A single genetic innovation at the origin of plant terrestrialization

Did one gene family help plants colonise land?

Moving from freshwater to land exposed early plants to dehydration, stronger ultraviolet radiation, and nutrient-poor substrates. Two traits associated with overcoming these challenges, the cuticle and arbuscular mycorrhizal (AM) symbiosis, are thought to have been present early in land-plant evolution. The cuticle is a hydrophobic barrier on aerial surfaces that limits water loss and protects against environmental stress. AM fungi extend the plant’s reach for water and mineral nutrients.
Despite their very different functions, both systems involve the movement of lipids out of plant cells. Cutin precursors must be exported to the epidermal surface to build the cuticle, and AM fungi rely on host-derived fatty acids because they have only a limited capacity for de novo fatty-acid synthesis (Wewer et al., 2014; Rich et al., 2021).

A particular class of glycerol-3-phosphate acyltransferases may be the connecting link between the two. In angiosperms, the land-plant-specific phosphatase-domain-containing GPATs (p-GPATs) acylate glycerol-3-phosphate at the sn-2 position and then dephosphorylate the product to give 2-monoacylglycerol (2-MAG). Several Arabidopsis p-GPATs contribute to cutin production, and Medicago truncatula RAM2 is required for normal arbuscule development. p-GPATs also take part in cuticle formation in the moss Physcomitrium patens. What remained unclear was whether the family was already doing both jobs in the earliest land plants. Answering this could reveal whether a single biochemical innovation contributed to multiple adaptations associated with the transition to life on land.

What they found
The authors began by tracing the evolution of p-GPAT across 438 Viridiplantae genomes. The signature pairing of acyltransferase and phosphatase domains was absent from the sampled algal genomes but present across land plants, consistent with a p-GPAT family that arose around the origin of terrestrial plants. Activity assays then showed that bryophyte p-GPATs retain the biochemical activities typical of the family. To test the link genetically, they turned to Marchantia paleacea. The single ram2b and ram2c mutants looked fairly similar to the wild type. The double mutant did not. Its thalli were severely abnormal, stunted, and largely unbranched, with no normal air pores and a strongly reduced cuticle, where cutin monomers were reduced by roughly 60–93%. Expressing MpaRAM2C from either its native promoter or the epidermis-specific SBG promoter rescued the double mutant.

The key experiment came next, when the authors examined AM symbiosis in these complemented plants. The native promoter allows RAM2C to function in both epidermal cells and arbuscule-containing cells, and it restored normally branched arbuscules. Epidermis-restricted expression brought back the cuticle but largely failed to restore arbuscule development. So the same p-GPAT family is required in two distinct cellular contexts, in epidermal cells for cutin formation and in fungus-colonised cells for arbuscule development.

The authors read this as support for the idea that p-GPATs provided plants with a biochemical means to shift lipids from intracellular metabolism to extracellular functions. That innovation, they suggest, may have opened a fairly simple route to two traits that mattered during terrestrialization.

Why I chose this preprint
I picked this work because it connects two aspects of terrestrialization that usually get discussed separately, protection from water loss and cooperation with AM fungi. It also goes beyond merely noting that p-GPATs appear in both pathways. Working with a liverwort, the authors show that a single enzyme family is required across different cell types for two distinct functions.
The promoter-restricted complementation is the most informative part. Restoring p-GPAT activity in the epidermis rescues the cuticle without restoring normal arbuscules, which is evidence that the symbiotic defect is not simply a secondary consequence of a damaged cuticle.
I would still be careful about reading the shared p-GPAT lineage as evidence that the cuticle and AM symbiosis are homologous traits. What the experiments most directly establish is a shared enzymatic requirement operating in two cellular contexts. The evolutionary sequence the authors propose remains a model rather than something directly observed: whether cuticle-associated lipid export came first, whether symbiotic lipid transfer was recruited afterward, and how the two functions came together in the ancestral land plant. That leaves a bigger question, and it’s the one I find most compelling. Did the origin of a new biochemical capability constrain or channel the evolution of several terrestrial adaptations?

Questions for the authors
• MpaRAM2C complements the Medicago truncatula ram2 phenotype, but MpaRAM2B does not, even though both paralogs contribute to cutin-related functions in M. paleacea. Would expressing MpaRAM2B under the MpaRAM2C promoter help distinguish differences in protein activity from differences in spatial or temporal expression?
• Could isotope labelling of host-derived lipids, combined with lipid profiling of Rhizophagus irregularis, show whether 2-MAG itself is transferred to the fungus or is first converted into another lipid species?

References
• Lee, S. B., Yang, S. U., Pandey, G., Kim, M. S., Hyoung, S., Choi, D., … & Suh, M. C. (2020). Occurrence of land‐plant‐specific glycerol‐3‐phosphate acyltransferases is essential for cuticle formation and gametophore development in Physcomitrella patens. New Phytologist, 225(6), 2468-2483.
• Rich, M. K., Vigneron, N., Libourel, C., Keller, J., Xue, L., Hajheidari, M., … & Delaux, P. M. (2021). Lipid exchanges drove the evolution of mutualism during plant terrestrialization. Science, 372(6544), 864-868.
• Wang, E., Schornack, S., Marsh, J. F., Gobbato, E., Schwessinger, B., Eastmond, P., … & Oldroyd, G. E. (2012). A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Current Biology, 22(23), 2242-2246.
• Wewer, V., Brands, M., & Dörmann, P. (2014). Fatty acid synthesis and lipid metabolism in the obligate biotrophic fungus R hizophagus Irregularis during mycorrhization of L otus japonicus. The Plant Journal, 79(3), 398-412.
• Yang, W., Pollard, M., Li-Beisson, Y., Beisson, F., Feig, M., & Ohlrogge, J. (2010). A distinct type of glycerol-3-phosphate acyltransferase with sn-2 preference and phosphatase activity producing 2-monoacylglycerol. Proceedings of the National Academy of Sciences, 107(26), 12040-12045.
Image credit
Reproduced from Mbadinga Zamar et al. (2026), bioRxiv, https://doi.org/10.64898/2026.08.14.744897, under a CC BY 4.0 licence (https://creativecommons.org/licenses/by/4.0/). No changes were made.