Soil chemistry determines whether defensive plant secondary metabolites promote or suppress herbivore growth.

Soil chemistry determines whether defensive plant secondary metabolites promote or suppress herbivore growth.
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DOI:
10.1073/pnas.2109602118
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发表时间:
2021-10-26
影响因子:
11.1
通讯作者:
Erb M
Erb M
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Hu L;Wu Z;Robert CAM;Ouyang X;Züst T;Mestrot A;Xu J;Erb M

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本研究表明,多功能玉米次生代谢物对主要害虫的保护作用与土壤化学成分有关。通过兼具消化率减少剂和铁载体的作用,苯并恶嗪类化合物将土壤化学与植物-环境相互作用联系起来。鉴于许多植物次生代谢物在根和叶中具有多种功能,这种联系可能是广泛存在的,并可能控制不同(农业)生态系统的群落组成和害虫动态。目前的研究结果还说明了使用多功能植物次生代谢物来对抗主要食草动物害虫的局限性和上下文依赖性。在秋季粘虫对全球玉米生产构成威胁的背景下,后者尤其重要。植物次生(或特殊)代谢产物在根际和叶圈中都起着重要的调节作用。这种划分的功能是否以及如何相互作用来确定植物与环境的相互作用还不是很清楚。在这里,我们研究了玉米苯并恶嗪类化合物作为叶防御和根铁载体的双重作用如何塑造玉米与一种主要的全球害虫秋季粘虫之间的相互作用。我们发现,当植物生长在有效铁含量很低的土壤中时,苯并恶嗪类化合物抑制秋季粘虫的生长,但在有效铁含量较高的土壤中,苯并恶嗪类化合物会促进秋季粘虫的生长。操纵实验证实,苯并恶嗪类化合物在缺铁条件下和存在螯合铁的情况下抑制食草动物的生长,但在生长介质中存在游离铁的情况下促进食草动物的生长。苯并恶嗪类化合物保护作用的这种逆转与植物初级代谢的重大变化无关。植物防御活性受土壤铁和苯并恶嗪类化合物相互作用的调节,但不能解释秋季粘虫的表现。相反,在存在游离铁的情况下,苯并恶嗪类化合物增加了秋季粘虫的铁供应,从而提高了幼虫的性能。这项工作确定土壤化学是影响植物次生代谢物对食草动物生长的决定性因素。它还展示了植物次生代谢物的多功能性如何驱动非生物和生物因素之间的相互作用,从而在可变环境中对植物的抗性产生潜在的影响。
This study demonstrates that the protective effects of multifunctional maize secondary metabolites against a major pest are dependent on soil chemical composition. By functioning as both digestibility reducers and siderophores, benzoxazinoids link soil chemistry to plant–environment interactions. Given that many plant secondary metabolites have multiple functions in roots and leaves, such links are likely widespread and may govern community composition and pest dynamics across different (agro)ecosystems. The presented findings also illustrate the limits and context dependency of using multifunctional plant secondary metabolites to combat major herbivore pests. The latter is particularly important in the context of the threat that the fall armyworm poses for global maize production. Plant secondary (or specialized) metabolites mediate important interactions in both the rhizosphere and the phyllosphere. If and how such compartmentalized functions interact to determine plant–environment interactions is not well understood. Here, we investigated how the dual role of maize benzoxazinoids as leaf defenses and root siderophores shapes the interaction between maize and a major global insect pest, the fall armyworm. We find that benzoxazinoids suppress fall armyworm growth when plants are grown in soils with very low available iron but enhance growth in soils with higher available iron. Manipulation experiments confirm that benzoxazinoids suppress herbivore growth under iron-deficient conditions and in the presence of chelated iron but enhance herbivore growth in the presence of free iron in the growth medium. This reversal of the protective effect of benzoxazinoids is not associated with major changes in plant primary metabolism. Plant defense activation is modulated by the interplay between soil iron and benzoxazinoids but does not explain fall armyworm performance. Instead, increased iron supply to the fall armyworm by benzoxazinoids in the presence of free iron enhances larval performance. This work identifies soil chemistry as a decisive factor for the impact of plant secondary metabolites on herbivore growth. It also demonstrates how the multifunctionality of plant secondary metabolites drives interactions between abiotic and biotic factors, with potential consequences for plant resistance in variable environments.
DOI: 10.1111/j.1461-0248.2006.00925.x
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影响因子: 8.8
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