气候变暖和寄生虫对根系特征和根系经济学空间的影响

IF 4.6 1区 环境科学与生态学 Q1 ECOLOGY
Yongge Yuan, Mark van Kleunen, Junmin Li
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Alongside climate-induced abiotic stresses, plants face biotic stresses, such as herbivory, pathogen infection and parasitism by other plants (Albornoz et al., <span>2017</span>; Bardgett et al., <span>2006</span>; Sentis et al., <span>2020</span>). Although the effects of climate change on herbivores and pathogens have been studied (Laughton et al., <span>2017</span>; Lemoine et al., <span>2017</span>), its impact on the interactions between host plants and parasites remains less understood.</p>\n<p>Parasitic plants often cause serious damage to host plants by directly extracting nutrients from the host or indirectly reducing the host's nutrient acquisition capabilities (Yuan et al., <span>2021</span>; Yuan, Gao, et al., <span>2023</span>; Yuan &amp; Li, <span>2022</span>). To enhance nutrient uptake, plants have evolved various strategies involving different root functional traits (Carmona et al., <span>2021</span>; Wang et al., <span>2023</span>). First, to increase nutrient foraging efficiency and uptake, plants can grow longer and thinner roots, resulting in a higher specific root length (SRL) and specific root area (SRA), and a lower root diameter (RD). Symbiotic relationship with arbuscular mycorrhizal fungi (AMF) further enhances nutrient extraction from the soil (Yaffar et al., <span>2022</span>). Second, to increase the nutrient uptake rate, plants can decrease root construction costs by having a lower root tissue density (RTD) and increase the metabolic rate by having a higher root nitrogen content (Bergmann et al., <span>2020</span>; Ding et al., <span>2023</span>; Wang et al., <span>2023</span>). Enzymatic activities, such as acid phosphatase (APase) release, also play a role in nutrient availability by enhancing organic matter mineralization (Bi et al., <span>2023</span>). Measuring the root functional traits of plants under different environmental conditions may help to predict how plant performance will respond to environmental change.</p>\n<p>To better understand the relationships among root functional traits and to predict root responses to environmental changes, ecologists have recently used multiple root traits to define the ‘root economics space’ (Bi et al., <span>2023</span>; Ding et al., <span>2023</span>; Han et al., <span>2022</span>; Kramer-Walter et al., <span>2016</span>; Ren et al., <span>2023</span>). This framework includes two primary dimensions: the collaboration gradient, ranging from a ‘do-it-yourself’ strategy with thin roots to an ‘outsourcing’ strategy with thick roots facilitating AMF symbiosis and the conservation gradient, ranging from a ‘slow’ resource acquisition strategy with high roots tissue density to a ‘fast’ resource acquisition strategy with high root nitrogen content (Figure S1) (Bergmann et al., <span>2020</span>; Ding et al., <span>2020</span>). The root economics space was initially based on RD, SRL, root nitrogen content and RTD (Bergmann et al., <span>2020</span>). Several other root traits have aligned with the two main dimensions. For example, the percentage mycorrhizal colonization was found to be correlate with RD, reflecting the ‘outsourcing’ strategy. Furthermore, root phosphatase activity exhibited a positive relationship with SRL and a negative relationship with AMF colonization, indicating that root phosphatase activity contributes to the ‘do-it-yourself’ strategy along the collaboration gradient (Han et al., <span>2022</span>). Additionally, nitrogen-fixing bacteria, like rhizobia in legumes, represent another form of nutrient acquisition outsourcing (Thilakarathna &amp; Raizada, <span>2017</span>), though their relationship with the root functional traits that define the root economics space remains poorly understood.</p>\n<p>The position of plants in the root economics space has been used to predict their nutrient acquisition strategies (Carmona et al., <span>2021</span>; Ren et al., <span>2023</span>; Sun et al., <span>2021</span>; Sweeney et al., <span>2021</span>). For example, Wang et al. (<span>2023</span>) found that relative to tree species, liana species have higher SRL and nitrogen contents, positioning them on the fast resource acquisition side of the root economics space. It has also been shown that nutrient-rich grasslands are characterized by ‘fast’ plant communities, while moist grasslands are characterized by ‘do-it-yourself’ plant communities (Lachaise et al., <span>2022</span>). Although many studies have assessed the position of different species and plant communities in the root economics space, few have examined how the position of individual species changes with environmental conditions.