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Natural variation in life history strategy of Arabidopsis thaliana determines stress responses to drought and insects of different feeding guilds
Davila Olivas, Nelson H. ; Frago Clols, Enric ; Thoen, Manus P.M. ; Kloth, Karen J. ; Becker, Frank F.M. ; Loon, Joop J.A. van; Gort, Gerrit ; Keurentjes, Joost J.B. ; Heerwaarden, Joost van; Dicke, Marcel - \ 2017
Molecular Ecology 26 (2017)11. - ISSN 0962-1083 - p. 2959 - 2977.
Biotic stress - Drought - Fungal pathogen - Generalist - Herbivory - Specialist - Summer annual - Winter annual - 017-4016
Plants are sessile organisms and, consequently, are exposed to a plethora of stresses in their local habitat. As a result, different populations of a species are subject to different selection pressures leading to adaptation to local conditions and intraspecific divergence. The annual brassicaceous plant Arabidopsis thaliana is an attractive model for ecologists and evolutionary biologists due to the availability of a large collection of resequenced natural accessions. Accessions of A. thaliana display one of two different life cycle strategies: summer and winter annuals. We exposed a collection of 308 European Arabidopsis accessions, that have been genotyped for 250K SNPs, to a range of stresses: one abiotic stress (drought), four biotic stresses (Pieris rapae caterpillars, Plutella xylostella caterpillars, Frankliniella occidentalis thrips and Myzus persicae aphids) and two combined stresses (drought plus P. rapae and Botrytis cinerea fungus plus P. rapae). We identified heritable genetic variation for responses to the different stresses, estimated by narrow-sense heritability. We found that accessions displaying different life cycle strategies differ in their response to stresses. Winter annuals are more resistant to drought, aphids and thrips and summer annuals are more resistant to P. rapae and P. xylostella caterpillars. Summer annuals are also more resistant to the combined stresses of drought plus P. rapae and infection by the fungus Botryris cinerea plus herbivory by P. rapae. Adaptation to drought displayed a longitudinal gradient. Finally, trade-offs were recorded between the response to drought and responses to herbivory by caterpillars of the specialist herbivore P. rapae.
Genome-wide association analysis reveals distinct genetic architectures for single and combined stress responses in Arabidopsis thaliana
Davila Olivas, Nelson H. ; Kruijer, Willem ; Gort, Gerrit ; Wijnen, Cris L. ; Loon, Joop J.A. van; Dicke, Marcel - \ 2017
New Phytologist 213 (2017)2. - ISSN 0028-646X - p. 838 - 851.
abiotic stress - biotic stress - combined stresses - genome-wide association - specialist herbivores
Plants are commonly exposed to abiotic and biotic stresses. We used 350 Arabidopsis thaliana accessions grown under controlled conditions. We employed genome-wide association analysis to investigate the genetic architecture and underlying loci involved in genetic variation in resistance to: two specialist insect herbivores, Pieris rapae and Plutella xylostella; and combinations of stresses, i.e. drought followed by P. rapae and infection by the fungal pathogen Botrytis cinerea followed by infestation by P. rapae. We found that genetic variation in resistance to combined stresses by drought plus P. rapae was limited compared with B. cinerea plus P. rapae or P. rapae alone. Resistance to the two caterpillars is controlled by different genetic components. There is limited overlap in the quantitative trait loci (QTLs) underlying resistance to combined stresses by drought plus P. rapae or B. cinerea plus P. rapae and P. rapae alone. Finally, several candidate genes involved in the biosynthesis of aliphatic glucosinolates and proteinase inhibitors were identified to be involved in resistance to P. rapae and P. xylostella, respectively. This study underlines the importance of investigating plant responses to combinations of stresses. The value of this approach for breeding plants for resistance to combinatorial stresses is discussed.
