LSU-peptiden en hun cruciale rol als regulatorische hubs tijdens de stressrespons van Arabidopsis thaliana

Hanne Claessen Barbara De Coninck
Persbericht

Het Ontrafelen van de Functie van Vier Kleine LSU-Genen

DNA, genomen en genen spreken al sinds hun ontdekking tot de verbeelding. De huidige genetica staat al verbazend ver. Hoewel er nog veel is dat we nog niet weten, heeft de combinatie van kennis uit de biochemie en de genetica ervoor gezorgd dat we de functie van vele genen hebben kunnen linken aan essentiële biochemische processen zoals fotosynthese of immuunrespons in planten en dieren. Maar heeft u zich ooit al eens afgevraagd hoe onderzoekers dit voor elkaar krijgen? Hoe wordt de functie van een gen eigenlijk achterhaald? De thesis van Hanne Claessen, geschreven in het kader van de masteropleiding Bio-ingenieurswetenschappen aan de KU Leuven, beschrijft zo’n genetisch onderzoek. Het is een zoektocht naar de functie van vier kleine genen, namelijk LSU1, LSU2, LSU3 en LSU4 in Arabidopsis thaliana, een klein onkruidplantje dat ook wel Zandraket genoemd wordt en vaak gebruikt wordt in genetisch onderzoek in planten. De afkorting “LSU” staat voor “response to Low Sulfur”, wat betekent dat ze voor het eerst ontdekt werden als genen die verhoogd tot expressie komen wanneer de plant een tekort heeft aan zwavel in zijn voedingsoplossing. De LSU-genen worden vertaald in LSU-peptiden (peptiden zijn hele kleine proteïnen), maar hun functie in de cel is nog grotendeels onbekend.  

De zoektocht naar de functie van de LSU-peptiden moest gelukkig niet van nul beginnen. Voor de aanvang van het onderzoek was reeds geweten dat LSU1, LSU2 en LSU3 interageren met GBFP (Guanylate Binding Family Protein), een proteïne dat in de mens betrokken is bij de verdediging van het lichaam tegen bacteriën en virussen, en FSD2 (Fe Superoxide Dismutase 2) een proteïne dat in planten instaat voor de afbraak van zuurstofradicalen die vrijkomen bij stress of ziekte en zeer schadelijk kunnen zijn voor de cel. De interactie met deze proteïnen wijst erop dat de LSU-peptiden mogelijks betrokken zijn bij de immuunrespons van de plant tegen ziekten en stress. Anderzijds was het ook al bekend dat LSU4 voornamelijk betrokken is bij de bloemontwikkeling. Dit waren de eerste aanwijzingen voor de mogelijke functies van de verschillende LSU-peptiden en op basis daarvan moest het thesisonderzoek meer informatie verzamelen. Het was niet de bedoeling om werkelijk de exacte moleculaire functie van de LSU-peptiden te vinden, aangezien dit een veel te ambitieuze doelstelling zou zijn, maar eerder om het begrip van de LSU-peptiden te vergroten zodat andere onderzoekers hierop verder kunnen bouwen.

De LSU-peptiden werden op drie manieren onderzocht. Ten eerste werd er gekeken in welk plantenweefsel het gen actief is (bloemen, stengel, bladeren…) en waar het proteïne zich in de plantencel bevindt (kern, cytoplasma, mitochondriën…). Deze lokalisatiestudies werden uitgevoerd aan de hand van respectievelijk GUS-kleuring en GFP-kleuring. De eerste techniek zorgt ervoor dat het plantenweefsel waar het LSU-gen actief is blauw kleurt, de tweede techniek hangt een fluorescerende staart aan het LSU-proteïne waardoor het fluoresceert en er met een speciale microscoop gekeken kan worden waar het zich in de plantencel bevindt. Deze lokalisatiestudies zijn belangrijk aangezien de plaats waar het proteïne actief is een duidelijke aanwijzing kan geven over zijn functie. De LSU-genen bleken zeer actief in het vasculair weefsel (de “aders”) van de plant en de LSU-peptiden bleken zich voornamelijk in de kern te bevinden. Ten tweede werden genexpressieanalyses uitgevoerd, waarbij gemeten werd hoe actief het LSU-gen vertaald werd naar het overeenkomstige LSU-peptide naargelang de omgevingsomstandigheden die werden opgelegd. Er was een sterk verhoogde expressie van LSU1 en LSU3 wanneer de plant blootgesteld werd aan hoge concentraties van tafelsuiker (sucrose) in het medium. Sucrose is de belangrijkste vorm waarin glucose, de energiebron van de plant, getransporteerd wordt doorheen het vasculair weefsel. Dit zou erop kunnen wijzen dat de LSU-peptiden betrokken zijn in het energiemetabolisme van planten. Tenslotte werden fenotypische ziektetesten uitgevoerd waarbij mutante plantjes werden aangemaakt met een sterk verlaagde of zelfs helemaal geen expressie van de verschillende LSU-genen. Hierna werd gekeken hoe goed deze mutante plantjes overleven wanneer ze blootgesteld worden aan ziekte of stress. Het klinkt tegenstrijdig, maar een van de beste manieren om de functie van een gen te onderzoeken is om na te gaan wat er gebeurt met het plantje als het gen volledig wordt uitgeschakeld. Deze techniek, die ook wel aangeduid wordt als de “knock-out” techniek, is daarom een standaardmethode geworden om genenfunctie te onderzoeken. De mutanten werden blootgesteld aan schimmel- en bacterieziekten en zoutstress en de hevigheid van de ziektesymptomen werden nauwgezet bijgehouden. Echter, er konden in dit thesisonderdeel nog geen eenduidige conclusies getrokken worden uit de resultaten en deze ziektetesten zullen in een volgend onderzoek best herhaald worden.