</p>\n<p>Climate warming has been shown to affect individual root functional traits (Birgander et al., <span>2017</span>; Qiu et al., <span>2021</span>). For example, Qiu et al. (<span>2021</span>) found that warming increased AMF colonization and RTD while decreasing SRL in soybean (<i>Glycine max</i>). These results suggest that, in response to warming, soybean may shift in the root economics space towards the ‘outsourcing’ and ‘slow’ strategies. Recently, species distribution models predicted that climate warming could increase the potential niche overlap between soybean and one of its major pests, parasitic plants in the genus <i>Cuscuta</i>, by up to sixfold by 2070 (Cai et al., <span>2022</span>; Shao, <span>1990</span>). Parasitic plants can strongly suppress the growth of their host plants and decrease carbon allocation of host plants to below-ground structures (Yuan, Gao, et al., <span>2023</span>; Yuan &amp; Li, <span>2022</span>; Yuan, Lin, et al., <span>2023</span>). For example, one of our previous studies showed that <i>Cuscuta</i> parasitism decreased root growth and AMF colonization in <i>Bidens pilosa</i>, while increasing nitrogen and phosphorus concentrations (Yuan, Lin, et al., <span>2023</span>). If this holds true for soybeans as well, parasitism may cause them to shift in the root economics space towards the ‘do-it-yourself’ and ‘fast’ strategies. Thus, the concurrent effects of warming and parasitism on root traits might neutralize each other.</p>\n<p>To test whether the root functional traits of soybean and its position in the root economics space are affected by climate warming and parasitism by <i>Cuscuta gronovii</i>, we conducted a factorial pot experiment outdoors. On the host plants, we measured SRL, SRA, RD, root nitrogen concentration (RN), RTD, AMF colonization (MC), rhizobia nodule biomass (NB) and APase activity in the rhizosheath. We characterized changes in the relationships among these root traits and the positions of soybean plants along the axes of the root economics space in response to warming and parasitism. We hypothesized that (i) AMF and rhizobial colonization are positively correlated and align with the ‘outsourcing’ strategy within the root economics space; (ii) warming will shift soybean plants from a ‘do-it-yourself’ to an ‘outsourcing’ strategy by increasing colonization by both AMF and rhizobia, and from a ‘fast’ to a ‘slow’ nutrient acquisition strategy by producing roots with higher RTD and lower RN; (iii) parasitism will shift soybean plants from an ‘outsourcing’ strategy to a ‘do-it-yourself’ strategy by reducing colonization by both AMF and rhizobia, and from a ‘slow’ to a ‘fast’ nutrient acquisition strategy by producing roots with lower RTD and higher RN; and (iv) when plants are exposed to both warming and parasitism, their individual effects on root traits will neutralize each other.</p>","PeriodicalId":172,"journal":{"name":"Functional Ecology","volume":null,"pages":null},"PeriodicalIF":4.6000,"publicationDate":"2024-09-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Effects of warming and parasitism on root traits and the root economics space\",\"authors\":\"Yongge Yuan, Mark van Kleunen, Junmin Li\",\"doi\":\"10.1111/1365-2435.14658\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<h2>1 INTRODUCTION</h2>\\n<p>Global surface temperatures have risen by approximately 1.2°C since 1850 (NOAA, <span>2020</span>) and are projected to increase by an additional 2.2°C by 2100 (Lyon et al., <span>2022</span>). Climate warming can impact the fitness and distribution of plants by altering root morphology, symbiosis and nutrient acquisition strategies (Arndal et al., <span>2013</span>; Dukes et al., <span>2005</span>; Liu et al., <span>2013</span>; Meza-Lopez &amp; Siemann, <span>2017</span>; Nijs et al., <span>1996</span>; Olsrud et al., <span>2010</span>; Qiu et al., <span>2021</span>; Rillig et al., <span>2002</span>; Wertin et al., <span>2017</span>; Zhou et al., <span>2022</span>). Alongside climate-induced abiotic stresses, plants face biotic stresses, such as herbivory, pathogen infection and parasitism by other plants (Albornoz et al., <span>2017</span>; Bardgett et al., <span>2006</span>; Sentis et al., <span>2020</span>). Although the effects of climate change on herbivores and pathogens have been studied (Laughton et al., <span>2017</span>; Lemoine et al., <span>2017</span>), its impact on the interactions between host plants and parasites remains less understood.