Metal Hyperaccumulation Armors Plants against Disease
Metal hyperaccumulation, in which plants store exceptional concentrations of metals in their shoots, is an unusual trait whose evolutionary and ecological significance has prompted extensive debate. Hyperaccumulator plants are usually found on metalliferous soils, and it has been proposed that hyperaccumulation provides a defense against herbivores and pathogens, an idea termed the ‘elemental defense’ hypothesis. We have investigated this hypothesis using the crucifer Thlaspi caerulescens, a hyperaccumulator of zinc, nickel, and cadmium, and the bacterial pathogen Pseudomonas syringae pv. maculicola (Psm). Using leaf inoculation assays, we have shown that hyperaccumulation of any of the three metals inhibits growth of Psm in planta. Metal concentrations in the bulk leaf and in the apoplast, through which the pathogen invades the leaf, were shown to be sufficient to account for the defensive effect by comparison with in vitro dose–response curves. Further, mutants of Psm with increased and decreased zinc tolerance created by transposon insertion had either enhanced or reduced ability, respectively, to grow in high-zinc plants, indicating that the metal affects the pathogen directly. Finally, we have shown that bacteria naturally colonizing T. caerulescens leaves at the site of a former lead–zinc mine have high zinc tolerance compared with bacteria isolated from non-accumulating plants, suggesting local adaptation to high metal. These results demonstrate that the disease resistance observed in metal-exposed T. caerulescens can be attributed to a direct effect of metal hyperaccumulation, which may thus be functionally analogous to the resistance conferred by antimicrobial metabolites in non-accumulating plants.
Vyšlo v časopise:
Metal Hyperaccumulation Armors Plants against Disease. PLoS Pathog 6(9): e32767. doi:10.1371/journal.ppat.1001093
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1001093
Souhrn
Metal hyperaccumulation, in which plants store exceptional concentrations of metals in their shoots, is an unusual trait whose evolutionary and ecological significance has prompted extensive debate. Hyperaccumulator plants are usually found on metalliferous soils, and it has been proposed that hyperaccumulation provides a defense against herbivores and pathogens, an idea termed the ‘elemental defense’ hypothesis. We have investigated this hypothesis using the crucifer Thlaspi caerulescens, a hyperaccumulator of zinc, nickel, and cadmium, and the bacterial pathogen Pseudomonas syringae pv. maculicola (Psm). Using leaf inoculation assays, we have shown that hyperaccumulation of any of the three metals inhibits growth of Psm in planta. Metal concentrations in the bulk leaf and in the apoplast, through which the pathogen invades the leaf, were shown to be sufficient to account for the defensive effect by comparison with in vitro dose–response curves. Further, mutants of Psm with increased and decreased zinc tolerance created by transposon insertion had either enhanced or reduced ability, respectively, to grow in high-zinc plants, indicating that the metal affects the pathogen directly. Finally, we have shown that bacteria naturally colonizing T. caerulescens leaves at the site of a former lead–zinc mine have high zinc tolerance compared with bacteria isolated from non-accumulating plants, suggesting local adaptation to high metal. These results demonstrate that the disease resistance observed in metal-exposed T. caerulescens can be attributed to a direct effect of metal hyperaccumulation, which may thus be functionally analogous to the resistance conferred by antimicrobial metabolites in non-accumulating plants.
Zdroje
1. BakerAJM
BrooksRR
1989 Terrestrial higher plants which hyperaccumulate metallic elements – a review of their distribution, ecology and phytochemistry. Biorecovery 1 81 126
2. ReevesRD
BakerAJM
2000 Metal-accumulating plants.
RaskinI
EnsleyBD
Phytoremediation of Toxic Metals: Using Plants to Clean-up the Environment New York John Wiley & Sons 193 230
