Constitutive salicylic acid defences do not compromise seed yield, drought tolerance and water productivity in the Arabidopsis accession C24

Plant, Cell and Environment

Volumn 33, Issue 11, 2010, Pages 1959-1973

  Bechtold, Ulrike ^a   Lawson, Tracy ^a   Mejia Carranza, Jaime ^b   Meyer, Rhonda C ^c   Brown, Ian R ^d   Altmann, Thomas ^c   Ton, Jurriaan ^e   Mullineaux, Philip M ^a  

^a UNIVERSITY OF ESSEX   (United Kingdom)

^b JOHN INNES CENTRE   (United Kingdom)

^c LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^d UNIVERSITY OF KENT   (United Kingdom)

^e ROTHAMSTED RESEARCH   (United Kingdom)

Author keywords

Abiotic stress; Basal disease resistance; Biotic stress; Plant fitness; Transpiration efficiency; Water limitation

Indexed keywords

GLUTATHIONE; HYDROGEN PEROXIDE; PLANT RNA; SALICYLIC ACID; WATER;

DISEASE RESISTANCE; DROUGHT STRESS; FITNESS; GENOTYPE; HERB; ORGANIC ACID; PATHOGENICITY; RESOURCE USE; SEED; TOLERANCE; TRANSPIRATION; WATER USE EFFICIENCY; YIELD;

ARABIDOPSIS; ARTICLE; DNA MICROARRAY; DROUGHT; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; INNATE IMMUNITY; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT SEED; REPRODUCTIVE FITNESS;

ARABIDOPSIS; DROUGHTS; GENETIC FITNESS; GENOTYPE; GLUTATHIONE; HYDROGEN PEROXIDE; IMMUNITY, INNATE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, PLANT; SALICYLIC ACID; SEEDS; STRESS, PHYSIOLOGICAL; WATER;

ARABIDOPSIS;

EID: 77958605327     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2010.02198.x     Document Type: Article

References (93)

