Invasive plants have caused huge damages in ecosystems. Arbuscular mycorrhizal fungi (AMF) play important roles in plant growth. However, the importance of AMF in pathogenic stress on invasive plants were rarely studied. The effects of AMF (Glomus etunicatum) on the resistance to pathogenic fungus Rhizoctonia solani of an invasive plant Alternanthera philoxeroides were examined in this study. Our results showed that AMF significantly promoted stem length, spacer length, and leaf area of A. philoxeroides. The pathogen R. solani negatively impacted plant growth, including above-ground biomass and root characteristics. However, AMF inoculation mitigated these negative effects. Notably, AMF colonization rates increased significantly in the presence of pathogen. AMF significantly promoted the above-ground growth and decreased the root/shoot ratio to help resist pathogen. These findings indicate that AMF can enhance A. philoxeroides resistance to pathogenic stress, potentially contributing to its invasive success. This study provides insights into the complex interactions between invasive plants, beneficial fungi, and pathogens, which may have implications for understanding and managing plant invasions.
Research Article
Arbuscular mycorrhizal fungi alleviate the pathogenic stress on the invasive weed Alternanthera philoxeroides
https://doi.org/10.21203/rs.3.rs-5272150/v1
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Invasive plant
Alligator weed
arbuscular mycorrhizal fungi
plant-microbe interactions
pathogen resistance
Biological invasions represent one of the most significant threats to global biodiversity and ecosystem function in the 21st century (Pyšek et al., 2020). Invasive plant species, in particular, can dramatically alter native plant communities, disrupt ecosystem processes, and cause substantial economic damage (Vilà et al., 2011). Understanding the mechanisms that contribute to the success of invasive plants is crucial for developing effective management strategies and predicting future invasions (Van Kleunen et al., 2018; Zhang et al., 2020). While numerous factors have been identified as contributing to plant invasiveness, including rapid growth rates, and phenotypic plasticity, increasing attention is being paid to the role of belowground interactions, particularly those involving soil microorganisms (Traveset and Richardson, 2020). Among the myriad of soil microorganisms, arbuscular mycorrhizal fungi (AMF) have emerged as key players in plant invasion ecology (Pringle et al., 2009). These ubiquitous soil fungi form symbiotic associations with the roots of approximately 80% of terrestrial plant species, including many invasive plants (Monaco et al., 2024; Pickett et al., 2018). AMF symbiosis is characterized by the exchange of soil-derived nutrients, particularly phosphorus, for plant-derived carbon compounds (Lanfranco et al., 2016). Beyond nutrient provision, AMF have been shown to confer numerous benefits to their host plants, including enhanced water relations, improved soil structure, and increased resistance to both abiotic and biotic stresses (Cameron et al., 2013a; Kumar et al., 2024).
The potential role of AMF in facilitating plant invasions has been the subject of growing research interest. Several hypotheses have been proposed to explain how invasive plants might leverage AMF associations to their advantage in novel environments (George and Ray, 2023). The "enhanced mutualisms hypothesis" suggests that invasive plants may form more beneficial associations with AMF in their introduced ranges compared to their native ranges, potentially due to encountering more compatible fungal partners or escaping less beneficial associations (Bard et al., 2024; Reinhart and Callaway, 2006). Recent meta-analyses have provided evidence that invasive plants often respond more positively to AMF colonization than native species, particularly in terms of growth and biomass production (Bunn et al., 2015; Cheeke et al., 2019). However, the mechanisms underlying these responses and their ecological consequences remain subjects of ongoing investigation. One particularly intriguing aspect is the potential role of AMF in mediating plant-pathogen interactions in the context of biological invasions (Priyashantha et al., 2023). Plant pathogens, especially soil-borne fungi, can exert strong selective pressures on plant populations and play crucial roles in regulating plant community composition (Bever et al., 2015; García-Garrido and Ocampo, 2002). The "enemy release hypothesis" proposes that invasive plants may benefit from escaping their co-evolved pathogens when introduced to new environments (Gundale et al., 2014; Keane and Crawley, 2002). However, invasive plants are not entirely free from pathogen pressure in their introduced ranges and may encounter novel pathogens to which they lack specific defense mechanisms (Flory and Clay, 2013). AMF have been shown to enhance plant resistance to a wide range of pathogens, including soil-borne fungi, through various mechanisms (Bagyaraj, 2018; Weng et al., 2022). These include improved plant nutrition, competition for infection sites, changes in root system morphology, and the activation of plant defense responses (Cameron et al., 2013b). The ability of invasive plants to form effective AMF associations that confer pathogen resistance could therefore represent a significant advantage in their introduced ranges, potentially contributing to their invasive success (Hilbig and Allen, 2019).