</p>\\n<p>Parasitic plants often cause serious damage to host plants by directly extracting nutrients from the host or indirectly reducing the host's nutrient acquisition capabilities (Yuan et al., <span>2021</span>; Yuan, Gao, et al., <span>2023</span>; Yuan &amp; Li, <span>2022</span>). To enhance nutrient uptake, plants have evolved various strategies involving different root functional traits (Carmona et al., <span>2021</span>; Wang et al., <span>2023</span>). First, to increase nutrient foraging efficiency and uptake, plants can grow longer and thinner roots, resulting in a higher specific root length (SRL) and specific root area (SRA), and a lower root diameter (RD). Symbiotic relationship with arbuscular mycorrhizal fungi (AMF) further enhances nutrient extraction from the soil (Yaffar et al., <span>2022</span>). Second, to increase the nutrient uptake rate, plants can decrease root construction costs by having a lower root tissue density (RTD) and increase the metabolic rate by having a higher root nitrogen content (Bergmann et al., <span>2020</span>; Ding et al., <span>2023</span>; Wang et al., <span>2023</span>). Enzymatic activities, such as acid phosphatase (APase) release, also play a role in nutrient availability by enhancing organic matter mineralization (Bi et al., <span>2023</span>). Measuring the root functional traits of plants under different environmental conditions may help to predict how plant performance will respond to environmental change.</p>\\n<p>To better understand the relationships among root functional traits and to predict root responses to environmental changes, ecologists have recently used multiple root traits to define the ‘root economics space’ (Bi et al., <span>2023</span>; Ding et al., <span>2023</span>; Han et al., <span>2022</span>; Kramer-Walter et al., <span>2016</span>; Ren et al., <span>2023</span>). This framework includes two primary dimensions: the collaboration gradient, ranging from a ‘do-it-yourself’ strategy with thin roots to an ‘outsourcing’ strategy with thick roots facilitating AMF symbiosis and the conservation gradient, ranging from a ‘slow’ resource acquisition strategy with high roots tissue density to a ‘fast’ resource acquisition strategy with high root nitrogen content (Figure S1) (Bergmann et al., <span>2020</span>; Ding et al., <span>2020</span>). The root economics space was initially based on RD, SRL, root nitrogen content and RTD (Bergmann et al., <span>2020</span>). Several other root traits have aligned with the two main dimensions. For example, the percentage mycorrhizal colonization was found to be correlate with RD, reflecting the ‘outsourcing’ strategy. Furthermore, root phosphatase activity exhibited a positive relationship with SRL and a negative relationship with AMF colonization, indicating that root phosphatase activity contributes to the ‘do-it-yourself’ strategy along the collaboration gradient (Han et al., <span>2022</span>). Additionally, nitrogen-fixing bacteria, like rhizobia in legumes, represent another form of nutrient acquisition outsourcing (Thilakarathna &amp; Raizada, <span>2017</span>), though their relationship with the root functional traits that define the root economics space remains poorly understood.</p>\\n<p>The position of plants in the root economics space has been used to predict their nutrient acquisition strategies (Carmona et al., <span>2021</span>; Ren et al., <span>2023</span>; Sun et al., <span>2021</span>; Sweeney et al., <span>2021</span>). For example, Wang et al. (<span>2023</span>) found that relative to tree species, liana species have higher SRL and nitrogen contents, positioning them on the fast resource acquisition side of the root economics space. It has also been shown that nutrient-rich grasslands are characterized by ‘fast’ plant communities, while moist grasslands are characterized by ‘do-it-yourself’ plant communities (Lachaise et al., <span>2022</span>). Although many studies have assessed the position of different species and plant communities in the root economics space, few have examined how the position of individual species changes with environmental conditions.</p>\\n<p>Climate warming has been shown to affect individual root functional traits (Birgander et al., <span>2017</span>; Qiu et al., <span>2021</span>). For example, Qiu et al. (<span>2021</span>) found that warming increased AMF colonization and RTD while decreasing SRL in soybean (<i>Glycine max</i>). 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引用次数: 0

