-stress exposure was quantified in detail using primary kinetics models. The adaptive salt stress response was influenced by the adaptation-stress concentration, the growth phase of the cells, strain diversity and the culturing temperature during adaptation-stress treatment. The nonlinear nature of the heat inactivation kinetics suggested heterogeneity within the population with respect to stress adaptive behavior. The direct-imaging-based Anopore technology was used to quantitatively describe the population heterogeneity of B. cereus upon mild and severe salt stress treatments and during low temperature growth. Fluorescent labeling of cells provided insights in the origin of stress-induced population heterogeneity. Then, to elucidate adaptive salt stress responses at molecular level, the genome-wide transcriptome profiles of mildly and severely salt-stressed cells were compared. Various transcriptome responses could be correlated to phenotypic features of salt stress-adapted cells. Comparison of the transcriptome profiles of salt stress-adapted cells to those that were exposed to mild heat, acid and oxidative stress, directed to potential cellular biomarkers for stress adaptation. The selected candidate-biomarkers  the transcriptional regulator B (activating general stress responses), catalases (removing reactive oxygen species), and chaperones and proteases (maintaining protein quality)  were measured upon adaptation-stress treatment at transcript, protein and/or activity level, and their induction was correlated to adaptation-stress induced robustness towards challenge-stress. Various candidate-biomarkers were suitable to predict the robustness level of adaptation-stress pretreated cells towards challenge-stress, and are therefore potential predictive cellular indicators for adaptation-stress induced robustness. The predictive potential of transcripts differed from that of proteins and activity level, underlining the significance to evaluate predictive potential of candidate-biomarkers at different functional cell levels. This quantitative understanding of B. cereus’ stress adaptive behavior provides mechanistic insights and opens up avenues to come to a mechanism-based approach for designing mild preservation strategies.
Regulation of cyclic lipopeptide biosynthesis in Pseudomonas fluorescens by the ClpP protease
Bruijn, I. de; Raaijmakers, J.M. - \ 2009
Journal of Bacteriology 191 (2009)6. - ISSN 0021-9193 - p. 1910 - 1923.
syringae pv.-syringae - atp-dependent proteases - escherichia-coli - biofilm formation - bacillus-subtilis - stress tolerance - staphylococcus-aureus - putisolvin-ii - gene-cluster - swarming motility
Cyclic lipopeptides produced by Pseudomonas species exhibit potent surfactant and broad-spectrum antibiotic properties. Their biosynthesis is governed by large multimodular nonribosomal peptide synthetases, but little is known about the genetic regulatory network. This study provides, for the first time, evidence that the serine protease ClpP regulates the biosynthesis of massetolides, cyclic lipopeptides involved in swarming motility, biofilm formation, and antimicrobial activity of Pseudomonas fluorescens SS101. The results show that ClpP affects the expression of luxR(mA), the transcriptional regulator of the massetolide biosynthesis genes massABC, thereby regulating biofilm formation and swarming motility of P. fluorescens SS101. Transcription of luxR(mA) was significantly repressed in the clpP mutant, and introduction of luxR(mA) restored, in part, massetolide biosynthesis and swarming motility of the clpP mutant. Site-directed mutagenesis and expression analyses indicated that the chaperone subunit ClpX and the Lon protease are not involved in regulation of massetolide biosynthesis and are transcribed independently of clpP. Addition of Casamino Acids enhanced the transcription of luxR(mA) and massABC in the clpP mutant, leading to a partial rescue of massetolide production and swarming motility. The results further suggested that, at the transcriptional level, ClpP-mediated regulation of massetolide biosynthesis operates independently of regulation by the GacA/GacS two-component system. The role of amino acid metabolism and the putative mechanisms underlying ClpP-mediated regulation of cyclic lipopeptide biosynthesis, swarming motility, and growth in P. fluorescens are discussed.
Genome-wide screen for Listeria monocytogenes genes important for growth at high temperatures
Veen, S. van der; Abee, T. ; Vos, W.M. de; Wells-Bennik, M.H.J. - \ 2009
FEMS Microbiology Letters 295 (2009)2. - ISSN 0378-1097 - p. 195 - 203.