The pathogenic fungus Rhizoctonia solani is a widespread soil-borne fungal pathogen, poses significant threats to many plants, including invasive species (Li et al., 2020; Wu et al., 2023). The interaction between AMF and pathogens is complex and influenced by various factors, including plant host, AMF species, and pathogen identity (Jiang et al., 2024). Some studies suggest that pathogen presence can enhance mycorrhizal colonization, a phenomenon known as "mycorrhizal priming," potentially relevant for invasive plants facing novel pathogens (Qi et al., 2020). Understanding the tripartite interactions between invasive plants, AMF, and pathogens is crucial for effective invasive species management (Schweiger and Müller, 2015). If AMF associations confer pathogen resistance to invasive plants, it could impact the efficacy of biological control strategies using pathogens (Li et al., 2016). Manipulating soil microbial communities, including AMF, could be a potential management tool for controlling invasive plants (Inderjit et al., 2021). Despite the potential importance of AMF-mediated pathogen resistance, few studies have focused on this aspect in invasive plants. Most research has centered on aboveground pathogens or herbivores, leaving a gap in our understanding of belowground pathogen interactions (Jung et al., 2012; Tanner et al., 2013).
Alternanthera philoxeroides (Mart.) Griseb., commonly known as alligator weed, is native to South America. A. philoxeroides has become a problematic invader in many regions worldwide, including parts of North America, Asia, and Australia (Tanveer et al., 2018; Williams et al., 2020). This clonal, amphibious plant is capable of rapid growth and vegetative reproduction, forming dense mats that outcompete native vegetation in both terrestrial and aquatic habitats (Eckert et al., 2016). Previous studies have shown that A. philoxeroides can form associations with AMF, enhancing its growth and stress tolerance, potentially aiding its invasive capabilities (Zhang et al., 2017). However, the role of AMF in interactions between A. philoxeroides and soil-borne pathogens is largely unexplored.
This study investigates the role of AMF in alleviating pathogenic stress on A. philoxeroides by examining the effects of the AMF species Glomus etunicatum and the soil-borne pathogen R. solani, both individually and in combination, on various growth parameters and root colonization patterns of A. philoxeroides (Chen et al., 2021; Dames and Ridsdale, 2012; Ma et al., 2022). This study aims to advance understanding of the mechanisms underlying invasive plant success, particularly their interactions with soil microbes. Findings may have practical implications for managing A. philoxeroides and other invasive plants, potentially informing more effective control strategies involving soil microbial community manipulation or the selection of more virulent pathogens for biological control.
2.1 Experimental materials
A. philoxeroides stems were collected from a greenhouse of Jiangsu University. Healthy stems with similar size and length were surface sterilized in 5% sodium hypochlorite solution for 10 minutes, and then washed three times with sterile water.
The AMF species, Glomus etunicatum (GE), was obtained from the Bank of Glomeromycota at the Institute of Plant Nutrition and Resources, Beijing Academy of Agriculture and Forestry Sciences (Beijing, China). The propagation of GE was according to (David et al., 2017). And the GE used in the experiment was a mixture of culture medium, spores, mycelium and infested root segments, and the AMF inoculum contained about 13 spores per gram.
The pathogenic fungi Rhizoctonia solani (Rs), which is a conserved strain in our laboratory and was re-incubated with potato dextrose solid (PDA) medium at 28°C for 4 days when used for the experiment.
2.2 Experimental design
In order to investigate the effect of AMF on the growth and pathogen resistance of A. philoxeroides, four treatments were set up: Ten grams of viable G. etunicatum containing about 134 spores (treatment: +AMF) or sterile G. etunicatum (treatment: -AMF) was mixed with 240 g sterilized and dried river sand and then added into the flowerpots. Stems of A. philoxeroides was planted into the flower pot. After two weeks of growth, six 5-mm diameter of R. solani mycelial plugs (treatment: +Rs) or six 5-mm diameter of PDA medium plugs (treatment: -Rs) were added to the sand in the pots around the roots of A. philoxeroides. There are five replicates for each treatment. All the plants were randomly arranged in the greenhouse and rotated once per week with a constant temperature of 28 ℃, a relative humidity of 70% and natural light. The plants were added once a week with Hoagland nutrient solution (Hoagland and Arnon, 1950) for plant growth nutrient requirement.
