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).