De thesis bracht verschillende interessante conclusies naar voren, maar er is nog veel onderzoek nodig om duidelijkheid te vinden over de moleculaire functie van de LSU-peptiden. Net als bij vele andere disciplines in fundamenteel onderzoek is het achterhalen van de functie van genen een werk van lange adem en vaak zijn er verschillende onafhankelijke onderzoekers bezig met een sterk gelijkaardig onderzoek, maar komen ze tot schijnbaar tegengestelde resultaten. Het werk is gecompliceerd en vaak is het niet meteen duidelijk hoe het onderzoek in de praktijk toegepast kan worden. Deze eigenschappen van fundamenteel onderzoek maken dat het onderzoek vaak te vaag of te complex is om de interesse van leken te wekken. Toch is het een onontbeerlijke stap in het hedendaags onderzoek aangezien het de basis levert voor toegepast onderzoek dat vervolgens concrete toepassingen in de praktijk teweeg kan brengen. Indien bevestigd wordt dat LSU-peptiden betrokken zijn bij de plantverdediging tegen ziekten, kan deze kennis gebruikt worden in het praktijkgericht onderzoek om onze landbouwgewassen resistenter te maken tegen ziekten en plagen. Voor zij die geïnteresseerd zijn om te weten te komen hoe fundamenteel onderzoek te werk gaat en hoe men precies de specifieke functies van genen achterhaalt, is deze thesis zeker interessante literatuur.

Bibliografie

Abramovitch, R.B., Anderson, J.C. & Martin, G.B., 2006. Bacterial elicitation and evasion of plant innate immunity. Nature
reviews. Molecular cell biology, 7(8), pp.601–11.
Achuo, E.A. et al., 2004. The salicylic acid-dependent defence pathway is effective against different pathogens in tomato and
tobacco. Plant Pathology, 53(1), pp.65–72.
Agrios, G., 2012. Plant Pathology, Elsevier.
Albert, R., 2005. Scale-free networks in cell biology. Journal of cell science, 118(Pt 21), pp.4947–57.
Albert, R., Jeong, H. & Barabasi, A., 2000. Error and attack tolerance of complex networks. Nature, 406(6794), pp.378–82.
Anand, A. et al., 2007. Salicylic Acid and Systemic Acquired Resistance Play a Role in Attenuating Crown Gall Disease
Caused by Agrobacterium tumefaciens. PLANT PHYSIOLOGY, 146(2), pp.703–715.
Andorf, C.M., Honavar, V. & Sen, T.Z., 2013. Predicting the binding patterns of hub proteins: a study using yeast protein
interaction networks. PloS one, 8(2), p.e56833.
Arabidopsis Interactome Mapping Consortium, 2011. Evidence for network evolution in an Arabidopsis interactome map.
Science (New York, N.Y.), 333(6042), pp.601–7.
Ben Arfa, A. et al., 2006. Antimicrobial activity of carvacrol related to its chemical structure. Letters in Applied
Microbiology, 43(2), pp.149–154.
Aroca, R., 2012. Plant Responses to Drought Stress: From Morphological to Molecular Features, Springer Science &
Business Media.
Ashraf, M., 2010. Inducing drought tolerance in plants: recent advances. Biotechnology advances, 28(1), pp.169–83.
Bakshi, A. et al., 2015. History of Research on the Plant Hormone Ethylene. Journal of Plant Growth Regulation, 34(4),
pp.809–827.
Ballaré, C.L., 2011. Jasmonate-induced defenses: a tale of intelligence, collaborators and rascals. Trends in plant science,
16(5), pp.249–57.
Bano, A. et al., 1994. Changes in the contents of free and conjugated abscisic acid, phaseic acid and cytokinins in xylem sap
of drought stressed sunflower plants. Phytochemistry, 37(2), pp.345–347.
Bari, 2008. Role of plant hormones in plant defece responses. Available at: file:///C:/Users/Hanne Claessen/Downloads/Bari
& Jones 2009 (1).pdf [Accessed September 16, 2015].
Bari, R. & Jones, J.D.G., 2009. Role of plant hormones in plant defence responses. Plant molecular biology, 69(4), pp.473–
88.
Baxter, A., Mittler, R. & Suzuki, N., 2014. ROS as key players in plant stress signalling. Journal of experimental botany,
65(5), pp.1229–40.
Berr, A. et al., 2010. Arabidopsis histone methyltransferase SET DOMAIN GROUP8 mediates induction of the
jasmonate/ethylene pathway genes in plant defense response to necrotrophic fungi. Plant physiology, 154(3), pp.1403–
14.
Birch, P.R.J. et al., 2006. Trafficking arms: oomycete effectors enter host plant cells. Trends in microbiology, 14(1), pp.8–11.
Boudsocq, M. & Sheen, J., 2013. CDPKs in immune and stress signaling. Trends in plant science, 18(1), pp.30–40.
Burkhard, P., Stetefeld, J. & Strelkov, S. V, 2001. Coiled coils: a highly versatile protein folding motif. Trends in Cell
Biology, 11(2), pp.82–88.
