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Soil microbes alleviate allelopathy of invasive plants

Authors:
  • Xishuangbanna Tropical Botanical Garden Chinese Academy of Sciences

Abstract

Soil microbes are one of the most important determinants of allelopathic effects in the field. However, most studies testing the role of allelopathy in biological invasions did not consider the roles of soil microbes. Here we tested the hypothesis that soil microbes which can degrade allelochemicals may accumulate in soils over time by adaptation and therefore increase the degradation of allelochemicals and alleviate the allelopathic effects in biological invasions. As expected, soil microbes significantly decreased the allelopathic effects of leaf leachates of eight in the nine invasive plant species studied. In addition, Ageratina adenophora showed lower allelopathic effects in soil with long or intermediately invasion history than those in soil with short invasion history. The two main allelochemicals of the invader were degraded more rapidly with increasing invasion history in the soil. Correspondingly, biomass and activity of the soil microbes were higher in the soils with long invasion history than in that with short invasion history. Our results indicate that soil microbes may gradually adapt to the allelochemicals of Ageratina and alleviate its allelopathic effects and thus support the above hypothesis. It is necessary to consider the effects of soil microbes when testing the roles of allelopathy or the novel weapons hypothesis in biological invasions. © 2015, Science China Press and Springer-Verlag Berlin Heidelberg.
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... Different small and capital letters above error bars represent significant (p < 0.05) differences among treatments on test species B. asiatica and R. ellipticus, respectively, according to Tukey's post hoc test. (Inderjit 2005;Zhu et al. 2011;Li et al. 2015). Invasive plant allelopathy are substrates (e.g. ...
... Invasive plant allelopathy are substrates (e.g. natural soil, compost, charcoal and fertilizer) depended on which residue amendment experiment was tested (Inderjit 2005;Qasem 2010;Li et al. 2015). To avoid misleading results for allelopathic impacts of bioassay, experiments need to be conducted with natural soil in laboratory or field conditions (Parepa and Bossdorf 2016). ...
... Most bioassay studies have reported significant allelopathy impacts on test plants, whereas in natural conditions it showed low or no inhibition (Qasem 2010). However, a few studies reported, already invaded soil has low allelopathy impact because there are specific microbes that can degrade the allelochemical secretions of the invasive species in the soil (Li et al. 2015(Li et al. , 2017. Use of such identified allelochemical degrading microbes in already invaded sites may help in the establishment of native plants (Li et al. 2017). ...
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... To this end, we need to first assess the impacts of alien plant invasions on ecosystem functions such as soil microbial communities [13][14][15][16]. Soil microbial communities can alleviate the effects of invasive plants on local plant communities by degrading allelopathic substances [17], promoting further invasion via symbiosis with arbuscular mycorrhizal fungi or inhibiting further invasion via the accumulation of pathogens [18,19]. ...
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... While the potential role of microorganisms in allelopathy remains to be elucidated, microorganisms can modulate the effects of allelopathy on plants in a variety of ways. Furthermore, microorganisms can mitigate allelopathic effects by degrading allelochemicals, thereby increasing the tolerance of target plants to allelopathic effects (Barazani and Friedman, 2001;Foy and Inderjit, 1999;Inderjit et al., 2010;Li et al., 2015;Liu et al., 2018;Giuliano et al., 2021). They can also release insoluble phytotoxins attached to stubborn components and convert harmless compounds into phytotoxins to exacerbate allelopathic effects (Barto et al., 2011;Cipollini et al., 2012). ...
