Common Mycorrhizal Network Induced JA/ET Genes Expression in Healthy Potato Plants Connected to Potato Plants Infected by Phytophthora infestans

Abstract

Most plants are connected belowground via common mycorrhizal networks (CMNs). In their presence, the transmission of warning signals from diseased to uninfected plants has been reported. However, current studies have all been conducted in pots making it difficult to discriminate direct from indirect contribution of hyphae to the transmission of the signals. Here, we conducted an in vitro study with potato plantlets connected by a CMN of the arbuscular mycorrhizal fungus Rhizophagus irregularis. The plantlets were grown in physically separated compartments and their connection ensured only by the CMN. The donor potato plantlets were infected by Phytophthora infestans and defense genes analyzed 24, 48 and 120 h post-infection (hpi) in the uninfected receiver potato plantlets. Twenty-four hpi by the pathogen, PAL, PR-1b, ERF3, and LOX genes were significantly upregulated, whereas no significant transcript variation was noticed 48 and 120 hpi. The exact nature of the warning signals remains unknown but was not associated to microorganisms other than the AMF or to diffusion mechanisms through the growth medium or induced by volatile compounds. The defense response appeared to be transitory and associated with the jasmonic acid or ethylene pathway. These findings demonstrate the direct involvement of hyphae in the transmission of warning signals from diseased to uninfected potato plantlets and their indubitable role in providing a route for activating defense responses in uninfected plants.

Can common mycorrhizal fungal networks be managed to enhance ecosystem functionality?

“…Indeed, the absence of differences in e.g. P content or fresh weight between the leaves of potato plantlets newly incorporated in a CMN versus non‐mycorrhizal plantlets have been measured, suggesting that the cost of establishment of AM fungi was probably smaller for the incorporated plantlets and mostly taken by the donor plant (Alaux et al., 2020; Gallou et al., 2012). Seedlings may establish more easily within an existing mycorrhizal network because they have a direct access to a large pool of soil nutrients and water through the CMN, or in some situations even directly from other plants (Van der Heijden, 2004; Voets et al., 2008).…”

“…Below‐ground signaling can occur between plants infected with pests to non‐infested neighbors via CMNs formed by AM fungi (Babikova, Gilbert, et al., 2013; Song et al., 2010, 2014), endophyte fungi (Vahabi et al., 2018), and ECM fungi (Song et al., 2015). CMNs formed by AM fungi can elicit defence against various biological stressors such as insect herbivores (Babikova, Gilbert, et al., 2013), herbivory‐elicitors (Song et al., 2019), foliar necrotrophic fungi (Song et al., 2010), and hemibiotrophs, such as Oomycota (Alaux et al., 2020), by acting as a conduit for interplant signaling (Johnson & Gilbert, 2015). Many of these studies were undertaken on plants relevant to horticulture and agriculture such as broad bean, tomato, tobacco, and potato, reflecting the potential application of CMNs to agroecosystems.…”

“…The concept of a sentinel plant, whereby susceptible plants are inspected at regular intervals for signs and symptoms of pest attack, could be developed further to consider the capacity of those plants to warn neighbors (Figure 1). However, the importance of signaling in nature remains largely unclear, especially regarding the mechanism of signal transfer (Alaux et al., 2020) and the overall fitness benefits to fungi (Babikova, Gilbert, et al., 2013). Signals have been shown to travel through CMNs of at least 20 cm in length (Babikova, Johnson, et al., 2013).…”

“…The signal has been indirectly detected in terms of measurable response by the receiver plant (i.e. plant defence: genes or compounds) within 24 hr or even 6 hr after donor plant being exposed to the stressor (Alaux et al., 2020; Song et al., 2019), with peak response on the receiver plant between 48 hr and 100 hr (Gilbert & Johnson, 2015). The duration over which signals are effective remains unknown (Gilbert & Johnson, 2017) but in recent studies appeared transitory, suggesting a priming phase (Alaux et al., 2020).…”

Social networking in crop plants: Wired and wireless cross‐plant communications

“…In the receiver plants, the relative expression levels of defence‐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 et al, 2010). Alaux, Naveau, Declerck, and Cranenbrouck (2020) also set up a sophisticated in vitro experiment to confirm the role of mycorrhizae in plant–plant signal transduction. The results showed that a Phytophthora infestans infected tomato plant could transfer a signal to healthy neighbours via mycorrhizae hypha to activate the transient expression of JA related genes.…”