Genetic architecture of plant stress resistance: multi-trait genome-wide association mapping
Thoen, H.P.M. ; Davila Olivas, N.H. ; Kloth, K.J. ; Coolen, Silvia ; Huang, P. ; Aarts, M.G.M. ; Molenaar, J.A. ; Bakker, J. ; Bouwmeester, H.J. ; Broekgaarden, C. ; Bucher, J. ; Busscher-Lange, J. ; Cheng, X. ; Dijk-Fradin, E.F. van; Jongsma, M.A. ; Julkowska, Magdalena M. ; Keurentjes, J.J.B. ; Ligterink, W. ; Pieterse, Corné M.J. ; Ruyter-Spira, C.P. ; Smant, G. ; Schaik, C.C. van; Wees, Saskia C.M. van; Visser, R.G.F. ; Voorrips, R.E. ; Vosman, B. ; Vreugdenhil, D. ; Warmerdam, S. ; Wiegers, G.L. ; Heerwaarden, J. van; Kruijer, W.T. ; Eeuwijk, F.A. van; Dicke, M. - \ 2017
New Phytologist 213 (2017)3. - ISSN 0028-646X - p. 1346 - 1362.
Plants are exposed to combinations of various biotic and abiotic stresses, but stress responses are usually investigated for single stresses only. Here, we investigated the genetic architecture underlying plant responses to 11 single stresses and several of their combinations by phenotyping 350 Arabidopsis thaliana accessions. A set of 214 000 single nucleotide polymorphisms (SNPs) was screened for marker-trait associations in genome-wide association (GWA) analyses using tailored multi-trait mixed models. Stress responses that share phytohormonal signaling pathways also share genetic architecture underlying these responses. After removing the effects of general robustness, for the 30 most significant SNPs, average quantitative trait locus (QTL) effect sizes were larger for dual stresses than for single stresses. Plants appear to deploy broad-spectrum defensive mechanisms influencing multiple traits in response to combined stresses. Association analyses identified QTLs with contrasting and with similar responses to biotic vs abiotic stresses, and below-ground vs above-ground stresses. Our approach allowed for an unprecedented comprehensive genetic analysis of how plants deal with a wide spectrum of stress conditions.
Transcriptome dynamics of Arabidopsis during sequential biotic and abiotic stresses
Coolen, Silvia ; Proietti, Silvia ; Hickman, Richard ; Davila Olivas, Nelson H. ; Huang, Pingping ; Verk, Marcel C. van; Pelt, Johan A. van; Wittenberg, Alexander H.J. ; Vos, Martin de; Prins, Marcel ; Loon, Joop J.A. van; Aarts, Mark G.M. ; Dicke, Marcel ; Pieterse, Corné M.J. ; Wees, Saskia C.M. van - \ 2016
The Plant Journal 86 (2016)3. - ISSN 0960-7412 - p. 249 - 267.
Arabidopsis thaliana - Botrytis cinerea - combinatorial plant stress - drought stress - gene regulatory network - Pieris rapae - plant hormones - RNA-Seq - transcript profiling - 016-3950
In nature, plants have to cope with a wide range of stress conditions that often occur simultaneously or in sequence. To investigate how plants cope with multi-stress conditions, we analyzed the dynamics of whole-transcriptome profiles of Arabidopsis thaliana exposed to six sequential double stresses inflicted by combinations of: (i) infection by the necrotrophic fungus Botrytis cinerea, (ii) herbivory by chewing larvae of Pieris rapae, and (iii) drought stress. Each of these stresses induced specific expression profiles over time, in which one-third of all differentially expressed genes was shared by at least two single stresses. Of these, 394 genes were differentially expressed during all three stress conditions, albeit often in opposite directions. When two stresses were applied in sequence, plants displayed transcriptome profiles that were very similar to the second stress, irrespective of the nature of the first stress. Nevertheless, significant first-stress signatures could be identified in the sequential stress profiles. Bioinformatic analysis of the dynamics of co-expressed gene clusters highlighted specific clusters and biological processes of which the timing of activation or repression was altered by a prior stress. The first-stress signatures in second stress transcriptional profiles were remarkably often related to responses to phytohormones, strengthening the notion that hormones are global modulators of interactions between different types of stress. Because prior stresses can affect the level of tolerance against a subsequent stress (e.g. prior herbivory strongly affected resistance to B. cinerea), the first-stress signatures can provide important leads for the identification of molecular players that are decisive in the interactions between stress response pathways.
Effect of prior drought and pathogen stress on Arabidopsis transcriptome changes to caterpillar herbivory
Davila Olivas, Nelson H. ; Coolen, Silvia ; Huang, Pingping ; Severing, Edouard ; Verk, Marcel C. van; Hickman, Richard ; Wittenberg, Alexander H.J. ; Vos, Martin de; Prins, Marcel ; Loon, Joop J.A. van; Aarts, Mark G.M. ; Wees, Saskia C.M. van; Pieterse, Corné M.J. ; Dicke, Marcel - \ 2016
New Phytologist 210 (2016)4. - ISSN 0028-646X - p. 1344 - 1356.