Callaway, D.S. et al., 2000. Network robustness and fragility: percolation on random graphs. Physical review letters, 85(25),
pp.5468–71.
Caruso, F. et al., 2011. Antifungal activity of resveratrol against Botrytis cinerea is improved using 2-furyl derivatives. PloS
one, 6(10), p.e25421.
Chaves, M.M., Maroco, J.P. & Pereira, J.S., 2003. Understanding plant responses to drought — from genes to the whole
plant. Functional Plant Biology, 30(3), p.239.
Chen, Z. et al., 2009. Biosynthesis of salicylic acid in plants. Plant signaling & behavior, 4(6), pp.493–6.
Chinchilla, D. et al., 2007. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature,
448(7152), pp.497–500.
Chisholm, S.T. et al., 2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell, 124(4),
pp.803–14.
Cohen, R. et al., 2001. Breakdown of the Internet under Intentional Attack. Physical Review Letters, 86(16), pp.3682–3685.
Cohen, R. et al., 2000. Resilience of the Internet to Random Breakdowns. Physical Review Letters, 85(21), pp.4626–4628.
Creelman, R.A. & Mullet, J.E., 1997. BIOSYNTHESIS AND ACTION OF JASMONATES IN PLANTS. Annual review of
plant physiology and plant molecular biology, 48, pp.355–381.
Cui, H. et al., 2010. Pseudomonas syringae effector protein AvrB perturbs Arabidopsis hormone signaling by activating MAP
kinase 4. Cell host & microbe, 7(2), pp.164–75.
Dang, T.V.T., 2015. Exploring the potential of a newly discovered Arabidopsis gene as a molecular trait in banana for
increasing resistance against fungal diseases.
Daryanto, S., Wang, L. & Jacinthe, P.-A., 2015. Global Synthesis of Drought Effects on Food Legume Production. PloS one,
75
10(6), p.e0127401.
Davenport, R. et al., 2005. Control of sodium transport in durum wheat. Plant physiology, 137(3), pp.807–18.
Denancé, N. et al., 2013. Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness
costs. Frontiers in plant science, 4, p.155.
Djamei, A. et al., 2007. Trojan horse strategy in Agrobacterium transformation: abusing MAPK defense signaling. Science
(New York, N.Y.), 318(5849), pp.453–6.
Dodds, P.N. & Rathjen, J.P., 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nature
reviews. Genetics, 11(8), pp.539–48.
Dombrecht, B. et al., 2007. MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. The Plant
cell, 19(7), pp.2225–45.
Dong, X., 2004. NPR1, all things considered. Current opinion in plant biology, 7(5), pp.547–52.
Dunlop, J. & Gradiner, S., 1993. Phosphate Uptake, Proton Extrusion and Membrane Electropotentials of Phosphorus-
Deficient Trifolium repens L. Journal of Experimental Botany, 44(12), pp.1801–1808.
Dupont, C.D. & Hunter, C.A., 2012. Guanylate-binding proteins: niche recruiters for antimicrobial effectors. Immunity,
37(2), pp.191–3.
Ekman, D. et al., 2006. What properties characterize the hub proteins of the protein-protein interaction network of
Saccharomyces cerevisiae? Genome biology, 7(6), p.R45.
Van den Ende, W. & El-Esawe, S.K., 2014. Sucrose signaling pathways leading to fructan and anthocyanin accumulation: A
dual function in abiotic and biotic stress responses? Environmental and Experimental Botany, 108, pp.4–13.
Farooq, M. et al., 2009. Improving the Drought Tolerance in Rice ( Oryza sativa L.) by Exogenous Application of Salicylic
Acid. Journal of Agronomy and Crop Science, 195(4), pp.237–246.
Figueiredo, M.V.B. et al., 2008. Alleviation of drought stress in the common bean (Phaseolus vulgaris L.) by co-inoculation
with Paenibacillus polymyxa and Rhizobium tropici. Applied Soil Ecology, 40(1), pp.182–188.
Filipenko, E.A. et al., 2013. PR-proteins with ribonuclease activity and plant resistance against pathogenic fungi. Russian
Journal of Genetics: Applied Research, 3(6), pp.474–480.
Flexas, J. & Medrano, H., 2002. Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations
revisited. Annals of botany, 89(2), pp.183–9.
Flor, H.H., 1971. Current Status of the Gene-For-Gene Concept. Annual Review of Phytopathology, 9(1), pp.275–296.
Flores-Sanchez, I.J. & Verpoorte, R., 2009. Plant polyketide synthases: a fascinating group of enzymes. Plant physiology and
biochemistry : PPB / Socié té franç aise de physiologie vé gétale, 47(3), pp.167–74.
Flowers, T.J., 2004. Improving crop salt tolerance. Journal of experimental botany, 55(396), pp.307–19.
Freeman, B. & Beattie, G.., 2008. Overview of Plant Defenses. The Plant Health Instructor. DOI: 10.1094/PHI-I-2008-0226-
01.
Fu, Z.Q. et al., 2012. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature, 486(7402),
pp.228–32.
Fujita, M. et al., 2006. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in
the stress signaling networks. Current opinion in plant biology, 9(4), pp.436–42.
Gilland, B., 2002. World population and food supply. Food Policy, 27(1), pp.47–63.
Gilroy, S. et al., 2014. A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends in plant
science, 19(10), pp.623–30.
Glazebrook, J., 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual review of
phytopathology, 43, pp.205–27.