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Productivity decline of Casuarina equisetifolia plantation and difficulty in natural regeneration remains a serious problem because of allelopathy. Previous studies have confirmed that 2,4-di-tert-butylphenol (2,4-DTBP) are the major allelochemicals of the C. equisetifolia litter exudates. The production of these allelochemicals may derive from decomposition of litter or from the litter endophyte and microorganisms adhering to litter surfaces. In the present study, we aimed to evaluate the correlation between allelochemicals in litter and endophytic and epiphytic fungi and bacteria from litter. A total of 100 fungi and 116 bacteria were isolated from the interior and surface of litter of different forest ages (young, half-mature, and mature plantation). Results showed that the fermentation broth of fungal genera Mycosphaerella sp. and Pestalotiopsis sp., and bacterial genera Bacillus amyloliquefaciens, Burkholderia-Paraburkholderia, and Pantoea ananatis had the strongest allelopathic effect on C. equisetifolia seeds. Allelochemicals, such as 2,4-DTBP and its analogs were identified in the fermentation broths of these microorganisms using GC/MS analysis. These results indicate that endophytic and epiphytic fungi and bacteria in litters are involved in the synthesis of allelochemicals of C. equisetifolia. To further determine the abundance of the allelopathic fungi and bacteria, Illumina MiSeq high-throughput sequencing was performed. The results showed that bacterial genera with strong allelopathic potential were mainly distributed in the young and half-mature plantation with low abundance, while the abundance of fungal genera Mycosphaerella sp. and Pestalotiopsis sp. were higher in the young and mature plantations. In particular, the abundance of Mycosphaerella sp. in the young and mature plantations were 501.20% and 192.63% higher than in the half-mature plantation, respectively. Overall, our study demonstrates that the litter fungi with higher abundance in the young and mature plantation were involved in the synthesis of the allelochemical 2,4-DTBP of C. equisetifolia. This finding may be important for understanding the relationship between autotoxicity and microorganism and clarifying the natural regeneration problem of C. equisetifolia.
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... Effect of soil microbes on the community invasion resistance The higher invasion resistance of the more diverse plant communities induced by soil microbes may be attributed to two mechanisms. One mechanism is that a higher level of diversity and/or abundance of microbial species in more diverse communities may lead to the stability of the underground bio-system in response to disturbance (Lankau 2010;Li et al. 2015;Zhu et al. 2011), which can be ascribed to a higher insurance or portfolio effect (Isbell et al. 2009;Wang et al. 2021). The other mechanism is that more diverse communities have a higher probability of including more resistant soil microbial species that in uence exotic plants, i.e., a selection effect (Isbell et Zhang et al. (2020) showed that more speciesrich plant communities contained a greater diversity of plant pathogens and thus had strong negative impacts on invasive species. ...
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Background Soil microbes can affect both the invasiveness of exotic plants and the invasibility of native plant communities, but it still remains unclear whether soil microbes can influence the relationship between native plant diversity and community invasibility. Methods We constructed native plant communities with three levels of species richness (one, three, or six species) in unsterilized or sterilized soil (i.e., with or without soil microbes) and either prevented their invasion by exotic plants or allowed them to be invaded by each of three exotic species (Solidago canadensis, Erigeron canadensis or Symphyotrichum subulatum), which are highly invasive in China. The soils conditioned by the native plant communities that were not invaded by the exotic species were used as soil microbe inocula to test whether species richness-induced differences in soil microbes affected the growth of each of the three invasive species. Results Compared with soils containing microbes, the absence of soil microbes weakened the negative species richness-invasibility relationship, indicating that soil microbes can contribute to higher invasion resistance in more diverse native plant communities. In the presence of soil microbes, the higher invasion resistance of more diverse communities was mainly ascribed to the complementarity effect. However, soil microbes from communities with a higher species richness did not have a stronger negative effect on the growth of any of the three invasive species. Conclusion Soil microbes can alter the diversity-invasibility relationship by promoting the complementarity effect on community invasion resistance. Our results highlight the importance of integrating the role of soil microbes when testing the diversity-invasibility hypothesis.
... Current results imply that allelopathic effects are complex in the field and highly context dependent. Soil characteristics such as soil nutrient status and pH also affect allelopathic effects of plants by influencing allelochemicals, seed germination and growth of target species (Li et al., 2015). Understanding the mechanisms of and the effects that environmental stimuli have on the magnitude and type of root exudation will ultimately improve our knowledge of processes determining soil CO2 emissions, ecosystem functioning, and how to improve the sustainability of agricultural production (Canarini et al., 2019). ...
... The relationship between the donor and the target plant exerts multiple effects on retention, transport and transformation processes of allelochemicals in the soil [4]. In addition, the microbial degradation/transformation of allelochemicals in the soil affects the dose of allelochemicals that can cause plant inhibition [26][27][28]. One well-researched example of this is the bacterial degradation of juglone, an allelochemical produced by black walnut trees [29]. ...