Abiotic stress - Botrytis cinerea - Combined stresses - Insect herbivory - Multiple stresses - Pieris rapae - RNAseq - Transcriptome - 016-3939
In nature, plants are exposed to biotic and abiotic stresses that often occur simultaneously. Therefore, plant responses to combinations of stresses are most representative of how plants respond to stresses. We used RNAseq to assess temporal changes in the transcriptome of Arabidopsis thaliana to herbivory by Pieris rapae caterpillars, either alone or in combination with prior exposure to drought or infection with the necrotrophic fungus Botrytis cinerea. Pre-exposure to drought stress or Botrytis infection resulted in a significantly different timing of the caterpillar-induced transcriptional changes. Additionally, the combination of drought and P. rapae induced an extensive downregulation of A. thaliana genes involved in defence against pathogens. Despite a more substantial growth reduction observed for plants exposed to drought plus P. rapae feeding compared with P. rapae feeding alone, this did not affect weight increase of this specialist caterpillar. Plants respond to combined stresses with phenotypic and transcriptional changes that differ from the single stress situation. The effect of a previous exposure to drought or B. cinerea infection on transcriptional changes to caterpillars is largely overridden by the stress imposed by caterpillars, indicating that plants shift their response to the most recent stress applied.
Ecogenomics of plant resistance to biotic and abiotic stresses
Davila Olivas, N.H. - \ 2016
Wageningen University. Promotor(en): Marcel Dicke; Joop van Loon. - Wageningen : Wageningen University - ISBN 9789462576575 - 259
016-3932 - arabidopsis thaliana - defence mechanisms - drought resistance - insect pests - plant pathogenic fungi - stress - stress response - transcriptomics - genomics - genetic mapping - arabidopsis thaliana - verdedigingsmechanismen - droogteresistentie - insectenplagen - plantenziekteverwekkende schimmels - stress - stressreactie - transcriptomica - genomica - genetische kartering
In natural and agricultural ecosystems, plants are exposed to a wide diversity of abiotic and biotic stresses such as drought, salinity, pathogens and insect herbivores. Under natural conditions, these stresses do not occur in isolation but commonly occur simultaneously. However, plants have developed sophisticated mechanisms to survive and reproduce under suboptimal conditions. Genetic screenings and molecular genetic assays have shed light on the molecular players that provide resistance to single biotic and abiotic stresses. Induced defenses are attacker specific and phytohormones play an essential role in tailoring these defense responses. Because phytohormones display antagonistic and synergistic interactions, the question emerges how plants elicit an effective defense response when exposed to conflicting signals under multiple attack. Recent studies have shed light on this issue by studying the effects of combinations of stresses at the phenotypic, transcriptomic and genetic level. These studies have concluded that the responses to combined stresses can often not be predicted based on information about responses to the single stress situations or the phytohormones involved. Thus, combined stresses are starting to be regarded as a different state of stress in the plant. Studying the effects of combinations of stresses is relevant since they are more representative of the type of stresses experienced by plants in natural conditions.
In a coordinated effort, responses of Arabidopsis thaliana to a range of abiotic and biotic stresses and stress combinations have been explored at the genetic, phenotypic, and transcriptional level. For this purpose we used an ecogenomic approach in which we integrated the assessment of phenotypic variation and Genome-Wide Association (GWA) analysis for a large number of A. thaliana accessions with an in-depth transcriptional analysis. The focus of this thesis is especially on (but not limited to) three stresses, i.e. drought, herbivory by Pieris rapae caterpillars, and infection by the necrotrophic fungal pathogen Botrytis cinerea. These stresses were chosen because the responses of A. thaliana to these three stresses are highly divergent but at the same time regulated by the plant hormones JA and/or ABA. Consequently, analysis of responses to combinatorial stresses is likely to yield information on signaling nodes that are involved in tailoring the plant’s adaptive response to combinations of these stresses. Responses of A. thaliana to other biotic and abiotic stresses are included in an integrative study (Chapter 6).