3. BrooksRR
1998 Plants that Hyperaccumulate Heavy Metals. Wallingford CAB International 380
4. VerbruggenN
HermansC
SchatH
2009 Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181 759 776
5. PollardAJ
PowellKD
HarperFA
SmithJAC
2002 The genetic basis of metal hyperaccumulation in plants. Crit Rev Plant Sci 21 539 566
6. BoydRS
MartensSN
1992 The raison d'être for metal hyperaccumulation by plants.
BakerAJM
ProctorJ
ReevesRD
The Vegetation of Ultramafic (Serpentine) Soils Andover Intercept Limited 279 289
7. PoschenriederC
TolràR
BarcelóJ
2006 Can metals defend plants against biotic stress? Trends Plant Sci 11 288 295
8. BoydRS
2007 The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant Soil 293 153 176
9. VeskPA
ReichmanS
2009 Hyperaccumulators and herbivores – a Bayesian meta-analysis of feeding choice trials. J Chem Ecol 35 289 296
10. HansonB
LindblemSD
LoefflerML
Pilon-SmithEAH
2004 Selenium protects plants from phloem-feeding aphids due to both deterrence and toxicity. New Phytol 162 655 662
11. BehmerST
LloydCM
RaubenheimerD
Stewart-ClarkJ
KnightJ
2005 Metal hyperaccumulation in plants: mechanisms of defence against insect herbivores. Funct Ecol 19 55 66
12. JiangRF
MaDY
ZhaoFJ
McGrathSP
2005 Cadmium hyperaccumulation protects Thlaspi caerulescens from leaf feeding damage by thrips (Frankliniella occidentalis). New Phytol 167 805 814
13. NoretN
MeertsP
TolràR
PoschenriederC
BarcelóJ
2005 Palatability of Thlaspi caerulescens for snails: influence of zinc and glucosinolates. New Phytol 165 763 772
14. NoretN
MeertsP
VanhaelenM
Dos SantosA
EscarréJ
2007 Do metal-rich plants deter herbivores? A field test of the defence hypothesis. Oecologia 152 92 100
15. JheeEM
BoydRS
EubanksMD
2005 Nickel hyperaccumulation as an elemental defense of Streptanthus polygaloides (Brassicaceae): influence of herbivore feeding mode. New Phytol 168 331 344
16. GhaderianYSM
LyonAJE
BakerAJM
2000 Seedling mortality of metal hyperaccumulator plants resulting from damping off by Pythium spp. New Phytol 146 219 224
17. BoydRS
ShawJJ
MartensSN
1994 Nickel hyperaccumulation defends Streptanthus polygaloides (Brassicaceae) against pathogens. Am J Bot 81 294 300
18. ReevesRD
SchwartzC
MorelJL
EdmondsonJ
2001 Distribution and metal-accumulating behavior of Thlaspi caerulescens and associated metallophytes in France. Int J Phytorem 3 145 172
19. BakerAJM
ReevesRD
HajarASM
1994 Heavy metal accumulation and tolerance in British populations of the metallophyte Thlaspi caerulescens J & C Presl (Brassicaceae). New Phytol 127 61 68
20. RoosensN
VerbruggenN
MeertsP
Ximénez-EmbúnP
SmithJAC
2003 Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from western Europe. Plant Cell Environ 26 1657 1672
21. HammondJP
BowenHC
WhitePJ
MillsV
PykeKA
2006 A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes. New Phytol 170 239 260
22. AssunçãoAGL
SchatH
AartsMGM
2003 Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol 159 351 360
23. CobbettC
2003 Heavy metals and plants – model systems and hyperaccumulators. New Phytol 159 289 293
24. PeerWA
MahmoudianM
FreemanJL
LahnerB
RichardsEL
2006 Assessment of plants from the Brassicaceae family as genetic models for the study of nickel and zinc hyperaccumulation. New Phytol 172 248 260
25. MilnerMJ
KochianLV
2008 Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102 3 13
26. DebenerT
LehnackersH
ArnoldM
DanglJL
1991 Identification and molecular mapping of a single Arabidopsis thaliana locus determining resistance to a phytopathogenic Pseudomonas syringae isolate. Plant J 289 302
27. KüpperH
ZhaoFJ
McGrathSP
1999 Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 119 305 311
28. KüpperH
MijovilovichA
Meyer-KlauckeW
KroneckPMH
2004 Tissue- and age-dependent differences in the complexation of cadmium and zinc in the cadmium/zinc hyperaccumulator Thlaspi caerulescens (Ganges ecotype) revealed by X-ray absorption spectroscopy. Plant Physiol 134 748 757
29. CosioC
DeSantisL
FreyB
DialloS
KellerC
2005 Distribution of cadmium in leaves of Thlaspi caerulescens. J Exp Bot 56 765 775
30. DongX
MindrinosM
DavisKR
AusubelFM
1991 Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell 3 61 72
31. ChmielowskaJ
VelosoJ
GutiérrezJ
SilvarC
DíazJ