1. Abramoff M.D., Magalhaes P.J. & Ram S.J. (2004) Image processing with ImageJ. Biophotonics International 11, 36-42.
2. Agrios G.N. (1997) Plant Pathology, 4th edn. Academic Press Inc., San Diego, CA, USA.
3. Apel K. & Hirt H. (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373-399.
4. Asselbergh B., Vleesschauwer D. & Höfte M. (2008) Global switches and fine-tuning-ABA modulates plants pathogen defense. Molecular Plant-Microbe Interactions 21, 709-719.
5. Baldwin I.T. (1998) Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proceedings of the National Academy of Sciences of the United States of America 95, 8113-8118.
6. Ball L., Accotto G.-P., Bechtold U., et-al. (2004)Evidence for a direct link between glutathione biosynthesis and stress defence gene expression in Arabidopsis. The Plant Cell 16, 2448-2462.
7. Bechtold U., Karpinski S. & Mullineaux P.M. (2005) The influence of the light environment and photosynthesis on oxidative signalling responses in plant-biotrophic pathogen interactions. Plant, Cell & Environment 28, 1046-1055.
8. Bechtold U., Rabbani N., Mullineaux P.M. & Thornalley P.J. (2009) Quantitative measurement of specific biomarkers for protein oxidation, nitration and glycation in Arabidopsis leaves. The Plant Journal 59, 661-671.
9. Bestwick C.S., Brown I.R., Bennett M.H. & Mansfield J.W. (2002) Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. The Plant Cell 9, 209-221.
10. Bowling S.A., Clarke J.D., Liu Y., Klessig D.F. & Dong X. (1997) The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. The Plant Cell 9, 1573-1584.
11. Boyer J.S. (1970) Leaf enlargement and metabolic rates in corn, soybean and sunflower at various leaf water potentials. Plant Physiology 46, 233-235.
12. Boyes D.C., Zayed A.M., Ascenzi R., McCaskill A.J., Hoffman N.E., Davis K.R. & Görlach J. (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. The Plant Cell 13, 1499-1510.
13. Breitling R. & Herzyk P. (2005) Rank-based methods as a non-parametric alternative of the T-statistic for the analysis of biological microarray data. Journal of Bioinformatics and Computational Biology 3, 1171-1189.
14. Brosché M., Merilo E., Mayer F., Pechter P., Puzõrjova I., Brader G., Kangasjärvi J. & Kollist H. (2010) Natural variation in ozone sensitivity among Arabidopsis thaliana accessions and its relation to stomatal conductance. Plant, Cell & Environment 33, 914-925.
15. Brown J.K.M. (2002) Yield penalties of disease resistance in crops. Current Opinion in Plant Biology 5, 339-344.
16. Brown J.K.M. (2003) A cost of disease resistance: paradigm or peculiarity? Trends in Genetics 19, 667-671.
17. Chandra-Shekara A.C., Gupte M., Navarre D., Raina S., Raina R., Klessig D. & Kachroo P. (2006) Light-dependent hypersensitive response and resistance signaling against turnip crinkle virus in Arabidopsis. The Plant-- Journal 45, 320-334.
18. Chaves M.M., Pereira J.S., Maroco J., Rodrigues M.L., Ricardo C.P.P., Osorio M.L., Carvalho I., Faria T. & Pinheiro C. (2002) How plants cope with water stress in the field. Photosynthesis and growth. Annals of Botany 89, 907-916.
19. Clarke J.D., Liu Y., Klessig D.F. & Dong X. (1998) Uncoupling PR-gene expression from NPR1 and bacterial resistance: characterization of the dominant Arabidopsis cpr6 mutant. The Plant Cell 10, 557-567.
20. Cline M.S., Smoot M., Cerami E., et-al. (2007) Integration of biological networks and gene expression data using Cytoscape. Nature Protocols 2, 2366-2382.
21. Condon A.G., Richards R.A., Rebetzke G.J. & Farquhar G.D. (2004) Breeding for high water-use efficiency. Journal of Experimental Botany 55, 2447-2460.
22. Creissen G., Firmin J., Fryer M., et al. (1999) Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress. The Plant Cell 11, 1277-1291.
23. Cross A.R. & Jones O.T.G. (1986) The effect of the inhibitor diphenylene iodonium on the superoxide-generating system of neutrophils. The Biochemical Journal 237, 111-116.
24. Custers J.H., Harrison S.J., Sela-Buurlage M.B., et al. (2004) Isolation and characterisation of a class of carbohydrate oxidases from higher plants, with a role in active defence. The Plant Journal 39, 147-160.
25. Damgaard C. & Jensen B.D. (2002) Disease resistance in Arabidopsis thaliana increases the competitive ability and the predicted probability of long-term ecological success under disease pressure. Oikos 98, 459-466.