摘要

(2021 年)发现,气候变暖增加了大豆(Glycine max)的 AMF 定殖和 RTD,同时降低了 SRL。这些结果表明,为了应对气候变暖,大豆可能会在根系经济学空间中转向 "外包 "和 "缓慢 "策略。最近,物种分布模型预测,到 2070 年,气候变暖可能会使大豆与其主要害虫之一--菟丝子属寄生植物--之间的潜在生态位重叠增加多达六倍(Cai 等人,2022 年;Shao,1990 年)。寄生植物会强烈抑制寄主植物的生长,并减少寄主植物对地下结构的碳分配(Yuan,Gao,et al.,2023;Yuan &amp; Li,2022;Yuan,Lin,et al.,2023)。例如,我们之前的一项研究表明,菟丝子寄生会减少根系生长和 AMF 在 Bidens pilosa 中的定殖,同时增加氮和磷的浓度(Yuan, Lin, et al.)如果大豆的情况也是如此,寄生虫可能会导致大豆在根系经济学空间中转向 "自己动手 "和 "快速 "策略。为了检验大豆的根系功能特性及其在根系经济空间中的位置是否受到气候变暖和菟丝子寄生的影响,我们在室外进行了一个因子盆栽实验。在寄主植物上,我们测量了根鞘中的SRL、SRA、RD、根氮浓度(RN)、RTD、AMF定殖率(MC)、根瘤生物量(NB)和AP酶活性。我们描述了这些根系性状之间的关系以及大豆植株沿根系经济学空间轴线的位置随气候变暖和寄生现象而发生的变化。我们的假设是:(i) AMF 和根瘤菌的定殖与根系经济学空间中的 "外包 "策略呈正相关;(ii) 气候变暖将通过增加 AMF 和根瘤菌的定殖使大豆植株从 "自己动手 "策略转变为 "外包 "策略,并通过产生具有较高 RTD 和较低 RN 的根系使养分获取策略从 "快 "转变为 "慢";(iii) 寄生虫会减少 AMF 和根瘤菌的定殖,从而使大豆植物从 "外包 "战略转向 "自己动手 "战略,并通过产生较低 RTD 和较高 RN 的根系,使大豆植物从 "慢 "战略转向 "快 "战略;以及 (iv) 当植物同时受到变暖和寄生虫的影响时,它们各自对根系特征的影响将相互中和。
本文章由计算机程序翻译,如有差异,请以英文原文为准。

Effects of warming and parasitism on root traits and the root economics space

Effects of warming and parasitism on root traits and the root economics space

1 INTRODUCTION

Global surface temperatures have risen by approximately 1.2°C since 1850 (NOAA, 2020) and are projected to increase by an additional 2.2°C by 2100 (Lyon et al., 2022). Climate warming can impact the fitness and distribution of plants by altering root morphology, symbiosis and nutrient acquisition strategies (Arndal et al., 2013; Dukes et al., 2005; Liu et al., 2013; Meza-Lopez & Siemann, 2017; Nijs et al., 1996; Olsrud et al., 2010; Qiu et al., 2021; Rillig et al., 2002; Wertin et al., 2017; Zhou et al., 2022). Alongside climate-induced abiotic stresses, plants face biotic stresses, such as herbivory, pathogen infection and parasitism by other plants (Albornoz et al., 2017; Bardgett et al., 2006; Sentis et al., 2020). Although the effects of climate change on herbivores and pathogens have been studied (Laughton et al., 2017; Lemoine et al., 2017), its impact on the interactions between host plants and parasites remains less understood.

Parasitic plants often cause serious damage to host plants by directly extracting nutrients from the host or indirectly reducing the host's nutrient acquisition capabilities (Yuan et al., 2021; Yuan, Gao, et al., 2023; Yuan & Li, 2022). To enhance nutrient uptake, plants have evolved various strategies involving different root functional traits (Carmona et al., 2021; Wang et al., 2023). First, to increase nutrient foraging efficiency and uptake, plants can grow longer and thinner roots, resulting in a higher specific root length (SRL) and specific root area (SRA), and a lower root diameter (RD). Symbiotic relationship with arbuscular mycorrhizal fungi (AMF) further enhances nutrient extraction from the soil (Yaffar et al., 2022). Second, to increase the nutrient uptake rate, plants can decrease root construction costs by having a lower root tissue density (RTD) and increase the metabolic rate by having a higher root nitrogen content (Bergmann et al., 2020; Ding et al., 2023; Wang et al., 2023). Enzymatic activities, such as acid phosphatase (APase) release, also play a role in nutrient availability by enhancing organic matter mineralization (Bi et al., 2023). Measuring the root functional traits of plants under different environmental conditions may help to predict how plant performance will respond to environmental change.

