DOES ARBUSCULAR MYCORRHIZA FAVOR INVASION OF SOME ASTERACEAE TRIBES?

Invasive species, including more than three dozen Asteraceae, such as Solidago canadensis, Leucanthemum vulgare, Senecio inaequidens etc, pose serious threat to ecosystem health. Arbuscular mycorrhizal symbiosis is a key factor for distribution of invasive species of some Asteraceae tribes, including Astereae, Anthemideae, Senecioneae, Gnaphalieae, Cardueae, and Cichorieae. The formation of invasion-friendly plant communities has occurred through increasing nutrient and water availability, hormonal regulation, production of bioactive compounds, and mycorrhiza-induced resistance of host plants. Native species are displaced through the influence on soil microbiota, mycorrhizal and nutrient status of neighboring plants, and several other parameters. Allelopathic influences and symbiotic interactions with bacteria and other fungi can inhibit these processes. Understanding the mycorrhizal status of invasive weeds, in our opinion, is a necessary condition for their successful control.

Invasive weeds, including more than three dozen species of Asteraceae, pose serious threat to ecosystem health (Medve, 1984;Mehraj et al., 2021). An important feature of Asteraceae, which often manifests itself alongside allelopathic effects, is the ability to form arbuscular mycorrhiza (AM) and common mycorrhizal networks (CMN) (Bongard et al., 2013;Yuan et al., 2014;Li et al., 2016;Chagnon et al., 2019;Qin, Yu, 2019). For invasive species like Solidago canadensis (Astereae), Helianthus tuberosus (Heliantheae), and Echinops sphaerocephalus (Cardueae), it was shown that AM and CMN contribute to their distribution and introduction successes (Bongard et al., 2013;Dong et al., 2015, Awaydul et al., 2018, Řezáčová et al., 2020, Nacoon et al., 2021. Analysis of scientific literature has established four tribes (Anthemideae, Astereae, Cardueae and Senecioneae) that rely on AM in their distribution (Table 1, Fig. 1). In addition, the analysis of about 40 thousand nucleotide DNA sequences of fungi from 32 genera in Asteraceae family contained in NCBI database and including the most noxious weeds was carried out. The percentage of AMF occurrence among all fungi associated with theseplants was calculated. The soil mycobiota of Senecioneae, Anthemideae, Astereae, Gnaphaliae, Cichorieae, and Cardueae tribes was represented by AMF in more than 50 % of the cases. It was also revealed that the mycobiota of monophyletic Senecioneae, Anthemideae, Astereae, and Gnaphalieae tribes contain AMF species belonging to four orders (Paraglomerales, Archaeosporales, Diversisporales, and Glomerales). In contrast, the Cichorieae and Cardueae tribes are associated mainly with Glomerales (Malygin, Sokornova, 2021). We believe that AM is the key factor for invasion of the species belonging to these tribes.
Senecioneae, Anthemideae, Astereae, and Gnaphalieae tribes originated in South Africa (Mandel et al., 2019). It is possible that mycorrhiza helped them to spread around the world.
AM is the most ancient and frequent type of mycorrhiza. It is suggested that mycorrhiza helped first plants to leave water and adapt to the aridity of land about 450 million years ago (Provorov, Shtark, 2014;Redecker et al., 2000;Rich et al., 2021).
Assessment of host specificity in mycorrhizal communities is difficult due to the large phylogenetic diversity of plants and fungi that can form AM. Earlier, it was believed that AMF are associated with a wide range of plants (Molina et al., 1992). However, more and more data are now emerging that reveal the association of different genotypes of AMF withh geographic regions or/and host-plant species (Alguacil et al., 2019). Changes in AMF composition of the soil biome occur simultaneously with the development of plant communities (Öpik et al., 2013;Mony et al., 2021).
