The Elegant Simplicity of the Liverwort Marchantia polymorpha.

Plants have evolved several ways to remain dormant until the time is right for growth. For example, seeds maintain dormancy through the antagonistic effects of the phytohormones abscisic acid (ABA) and gibberellic acid. Auxin (indole-3-acetic acid [IAA]), in turn, regulates ABA-induced seed dormancy through its interaction with the ABA signaling pathway (Liu et al., 2013). Dormancy is also crucial for non-seed-bearing plants such as liverworts, a basal lineage of land plants. In the liverwort Marchantia polymorpha, tiny, disc-like propagules (of the haploid gametophyte generation) called gemmae lay dormant in gemma cups on the thallus of the parent plant until they are dispersed by rainfall and released from their dormant state, a process that has long fascinated botanists. Early studies employing techniques such as removing gemmae from their cups, applying exogenous auxins and antiauxins, and careful microscopic observation have suggested that gemma dormancy is imposed, at least in part, by auxin emanating from the thallus apical meristem of the parent plant (LaRue and Narayanaswami, 1957). Until recently, the details of this process, including how the auxin in the thallus is biosynthesized, have remained a mystery. In angiosperms, most auxin is derived from Trp via indole-3-pyruvic acid (IPyA) in a two-step pathway catalyzed by numerous auxin biosynthetic enzymes encoded by multigene families, with TRYPTOPHANAMINOTRANSFERASEOFARABIDOPSIS (TAA) enzymes catalyzing the Trp-to-IPyA conversion and YUCCA (YUC) enzymes catalyzing the IPyA-to-IAA conversion. The recent development of M. polymorpha as a model system (including the availability of mutants, a transformation system, and bioinformatic tools) has allowed Eklund et al. (2015) to uncover the elegant simplicity of the auxin biosynthetic pathway in this species. The authors found that M. polymorpha contains only one TAA gene and two YUC genes, making this IPyA-dependent auxin biosynthesis toolkit the simplest known in any landplant. The authors constitutively expressed YUC1 and YUC2 in M. polymorpha, producing plants that appeared similar to those treated with high levels of exogenous auxin. Constitutive expression of TAA produced a similar (but milder) phenotype, with YUC or TAA transcript levels in the transgenic lines positively correlated with the severity of the phenotype. YUC overexpression was correlated with increased IAA levels, as expected. These findings leave little doubt that the biochemical roles of TAA and YUC1/2 in the IPyA pathway are conserved between liverworts and angiosperms. Moreover, the observation that TAA overexpression had a much milder effect than YUC overexpression suggests that conversion from IPyA to IAA by YUC2 is the rate-limiting step in this pathway during normalM. polymorpha thallus development. Expression analysis revealed that YUC1 is sporophyte specific, while YUC2 and TAA are expressed in both the sporophyte and thallus. Experiments employing GUS fused to the TAA or YUC2 promoter revealed that these genes are expressed in meristematic tissue, i.e., shoot apical regions of thalli and gemma cup bases, the main sites of IAA production. Dormant gemmae produced almost no GUS signals, suggesting that little or no IAA is produced in the gemmae via the IPyA pathway. The authors then eliminated or reduced the contribution of the IPyA pathway to the total IAA pool in M. polymorpha gametophytes through the creation of various TAA knockout and YUC2 knockdown lines, which exhibited severe developmental defects that were partially rescued by the application of IAA (see figure). Strikingly, when gemmae did form in the gemma cups of these lines, they did not maintain dormancy. These findings indicate that auxin is essential for gametophyte development and that it promotes gemma dormancy. They also demonstrate the promise of M. polymorpha as a simple, elegant model system.