Govrin, E.M. & Levine, A., 2000a. The hypersensitive response facilitates plant infection by the necrotrophic pathogen
Botrytis cinerea. Current Biology, 10(13), pp.751–757.
Govrin, E.M. & Levine, A., 2000b. The hypersensitive response facilitates plant infection by the necrotrophic pathogen
Botrytis cinerea. Current Biology, 10(13), pp.751–757.
Goyal, K., Walton, L.J. & Tunnacliffe, A., 2005. LEA proteins prevent protein aggregation due to water stress. The
Biochemical journal, 388(Pt 1), pp.151–7.
Grant, S.R. et al., 2006. Subterfuge and manipulation: type III effector proteins of phytopathogenic bacteria. Annual review of
microbiology, 60, pp.425–49.
Gruner, K. et al., 2013. Reprogramming of plants during systemic acquired resistance. Frontiers in Plant Science, 4.
Guo, H. & Ecker, J.R., 2004. The ethylene signaling pathway: new insights. Current Opinion in Plant Biology, 7(1), pp.40–
49.
Halter, T. et al., 2014. The leucine-rich repeat receptor kinase BIR2 is a negative regulator of BAK1 in plant immunity.
Current biology : CB, 24(2), pp.134–43.
Hammond, J.P. et al., 2003. Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential
for developing smart plants. Plant physiology, 132(2), pp.578–96.
Hanaoka, H. et al., 2002. Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an
Arabidopsis autophagy gene. Plant physiology, 129(3), pp.1181–93.
Hayat, S., Ali, B. & Ahmad, A., 2007. Salicylic Acid: A Plant Hormone S. Hayat & A. Ahmad, eds., Dordrecht: Springer
Netherlands.
76
Hayward, A.P. & Dinesh-Kumar, S.P., 2011. What can plant autophagy do for an innate immune response? Annual review of
phytopathology, 49, pp.557–76.
Heese, A. et al., 2007. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants.
Proceedings of the National Academy of Sciences of the United States of America, 104(29), pp.12217–22.
Herrera, J.M. et al., 2015. Terpene ketones as natural insecticides against Sitophilus zeamais. Industrial Crops and Products,
70, pp.435–442.
Higurashi, M., Ishida, T. & Kinoshita, K., 2008. Identification of transient hub proteins and the possible structural basis for
their multiple interactions. Protein science : a publication of the Protein Society, 17(1), pp.72–8.
Hirai, M.Y. et al., 2003. Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O -
acetyl-l-serine as a general regulator of gene expression in response to sulfur nutrition. The Plant Journal, 33(4),
pp.651–663.
Hirai, M.Y. et al., 2004. Integration of transcriptomics and metabolomics for understanding of global responses to nutritional
stresses in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America,
101(27), pp.10205–10.
Hirai, M.Y. & Saito, K., 2004. Post-genomics approaches for the elucidation of plant adaptive mechanisms to sulphur
deficiency. Journal of experimental botany, 55(404), pp.1871–9.
Holbrook, M. & Zwieniecki, M., 2011. Vascular Transport in Plants,
Huang, B. & Xu, C., 2008. Identification and characterization of proteins associated with plant tolerance to heat stress.
Journal of integrative plant biology, 50(10), pp.1230–7.
Hückelhoven, R., 2007. Cell wall-associated mechanisms of disease resistance and susceptibility. Annual review of
phytopathology, 45, pp.101–27.
Jakubowicz, M. et al., 2010. Exogenously induced expression of ethylene biosynthesis, ethylene perception, phospholipase
D, and Rboh-oxidase genes in broccoli seedlings. Journal of experimental botany, 61(12), pp.3475–91.
Jia, W. & Davies, W.J., 2007. Modification of leaf apoplastic pH in relation to stomatal sensitivity to root-sourced abscisic
acid signals. Plant physiology, 143(1), pp.68–77.
Jones, J.D.G. & Dangl, J.L., 2006. The plant immune system. Nature, 444(7117), pp.323–9.
Kamoun, S., 2007. Groovy times: filamentous pathogen effectors revealed. Current opinion in plant biology, 10(4), pp.358–
65.
Kelly, G. et al., 2013. Hexokinase mediates stomatal closure. The Plant journal : for cell and molecular biology, 75(6),
pp.977–88.
Kemmerling, B. et al., 2007. The BRI1-associated kinase 1, BAK1, has a brassinolide-independent role in plant cell-death
control. Current biology : CB, 17(13), pp.1116–22.
Keskin, O. et al., 2008. Principles of Protein−Protein Interactions: What are the Preferred Ways For Proteins To Interact?
Chemical Reviews, 108(4), pp.1225–1244.
Khan, M., Subramaniam, R. & Desveaux, D., 2015. Of guards, decoys, baits and traps: pathogen perception in plants by type
III effector sensors. Current opinion in microbiology, 29, pp.49–55.
Kim, B.-H. et al., 2011. A family of IFN-γ-inducible 65-kD GTPases protects against bacterial infection. Science (New York,
N.Y.), 332(6030), pp.717–21.
Kim, B.H., Kim, S.Y. & Nam, K.H., 2013. Assessing the diverse functions of BAK1 and its homologs in arabidopsis, beyond
BR signaling and PTI responses. Molecules and cells, 35(1), pp.7–16.
Kim, P.M. et al., 2006. Relating three-dimensional structures to protein networks provides evolutionary insights. Science
(New York, N.Y.), 314(5807), pp.1938–41.
Kim, P.M. et al., 2008. The role of disorder in interaction networks: a structural analysis. Molecular systems biology, 4(1),
p.179.