AM can significantly improve plant nutrition, water availability, soil structure and fertility, as well as stress resistance and tolerance (Augé, 2001). For example, AM reduces stress consequences caused by pathogens, heavy metals, and soil salinization (Jentschke, Godbold, 2000;Harrier, Watson, 2004;Whipps, 2004;Smith, Read, 2008). Plants do not receive large benefits from AM when there is high availability of nutrients, but AM enhances plant development under conditions of nutrient deficiency (Höpfner et al., 2015). Depending on the timing of S. canadensis invasion in arid habitats, the relative abundance of the two dominant AMF species significantly varied. For example, on the Chongming island, China, in dry habitats AMF colonization rate increased with distribution of S. canadensis but in lowland habitats there was no such effect (Jin et al., 2004). AMF can stimulate seed germination, enhance growth, and improve the synthesis of biologically active compounds of plants. For example,  Bennett, Bever, 2007;Smith, Read, 2008). Сuccess of mycorrhizal colonization of plants may also depend on the soil state. In the case of invasive Ambrosia artemisiifolia, for example, the most intensive mycorrhizal colonization was observed in disturbed areas such as roadsides and wastelands while the minimal percentage of mycorrhizal colonization occurred in cultivated areas. This may be due to the differences in physicochemical properties of soils (soil texture, moisture, pH, nutrients) or to the cessation of agricultural methods such as application of fungicides or soil tillage (Fumanal et al., 2006). Moreover, the unfavorable ecological factors (acid precipitation, soil contamination by heavy metal ions, herbicides, etc.) can promote an invasion enhanced by AM (Richardson, Pyšek, 2012).
AM can inhibit soil pathogens such as Aphanomyces, Cylindrocladium spathiphylli, Fusarium, Macrophomina phaseolina, Phytophthora, Pythium, Rhizoctonia, Sclerotinium, Verticillium, and Thielaviopsis basicol, as well as nematodes such as Heterodera, Meloidogyne, Pratylenchus and Radopholus (Harrier, Watson, 2004;Zhang et al., 2009;2011). The soil microbiota in this case depends on the plant species and AM genotype. AMF are also able to induce nonspecific immune responses in their host plants (Qu et al., 2021). In turn, bacterial soil community can inhibit the development of AMF. For example, analysis of microbial community of Arctium lappa (Asteraceae) rhizosphere showed exceptionally low level (0.05 %) of AMF in presence of a diverse bacterial community (Xing et al., 2020).
There is a relationship between AM and the synthesis of plant phytohormones (Hanlon, Coenen, 2011). Sometimes, allelopathic effects on native flora were observed along with AM. Classic examples of such Asteraceae plant invasions are those of Solidago canadensis (Astereae) and Centaurea maculosa (Cardueae) (Yang et al., 2007;Abhilasha et al., 2008;Zhang et al., 2009;Yuan et al., 2013 (Selosse et al., 2006;Horton, van der Heijden, 2008;van der Heijden, Horton, 2009;Horton, 2015). A necessary condition for the formation and functioning of a mycorrhizal network is the ability of neighboring plants to be colonized by CMN (Lucero et al., 2020). . They also participate in the distribution of mineral nutrients between the plants (Walder et al., 2012;Merrild et al., 2013;Weremijewicz, Janos, 2013;Fellbaum et al., 2014;Jakobsen, Hammer, 2015;Walder, van der Heijden, 2015;Weremijewicz et al., 2016Weremijewicz et al., , 2017. For example, CMN promotes the growth of Linum usitatissimum (Linaceae) by transferring nitrogen, phosphorus, and carbon from Sorghum bicolor (Poaceae) (Walder et al., 2012). It is interesting to note that the functioning of the CMN depends on physiological characteristics of participating plants as well. For example, some AM fungi supply nitrogen preferentially to large light-loving plants (Weremijewicz et al., 2016). CMN of the invasive S. canadensis enhances the uptake of nitrogen and phosphorus and, consequently, enhances the growth of this plant by decreasing the uptake of these elements by Kummerowia striata (Fabaceae). Thus, CMN influence on intraspecific and interspecific competition via unequal distribution of mineral nutrients between plants.
