2.3  Wired connections between plants via fungal hyphae of the mycorrhizal or endophytic fungal network
Fungi can act as messengers to transfer information between independent plants. Plant-mycorrhiza symbiosis is an ancient system that arose more than 450 million years ago (Waters, Gutjahr, Bennett & Nelson, 2017). This symbiosis had a crucial role in land colonization by plants. Different fungal phyla have evolved different types of plant-mycorrhiza symbiosis (Tedersoo, Bahram & Zobel, 2020). Some Brassicaceaeand Proteaceae plants do not participate in mycorrhizal relationships, and are considered to be non-mycorrhizal symbiotic plants (Tedersoo et al. , 2020). These plants can interfere in the mycorrhizal establishment of other plants (Cipollini, Rigsby & Barto, 2012). For example, Alliaria petiolata produces glucosinolate-derived exudate that suppresses the mycorrhizae of neighboring plants (Cipollini et al. , 2012).
Mycorrhizae have important roles in inter-plant nutrient transfer (especially carbon, phosphorus, and nitrogen), allelochemicals, and signal molecules. Mycorrhizae are common in soil, as 1 g of soil contains 10–100 meters of mycorrhizal fungi (Gilbert & Johnson, 2017). These fungi have broad host ranges and can connect several plants from different taxa. Closely-related mycorrhiza fungi can perform anastomosis to generate a network (Figure 1), which is called a common mycorrhiza network (Deja-Sikora, Mercy, Baum & Hrynkiewicz, 2019). Some plant species exploit the common mycorrhiza network, especially EcM, to transfer nutrients and signals and promote the establishment and survival of conspecific seedlings (Bennett, Cahill & van der Heijden, 2016, Hortal, Lozano, Bastida, Armas, Moreno, Garcia & Pugnaire, 2017).
Plants exploit mycorrhizae fungi for long-distance transfer of plant signals and allelochemicals. Tagetes tenuifolia secretes the lipophilic allelopathic compound thiophene and the hydrophilic allelopathic compound imazamox, which can diffuse more than 12 cm via the common mycorrhiza network (Barto, Hilker, Muller, Mohney, Weidenhamer & Rillig, 2011). Mycorrhizae fungi can translocate defense signals to neighboring unstressed plants, similar to dodder. Tomato plants infected with the nectrotrophic pathogenic fungusAlternaria solani transfer a signal to non-infected neighbors at 18 h post-inoculation via mycorrhizae hypha. In the receiver plants, the relative expression levels of defense-related genes such as phenylalanine ammonia-lyase (PAL), lipoxygenase, polyphenol oxidase, and pathogenesis-related proteins (PR1, PR2, and PR4) were the same as those in the donor plants (Song, Zeng, Xu, Li, Shen & Yihdego, 2010). Alaux, Naveau, Declerck and Cranenbrouck (2020) also set up a sophisticatedin vitro experiment to confirm the role of mycorrhizae in plant-plant signal transduction. The results showed that aPhytophthora infestans infected tomato plant could transfer a signal to healthy neighbors via mycorrhizae hypha to activate the transient expression of JA related genes. Signal transduction via the common mycorrhiza network also has been detected for herbivore-damaged plants (Babikova, Gilbert, Bruce, Birkett, Caulfield, Woodcock, Pickett & Johnson, 2013, Song, Ye, Li, He, Zhu-Salzman, Wang, Su, Luo & Zeng, 2014).
Fungal signal transduction is not exclusive to mycorrhizae. Other mutual and pathogenic fungi with long-term endophytic relationships with plants have the potential to transfer signals between plants. Some soil fungi can serve as a bridge between host plants. For example,Piriformospora indica transfers signals from infectedArabidopsis to neighboring Arabidopsis plants.Alternaria brassicae activates JA pathways in infected focal plants. By contrast, endophytic fungi convert a specific JA signal to generate an ABA signal in neighboring (receiver) plants (Vahabi et al. , 2018).
Fungi serve as vectors for the transfer of plant viruses among plants. Although plants and fungi are not phylogenetically related, they can be infected by phylogenetically-related viruses (Roossinck, 2019). Some plant viruses propagate in the fungal cytosol and transfer between host plants based on the host range of both fungi and viruses. A virus from the saprophytic endophyte Penicillium aurantiogriseum replicates in the host plant (Nerva, Varese, Falk & Turina, 2017). Cucumber mosaic virus is a broad-range virus that can survive in the pathogenic fungus Rhizoctonia solani , which has a broad host range. R. solani transfers this virus to a neighboring host (Andika, Wei, Cao, Salaipeth, Kondo & Sun, 2017). There is evidence that plant virus enters fungal spores and achieves long-distance dissemination via wind dispersal of the fungal spores. Cryphonectria transferCryphonectria hypovirus 1 to tobacco, which subsequently propagates and spreads systemically throughout the plant with the help of Tobacco mosaic virus (TMV) movement protein. TMV also enters fungi and propagates with the help of Cryphonectria hypovirus 1 , which can spread to other hosts via fungal spores (Bian, Andika, Pang, Lian, Wei, Niu, Wu, Kondo, Liu & Sun, 2020).