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18OECD+WoS: 1.06+RQ (Mycology) https://doi.org/10.31993/2308-6459-2021-104-3-14993
Mini-review
DOES ARBUSCULAR MYCORRHIZA FAVOR INVASION OF SOME ASTERACEAE TRIBES? D.M. Malygin1, M.N. Mandryk-Litvinkovich2, S.V. Sokornova1*
1Russian Institute of Plant Protection, St. Petersburg, Russia 2Institute of Microbiology, National Academy of Science, Minsk, Belarus
*corresponding author, e-mail: svsokornova@vizr.spb.ru
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.
Keywords: common mycorrhizal networks, invasive weeds, Cardueae, Astereae, Anthemideae, Senecioneae, Cichorieae
Submitted: 17.04.2021 Accepted: 05.09.2021
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, 2021, Awaydul et al., 2018, Rezácová 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 (Opik 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 (Auge, 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 (Hopfner 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,
© Malygin D.M., Mandryk-Litvinkovich M.N., Sokornova S.V., published by All-Russian Institute of Plant Protection (St. Petersburg). This is an open access article distributed under the terms of the Creative Commons Attribution License 4.0 (http://creativecommons.org/licenses/by/4.0/).
Table 1. Distribution and proven ability to form AM of some species of Asteraceae family
Species Tribe Geographic origin Establishment and spread of invasive species AM Reference
Anthemis arvensis Anthemideae Europe, Northern Africa North and South Americas, Australia, New Zealand, Africa + Symbio data
Anthemis cotula Anthemideae Mediterranean Europe, Northern Africa North and South Americas, Australia, North-East Asia, Europe, Siberia + Shah et al., 2008
Anthemis tinctoria Anthemideae Northern part of Eurasia Southern Europe, Eastern Asia, North America + Symbio data
Artemisia campestris Anthemideae Eurasia, North America — + Symbio data
Artemisia maritima Anthemideae Europe, Siberia — + Symbio data
Artemisia verlotiorum Anthemideae China Eurasia, Africa, Australia, New Zealand, North America + Kempel et al., 2013
Artemisia vulgaris Anthemideae Eurasia, Northern Africa North America China, India, North America, southern + Symbio data
Leucanthemum vulgare Anthemideae Europe, Central Asia part of South America, South Africa, Australia, New Zealand + Noori et al., 2014
Eastern and Central Europe Western Europe, Eastern Asia, Australia,
Tanacetum vulgare Anthemideae New Zealand, North America, + Lucero et al., 2020
Tanacetum cinerariifolium southern part of South America
Anthemideae Balkan Peninsula — + Waceke et al., 2002
Tanacetum parthenium Anthemideae South-West Europe Europe, North America, Chile - Symbio data
Tripleurospermum inodorum Anthemideae Eurasia North America + Symbio data
Tripleurospermum maritimum Anthemideae Northern Europe — + Symbio data
Erigeron annuus Astereae North America Western Europe, China + Gucwa-Przepiôra et al., 2016
Erigeron canadensis Astereae North America Eurasia, Australia, New Zealand, North Africa North America, northern and eastern parts + Rezacova, 2020
Erigeron karvinskianus Astereae Central America of South America, Africa, South-West Asia, Australia, New Zealand + Oliveira et al., 2005
Solidago canadensis Astereae North America Europe, Russia, China, India, Australia, New Zealand, Brazil + Awaydul et al., 2018
Solidago gigantea Astereae North America Europe, Asia + Harkes et al., 2021
Solidago nemoralis Astereae North America — + Cumming, Kelly, 2009
Solidago virgaurea Astereae Europe — + Betekhtina et al., 2016
Symphyotrichum x salignum Astereae Europe Western Siberia, Far East of Russia, Japan +* Pendergast IV et al., 2013
Symphyotrichum subu-latus Astereae Southern USA, Mexico, South America China, Iran, South Korea + Wang et al., 2021
Arctium lappa Cardueae Eurasia North America, Australia, New Zealand + Symbio data
Carduus nutans Cardueae Eurasia North America, Argentina, Australia, New Zealand - Wardle et al., 1998
Centaurea cyanus Cardueae Central Europe Eurasia, North America, Australia + Symbio data
Centaurea maculosa Cardueae Eastern Europe North America, New Zealand, Western Europe + Mummey et al., 2006
Centaurea melitensis Cardueae Northern Africa, Southern Europe USA, New Zealand, Australia, South America + Callaway et al., 2001
Centaurea solstitialis Cardueae Mediterranean Europe, Northern Africa Eurasia, North America, Southern South America, Australia, New Zealand + Waller et al., 2016
Cirsium arvense Cardueae Southeastern Europe Eurasia, Australia, New Zealand, South Africa, North America + Eschen et al., 2010
Echinops sphaeroceph-alus Cardueae Southeastern Europe Europe, USA + Rezacova et al., 2020
Cichorium intybus Cichorieae Eurasia, North Africa Australia, New Zealand, South Africa, North and South America + Awaydul et al., 2018
Hieracium alpinum Cichorieae Europe — + Symbio data
Hieracium bifidum Cichorieae Europe — + Symbio data
Hieracium lachenalii Cichorieae Europe North America, Australia + Symbio data
Table 1 continued
Species Tribe Geographic origin Establishment and spread of invasive species AM Reference
Hieracium oistophyllum Cichorieae Europe — + Symbio data
Hieracium umbellatum Cichorieae Eurasia, North America — + Symbio data
Pilosella aurantiacum Cichorieae Europe North America, Russia, Mongolia, Japan, Australia, New Zealand + Weed Control..., 2013
Pilosella officinarum Cichorieae Europe, South-West Asia North America, Argentina, New Zealand + Hopfner et al., 2015
Sonchus arvensis Cichorieae Europe Asia, Australia, New Zealand, North America, few regions of Africa + Symbio data