Konings, H. & Verschuren, G., 1980. Formation of aerenchyma in roots of Zea mays in aerated solutions, and its relation to
nutrient supply. Physiologia Plantarum, 49(3), pp.265–270.
Krishna, P., 2003. Brassinosteroid-Mediated Stress Responses. Journal of plant growth regulation, 22(4), pp.289–297.
Kutz, A. et al., 2002. A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana. The
Plant Journal, 30(1), pp.95–106.
Kvitko, B.H. et al., 2009. Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector
genes reveal functional overlap among effectors. PLoS pathogens, 5(4), p.e1000388.
Lalonde, S., 1999. The Dual Function of Sugar Carriers: Transport and Sugar Sensing. THE PLANT CELL ONLINE, 11(4),
pp.707–726.
Lamb, C. & Dixon, R.A., 1997. THE OXIDATIVE BURST IN PLANT DISEASE RESISTANCE. Annual review of plant
physiology and plant molecular biology, 48, pp.251–275.
Lawlor, D.W. & Cornic, G., 2002. Photosynthetic carbon assimilation and associated metabolism in relation to water deficits
in higher plants. Plant, Cell and Environment, 25(2), pp.275–294.
Lemoine, R. et al., 2013. Source-to-sink transport of sugar and regulation by environmental factors. Frontiers in plant
science, 4, p.272.
Lewandowska, M. et al., 2010. A contribution to identification of novel regulators of plant response to sulfur deficiency:
characteristics of a tobacco gene UP9C, its protein product and the effects of UP9C silencing. Molecular plant, 3(2),
77
pp.347–60.
Li, J. et al., 2002. BAK1, an Arabidopsis LRR Receptor-like Protein Kinase, Interacts with BRI1 and Modulates
Brassinosteroid Signaling. Cell, 110(2), pp.213–222.
Li, J., 2000. Regulation of Abscisic Acid-Induced Stomatal Closure and Anion Channels by Guard Cell AAPK Kinase.
Science, 287(5451), pp.300–303.
Li, J. & Nam, K.H., 2002. Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science (New York,
N.Y.), 295(5558), pp.1299–301.
Liu, T. et al., 2012. Chitin-induced dimerization activates a plant immune receptor. Science (New York, N.Y.), 336(6085),
pp.1160–4.
Lorenzo, O., 2002. ETHYLENE RESPONSE FACTOR1 Integrates Signals from Ethylene and Jasmonate Pathways in Plant
Defense. THE PLANT CELL ONLINE, 15(1), pp.165–178.
Lorenzo, O. et al., 2004. JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate
between different jasmonate-regulated defense responses in Arabidopsis. The Plant cell, 16(7), pp.1938–50.
Lozano-Durán, R. & Zipfel, C., 2015. Trade-off between growth and immunity: role of brassinosteroids. Trends in plant
science, 20(1), pp.12–9.
Luhua, S. et al., 2013. Linking genes of unknown function with abiotic stress responses by high-throughput phenotype
screening. Physiologia plantarum, 148(3), pp.322–33.
Maruyama-Nakashita, A. et al., 2004a. A novel regulatory pathway of sulfate uptake in Arabidopsis roots: implication of
CRE1/WOL/AHK4-mediated cytokinin-dependent regulation. The Plant journal : for cell and molecular biology,
38(5), pp.779–89.
Maruyama-Nakashita, A. et al., 2005. Identification of a novel cis-acting element conferring sulfur deficiency response in
Arabidopsis roots. The Plant journal : for cell and molecular biology, 42(3), pp.305–14.
Maruyama-Nakashita, A., 2004. Induction of SULTR1;1 Sulfate Transporter in Arabidopsis Roots Involves Protein
Phosphorylation/Dephosphorylation Circuit for Transcriptional Regulation. Plant and Cell Physiology, 45(3), pp.340–
345.
Maruyama-Nakashita, A. et al., 2004b. Regulation of high-affinity sulphate transporters in plants: towards systematic
analysis of sulphur signalling and regulation. Journal of experimental botany, 55(404), pp.1843–9.
Maruyama-Nakashita, A. et al., 2003. Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global
effects of sulfur nutrition on multiple metabolic pathways. Plant physiology, 132(2), pp.597–605.
Mengiste, T., 2012. Plant immunity to necrotrophs. Annual review of phytopathology, 50, pp.267–94.
Miller, G. et al., 2010. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, cell &
environment, 33(4), pp.453–67.
Mittler, R. et al., 2004. Reactive oxygen gene network of plants. Trends in plant science, 9(10), pp.490–8.
Mittler, R. et al., 2011. ROS signaling: the new wave? Trends in plant science, 16(6), pp.300–9.
Moniuszko, G. et al., 2013. Tobacco LSU-like protein couples sulphur-deficiency response with ethylene signalling pathway.
Journal of experimental botany, 64(16), pp.5173–82.
Mudgett, M.B., 2005. New insights to the function of phytopathogenic bacterial type III effectors in plants. Annual review of
plant biology, 56, pp.509–31.
Mühlenbock, P. et al., 2008. Chloroplast signaling and LESION SIMULATING DISEASE1 regulate crosstalk between light
acclimation and immunity in Arabidopsis. The Plant cell, 20(9), pp.2339–56.
Mukhtar, M.S. et al., 2011. Independently evolved virulence effectors converge onto hubs in a plant immune system network.
Science (New York, N.Y.), 333(6042), pp.596–601.