26. Desprez-Loustau M.L., Marcais B., Nageleisen L.M., Piou D. & Vannini A. (2006) Interactive effects of drought and pathogens in forest trees. Annals of Forest Science 63, 597-612.
27. Donovan L.A. & Ehleringer J.R. (1992) Contrasting water-use patterns among size and life-history classes of a semi-arid shrub. Functional Ecology 3, 482-488.
28. Dudley S.A. (1996) Differing selection on plant physiological traits in response to environmental water availability: a test of adaptive hypotheses. Evolution 50, 92-102.
29. Edwards K.D., Anderson P.E., Hall A., Salathia N.S., Locke J.C., Lynn J.R., Straume M., Smith J.Q. & Millar A.J. (2006) FLOWERING LOCUS C mediates natural variation in the high-temperature response of the Arabidopsis circadian clock. The Plant Cell 18, 639-650.
30. Ellis J. (2006) Insights into non-host disease resistance: can they assist disease control in agriculture? The Plant Cell 18, 523-528.
31. Fan J., Hill L., Crooks C., Doerner P. & Lamb C. (2009) Absicisic acid has a key role in modulating diverse plant-pathogen interactions. Plant Physiology 150, 1750-1761.
32. Forcat S., Bennett M.H., Mansfield J.W. & Grant M.R. (2008) A rapid and robust method for simultaneously measuring changes in the phytohomrones ABA, JA and SA in plants following biotic and abiotic stress. Plant Methods 4, 16.
33. Foyer C. & Noctor G. (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. The Plant Cell 17, 1866-1875.
34. Galvez-Valdivieso G., Fryer M., Lawson T., et al. (2009) The high light response in Arabidopsis involves ABA signaling between vascular and bundle sheath cells. The Plant Cell 21, 2143-2162.
35. Geber M.A. & Dawson T.E. (1997) Genetic variation in stomatal and biochemical limitations to photosynthesis in the annual plant, Polygonum arenastrum. Oecologia 109, 535-546.
36. Gregory P.J. (2004) Agronomic approaches to increasing water use efficiency. In Water Use Efficiency in Plant Biology (ed. M.A. Bacon ), pp. 142-170. Blackwell Publishing, Oxford, UK.
37. Hannah M.A., Wiese D., Freund S., Fiehn O., Heyer A.G. & Hincha D.K. (2006) Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiology 142, 98-112.
38. Heidel A.J. & Dong X. (2006) Fitness benefits of systemic acquired resistance during Hyaloperonospora parasitica infection in Arabidopsis thaliana. Genetics 173, 1621-1628.
39. Heil M. & Baldwin I.T. (2002) Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends in Plant Science 7, 61-67.
40. Heschel M.S., Donohue K., Hausmann N.J. & Schmitt J. (2002) Population differentiation and natural selection for water-use efficiency in Impatiens capensis (Balsaminaceae). International Journal of Plant Sciences 163, 907-912.
41. Holub E.B. & Beynon J.L. (1997) Symbiology of mouse ear cress (Arabidopsis thaliana) and oomycetes. Advances in Botanical Research 24, 227-273.
42. Van Hulten M., Pelser M., Van Loon L.C., Pieterse C.M. & Ton J. (2006) Costs and benefits of priming for defense in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 103, 5602-5607.
43. Jambunathan N., Siani J.M. & McNellis T.W. (2001) A humidity-sensitive Arabidopsis copine mutant exhibits precocious cell death and increased disease resistance. The Plant Cell 13, 2225-2240.
44. Jimenez A., Creissen G., Kular B., Firmin J., Robinson S., Verhoeyen M. & Mullineaux P. (2002) Changes in oxidative processes and components of the antioxidant system during tobacco fruit ripening. Planta 214, 751-758.
45. Jing H.-C., Hebeler R., Oeljeklaus S., Sitek B., Stühler K., Meyer H.E., Sturre M.J.G., Hille J., Warscheid B. & Dijkwel P.P. (2008) Early leaf senescence is associated with an altered cellular redox balance in Arabidopsis cpr5/old1 mutants. Plant Biology 10, 85-98.
46. Juenger T.E., McKay J.K., Hausmann N., Keurentjes J.J.B., Sen S., Stowe K.A., Dawson T.E., Simms E.L. & Richards J.H. (2005) Identification and characterization of QTL underlying whole-plant physiology in Arabidopsis thaliana: -13C, stomatal conductance and transpiration efficiency. Plant, Cell & Environment 28, 697-708.
47. Karpinski S., Gabrys H., Mateo A., Karpinska B. & Mullineaux P.M. (2003) Light perception in plant disease defence signalling. Current Opinion in Plant Biology 6, 390-396.
