Lipoxygenase pathway in model bryophytes: 12-oxo-9(13),15-phytodienoic acid is a predominant oxylipin in Physcomitrella patens.

The model moss Physcomitrella patens and liverwort Marchantia polymorpha possess all enzymatic machinery responsible for the initial stages of jasmonate pathway, including the active 13(S)-lipoxygenase, allene oxide synthase (AOS) and allene oxide cyclase (AOC). At the same time, the jasmonic acid is missing from both P. patens and M. polymorpha. Our GC-MS profiling of oxylipins of P. patens gametophores and M. polymorpha tissues revealed some distinctive peculiarities. The 15(Z)-cis-12-oxo-10,15-phytodienoic acid (12-OPDA) was the major oxylipin in M. polymorpha. In contrast, the 12-OPDA was only a minor constituent in P. patens, while another cyclopentenone 1 was the predominant oxylipin. Product 1 was identified by its MS, 1H-NMR, 1H-1H-COSY, HSQC and HMBC data as 15(Z)-12-oxo-9(13),15-phytodienoic acid, i.e., the iso-12-OPDA. The corresponding C16 homologue, 2,3-dinor-iso-12-OPDA (2), have also been detected as a minor component in P. patens and a prominent product in M. polymorpha. Besides, the 2,3-dinor-cis-12-OPDA (3) was also present in M. polymorpha. Apparently, the malfunction of cyclopentenone reduction by the 12-OPDA reductase in P. patens and (to a lesser extent) in M. polymorpha leads to the isomerization of 12-OPDA and formation of specific cyclopentenones 1 and 2, which are uncommon in flowering plants.

Isolation of Natural Fungal Pathogens from Marchantia polymorpha Reveals Antagonism between Salicylic Acid and Jasmonate during Liverwort-Fungus Interactions.

The evolution of adaptive interactions with beneficial, neutral and detrimental microbes was one of the key features enabling plant terrestrialization. Extensive studies have revealed conserved and unique molecular mechanisms underlying plant-microbe interactions across different plant species; however, most insights gleaned to date have been limited to seed plants. The liverwort Marchantia polymorpha, a descendant of early diverging land plants, is gaining in popularity as an advantageous model system to understand land plant evolution. However, studying evolutionary molecular plant-microbe interactions in this model is hampered by the small number of pathogens known to infect M. polymorpha. Here, we describe four pathogenic fungal strains, Irpex lacteus Marchantia-infectious (MI)1, Phaeophlebiopsis peniophoroides MI2, Bjerkandera adusta MI3 and B. adusta MI4, isolated from diseased M. polymorpha. We demonstrate that salicylic acid (SA) treatment of M. polymorpha promotes infection of the I. lacteus MI1 that is likely to adopt a necrotrophic lifestyle, while this effect is suppressed by co-treatment with the bioactive jasmonate in M. polymorpha, dinor-cis-12-oxo-phytodienoic acid (dn-OPDA), suggesting that antagonistic interactions between SA and oxylipin pathways during plant-fungus interactions are ancient and were established already in liverworts.