Munns, R., 2002. Comparative physiology of salt and water stress. Plant, cell & environment, 25(2), pp.239–250.
Munns, R. & Tester, M., 2008. Mechanisms of salinity tolerance. Annual review of plant biology, 59, pp.651–81.
Myakushina, Y.A. et al., 2009. Mutation in LSU4 gene affects flower development in Arabidopsis thaliana. Doklady
Biochemistry and Biophysics, 428(1), pp.257–260.
Nam, K.H. & Li, J., 2002. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell, 110(2), pp.203–12.
Nicaise, V., Roux, M. & Zipfel, C., 2009. Recent advances in PAMP-triggered immunity against bacteria: pattern recognition
receptors watch over and raise the alarm. Plant physiology, 150(4), pp.1638–47.
Nikiforova, V., Daub, C., et al., 2005. Integrative gene-metabolite network with implemented causality deciphers
informational fluxes of sulphur stress response. Journal of experimental botany, 56(417), pp.1887–96.
Nikiforova, V., Kopka, J., et al., 2005. Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by
metabolome analysis of Arabidopsis plants. Plant physiology, 138(1), pp.304–18.
Nurnberger, T. et al., 2004. Innate immunity in plants and animals: striking similarities and obvious differences.
Immunological Reviews, 198(1), pp.249–266.
Nürnberger, T. & Kemmerling, B., 2006. Receptor protein kinases--pattern recognition receptors in plant immunity. Trends
in plant science, 11(11), pp.519–22.
O’Connell, R.J. & Panstruga, R., 2006. Tête à tête inside a plant cell: establishing compatibility between plants and
biotrophic fungi and oomycetes. The New phytologist, 171(4), pp.699–718.
Pajerowska-Mukhtar, K.M. et al., 2012. The HSF-like transcription factor TBF1 is a major molecular switch for plant
growth-to-defense transition. Current biology : CB, 22(2), pp.103–12.
78
Petronia Carillo, M.G.A.G.P.A.F. and P.W., 2011. Abiotic Stress in Plants - Mechanisms and Adaptations A. Shanker, ed.,
InTech.
Petrov, V. et al., 2015. ROS-mediated abiotic stress-induced programmed cell death in plants. Frontiers in plant science, 6,
p.69.
Pieterse, C.M.J. et al., 2012. Hormonal modulation of plant immunity. Annual review of cell and developmental biology, 28,
pp.489–521.
Pieterse, C.M.J. et al., 2009. Networking by small-molecule hormones in plant immunity. Nature chemical biology, 5(5),
pp.308–16.
Poovaiah, B.W. et al., 2013. Recent advances in calcium/calmodulin-mediated signaling with an emphasis on plant-microbe
interactions. Plant physiology, 163(2), pp.531–42.
Pré, M. et al., 2008. The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant
defense. Plant physiology, 147(3), pp.1347–57.
Pusztahelyi, T., Holb, I.J. & Pócsi, I., 2015. Secondary metabolites in fungus-plant interactions. Frontiers in plant science, 6,
p.573.
Rahbarian, R. et al., 2011. Drought Stress Effects on Photosynthesis, Chlorophyll Fluorescence and Water Relations in
Tolerant and Susceptible Chickpea (Cicer Arietinum L.) Genotypes. Acta Biologica Cracoviensia Series Botanica,
53(1), pp.47–56.
Rajendran, K., Tester, M. & Roy, S.J., 2009. Quantifying the three main components of salinity tolerance in cereals. Plant,
cell & environment, 32(3), pp.237–49.
Rangeshwaran, R. et al., 2013. Analysis of proteins expressed by an abiotic stress tolerant Pseudomonas putida (NBAIIRPF9)
isolate under saline and high temperature conditions. Current microbiology, 67(6), pp.659–67.
Rao, A. et al., 2010. Mechanism of antifungal activity of terpenoid phenols resembles calcium stress and inhibition of the
TOR pathway. Antimicrobial agents and chemotherapy, 54(12), pp.5062–9.
Reuzeau, C. & Russinova, J., 2014. PLANTS HAVING ENHANCED YIELD-RELATED TRAITS AND METHOD FOR
MAKING THE SAME (US20140090110 A1). , 1(61).
del Rio, L.A., 2015. ROS and RNS in plant physiology: an overview. Journal of Experimental Botany, 66(10), pp.2827–
2837.
Robert-Seilaniantz, A., Grant, M. & Jones, J.D.G., 2011. Hormone crosstalk in plant disease and defense: more than just
jasmonate-salicylate antagonism. Annual review of phytopathology, 49, pp.317–43.
Rosebrock, T.R. et al., 2007. A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature,
448(7151), pp.370–4.
Rossi, F.R. et al., 2011. The sesquiterpene botrydial produced by Botrytis cinerea induces the hypersensitive response on
plant tissues and its action is modulated by salicylic acid and jasmonic acid signaling. Molecular plant-microbe
interactions : MPMI, 24(8), pp.888–96.
Ruckle, M.E. et al., 2012. Plastids are major regulators of light signaling in Arabidopsis. Plant physiology, 159(1), pp.366–
90.
Ruduś, I., Sasiak, M. & Kępczyński, J., 2012. Regulation of ethylene biosynthesis at the level of 1-aminocyclopropane-1-
carboxylate oxidase (ACO) gene. Acta Physiologiae Plantarum, 35(2), pp.295–307.