Plants connected through CMN can quickly change their behavior in response to external factors. This is manifested Figure 1. The occurrence of AMF among Asteraceae tribes. Phylogenetic relations of weed species representing the respective tribes are inferred from a 342 bp long rDNA sequence dataset (18S ribosomal RNA gene, partial sequence; internal transcribed spacer 1, 5.8S ribosomal RNA gene, and internal transcribed spacer 2, complete sequence) using the Maximum Likelihood method based on the Tamura-Nei model. The bootstrap consensus tree is obtained using 400 replicates in MEGA7 (Kumar et al., 1993). Branches corresponding to partitions reproduced in less than 40 % bootstrap replicates are collapsed by a change in the growth rate of roots and shoots, in the processes of photosynthesis and nutrition, and in the plant defense reactions. It was shown that Tanacetum vulgare in association with Solidago canadensis was less attacked by insects and tolerated losses of biomass to a greater extent than the association-free plants (Lucero et al., 2020). The process of CMN development by an invasive plant can affect plant communities, including intra-and interspecific interactions, species coexistence, and biodiversity. These changes are wave-like (Gorzelak et al., 2015). AM is formed by fungi of the subphylum Glomeromycotina (phylum Mucoromycota) (Spatafora et al. 2016). Currently, species of Glomeromycotina are arranged in three classes, five orders, 16 families, and 41 genera (Goto, Jobim, 2018). The largest order is Glomerales, comprised by about 230 species (Bagyaraj, 2014;Spatafora et al., 2016). According to NCBI, plants in the subfamily Asteroideae are frequently associated with Glomus, Claroideoglomus, Rhizophagus, Septoglomus, Funneliformis, Paraglomus, Diversispora, Acaulospora, Achaeospora, Scutellospora, and Pacispora. There are certain difficulties associated with the identification of these fungi. AMF do not grow on artificial media. Therefore, traditional method for detecting AM is microscopic identification. There are many morphological types of mycorrhizas (Beck et al., 2007). Molecular research methods used for detection of AMF include nucleic acid amplification techniques, DNA sequencing, and nextgeneration sequencing (NGS). As many as ten pairs of primers are designed on the base of the LSU-ITS-SSU rDNA to perform phylogenetic analysis with species level resolution (Schwarzott, Schüßler, 2001;Da Silva et al., 2006;Walker et al., 2007;Gamper, Leuchtmann, 2007;Krüger et al., 2009;Kohout et al., 2014;Morgan, Egerton-Warburton, 2017;Higo et al., 2020). By a high coverage reference transcriptome assembly of pea Pisum sativum mycorrhizal roots, gene markers of AM development were discovered (Afonin et al., 2020). The study of homologous genes can be used to develop methods for assessing the development of weed AM.
To explain the relationship between AM and invasive plants, two hypotheses have been proposed: the enhanced mutualism (Reinhart, Callaway, 2006) and the degraded mutualism (Vogelsang, Bever, 2009). The first one suggests that invasive plants enhance their competitiveness in the presence of AM. The second one assumes that invasive plants do not form AM, but disrupt mycorrhizal associations among native plants, thereby weakening them and facilitating the process of invasion. Even though researchers contrast the hypotheses of enhanced and degraded mutualism (Shah et al., 2009;Bunn et al., 2015), in our opinion, these are two sides of the same coin. We assume that both scenarios are realized in nature and the prevalence of one over another is determined by the host-plant species and features of ecosystem. Invasive plants of some Asteraceae tribes implement the enhanced mutualism scenario.
Thus, we suggest that AM and CMN favor invasion of Cardueae, Astereae, Anthemideae, and Senecioneae tribes of Asteraceae family. Benefits provided by AM and CMN allows alien species to successfully invade to new areas. Therefore, it is necessary to take this into account when developing measures to control the invasion of Asteraceae weeds. Suppression of AMF in soil may possibly help to control invasive plants of the Asteraceae family without affecting plants that are independent of AM.