Plant–microbe interactions that have impacted plant terrestrializations

Abstract

Plants display a tremendous diversity of developmental and physiological features, resulting from gains and losses of functional innovations across the plant phylogeny. Among those, the most impactful have been undoubtedly the ones that allowed plant terrestrializations, the transitions from an aquatic to a terrestrial environment. Although the embryophyte terrestrialization has been particularly scrutinized, others occurred across the plant phylogeny with the involvement of mutualistic symbioses as a common theme. Here, we review the current pieces of evidence supporting that the repeated colonization of land by plants has been facilitated by interactions with mutualistic symbionts. In that context, we detail two of these mutualistic symbioses: the arbuscular mycorrhizal symbiosis in embryophytes and the lichen symbiosis in chlorophyte algae. We suggest that associations with bacteria should be revisited in that context, and we propose that overlooked symbioses might have facilitated the emergence of other land plant clades.

Auxin production in the green alga Chlamydomonas involves an extracellular L-amino acid oxidase and supports algal-bacterial mutualism with methylobacteria

“…Bacterial degradation of IAA has been shown to be essential for rhizosphere colonization and plant growth promotion (Zúñiga et al, 2013), and similar to how LAAO-mediated auxin production is involved in plant growth promotion by G. diazotrophicus (Rodrigues et al, 2016), auxin production by other LAAO-containing microbes in the rhizosphere like Chlamydomonas could have an impact on plant growth and fitness. Our findings suggest that future studies should carefully consider the role that terrestrial algae play in plant microbiomes (Lee and Ryu, 2021) and in the historical record of land plant evolution (Puginier et al, 2022).…”

What can hornworts teach us?

“…These associations of plants with AM fungi and cyanobacteria played an important role in land plant evolution ( Delaux and Schornack, 2021 ). Supplying the plants with essential nutrients might have enabled the adaptation to a terrestrial life in which organic matter was scarce ( Rensing, 2018 ; Puginier et al., 2022 ).…”

“…These associations involve two Mucoromycota subphyla, Mucoromycotina (that colonize 69% of hornworts) and Glomeromycotina (that colonize 78% of hornworts) ( Rimington et al., 2020 ). Both the Glomeromycotina and Mucoromycotina are known to have played a key role in the plant adaptation to the land ( Puginier et al., 2022 ). Often these different types of AM fungi occur simultaneously in the same thallus ( Desiro et al., 2013 ).…”

Plant structure and function: Evolutionary origins and underlying mechanisms

“…In this issue, Puginier et al (2022) review the current state of knowledge on the role of mutualistic associations in the colonization of land by green plants. Embryophyte terrestrialization, aided by mutualistic symbiosis with arbuscular mycorrhizal fungi, improved nutrient and water uptake in the challenging newly colonized environment.…”

“…The authors propose intriguing parallels between lichenization and mycorrhizal symbioses. Outstanding questions include elucidation of improved drought tolerance mechanisms in plants associated with arbuscular mycorrhizal fungi, and the possible role of a core bacterial microbiome in green plant terrestrialization ( Puginier et al, 2022 ).…”