Rybel, B. De et al., 2009. Article Chemical Inhibition of a Subset of Arabidopsis thaliana GSK3-like Kinases Activates
Brassinosteroid Signaling. cell, pp.594–604.
Santner, A. & Estelle, M., 2009. Recent advances and emerging trends in plant hormone signalling. Nature, 459(7250),
pp.1071–1078.
Schachtman, D.P. & Shin, R., 2007. Nutrient sensing and signaling: NPKS. Annual review of plant biology, 58, pp.47–69.
Schapendonk, A.H.C.M., Spitters, C.J.T. & Groot, P.J., 1989. Effects of water stress on photosynthesis and chlorophyll
fluorescence of five potato cultivars. Potato Research, 32(1), pp.17–32.
Schmittgen, T.D. & Livak, K.J., 2008. Analyzing real-time PCR data by the comparative C(T) method. Nature protocols,
3(6), pp.1101–8.
Schouten, A. et al., 2002. Functional analysis of an extracellular catalase of Botrytis cinerea. Molecular Plant Pathology,
3(4), pp.227–238.
Segmüller, N. et al., 2008. NADPH Oxidases Are Involved in Differentiation and Pathogenicity in Botrytis cinerea.
Seiler, C. et al., 2011. ABA biosynthesis and degradation contributing to ABA homeostasis during barley seed development
under control and terminal drought-stress conditions. Journal of experimental botany, 62(8), pp.2615–32.
Seki, M. et al., 2007. Regulatory metabolic networks in drought stress responses. Current opinion in plant biology, 10(3),
pp.296–302.
Seyfferth, C. & Tsuda, K., 2014. Salicylic acid signal transduction: the initiation of biosynthesis, perception and
transcriptional reprogramming. Frontiers in plant science, 5, p.697.
Shah, J., Tsui, F. & Klessig, D.F., 1997. Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana,
identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Molecular plant-microbe
interactions : MPMI, 10(1), pp.69–78.
Shan, L. et al., 2008. Bacterial Effectors Target the Common Signaling Partner BAK1 to Disrupt Multiple MAMP Receptor -
Signaling Complexes and Impede Plant Immunity. Cell Host & Microbe, 4(1), pp.17–27.
79
Shanker, A. & Venkateswarlu, B., 2011. Abiotic Stress Response in Plants - Physiological, Biochemical and Genetic
Perspectives,
Sharma, P.D., 2014. Plant Pathology, Rastogi Publications.
Shin, R., Berg, R.H. & Schachtman, D.P., 2005. Reactive oxygen species and root hairs in Arabidopsis root response to
nitrogen, phosphorus and potassium deficiency. Plant & cell physiology, 46(8), pp.1350–7.
Shin, R. & Schachtman, D.P., 2004. Hydrogen peroxide mediates plant root cell response to nutrient deprivation.
Proceedings of the National Academy of Sciences of the United States of America, 101(23), pp.8827–32.
Shinozaki, K. & Yamaguchi-Shinozaki, K., 2006. Gene networks involved in drought stress response and tolerance. Journal
of Experimental Botany, 58(2), pp.221–227.
Sirko, A. et al., 2014. The family of LSU-like proteins. Frontiers in plant science, 5(774), p.9.
Slusarenko, A.J., Fraser, R.S. & Loon, L.C., 2012. Mechanisms of Resistance to Plant Diseases, Springer Science & Business
Media.
Smith, F.W. et al., 1995. Plant members of a family of sulfate transporters reveal functional subtypes. Proceedings of the
National Academy of Sciences, 92(20), pp.9373–9377.
Solfanelli, C. et al., 2006. Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant
physiology, 140(2), pp.637–46.
Spalding, E.P., 1999. Potassium Uptake Supporting Plant Growth in the Absence of AKT1 Channel Activity . Inhibition by
Ammonium and Stimulation by Sodium. The Journal of General Physiology, 113(6), pp.909–918.
Staskawicz, B.J., 2001. Genetics of Plant-Pathogen Interactions Specifying Plant Disease Resistance. PLANT PHYSIOLOGY,
125(1), pp.73–76.
Stuart, L.M., Paquette, N. & Boyer, L., 2013. Effector-triggered versus pattern-triggered immunity: how animals sense
pathogens. Nature reviews. Immunology, 13(3), pp.199–206.
Sultan, B., 2012. Global warming threatens agricultural productivity in Africa and South Asia. Environmental Research
Letters, 7(4), p.041001.
Suzuki, N. et al., 2011. Respiratory burst oxidases: the engines of ROS signaling. Current opinion in plant biology, 14(6),
pp.691–9.
Tada, Y. et al., 2008. Plant immunity requires conformational changes [corrected] of NPR1 via S-nitrosylation and
thioredoxins. Science (New York, N.Y.), 321(5891), pp.952–6.
Takahashi, H. et al., 1997. Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved
roots plays a central role in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United
States of America, 94(20), pp.11102–7.
Takahashi, H. et al., 2011. Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of
transporters and assimilatory enzymes. Annual review of plant biology, 62, pp.157–84.
Takahashi, H. et al., 2000. The roles of three functional sulphate transporters involved in uptake and translocation of sulphate
in Arabidopsis thaliana. The Plant Journal, 23(2), pp.171–182.
Tang, W. et al., 2008. Proteomics studies of brassinosteroid signal transduction using prefractionation and two-dimensional
DIGE. Molecular & cellular proteomics : MCP, 7(4), pp.728–38.