48. Van Leeuwen H., Kliebenstein D.J., West M.A.L., Kim K., Van Poecke R., Katagiri F., Michelmore R.W., Doerge R.W. & St. Clair D.A. (2007) Natural variation among Arabidopsis thaliana accessions for transcriptome response to exogenous salicylic acid. The Plant Cell 19, 2099-2110.
49. Liu Q., Kasuga M., Sakuma Y., Abe H., Miura S., Yamaguchi-Shinozaki K. & Shinozaki K. (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain, separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. The Plant Cell 10, 1391-1406.
50. Loudet O., Chaillou S., Krapp A. & Daniel-Vedele F. (2003) Quantitative trait loci analysis of water and anion contents in interaction with nitrogen availability in Arabidopsis thaliana. Genetics 163, 711-722.
51. Loughlin A.F., Skiles G.L., Alberts D.W. & Schaefer W.H. (2001) An ion exchange liquid chromatography/mass spectrometry method for the determination of reduced and oxidized glutathione and glutathione conjugates in hepatocytes. Journal of Pharmaceutical and Biomedical Analysis 26, 131-142.
52. McKay J.K., Richards J.H., Nemali K.S., Sen S., Mitchell-Olds T., Boles S., Stahl E.A., Wayne T. & Juenger T.E. (2008) Genetics of drought adaptation in Arabidopsis thaliana II. QTL analysis of a new mapping population, Kas-1-×-Tsu-1. Evolution 62, 3014-3026.
53. Maere S., Heymans K. & Kuiper M. (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21, 3448-3449.
54. Masle J., Gilmore S.R. & Farquhar G.D. (2005) The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 436, 866-870.
55. Mateo A., Funck D., Mühlenbock P., Kular B., Mullineaux P.M. & Karpinski S. (2006) Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. Journal of Experimental Botany 57, 1795-1807.
56. Mattson W.J. & Haack R.A. (1987) The role of drought in outbreaks of plant-eating insects. BioScience 37, 110-118.
57. May M.J., Hammond-Kosack K.E. & Jones J. (1996) Involvement of reactive oxygen species, glutathione metabolism, and lipid peroxidation in the Cf-gene-dependent defence response of tomato cotyledons induced by race-specific elicitors of Cladosporium fulvum. Plant Physiology 110, 1367-1379.
58. Michaels S.D., He Y., Scortecci K.C. & Amasino R.M. (2003) Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 100, 10102-10107.
59. Miller G., Schlauch K., Tam R., Cortes D., Torres M.A., Shulaev V., Dangl J.L. & Mittler R. (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Science Signaling 2, ra45.
60. Monteith J.L. (1984) Consistency and convenience in the choice of units for agricultural science. Experimental Agriculture 20, 105-117.
61. Monteith J.L. (1993) The exchange of water and carbon by crops in a Mediterranean climate. Irrigation Science 14, 85-91.
62. Morison J.I.L., Baker N.R., Mullineaux P.M. & Davies W.J. (2008) Improving water use in crop production. Philosophical Transactions of the Royal Society of London, Series B 363, 639-658.
63. Mullineaux P.M. & Rausch T. (2005) Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynthesis Research 86, 459-474.
64. Mullineaux P.M., Karpinski S. & Baker N.R. (2006) Spatial dependence for hydrogen peroxide-directed signaling in light-stressed plants. Plant Physiology 141, 346-350.
65. Noutoshi Y., Ito T., Seki M., Nakashita H., Yoshida S., Marco Y., Shirasu K. & Shinozaki K. (2005) A single amino acid insertion in the WRKY domain of the Arabidopsis TIR-NBS-LRR-WRKY-type disease resistance protein SLH1 (sensitive to low humidity 1) causes activation of defense responses and hypersensitive cell death. The Plant Journal 43, 873-888.
66. Parisy V., Poinssot B., Owsianowski L., Buchala A., Glazebrook J. & Mauch F. (2006) Identification of PAD2 as a --glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. The Plant Journal 49, 159-172.
67. Parker J.E. (2003) Plant recognition of microbial patterns. Trends in Plant Science 8, 245-247.
68. Passioura J.B. (1977) Grain yield, harvest index and water use of wheat. Journal of Australian Institute of Agricultural Science 43, 117-121.
69. Passioura J.B. (2002) Environmental plant biology and crop improvement. Functional Plant Biology 29, 537-546.
70. Passioura J.B. (2007) The drought environment: physical, biological and agricultural perspectives. Journal of Experimental Botany 58, 113-117.
