The Rise of Evolutionary Molecular Plant–Microbe Interactions (EvoMPMI)

With the elucidation of the Marchantia polymorpha genome sequence, this liverwort established a strong position as the latest novel model system in plants (Bowman et al. 2017). In addition to its unique phylogenetic placement, its relatively low genetic redundancy in many regulatory processes has attracted the attention of plant biologists interested in using Marchantia as a promising model system for various evolutionary studies of land plants. In particular, the phytohormone signaling pathways involving auxins, jasmonates, abscisic acid and cytokinins, which regulate various developmental processes in Marchantia, have been intensively studied and compared with knowledge obtained from other model plant systems such as Arabidopsis thaliana (Flores-Sandoval et al. 2015, Kato et al. 2015, Eklund et al. 2018, Monte et al. 2018, Aki et al. 2019). These evolutionary developmental biology studies have contributed considerably to understanding the origin and evolution of phytohormone signaling pathways in land plants. Moreover, comparative studies using Marchantia are not only limited to investigating plant developmental biology but also being expanded to understand evolutionary molecular plant–microbe interactions (EvoMPMI) (Upson et al. 2018). However, the establishment of novel Marchantia pathosystems for use in such EvoMPMI studies is a highly laborious process.

In this issue, Matsui et al. (2020) report on the isolation and characterization of novel pathogens that naturally infect Marchantia. They ‘hunted’ natural pathogens of Marchantia by exposing lab-grown thalli to the open air and harvested those exhibiting disease-like symptoms. In the end, four fungal isolates belonging to the Polyporales order were obtained and, of these, three isolates were found to cause disease symptoms in Marchantia thalli using their in vitro infection system. The authors further focused on one of these isolates designated Marchantia infectious 1 (MI1), derived from the well-known necrotrophic white rot fungus Irpex lacteus (Fig. 1).

Fig. 1.

The dn-OPDA (JA)/SA cross talk found in the M. polymorpha–I. lacteus M1 pathosystem. In Marchantia, the COI1 ortholog MpCOI1 recognizes dn-OPDA isomers other than JA. The dn-OPDA pathway that is regulated by MpCOI1 is required for resistance to I. lacteus M1, a newly isolated potential necrotrophic pathogen of Marchantia. While exogenous application of SA promotes Marchantia disease development caused by I. lacteus M1, addition of dn-OPDA suppresses SA-mediated disease promotion in the Marchantia–I. lacteus M1 pathosystem, suggesting that the SA–JA cross talk that is widely observed in seed plants is also conserved albeit in a slightly different form in Marchantia, which utilizes dn-OPDA as the bioactive jasmonate.

In various seed plants, the jasmonic acid (JA) signaling pathway mediated by the JA receptor COI1 is known to function in defense responses against necrotrophic pathogens, herbivores and physical wounding, while the salicylic acid (SA) pathway is responsible for immunity against biotrophic pathogens (Thaler et al. 2012). Generally, these two phytohormone pathways act antagonistically to each other, with SA–JA antagonism being observed widely among seed plants (Thaler et al. 2012). A comparative and evolutionary study using Marchantia has recently revealed that the Marchantia COI1 ortholog, MpCOI1, recognizes dinor-12-oxo-phytodienoic acid (dn-OPDA) isomers other than JA, highlighting the co-evolution of phytohormone synthesis and receptor specificity in land plants (Monte et al. 2018). However, whether the dn-OPDA signaling pathway mediated by MpCOI1 functions in immunity against necrotrophic pathogens, by analogy to JA in seed plants, remained to be resolved.

Matsui et al. (2020) examined the roles of the JA (dn-OPDA) and SA pathways in resistance to the newly isolated I. lacteus MI1, a potential necrotrophic pathogen of Marchantia. First, exogenous application of SA was found to promote Marchantia disease development caused by I. lacteus MI1, resembling the activation of the SA pathway that compromises JA-mediated immunity in many seed plants (Fig. 1). Although exogenous application of dn-OPDA did not obviously promote immunity against I. lacteus MI1, co-treatment with SA and dn-OPDA suppressed SA-mediated disease promotion, suggesting the antagonistic action of dn-OPDA and SA in Marchantia immunity against I. lacteus MI1 (Fig. 1). Using the Mpcoi1 mutant, they further demonstrated that the endogenous dn-OPDA pathway regulated by MpCOI1 was required for Marchantia resistance against I. lacteus MI1 (Fig. 1). The notion that SA–JA cross talk in seed plants is conserved in a slightly different form in Marchantia, which utilizes dn-OPDA as the bioactive jasmonate, was also reported in another recent study describing Marchantia immunity to Pseudomonas syringae pv. tomato DC3000, a model bacterial pathogen used widely to study immunity in seed plants such as Arabidopsis and tomato (Gimenez-Ibanez et al. 2019). Taken together, EvoMPMI studies using different pathosystems are providing clues as to how the well-known SA–JA cross talk that regulates plant immunity may have evolved from its ancestral form.

To understand in evolutionary terms the complex cross talk among phytohormones involved in plant–microbe interactions, a variety of Marchantia-based pathosystems ranging from biotrophic to necrotrophic interactions is required (Carella and Schornack 2018, Upson et al. 2018). While the innovative isolation of novel natural pathogens of Marchantia by Matsui et al. (2020) has undoubtedly contributed to strengthening the field of EvoMPMI, further molecular characterization of the Marchantia–I. lacteus MI1 pathosystem, as well as pathological and ecological studies, is needed. Nevertheless, studies using Marchantia are proving extremely powerful as exemplified by many phytohormone studies published in the last few years (Flores-Sandoval et al. 2015, Kato et al. 2015, Eklund et al. 2018, Monte et al. 2018, Aki et al. 2019). In addition to the report by Matsui et al. (2020), a growing number of other pathogens and endophytes of Marchantia are being reported (Carella et al. 2018, Nelson et al. 2018, Gimenez-Ibanez et al. 2019), while conventional defense marker genes are also being identified (Gimenez-Ibanez et al. 2019). Thus, the time for EvoMPMI research is here and now.