Temme, N. & Tudzynski, P., 2009. Does botrytis cinerea Ignore H(2)O(2)-induced oxidative stress during infection?
Characterization of botrytis activator protein 1. Molecular plant-microbe interactions : MPMI, 22(8), pp.987–98.
Thoma, I. et al., 2003. Cyclopentenone isoprostanes induced by reactive oxygen species trigger defense gene activation and
phytoalexin accumulation in plants. The Plant Journal, 34(3), pp.363–375.
Tognetti, J.A., Pontis, H.G. & Martínez-Noël, G.M.A., 2013. Sucrose signaling in plants: a world yet to be explored. Plant
signaling & behavior, 8(3), p.e23316.
Tsai, C.-J., Ma, B. & Nussinov, R., 2009. Protein-protein interaction networks: how can a hub protein bind so many different
partners? Trends in biochemical sciences, 34(12), pp.594–600.
Verhage, A. et al., 2011. Rewiring of the Jasmonate Signaling Pathway in Arabidopsis during Insect Herbivory. Frontiers in
plant science, 2, p.47.
Vestal, D.J. & Jeyaratnam, J.A., 2011. The guanylate-binding proteins: emerging insights into the biochemical properties and
functions of this family of large interferon-induced guanosine triphosphatase. Journal of interferon & cytokine
research : the official journal of the International Society for Interferon and Cytokine Research, 31(1), pp.89–97.
Voigt, C.A., 2014. Callose-mediated resistance to pathogenic intruders in plant defense-related papillae. Frontiers in plant
science, 5, p.168.
Volko, S.M., Boller, T. & Ausubel, F.M., 1998. Isolation of New Arabidopsis Mutants With Enhanced Disease Susceptibility
to Pseudomonas syringae by Direct Screening. Genetics, 149(2), pp.537–548.
Vos, I.A. et al., 2015. Impact of hormonal crosstalk on plant resistance and fitness under multi-attacker conditions. Frontiers
in plant science, 6, p.639.
Vos, I.A. et al., 2013. Onset of herbivore-induced resistance in systemic tissue primed for jasmonate-dependent defenses is
activated by abscisic acid. Frontiers in plant science, 4, p.539.
Wan, D. et al., 2012. Calmodulin-binding protein CBP60g is a positive regulator of both disease resistance and drought
tolerance in Arabidopsis. Plant cell reports, 31(7), pp.1269–81.
Wang, D., Amornsiripanitch, N. & Dong, X., 2006. A genomic approach to identify regulatory nodes in the transcriptional
80
network of systemic acquired resistance in plants. PLoS pathogens, 2(11), p.e123.
Wang, L. et al., 2009. Arabidopsis CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is
involved in disease resistance against Pseudomonas syringae. PLoS pathogens, 5(2), p.e1000301.
Wang, L. et al., 2011. CBP60g and SARD1 play partially redundant critical roles in salicylic acid signaling. The Plant
journal : for cell and molecular biology, 67(6), pp.1029–41.
Wang, Y. et al., 2010. A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein
kinase kinases. The Plant cell, 22(6), pp.2033–44.
Wasternack, C. & Hause, B., 2013. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress
response, growth and development. An update to the 2007 review in Annals of Botany. Annals of botany, 111(6),
pp.1021–58.
Weßling, R. et al., 2014. Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms
of life. Cell host & microbe, 16(3), pp.364–75.
Wildermuth, M.C. et al., 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature,
414(6863), pp.562–5.
Xiong, L. et al., 2001. Modulation of Abscisic Acid Signal Transduction and Biosynthesis by an Sm-like Protein in
Arabidopsis. Developmental Cell, 1(6), pp.771–781.
Xiong, L. & Zhu, J.-K., 2003. Regulation of abscisic acid biosynthesis. Plant physiology, 133(1), pp.29–36.
Yoo, S.-D., Cho, Y. & Sheen, J., 2009. Emerging connections in the ethylene signaling network. Trends in plant science,
14(5), pp.270–9.
Yoo, S.-D., Cho, Y.-H. & Sheen, J., 2007. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene
expression analysis. Nature protocols, 2(7), pp.1565–72.
Zhang, J. et al., 2007. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants.
Cell host & microbe, 1(3), pp.175–85.
Zhang, Y. et al., 2010. Control of salicylic acid synthesis and systemic acquired resistance by two members of a plantspecific
family of transcription factors. Proceedings of the National Academy of Sciences of the United States of
America, 107(42), pp.18220–5.
Zhang, Z. et al., 2012. Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant
immunity mediated by the NB-LRR protein SUMM2. Cell host & microbe, 11(3), pp.253–63.
Zhao, M. & Running, S.W., 2010. Drought-induced reduction in global terrestrial net primary production from 2000 through
2009. Science (New York, N.Y.), 329(5994), pp.940–3.
Zientara-Rytter, K. et al., 2011. Identification and functional analysis of Joka2, a tobacco member of the family of selective
autophagy cargo receptors. Autophagy, 7(10), pp.1145–58.
Zipfel, C., 2008. Pattern-recognition receptors in plant innate immunity. Current Opinion in Immunology, 20(1), pp.10–16.
Zipfel, C. & Felix, G., 2005. Plants and animals: a different taste for microbes? Current opinion in plant biology, 8(4),
pp.353–60.

Universiteit of Hogeschool
Bio-ingenieurswetenschappen Major Gewasproductie Minor Voeding en Gezondheid
Publicatiejaar
2016
Promotor(en)
prof. Cammue
Kernwoorden
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