2.3 Mycorrhizal colonization rate
Mycorrhizal colonization rate was assessed following the method described in (Phillips and Hayman, 1970). Root samples are removed from the pot at a depth of 3 cm, washed with distilled water, and cut into small pieces 2 cm long. Then use 10% KOH in digestion for 10 minutes, followed by bleaching in hydrogen peroxide for 5–10 minutes, then acidification with 1% HCL for 1 minute, then staining with 0.05% Taipan Blue in a 75°C water bath for 10 minutes, and finally decolorization with 50% lactic acid and observation under a microscope. The ratio of the number of microscopic perspectives of all mycelia present to the total number of microscopic perspectives is the fungal colonization rate of the roots. Mycorrhizal colonization rate was calculated using the formula:
2.4 Growth trait measurements
After 2 months of growth, all plants were harvested and growth characters were measured, including stem length, stem node number, spacer length, leaf area, above-ground biomass, total root length, root surface area, below-ground biomass, total biomass and root-shoot ratio. The stem length was measured using a straightedge and the spacer length was calculated from the number of stem nodes to the stem length. Leaf area measurement used Image J (Qi et al., 2020). Total root length and root surface area were measured with the Win RHIZO root scanner system (Regent Instrument, Quebec, Canada). Both aboveground and belowground plant materials were dried in an oven to constant mass at 80°C for 72 h and dry mass determined, then calculated the above-ground biomass, below-ground biomass, total biomass and root-shoot ratio (The ratio of below-ground biomass and above-ground biomass).
2.5 Data analysis
Two-way analysis of variance was used to assess the effects of AMF and pathogenic fungi on the growth traits in A. philoxeroides. Duncan's test of significance was performed to investigate differences in all growth traits between AMF and Rs treatments using SPSS 27.0 software.
3.1 Mycorrhizal colonization rate of A. philoxeroides
A large number of vesicles and AMF hyphae were found in the roots of A. philoxeroides with AMF treatments. The mycorrhizal colonization rate was significantly increased in the + Rs treatment compared with -Rs treatment (p < 0.01) (Fig. 1).
3.2 Effects of AMF and pathogen on the above-ground growth of A. philoxeroides
AMF colonization significantly promoted the stem length and the leaf area of A. philoxeroides (Fig. 2a, c, Table 1), while Rs reduced the spacer length and the leaf area of A. philoxeroides to some extent, and significantly reduced the above-ground biomass. However, the colonization of AMF could significantly promote the stem length, spacer length, leaf area and the above-ground biomass under Rs infection (Fig. 2, Table 1).
| Traits | R. solani (Rs) | AMF | Rs×AMF | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| d.f. | F | p | d.f. | F | p | d.f. | F | p | |||
| Stem length | 1 | 2.064 | 0.170 | 1 | 33.766 | <0.001 | 1 | 2.764 | 0.116 | ||
| Spacer length | 1 | 0.328 | 0.575 | 1 | 36.734 | <0.001 | 1 | 6.894 | 0.018 | ||
| Leaf area | 1 | 8.629 | 0.010 | 1 | 43.069 | <0.001 | 1 | 1.027 | 0.326 | ||
| Above-ground biomass | 1 | 15.144 | 0.001 | 1 | 22.154 | <0.001 | 1 | 3.772 | 0.070 | ||
| Total root length | 1 | 47.067 | <0.001 | 1 | 12.783 | 0.003 | 1 | 2.517 | 0.132 | ||
| Root surface area | 1 | 20.289 | <0.001 | 1 | 11.622 | 0.004 | 1 | 1.793 | 0.199 | ||
| Below-ground biomass | 1 | 14.688 | 0.001 | 1 | 0.056 | 0.815 | 1 | 7.320 | 0.016 | ||
| Total biomass | 1 | 21.767 | <0.001 | 1 | 16.634 | <0.001 | 1 | 0.715 | 0.410 | ||
| Root/shoot | 1 | 0.000 | 0.986 | 1 | 12.947 | 0.002 | 1 | 17.435 | < 0.001 | ||
3.3 Effects of AMF and pathogens on the root growth of A. philoxeroides
The inoculation of AMF significantly reduced the total root length and root surface area of A. philoxeroides (Fig. 3a, b, c), but to some extent increased the below-ground biomass (Fig. 3d). The infection with Rs significantly reduced the root length and root surface area (Fig. 3b, c). When inoculated with both AMF and Rs, below-ground biomass of A. philoxeroides was significantly lower compared to no AMF or Rs treatments (Fig. 3d).
