Mycorrhizal arbitrage, a hypothesis: How mycoheterotrophs could profit from inefficiencies in the biological marketplace

IF 4.6 1区 环境科学与生态学 Q1 ECOLOGY Functional Ecology Pub Date : 2024-06-26 DOI:10.1111/1365-2435.14609
Brian S. Steidinger
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Abstract

Mycoheterotrophy, whereby plants acquire both carbon and nutrients from a fungal partner, is an evolutionarily puzzling phenomenon. According to biological market models, mycoheterotrophs have nothing to offer and thus should be shunned as trading partners by discriminating fungi. Nevertheless, mycoheterotrophy is common, particularly among orchids, and an estimated 10% of all plant species are facultatively mycoheterotrophic at early stages in their life cycle. Reconciling mycoheterotrophy with biological market models, I describe how mycoheterotrophs could use arbitrage trading to net a profit of carbon and nutrients, without acquiring either from the abiotic environment. The model requires that mycoheterotrophs simultaneously buy and sell both carbon and nutrients, exploiting variability in the trading ratios offered by mycorrhizal fungi. The model relies on several conditions, including the ability of the mycoheterotroph to form indirect hyphal associations with two or more neighbouring autotrophic mycorrhizal associations, the existence of variable carbon:nutrient exchange ratios among these associations and the ability of mycoheterotrophs to invert the net‐direction of resource trade. Evidence that these conditions occur in a state of nature varies from incontrovertible to plausible given available models. The arbitrage model provides evolutionary rationale for mycoheterotrophy from both the plant and fungal perspective. Accordingly, mycoheterotrophs match trading ratios offered by autotrophic plants and, thus, need not be antagonists. The model makes novel predictions that distinguish it from source‐sink models, most notably in the existence of resource exchange inversions at the plant‐mycorrhizal interface. Finally, the model emphasizes market inefficiencies as the foundation on which mycoheterotrophs construct an arbitrage niche. Read the free Plain Language Summary for this article on the Journal blog.

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菌根套利假说:菌根营养体如何从生物市场的低效率中获利
菌根营养体(mycoheterotrophy)是植物从真菌伙伴那里获得碳和养分的一种进化现象,令人费解。根据生物市场模型,霉菌异养生物没什么可提供的,因此应该被挑剔的真菌拒之门外。然而,霉菌嗜多糖现象很常见,尤其是在兰花中,估计有 10%的植物物种在生命周期的早期阶段是假性霉菌嗜多糖的。通过将蜕膜异养生物与生物市场模型相协调,我描述了蜕膜异养生物如何利用套利交易来获取碳和养分,而无需从非生物环境中获取这两种物质。该模型要求菌根菌同时买卖碳和养分,利用菌根真菌提供的交易比率的可变性。该模型依赖于几个条件,包括菌根真菌能够与两个或多个相邻的自养菌根真菌形成间接的菌丝联系,这些联系之间存在可变的碳-养分交换比,以及菌根真菌能够逆转资源交易的净方向。根据现有模型,这些条件在自然状态下发生的证据从无可争议到似是而非不等。从植物和真菌的角度来看,套利模型为嗜真菌生物的进化提供了理论依据。据此,霉菌营养体与自养植物提供的交易比率相匹配,因此不必成为拮抗剂。该模型做出了有别于源-汇模型的新颖预测,其中最显著的是在植物-菌根界面存在资源交换倒置现象。最后,该模型强调市场低效是菌根菌构建套利利基的基础。在期刊博客上免费阅读本文的通俗摘要。
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来源期刊
Functional Ecology
Functional Ecology 环境科学-生态学
CiteScore
9.00
自引率
1.90%
发文量
243
审稿时长
4 months
期刊介绍: Functional Ecology publishes high-impact papers that enable a mechanistic understanding of ecological pattern and process from the organismic to the ecosystem scale. Because of the multifaceted nature of this challenge, papers can be based on a wide range of approaches. Thus, manuscripts may vary from physiological, genetics, life-history, and behavioural perspectives for organismal studies to community and biogeochemical studies when the goal is to understand ecosystem and larger scale ecological phenomena. We believe that the diverse nature of our journal is a strength, not a weakness, and we are open-minded about the variety of data, research approaches and types of studies that we publish. Certain key areas will continue to be emphasized: studies that integrate genomics with ecology, studies that examine how key aspects of physiology (e.g., stress) impact the ecology of animals and plants, or vice versa, and how evolution shapes interactions among function and ecological traits. Ecology has increasingly moved towards the realization that organismal traits and activities are vital for understanding community dynamics and ecosystem processes, particularly in response to the rapid global changes occurring in earth’s environment, and Functional Ecology aims to publish such integrative papers.
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