#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

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 Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2010 Číslo 9
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#