3.4 Effects of AMF and pathogens on total biomass and root-shoot ratio of A. philoxeroides
The total biomass of A. philoxeroides was significantly reduced with the infection with Rs (Fig. 4a). However, AMF inoculation also enhanced the total biomass in the Rs treatment (Fig. 4a). The root-shoot ratio of A. philoxeroides was significantly increased after the infection with Rs, and AMF inoculation significantly reduced the root-shoot ratio (Fig. 4b).
Our study showed that AMF significantly increased the above-ground growth but reduce the root morphology of the invasive weed A. philoxeroides. And AMF could also compensate the above-ground growth which was significantly reduced by the pathogenic fungi R. solani.
4.1 Effects of AMF on the growth of A. philoxeroides
Our results revealed that AMF could significantly promote the shoot length of the invasive A. philoxeroides. These results align with the findings of Zhang et al. (2009) who reported similar growth-promoting effects of AMF on the invasive plant Solidago canadensis. The significant increase in spacer length by AMF colonization is particularly noteworthy (Fig. 2b). For a clonal plant like A. philoxeroides, increased spacer length could enhance its ability to explore and exploit patchy resources, potentially conferring a competitive advantage (Keser et al., 2014). This morphological plasticity in response to microbial interactions could be a key factor in the plant's invasive success. The increase in leaf area with AMF inoculation (Fig. 2c), further underscores the protective and growth-promoting effects of the symbiosis. Enhanced leaf area could translate to greater photosynthetic capacity, potentially offsetting the carbon cost of maintaining the mycorrhizal association. The observed promotion of stem length, spacer length, and leaf area by AMF inoculation supports previous findings that AMF enhance invasive plant growth (Basiru and Hijri, 2022; Bunn et al., 2015; Smith et al., 2008; Tian et al., 2013).
The alteration of root morphology by AMF highlights the profound influence of microbial interactions on plant architecture (Fig. 3a). The reduction in total root length and surface area with AMF colonization (Fig. 3b, c) may seem counterintuitive but could represent a more efficient resource acquisition strategy. Similar findings were reported by Zou et al. (2021) in their study on the effects of AMF on root system architecture of rice plants under drought stress. However, the moderation of these effects in the presence of AMF suggests a protective role of the symbiosis, possibly through improved plant nutrition. Mycorrhizal networks increase the area of nutrient absorption (Sharifi and Ryu, 2021). This could represent a trade-off where the plant allocates fewer resources to root growth in favor of supporting the mycorrhizal network for nutrient acquisition (Zou et al., 2021). Investigated the effects of AMF on root system architecture of rice plants under drought stress, showing alterations in root length and surface area, suggesting a more efficient resource acquisition strategy. Thirkell et al. (2021) explored how AMF colonization influences root morphology and biomass allocation in maize, highlighting changes in root length and biomass distribution under different nutrient regimes.
Bunn et al. (2015) found that while native and invasive plants responded similarly to AMF, invasive plants had higher AMF colonization when grown alongside native species. Conversely, Menzel et al. (2017) demonstrated that mycorrhizal mutualism could enhance the invasion success of neophyte plants. de Souza et al. (2018) also linked AMF presence with plant invasions by facilitating nutrient cycling. Consistent with these findings, our previous study showed that AMF support the growth of the invasive plant S. canadensis. In nutrient-poor soils, S. canadensis typically allocates more resources to below-ground growth for nutrient foraging when not colonized by AMF. However, with AMF colonization, S. canadensis shifts its resource allocation to favor above-ground growth and improve phosphorus uptake, reducing investment in below-ground biomass while increasing above-ground biomass efficiency (Qi et al., 2022). Similarly, Shen et al. (2024) observed that AMF increased phosphorus acquisition in the invasive Eupatorium adenophorum, with more phosphorus being allocated to above-ground parts than roots, which supports our results. Our findings provide empirical support for this concept in the context of an invasive species, highlighting a potential mechanism by which invasive plants may gain a competitive advantage in their introduced ranges.
