Institute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, Zhejiang University, Hangzhou 310058, China.
Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland.
Proc Natl Acad Sci U S A. 2021 Oct 26;118(43). doi: 10.1073/pnas.2109602118.
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.
植物次生（或特化）代谢物介导了根际和叶际中重要的相互作用。然而，这些分隔的功能如何相互作用以确定植物与环境的相互作用尚不清楚。在这里，我们研究了玉米苯并恶嗪类化合物作为叶片防御和根系铁载体的双重作用如何塑造玉米与主要全球害虫——秋粘虫之间的相互作用。我们发现，当植物在铁含量非常低的土壤中生长时，苯并恶嗪类化合物会抑制秋粘虫的生长，但在铁含量较高的土壤中会促进其生长。操作实验证实，在缺铁条件下以及螯合铁存在的情况下，苯并恶嗪类化合物会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会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物的重大变化无关。植物防御的激活受到土壤铁和苯并恶嗪类化合物相互作用的调节，但不能解释秋粘虫的表现。相反，苯并恶嗪类化合物在游离铁存在的情况下为秋粘虫提供了更多的铁供应，从而提高了幼虫的表现。这项工作确定了土壤化学是植物次生代谢物对食草动物生长影响的决定性因素。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，这对可变环境中的植物抗性具有潜在影响。
