Lipid exchanges drove the evolution of mutualism during plant terrestrialization

Area of Science:

• Plant biology
• Mycology
• Evolutionary biology

Background:

• Arbuscular mycorrhizal fungi (AMF) symbiosis enhances plant nutrition and is hypothesized to be key to plant terrestrialization.
• Understanding the molecular mechanisms of this ancient symbiosis is crucial for plant evolution studies.

Purpose of the Study:

• To identify conserved molecular responses to AMF symbiosis across land plants.
• To elucidate the role of lipid metabolism and the WRINKLED (WRI) gene in AMF mutualism.

Main Methods:

• Comparative transcriptomics to identify conserved responses to AMF.
• Gain-of-function and loss-of-function studies in *Marchantia paleacea* to assess WRI gene function.
• Analysis of arbuscule formation and symbiotic interactions.

Main Results:

• A conserved transcriptomic response to AMF, including lipid metabolism activation, was identified across land plants.
• Lipid transfer from *M. paleacea* to AMF was demonstrated and shown to be directly regulated by the WRI transcription factor.
• Loss-of-function *wri* mutants failed to form arbuscules, aborting the symbiotic mutualism.

Conclusions:

• The symbiotic transfer of lipids is an orthologous trait conserved across land plants.
• The WRI gene plays a critical role in establishing AMF symbiosis by regulating lipid transfer.
• AMF mutualism was established in the common ancestor of land plants over 450 million years ago.