4.2 The role of AMF in pathogen resistance
The increased AMF colonization rate in the presence of pathogen is a particularly intriguing finding (Fig. 1a). This response could be interpreted as a form of induced defense, where the plant promotes greater mycorrhizal association in response to pathogen pressure. Similar phenomena have been observed in other systems. For instance, Gallou et al. (2011) reported enhanced mycorrhizal colonization in potato roots challenged with Phytophthora infestans. The significant increase from 27.5–38.3% colonization represents a substantial shift in the plant's microbial associations. This change could have far-reaching implications for nutrient acquisition, water relations, and overall plant fitness. The ability of A. philoxeroides to rapidly modulate its mycorrhizal associations in response to pathogen presence may contribute to its invasive success by enhancing its adaptive capacity in novel environments. One of the most striking findings of our study is the significant increase in AMF colonization rates in the presence of R. solani. This observation suggests a potential priming effect, where the presence of a pathogen stimulates greater mycorrhizal association. This phenomenon has been observed in other plant-microbe systems and may represent an adaptive response to biotic stress (Martinez-Medina et al., 2016).
Although our results showed a decrease in total root length and surface area with AMF inoculation, the presence of R. solani may have induced changes in root branching patterns or fine root production that are more conducive to AMF colonization (Fusconi, 2014). The increased AMF colonization in the presence of a pathogen aligns with the "mycorrhizal-pathogen interaction" hypothesis proposed by Sikes et al. (2009). This hypothesis suggests that plants may invest more in mycorrhizal associations when under pathogen pressure as a means of enhancing their defense capabilities. There is ongoing debate about whether invasive plants benefit more from mutualism with AMF than native species.
Our results clearly demonstrated that pathogen significantly inhibited the growth of A. philoxeroides, however, AMF inoculation mitigates the negative impacts of pathogen on plant growth. This protective effect of AMF against soil-borne pathogens has been documented in various plant species (Muthukumar, 2021; Pozo and Azcón-Aguilar, 2007). For example, Ji et al. (2022) Investigated the role of AMF in mitigating the negative effects of Fusarium wilt on root development and biomass production in cucumber plants, emphasizing the protective role of AMF against pathogen-induced root damage. However, its implications for invasive plant success are particularly intriguing. There might some mechanisms to explain why AMF could enhance plant resistance to pathogen. First, AMF could improve plant nutrition uptake. Enhanced nutrient uptake, particularly phosphorus, via AMF can improve overall plant health and vigor, increasing resistance to pathogen attack (Diagne et al., 2020). Furthermore, AMF colonization can prime the plant's immune system, leading to faster and stronger defense responses upon pathogen challenge (Jung et al., 2012; Wang et al., 2023). Mycorrhizal plants often exhibit changes in their root exudation profiles, which can influence the rhizosphere microbiome and potentially suppress pathogen growth (Viola et al., 2010).
The enhanced pathogen resistance conferred by AMF could be a key factor in the invasive success of A. philoxeroides. The "enemy release hypothesis" posits that invasive plants benefit from escaping their co-evolved pathogens in their introduced ranges (Keane and Crawley, 2002). Our findings suggest that AMF associations might provide an additional layer of protection against novel pathogens encountered in the invaded ecosystem, further enhancing the plant's competitive advantage. Moreover, the concept of "functional versatility" in mycorrhizal symbioses, as proposed by Friese and Allen (1991) may be particularly relevant to invasive species. This concept suggests that the benefits of AMF associations can shift depending on environmental conditions and stressors. In the case of A. philoxeroides, the AMF symbiosis appears to display functional versatility by promoting growth under normal conditions and enhancing pathogen resistance under biotic stress.
Our findings support this concept, demonstrating that A. philoxeroides not only benefits from AMF association but also uses this symbiosis to better withstand pathogenic stress (Fig. 5). However, the interaction between AMF and pathogens in the context of plant invasions is complex and likely depends on various factors including plant species, fungal partners, and environmental conditions (Thomsen and Hart, 2018). Future research should explore the molecular mechanisms underlying the observed effects and investigate whether similar patterns occur in field conditions (Zhao et al., 2023).
Author Contributions: Conceptualization: SQ, ZD; Methodology: YZ, MY, ZH, Analysis: MN, HX; Writing-original draft preparation: YZ, MN, FKN; Writing-review and editing: SQ, ZD; Funding acquisition: SQ, ZD, DD; Supervision: ZD.
Funding: This research was funded by National Natural Science Foundation of China (32171509, 32271587, 32071521), Carbon peak and carbon neutrality technology innovation foundation of Jiangsu Province (BK20220030), Natural Science Foundation of Jiangsu Province (BK20211321). Part of the funding for this research was supported by Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD) and Priority Academic Program Development of Jiangsu Higher Education Institutions.
Statements and Declarations: The authors declare that there is no conflict of interests regarding the publication of this article.
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