staphylococcus-aureus - bacillus-subtilis - stress tolerance - escherichia-coli - cell-division - heat-shock - expression - virulence - identification - mutants
Listeria monocytogenes is a Gram-positive food-borne pathogen that is able to grow over a wide temperature range. Although the class I and class III heat-shock genes are known to play an important role in heat shock, information on genes that are essential for growth at high temperatures is scarce. To determine which genes are important for growth at high temperatures (42.5-43 degrees C), we performed a random insertion screening in L. monocytogenes, rendering 28 temperature-sensitive mutants. These mutants showed insertions in genes that play a role in transcription regulation, cell-wall biosynthesis, cell division, translation, transport, sensing, and specific stress responses like the SOS response and the class III heat-shock response. Some of these mutants showed altered morphological characteristics such as cell elongation, reduced cell length, or sickle shapes. Furthermore, the majority of the mutants showed increased heat inactivation after exposure to 55 degrees C compared with the wild-type strain. The role of the specific genes in relation to growth at high temperatures is discussed
Changes in allele frequencies in landraces, old and modern barley cultivars of marker loci close to QTL for grain yield under high and low input conditions
Pswarayi, A. ; Eeuwijk, F.A. van; Ceccarelli, S. ; Grando, S. ; Comadran, J. ; Russell, J.R. ; Pecchioni, N. ; Alessandro, T. ; Akar, T. ; Al-Yassin, A. ; Benbelkacem, A. ; Ouabbou, H. ; Thomas, W.T.B. ; Romagosa, I. - \ 2008
Euphytica 163 (2008)3. - ISSN 0014-2336 - p. 435 - 447.
quantitative trait loci - false discovery rate - field-grown barley - environmental covariables - stress tolerance - adaptation - genotype - genome - maize - dart
Changes in alleles frequencies of marker loci linked to yield quantitative trait loci (QTL) were studied in 188 barley entries (landraces, old and modern cultivars) grown in six trials representing low and high yielding conditions in Spain (2004) and Syria (2004, 2005). A genome wise association analysis was performed per trial, using 811 DArT® markers of known map position. At the first stage of analysis, spatially adjusted genotypic means were created per trial by fitting mixed models. At the second stage, single QTL models were fitted with correction for population substructure, using regression models. Finally, multiple QTL models were constructed by backward selection from a regression model containing all significant markers from the single QTL analyses. In addition to the association analyses per trial, genotype by environment interaction was investigated across the six trials. Landraces seemed best adapted to low yielding environments, while old and modern entries adapted better to high yielding environments. The number of QTL and the magnitude of their effects were comparable for low and high input conditions. However, none of the QTL were found within a given bin at any chromosome in more than two of the six trials. Changes in allele frequencies of marker loci close to QTL for grain yield in landraces, old and modern barley cultivars could be attributed to selection exercised in breeding, suggesting that modern breeding may have increased frequencies of marker alleles close to QTL that favour production particularly under high yield potential environments. Moreover, these results also indicate that there may be scope for improving yield under low input systems, as breeding so far has hardly changed allele frequencies at marker loci close to QTL for low yielding conditions.
Listeria monocytogenes growth limits and stress resistance mechanisms
Veen, S. van der - \ 2008
Wageningen University. Promotor(en): Tjakko Abee; Willem de Vos, co-promotor(en): M.H.J. Wells-Bennik. - [S.l.] : S.n. - ISBN 9789085852629 - 175
listeria monocytogenes - groei - stressreactie - stresstolerantie - listeria monocytogenes - growth - stress response - stress tolerance
The food-borne pathogen Listeria monocytogenes is a Gram-positive facultative anaerobic rod, which is the causative agent of listeriosis. Due to the severity of the disease and the fact that its incidence is increasing in numerous European countries, L. monocytogenes is of great public health concern. This bacterium shows relatively high resistance to environmental insults compared with many other non-spore-forming food-borne pathogens. It is able to grow at low pH, at high salt concentrations, and low temperatures. The possibility that this pathogen (cross-) contaminates food products is a major concern for the food industry. Therefore, it is important to investigate the diversity in growth potential and stress resistance (mechanisms) of L. monocytogenes strains during exposure to commonly used preservation conditions. Several approaches are described in this thesis, including comparison of stress resistance and growth limits of a large collection of natural isolates, screening a mutant library for stress sensitive mutants, and transcription profiling of stress responses. The function of various stress response genes and mechanisms including the so-called SOS response are furthermore investigated in detail.
Identification of plant genes for abiotic stress resistance
Dixit, S.A. - \ 2008
Wageningen University. Promotor(en): Maarten Koornneef, co-promotor(en): A.B. Pereira. - [S.l.] : S.n. - ISBN 9789085049050 - 190
planten - stress - droogte - gewassen - genen - zouttolerantie - transcriptiefactoren - genetica - droogteresistentie - plantenveredeling - stresstolerantie - plants - stress - drought - crops - genes - salt tolerance - transcription factors - genetics - drought resistance - plant breeding - stress tolerance
As water and salt stresses occur frequently and can affect many habitats, plants have developed several strategies to cope with these challenges: either adaptation mechanisms, which allow them to survive the adverse conditions, or specific growth habits to avoid stress conditions. Stress-tolerant plants have evolved certain adaptive mechanisms to display different degrees of tolerance, which are largely determined by genetic plasticity. Differential stress tolerance could be attributed to differences in plant reactivity in terms of stress perception, signal transduction and appropriate gene expression programs, or novel metabolic pathways that are restricted to tolerant plants. The hypothesis that the genetic program for tolerance is at least to some extent also present. ABA is an important phytohormone and plays a critical role in response to various stress signals. The application of ABA to plants mimics the effect of a stress condition
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