To better understand the relationships among root functional traits and to predict root responses to environmental changes, ecologists have recently used multiple root traits to define the ‘root economics space’ (Bi et al., 2023; Ding et al., 2023; Han et al., 2022; Kramer-Walter et al., 2016; Ren et al., 2023). This framework includes two primary dimensions: the collaboration gradient, ranging from a ‘do-it-yourself’ strategy with thin roots to an ‘outsourcing’ strategy with thick roots facilitating AMF symbiosis and the conservation gradient, ranging from a ‘slow’ resource acquisition strategy with high roots tissue density to a ‘fast’ resource acquisition strategy with high root nitrogen content (Figure S1) (Bergmann et al., 2020; Ding et al., 2020). The root economics space was initially based on RD, SRL, root nitrogen content and RTD (Bergmann et al., 2020). Several other root traits have aligned with the two main dimensions. For example, the percentage mycorrhizal colonization was found to be correlate with RD, reflecting the ‘outsourcing’ strategy. Furthermore, root phosphatase activity exhibited a positive relationship with SRL and a negative relationship with AMF colonization, indicating that root phosphatase activity contributes to the ‘do-it-yourself’ strategy along the collaboration gradient (Han et al., 2022). Additionally, nitrogen-fixing bacteria, like rhizobia in legumes, represent another form of nutrient acquisition outsourcing (Thilakarathna & Raizada, 2017), though their relationship with the root functional traits that define the root economics space remains poorly understood.

The position of plants in the root economics space has been used to predict their nutrient acquisition strategies (Carmona et al., 2021; Ren et al., 2023; Sun et al., 2021; Sweeney et al., 2021). For example, Wang et al. (2023) found that relative to tree species, liana species have higher SRL and nitrogen contents, positioning them on the fast resource acquisition side of the root economics space. It has also been shown that nutrient-rich grasslands are characterized by ‘fast’ plant communities, while moist grasslands are characterized by ‘do-it-yourself’ plant communities (Lachaise et al., 2022). Although many studies have assessed the position of different species and plant communities in the root economics space, few have examined how the position of individual species changes with environmental conditions.

Climate warming has been shown to affect individual root functional traits (Birgander et al., 2017; Qiu et al., 2021). For example, Qiu et al. (2021) found that warming increased AMF colonization and RTD while decreasing SRL in soybean (Glycine max). These results suggest that, in response to warming, soybean may shift in the root economics space towards the ‘outsourcing’ and ‘slow’ strategies. Recently, species distribution models predicted that climate warming could increase the potential niche overlap between soybean and one of its major pests, parasitic plants in the genus Cuscuta, by up to sixfold by 2070 (Cai et al., 2022; Shao, 1990). Parasitic plants can strongly suppress the growth of their host plants and decrease carbon allocation of host plants to below-ground structures (Yuan, Gao, et al., 2023; Yuan & Li, 2022; Yuan, Lin, et al., 2023). For example, one of our previous studies showed that Cuscuta parasitism decreased root growth and AMF colonization in Bidens pilosa, while increasing nitrogen and phosphorus concentrations (Yuan, Lin, et al., 2023). If this holds true for soybeans as well, parasitism may cause them to shift in the root economics space towards the ‘do-it-yourself’ and ‘fast’ strategies. Thus, the concurrent effects of warming and parasitism on root traits might neutralize each other.

To test whether the root functional traits of soybean and its position in the root economics space are affected by climate warming and parasitism by Cuscuta gronovii, we conducted a factorial pot experiment outdoors. On the host plants, we measured SRL, SRA, RD, root nitrogen concentration (RN), RTD, AMF colonization (MC), rhizobia nodule biomass (NB) and APase activity in the rhizosheath. We characterized changes in the relationships among these root traits and the positions of soybean plants along the axes of the root economics space in response to warming and parasitism. We hypothesized that (i) AMF and rhizobial colonization are positively correlated and align with the ‘outsourcing’ strategy within the root economics space; (ii) warming will shift soybean plants from a ‘do-it-yourself’ to an ‘outsourcing’ strategy by increasing colonization by both AMF and rhizobia, and from a ‘fast’ to a ‘slow’ nutrient acquisition strategy by producing roots with higher RTD and lower RN; (iii) parasitism will shift soybean plants from an ‘outsourcing’ strategy to a ‘do-it-yourself’ strategy by reducing colonization by both AMF and rhizobia, and from a ‘slow’ to a ‘fast’ nutrient acquisition strategy by producing roots with lower RTD and higher RN; and (iv) when plants are exposed to both warming and parasitism, their individual effects on root traits will neutralize each other.

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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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