We first investigated (Chapter 2) the extent of natural variation in the response to one abiotic stress (drought), four biotic stresses (Pieris rapae caterpillars, Plutella xylostella caterpillars, Frankliniella occidentalis thrips, Myzus persicae aphids) and two combined stresses (drought plus P. rapae, and B. cinerea plus P. rapae). Using 308 A. thaliana accessions originating from Europe, the native range of the species, we focused on the eco-evolutionary context of stress responses. We analyzed how the response to stress is influenced by geographical origin, genetic relatedness and life-cycle strategy, i.e. summer versus winter annual. We identified heritable genetic variation for responses to the different stresses. We found that winter annuals are more resistant to drought, aphids and thrips and summer annuals are more resistant to P. rapae and P. xylostella caterpillars and to the combined stresses of drought followed by P. rapae and infection by the fungus B. cinerea followed by herbivory by P. rapae. Furthermore, we found differential responses to drought along a longitudinal gradient.
We further investigated, using A. thaliana accession Col-0, how phenotypic and whole-genome transcriptional responses to one stress are altered by a preceding or co-occurring stress (Chapters 3 and 4). The whole-transcriptomic profile of A. thaliana triggered by single and combined abiotic (drought) and biotic (herbivory by caterpillars of P. rapae, infection by B. cinerea) stresses was analyzed by RNA sequencing (RNA-seq). Comparative analysis of plant gene expression triggered by single and double stresses revealed a complex transcriptional reprogramming. Mathematical modelling of transcriptomic data, in combination with Gene Ontology analysis highlighted biological processes specifically affected by single and double stresses (Chapters 3). For example, ethylene (ET) biosynthetic genes were induced at 12 h by B. cinerea alone or drought followed by B. cinerea inoculation. This induction was delayed when plants were pretreated with P. rapae by inducing ET biosynthetic genes only 18 hours post inoculation. Other processes affected by combined stresses include wound response, systemic acquired resistance (SAR), water deprivation and ABA response, and camalexin biosynthesis.
In Chapter 4, we focused on the stress imposed by P. rapae herbivory alone or in combination with prior exposure to drought or infection with B. cinerea. We found that pre-exposure to drought stress or B. cinerea infection resulted in a significantly different timing of the caterpillar-induced transcriptional changes. Additionally, the combination of drought and P. rapae induced an extensive downregulation of A. thaliana genes involved in defence against pathogens. Despite the larger reduction in plant biomass observed for plants exposed to drought plus P. rapae feeding compared to P. rapae feeding alone, this did not affect weight gain of this specialist caterpillar.
In Chapter 5, we used univariate GWA to (1) understand the genetic architecture of resistance to the different stresses and (2) identify regions of the genome and possible candidate genes associated with variation in resistance to those stresses. In Chapter 5 a subset of the stresses addressed in Chapter 1 (i.e. drought, herbivory by P. rapae and P. xylostella, and the combined stresses drought plus P. rapae and B. cinerea plus P. rapae) were investigated. Results from GWA were integrated with expression data generated in Chapters 3 and 4 or available from the literature. We identified differences in genetic architecture and QTLs underlying variation in resistance to (1) P. rapae andP. xylostella and (2) resistance to P. rapae and combined stresses drought plus P. rapae and B. cinerea plus P. rapae. Furthermore, several of the QTLs identified contained genes that were differentially expressed in response to the relevant stress. For example, for P. xylostella one of the QTLs contained only two genes encoding cysteine proteases (CP1 and CP2). The expression data indicated that these genes were induced by P. rapae and P. xylostella herbivory.
In Chapter 6, the genetic architecture underlying plant resistance to 11 single stresses and some of their combinations was investigated. First, the genetic commonality underlying responses to different stresses was investigated by means of genetic correlations,, revealing that stresses that share phytohormonal signaling pathways also share part of their genetic architecture. For instance, a strong negative genetic correlation was observed between SA and JA inducers. Furthermore, multi-trait GWA identified candidate genes influencing the response to more than one stress. For example, a functional RMG1 gene seems to be associated with susceptibility to herbivory by P. rapae and osmotic stress since loss of function mutants in RMG1 displayed higher resistance to both stresses. Finally, multi-trait GWA was used to identify QTLs with contrasting and with similar effects on the response to (a) biotic or abiotic stresses and (b) belowground or aboveground stresses.
