A subclass II bHLH transcription factor in Marchantia polymorpha gives insight into the ancestral land plant trait of spore formation.

Sporopollenin is often said to be one of the toughest biopolymers known to man. The shift in dormancy cell wall deposition from around the diploid zygotes of charophycean algae to sporopollenin around the haploid spores of land plants essentially imparted onto land plants the gift of passive motility, a key acquisition that contributed to their vast and successful colonization across terrestrial habitats.1,2 A putative transcription factor controlling the land plant mode of sporopollenin deposition is the subclass II bHLHs, which are conserved and novel to land plants, with mutants of genes in angiosperms and mosses divulging roles relating to tapetum degeneration and spore development.3,4,5,6,7 We demonstrate that a subclass II bHLH gene, MpbHLH37, regulates sporopollenin biosynthesis and deposition in the model liverwort Marchantia polymorpha. Mpbhlh37 sporophytes show a striking loss of secondary wall deposits of the capsule wall, the elaters, and the spore exine, all while maintaining spore viability, identifying MpbHLH37 as a master regulator of secondary wall deposits of the sporophyte. Localization of MpbHLH37 to the capsule wall and elaters of the sporophyte directly designates these tissue types as a bona fide tapetum in liverworts, giving support to the notion that the presence of a tapetum is an ancestral land plant trait. Finally, as early land plant spore walls exhibit evidence of tapetal deposition,8,9,10,11,12 a tapetal capsule wall could have provided these plants with a developmental mechanism for sporopollenin deposition.

The renaissance and enlightenment of Marchantia as a model system.

The liverwort Marchantia polymorpha has been utilized as a model for biological studies since the 18th century. In the past few decades, there has been a Renaissance in its utilization in genomic and genetic approaches to investigating physiological, developmental, and evolutionary aspects of land plant biology. The reasons for its adoption are similar to those of other genetic models, e.g. simple cultivation, ready access via its worldwide distribution, ease of crossing, facile genetics, and more recently, efficient transformation, genome editing, and genomic resources. The haploid gametophyte dominant life cycle of M. polymorpha is conducive to forward genetic approaches. The lack of ancient whole-genome duplications within liverworts facilitates reverse genetic approaches, and possibly related to this genomic stability, liverworts possess sex chromosomes that evolved in the ancestral liverwort. As a representative of one of the three bryophyte lineages, its phylogenetic position allows comparative approaches to provide insights into ancestral land plants. Given the karyotype and genome stability within liverworts, the resources developed for M. polymorpha have facilitated the development of related species as models for biological processes lacking in M. polymorpha.