Taraxacum officinale Cichorieae Greece Eurasia, North and South America, South Africa, Australia, New Zealand + Mariotte et al., 2012
Bidens frondosa Coreopsideae North America Eurasia, New Zealand, Marocco North America, Africa, Western Europe, + Stevens et al., 2010
Bidens pilosa Coreopsideae South and Central America South-West Asia, Australia, New Zealand and islands across Indian and Pacific oceans North and South Korea, Japan + Zhang et al., 2018
Coreopsis drummondii Coreopsideae North America + Chen et al., 2007
Coreopsis grandifola Coreopsideae North America Europe South and South-East Asia, Australia, + Yanfang et al., 2012
Ageratina adenophora Eupatorieae Central Mexico New Zealand, Western Europe, few regions of Africa + Li et al., 2016
Praxelis clematidea Eupatorieae South America China, Thailand, Australia - Intanon et al., 2020
Gnaphalium californicum Gnaphalieae USA — + Vogelsang, Bever, 2009
Gnaphalium supinum Gnaphalieae Eurasia, North America — + Symbio data
Gnaphalium sylvaticum Gnaphalieae Europe, North America — + Symbio data
Gnaphalium uliginosum Gnaphalieae Eurasia, North America — + Symbio data
Ambrosia artemisiifolia Heliantheae North and Central America South America, Eurasia, Australia, New Zealand, North and South Africa + Fumanal et al., 2006; Zhang et al., 2018
Ambrosia psilostachya Heliantheae Western North America Europe, India, Japan, Australia, South Africa + Montagnani et al., 2017
Helianthus annuus Heliantheae North America — + Symbio data
Helianthus tuberosus Heliantheae North America Eurasia, southern part of South America, Australia, New Zealand + Nacoon et al., 2021
Senecio jacobaea Senecioneae Eurasia North America, Brazil, Australia, New Zealand + Symbio data
Senecio vulgaris Senecioneae Eurasia, northern Africa North America, southern part of South America, Australia, New Zealand + Symbio data
* AM was detected in the parental form Symphyotrichum novae-angliae.
multifaceted effects on herbivores and growth of host plants were demonstrated (van der Heijden et al., 1998; Bennett, Bever, 2007; Smith, Read, 2008).
Cuccess 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, Pysek, 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). However, there are also examples of invasions that rely on allelopathic effect only, including Carduus nutans (Cardueae), Praxelis clematidea (Eupatorieae), and Mikania micrantha (Eupatorieae) (Wardle
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
et al., 1998; Chen et al., 2017; Intanon et al., 2020). AM can influence foliar fungal endophyte community, as it was shown in vitro for Cirsium arvense (Eschen et al., 2010).
Competitiveness of invasive and native plants can be influenced by CMN, which simultaneously colonize root systems of several plants, affecting ecosystem processes and dynamics of plant communities (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). Structures of mycorrhizal networks depend on the composition of plant species in a given area (Chagnon et al., 2019). The formation of mycorrhizal network was demonstrated for Tanacetum vulgare, S. canadensis, and Cichorium intybus (Awaydul et al., 2018; Lucero et al., 2020).
CMN serve as conductor of various signaling and allelochemical compounds (Barto et al., 2011; Babikova et al., 2013; Johnson and Gilbert, 2015). 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., 2016, 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
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 next-generation 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-Waiburton, 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.
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Вестник защиты растений, 2021, 104(3), с. 144-152
OECD+WoS: 1.06+RQ (Mycology) https://doi.org/10.31993/2308-6459-2021-104-3-14993
Мини-обзор
СПОСОБСТВУЕТ ЛИ АРБУСКУЛЯРНАЯ МИКОРИЗА ИНВАЗИИ ВИДОВ ASTERACEAE?
Д.М. Малыгин1, М.Н. Мандрик-Литвинкович2, С.В. Сокорнова1*
'Всероссийский научно-исследовательский институт защиты растений, Санкт-Петербург, Россия 2Институт микробиологии, Национальная академия наук, Минск, Беларусь
* ответственный за переписку, e-mail: svsokornova@vizr.spb.ru
Более трех десятков видов семейства Asteraceae, таких как Solidago canadensis, Leucanthemum vulgare, Senecio inaequidens etc, являются инвазивными и представляют серьезную опасность для экосистем. Арбускулярная микориза является ключевым фактором распространения инвазивных растений некоторых триб семейства Asteraceae, включая Astereae, Anthemideae, Senecioneae, Gnaphalieae, Cardueae, и Cichorieae. Формирование дружественного для инвазивного растения фитоценоза происходит, в том числе, за счет увеличения доступа питательных веществ и воды, гормональной регуляции и стимулирования неспецифического иммунного ответа растения-хозяина, изменения микоризного статуса окружающих видов, перераспределения между ними питательных веществ, подавления почвенной микробиоты и т.д. Аллелопатические воздействия на АМ со стороны почвенных микроорганизмов и других видов растений могут сдерживать этот процесс. Понимание микоризного статуса нежелательной растительности, на наш взгляд, является необходимым условием для успешного борьбы с ней.
Ключевые слова: арбускулярные микоризные сети, инвазивные сорные растения, Cardueae, Astereae, Anthemideae, Senecioneae, Cichorieae
Поступила в редакцию: 17.04.2021 Принята к печати: 05.09.2021
© Малыгин Д.М., Мандрик-Литвинкович М.Н., Сокорнова С.В. Статья открытого доступа, публикуемая Всероссийским институтом защиты растений (Санкт-Петербург) и распространяемая на условиях Creative Commons Attribution License 4.0 (http://creativecommons.org/licenses/by/4.0/).