Finally, In Chapter 7, I discuss the feasibility of obtaining plants that are resistant to multiple stresses from the point of view of genetic trade-offs and experimental limitations. The ecogenomic approach for gene discovery taken in this thesis is discussed, and recommendations are especially given on the use of herbivorous insects in quantitative genetic studies of stress resistance. Furthermore, alternatives to the use of insects in quantitative genetic studies of stress resistance are discussed and proposed. Finally, I discuss the feasibility of using an ecogenomic approach to study stress responses in other plant species than the model plant of molecular genetics, A. thaliana.
A wealth of candidate genes was generated by taking an ecogenomic approach, in particular transcriptome analysis and GWA analysis. Functional characterization of these genes is a next challenge, especially in the context of multiple stress situations. These genes constitute a rich source of potential factors important for resistance to abiotic, biotic and combined stresses that in the future may be applied for crop improvement.
In vitro chemical mutagenesis improves the turf quality of bahiagrass
Kannan, Baskaran ; Davila Olivas, N.H. ; Lomba, Paula ; Altpeter, Fredy - \ 2015
Plant Cell, Tissue and Organ Culture: an international journal on in vitro culture of higher plants 120 (2015)2. - ISSN 0167-6857 - p. 551 - 561.
Bahiagrass (Paspalum notatum Flugge) is a warm season, low-input, perennial turfgrass used for residential lawns and sides of road ways. The turf quality of bahiagrass is limited by its open growth habit, light green color, and prolific production of tall seedheads. Genetic improvement of the tetraploid bahiagrass turf cultivar ‘Argentine’ by conventional breeding is difficult due to its apomictic mode of reproduction. Our objective was to explore the potential of in vitro chemical mutagenesis for the generation of uniform, mutant seed progeny with improved turf quality. Scarified, surface sterilized bahiagrass seeds were treated with different concentrations of the chemical mutagen ‘sodium azide’. Callus was induced from these seeds and 19,630 plants were regenerated via somatic embryogenesis. 2,035 of these plants were selected based on their morphological characteristics and transferred to soil. Wildtype bahiagrass and 46 mutant lines (M1 lines) with reduced stem lengths, higher tiller densities or reduced or delayed seedhead formation were established under field conditions. Mutant lines with improved traits and production of viable apomictic seeds were identified and their apomictic M2 progeny was evaluated. A superior line displayed higher density, finer leaves, an upright growth habit, dark green color, reduced seedhead formation and uniform seed progeny in replicated, two location field trials. Beside this improved turf quality, this line also retained the superior drought tolerance and persistence that make bahiagrass a popular low-input turfgrass.
The influence of redox potential on the degradation of halogenated methanes
Olivas, Y. ; Dolfing, J. ; Smith, G.B. - \ 2002
Environmental Toxicology and Chemistry 21 (2002)3. - ISSN 0730-7268 - p. 493 - 499.
To determine the influence of redox potential on the reaction mechanism and to quantify kinetics of the dechlorination by digester sludge, the test compounds trichlorofluoromethane (CFCl3), carbon tetrachloride (CCl4), and chloroform (CHCl3) were incubated in the presence of sludge and variable concentrations of reducing agent. Different sources of dehalogenation were examined, including live sludge and heat-killed sludge, and abiotic mechanisms were quantified in the absence of sludge. Batch incubations were done under redox conditions ranging from +534 to -348 mV. The highest rates for the dehalogenation of the three compounds were observed at -348 mV. The dechlorination rate of all the compounds by the heat-resistant catalysts was approximately twofold higher than the live treatments. It was proposed that the higher degradation rates by heat-killed sludge were due to the absence of physical barriers such as cell wall and cell membranes. There was no abiotic dechlorination of CFCl3, whereas CCl4 and CHCl3 were both reduced in the absence of sludge catalyst by Ti (III) citrate at ≥2.5 mM. The degradation pathways of CFCl3 and CHCl3 appeared to be only partially reductive since the production of reduced metabolites was low in comparison with the total amount of original halogenated compounds degraded. For CFCl3, the partial reductive degradation implied that different intra- and extra-cellular pathways were concurrent. The Gibbs free energy and the redox potential for the dehalogenation reactions utilizing Ti (III) citrate and acetate as electron donors are reported here for the first time.