2009 Cross-protection of pepper plants stressed by copper against a vascular pathogen is accompanied by the induction of a defence response. Plant Sci 178 176 182
32. ByrdMS
SadovskayaI
VinogradovE
LuHP
SprinkleAB
2009 Genetic and biochemical analyses of the Pseudomonas aeruginosa Psl exopolysaccharide reveal overlapping roles for polysaccharide synthesis enzymes in Psl and LPS production. Mol Microbiol 73 622 638
33. ZhangLL
JiaYT
WangL
FangRX
2007 A proline iminopeptidase gene upregulated in planta by a LuxR homologue is essential for pathogenicity of Xanthomonas campestris pv. campestris. Mol Microbiol 65 121 136
34. ZhaoS
ZhuQ
SomervilleRL
2000 The σ70 transcription factor TyrR has zinc-stimulated phosphatase activity that is inhibited by ATP and tyrosine. J Bacteriol 182 1053 1061
35. BennettJ
VernonRW
1990 Mines of the Gwydyr Forest: Part 2. The Hafna Mine, Llanrwst and some early ventures in Gwydyr Nant Cuddington, Cheshire, UK Gwydyr Mines Publications
36. KrämerU
PickeringIJ
PrinceRC
RaskinI
SaltDE
2000 Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiol 122 1343 1354
37. Vogel-MikušK
RegvarM
Mesjasz-PrzybyłowiczJ
PrzybyłowiczWJ
SimčicJ
2008 Spatial distribution of cadmium in leaves of metal hyperaccumulating Thlaspi praecox using micro-PIXE. New Phytol 179 712 721
38. WójcikM
VangronsveldJ
D'HaenJ
TukiendorfA
2005 Cadmium tolerance in Thlaspi caerulescens. II. Localization of cadmium in Thlaspi caerulescens. Env Exp Bot 53 163 171
39. Freeman
JL
PersansMW
NiemanK
AlbrechtC
PeerW
2004 Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16 2176 2191
40. TuomainenMH
NunanN
LehesrantaSJ
TervahautaAI
HassinenVH
2006 Multivariate analysis of protein profiles of metal hyperaccumulator accessions. Proteomics 6 3696 3706
41. KrämerU
Cotter-HowellsJD
CharnockJM
BakerAJM
SmithJAC
1996 Free histidine as a metal chelator in plants that accumulate nickel. Nature 379 635 638
42. RoosensNH
LeplaeR
BernardC
VerbruggenN
2005 Variations in plant metallothioneins: the heavy metal hyperaccumulator Thlaspi caerulescens as a study case. Planta 222 716 729
43. FrankSA
1992 Models of plant pathogen coevolution. Trends Genet 8 213 219
44. KaweckiTJ
EbertD
2004 Conceptual issues in local adaptation. Ecol Lett 7 1225 1241
45. NuismerSL
GandonS
2008 Moving beyond common-garden and transplant designs: insights into the causes of local adaptation in species interactions. Am Nat 171 658 668
46. IdrisR
TrifonovaR
PuschenreiterM
WenzelWW
SessitschA
2004 Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Appl Env Microbiol 70 2667 2677
47. BarzantiR
OzinoF
BazzicalupoM
GabbrielliR
GalardiF
2007 Isolation and characterization of endophytic bacteria from the nickel hyperaccumulator plant Alyssum bertolonii. Microbial Ecol 53 306 316
48. AlexeyevMF
ShokolenkoIN
CroughanTP
1995 New mini-Tn5 derivatives for insertion mutagenesis and genetic engineering in Gram-negative bacteria. Can. J Microbiol 41 1053 1055
49. SambrookJ
RussellDW
2001 Molecular Cloning. New York Cold Spring Harbor Laboratory Press
50. KingEO
WardMK
RaneyDE
1954 Two simple media for the demonstration of pyocyanin and fluorescein. J Lab Clin Med 22 301 307
51. RicoA
PrestonGM
2008 Pseudomonas syringae pv. tomato DC3000 uses constitutive and apoplast-induced nutrient assimilation pathways to catabolize nutrients that are abundant in the tomato apoplast. Mol Plant–Microbe Interact 21 269 282
52. FigurskiDH
HelinskiDR
1979 Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci USA 76 1648 1652
53. LarionovA
KrauseA
MillerW
2005 A standard curve based method for relative real time PCR data processing. BMC Bioinformatics 6 62
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2010 Číslo 9
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Structure of the Extracellular Portion of CD46 Provides Insights into Its Interactions with Complement Proteins and Pathogens
- The Length of Vesicular Stomatitis Virus Particles Dictates a Need for Actin Assembly during Clathrin-Dependent Endocytosis
- Inhibition of TIR Domain Signaling by TcpC: MyD88-Dependent and Independent Effects on Virulence
- Cellular Entry of Ebola Virus Involves Uptake by a Macropinocytosis-Like Mechanism and Subsequent Trafficking through Early and Late Endosomes