71. Pimentel C., Laffray D. & Louguet P. (1999) Intrinsic water-use efficiency at the pollination stage as a parameter for drought tolerance selection in Phaseolus vulgaris. Physiologia Plantarum 106, 184-189.
72. Redei G.P. (1962) Supervital mutants of Arabidopsis. Genetics 47, 443-460.
73. Rohde P., Hincha D.K. & Heyer A.G. (2004) Heterosis in the freezing tolerance of crosses between two Arabidopsis thaliana accessions (Columbia-0 and C24) that show differences in non-acclimated and acclimated freezing tolerance. The Plant Journal 38, 290-799.
74. Sakuma Y., Maruyama K., Qin F., Osakabe Y., Shinozaki K. & Yamaguchi-Shinozaki K. (2006) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress--responsive gene expression. Proceedings of the National Academy of Sciences of the United States of America 103, 18222-18227.
75. Sanda S.L. & Amasino R.M. (1995) Genetic and physiological analysis of flowering time in the C24 line of Arabidopsis thaliana. Weeds World 2iii, 2-8.
76. Schmid K.J., Törjék O., Meyer R., Schmuths H., Hoffmann M.H. & Altmann T. (2006) Evidence for a large-scale population structure of Arabidopsis thaliana from genome-wide single nucleotide polymorphism markers. Theoretical and Applied Genetics 112, 1104-1114.
77. Schulze E.D. (1986a) Whole-plant responses to drought. Australian Journal of Plant Physiology 13, 127-141.
78. Schulze E.D. (1986b) Carbon dioxide and water vapor exchange in response to drought in the atmosphere and the soil. Annual Review of Plant Physiology 37, 247-274.
79. Senda K. & Ogawa K. (2004) Induction of PR-1 accumulation accompanied by runaway cell death in the lsd1 mutant of Arabidopsis is dependent on glutathione levels but independent of the redox state of glutathione. Plant Cell Physiology 45, 1578-1585.
80. Sheldon C.C., Rouse D.T., Finnegan E.J., Peacock W.J. & Dennis E.S. (2000) The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proceedings of the National Academy of Sciences of the United States of America 97, 3753-3758.
81. Solyu S., Brown I. & Mansfield J.A. (2005) Cellular reactions in Arabidopsis following challenge by strains of Pseudomonas syringae: from basal resistance to compatibility. Physiological and Molecular Plant Pathology 66, 232-243.
82. Steduto P., Hsiao T.C. & Fereres E. (2007) On the conservative behaviour of biomass water productivity. Irrigation Science 25, 189-207.
83. Suarez-Farinas M., Pellegrino M., Wittkowski K.M. & Magnasco M.O. (2005) Harshlight a corrective make-up program for microarray chips. BMC Bioinformatics 6, 294.
84. Swarup K., Alonso-Blanco C., Lynn J.R., Michaels S.D., Amasino R.M., Koornneef M. & Millar A.J. (1999) Natural allelic variation identifies new genes in the Arabidopsis circadian system. The Plant Journal 20, 67-77.
85. Tian D., Traw M.B., Chen J.Q., Kreitman M. & Bergelson J. (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423, 74-77.
86. Ton J., Pieterse C.M.J. & Van Loon L.C. (1999) Identification of a locus in Arabidopsis controlling both the expression of rhizobacteria-mediated induced systemic resistance (ISR) and basal resistance against Pseudomonas syringae pv. tomato. Molecular Plant-Microbe Interactions 12, 911-918.
87. Torres M.A., Jones J.D. & Dangl J.L. (2005) Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nature Genetics 10, 1130-1134.
88. De Torres-Zabala M., Truman W., Bennett M.H., Lafforgue G., Mansfield J.W., Rodriguez Egea P., Bögre L. & Grant M. (2007) Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. The EMBO Journal 26, 1434-1443.
89. Wu Z., Irizarry R., Gentleman R., Murillo F.M. & Spencer F. (2004) A model-based background adjustment for oligonucleotide expression arrays. Journal of the American Statistical Association 99, 909-917.
90. Yamaguchi-Shinozaki K. & Shinozaki K. (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. The Plant Cell 6, 251-264.
91. Yasuda M., Ishikawa A., Jikumaru Y., et-al. (2008) Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. The Plant Cell 20, 1678-1692.
92. Zeier J., Pink B., Mueller M.J. & Berger S. (2004) Light conditions influence specific defence responses in incompatible plant-pathogen interactions: uncoupling systemic resistance from salicylic acid and PR-1 accumulation. Planta 219, 673-683.
93. 2 production and defense gene expression. The Plant Journal 39, 920-932.