Metal hyperaccumulation armors plants against disease.

Metal hyperaccumulation armors plants against disease.
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DOI:
10.1371/journal.ppat.1001093
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发表时间:
2010-09-09
期刊:
影响因子:
6.7
通讯作者:
Preston GM
Preston GM
中科院分区:
医学1区
文献类型:
--
作者:
Fones H;Davis CA;Rico A;Fang F;Smith JA;Preston GM

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金属超积累是一种不同寻常的特征,其进化和生态意义引起了广泛的争论。超积累植物通常生长在含金属的土壤上,人们提出超积累对食草动物和病原体具有防御作用,这一观点被称为元素防御假说。我们用十字花科植物Tlaspi caerulescens(锌、镍和镉的超蓄积体)和细菌病原体紫丁香假单胞菌研究了这一假设。黄斑病毒(PSM)。通过叶片接种试验,我们已经证明了这三种金属中的任何一种的过度积累都抑制了植物PSM的生长。通过与体外剂量-反应曲线的比较,证明了病原菌侵入叶片的体叶和质外体中的金属浓度足以解释这种防御效应。此外,通过转座子插入产生的耐锌性增强和耐锌性降低的PSM突变体在高锌植物中的生长能力分别增强或降低,这表明金属直接影响病原菌。最后,我们发现,与从非积累植物中分离的细菌相比,自然定植于前铅锌矿遗址蓝藻叶片的细菌具有更高的锌耐受性,这表明它们对高金属的局部适应。这些结果表明,在暴露于金属的蓝藻中观察到的抗病能力可以归因于金属超积累的直接影响,因此在功能上可能类似于非积累植物中的抗菌代谢产物所产生的抗性。富含重金属的土壤支持着独特的耐金属植物群落,其中一些植物表现出一种被称为金属超积累的显著特征。这些植物的叶片中积累了异常高浓度的金属元素,但这一特征是否赋予了适应优势仍存在争议。在这项研究中,我们测试了金属超积累提供疾病保护的假设。我们证明了蓝斑刺蛾对由紫丁香假单胞菌PV引起的细菌性叶斑病产生了抗性。当黑斑病(PSM)积累锌、镍或镉时,这些植物中的金属浓度足以说明它们观察到的抗病能力。我们还发现,不同菌株的耐锌性与它们在高锌含量的紫云英叶片上的定殖能力密切相关。在一项实地研究中,从生长在前铅锌矿遗址上的蓝藻植物叶片中分离出的细菌被发现比从农作物中分离出来的细菌具有更高的金属耐受性。我们的发现表明,金属在植物中的过度积累可以作为一种机制来防止病原微生物的攻击,但耐受金属的病原体可以克服这种防御。
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. Soils rich in heavy metals support communities of distinctive metal-tolerant plants, a number of which exhibit a remarkable trait known as metal hyperaccumulation. These plants accumulate exceptionally high concentrations of metallic elements in their leaves, but whether this trait confers any adaptive advantage is controversial. In this study, we test the hypothesis that metal hyperaccumulation provides protection against disease. We demonstrate that Thlaspi caerulescens becomes resistant to bacterial leaf spot caused by Pseudomonas syringae pv. maculicola (Psm) when it accumulates zinc, nickel, or cadmium, and show that the metal concentrations in these plants are sufficient to account for their observed disease resistance. We also show that there is a close correlation between the zinc tolerance of different strains of Psm and their ability to colonize T. caerulescens leaves with high zinc content. In a field study, bacteria isolated from the leaves of T. caerulescens plants growing on the site of a former lead–zinc mine were found to possess a higher degree of metal tolerance than bacteria isolated from crop plants. Our findings show that metal hyperaccumulation in plants can act as a mechanism to prevent attack by pathogenic microorganisms, but that metal tolerant pathogens can overcome this defense.
DOI: 10.1111/j.1469-8137.2005.01504.x
发表时间: 2005-11-01
期刊: NEW PHYTOLOGIST
影响因子: 9.4
作者:
Jhee, EM;Boyd, RS;Eubanks, MD
通讯作者: Eubanks, MD
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期刊: FUNCTIONAL ECOLOGY
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发表时间: 2006-01-01
期刊: NEW PHYTOLOGIST
影响因子: 9.4
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DOI: 10.1105/tpc.104.023036
发表时间: 2004-08-01
期刊: PLANT CELL
影响因子: 11.6
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发表时间: 1979-01-01
影响因子: 11.1
作者:
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通讯作者: HELINSKI, DR