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... These results indicate that relative abundance of the invader in communities may influence abundance of the herbivores, and in turn influence its population expansion. Similarly, allelochemicalsdecomposing microbes accumulate in rizhosphere soil of the invasive plant Ageratina adenophora with increasing abundance and/or the extension of invasion time, decreasing its competition (Li et al., 2015;Li et al., 2017). ...
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Extended leaf phenology (early budbreak and/or delayed leaf drop) and allelopathy are potentially key invasion mechanisms in North American deciduous forests. Because extended phenology confers increased access to light energy and allelochemical production is energetically costly, these traits may interact synergistically to determine invader impact. Garlic mustard (Alliaria petiolata) exhibits both traits, and may also exploit high light in open habitats. We manipulated seasonal light availability to examine effects of light on garlic mustard’s growth, allelochemical production, and impact on native species. Invaded and not-invaded woodland microcosms were exposed to three light treatments: shading year-round (‘extended shade’), shading when the local tree canopy was closed (‘natural shade’), and ambient light year-round (‘no-shade’). Regardless of native presence, garlic mustard biomass was highest under natural shade and, due to apparent irradiation damage, lowest under no-shade. Similarly, growth and fruit production of garlic mustard monocultures were reduced in unshaded conditions. Consistent with these results, garlic mustard reduced the growth of native woodland forbs Blephilia hirsuta and Ageratina altissima most under natural shade, suggesting that extended leaf phenology mediates impact on these herbaceous species. However, garlic mustard growth did not predict reduction of whole-community biomass: invasion reduced native community growth most under no-shade, where invader biomass was lowest but allelochemical production was highest. This result may be driven by a ‘post-mortem’ pulse of allelochemicals from decaying garlic mustard tissue. We conclude that extended leaf phenology may mediate garlic mustard’s impact on some native species, and that light and allelopathy may interact to drive invasion.
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Present address for KLM: The Nature Conservancy, Southwest Oregon Field Office; 33 North Central Ave, Suite 405; Medford, OR 97501-5939, USA. When organisms interact in multi-species groups, the direct effects of facilitation and competition can be modified by indirect interactions. We explored multispecies interactions among the native Pinus ponderosa, the invasive annual grass Bromus tectorum, and the invasive forb Centaurea stoebe in intermountain prairie of the northern Rocky Mountains. Centaurea is much less abundant under Pinus than in surrounding open grassland and Bromus is more abundant under Pinus. We found that the more fertile soil associated with Pinus facilitated both invasive species and did not alter com-petitive outcomes. Pinus litter and litter leachate inhibited both species, but litter also shifted competitive outcomes in favor of Bromus and against Centaurea. The effects of Pinus litter leachate were also strong and leachate eliminated the competitive effect of Centaurea on Bromus while not changing the competitive effect of Bromus on Centaurea. There are many other ways that Pinus may affect understory composition, but by altering the competitive playing field through leaf litter Pinus appears to indirectly facilitate Bromus by more strongly inhibiting Centaurea chemically, an unusual case of a native inhibiting an invader through allelopathy. Our results also provide an unexpected and novel perspective on indirect interactions among competitors, but not through intransitive competitive relationships. Instead, one species (Pinus) strongly 'modified' interactions between two other species in addition to disproportionately affecting one species more than another.
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When introduced to new habitats by humans, some plant species become much more dominant. This is primarily attributed to escape from specialist consumers. Release from these specialist enemies is also thought by some to lead to the evolution of increased competitive ability, driven by a decrease in the plant's resource allocation to consumer defense and an increase in allocation to size or fecundity. Here, we discuss a new theory for invasive success - the "novel weapons hypothesis". We propose that some invaders transform because they possess novel biochemical weapons that function as unusually powerful allelopathic agents, or as mediators of new plant-soil microbial interactions. Root exudates that are relatively ineffective against their natural neighbors because of adaptation, may be highly inhibitory to newly encountered plants in invaded communities. In other words, the novel weapons of some plant invaders provide them with an advantage that may arise from differences in the regional coevolutionary trajectories of plant communities. Furthermore, the selective advantage of possessing a novel weapon may result in rapid evolution of that weapon - for example, the production of greater quantities of allelopathic or antimicrobial root exudates. Direct selection of competitive traits provides an alternative to the "grow versus defend" trade-offs that underpin the theory of the evolution of increased competitive ability.