Control of sporophyte secondary cell wall development in Marchantia by a Class II KNOX gene

Land plants evolved from an ancestral alga around 470 mya, evolving complex multicellularity in both haploid gametophyte and diploid sporophyte generations. The evolution of water-conducting tissues in the sporophyte generation was crucial for the success of land plants, paving the way for the colonization of a variety of terrestrial habitats. Class II KNOX (KNOX2) genes are major regulators of secondary cell wall formation and seed mucilage (pectin) deposition in flowering plants. Here, we show that, in the liverwort Marchantia polymorpha, loss-of-function alleles of the KNOX2 ortholog, MpKNOX2, or its dimerization partner, MpBELL1, have defects in capsule wall secondary cell wall and spore pectin biosynthesis. Both genes are expressed in the gametophytic calyptra surrounding the sporophyte and exert maternal effects, suggesting intergenerational regulation from the maternal gametophyte to the sporophytic embryo. These findings also suggest the presence of a secondary wall genetic program in the non-vascular liverwort capsule wall, with attributes of secondary walls in vascular tissues. [Display omitted] •Marchantia Class II KNOX is maternally expressed in the calyptra post-fertilization•MpKNOX2 non-cell autonomously directs sporophytic capsule wall formation•MpKNOX2 is involved in pectin biosynthesis during microsporogenesis•Secondary cell wall and pectin biosynthesis by KNOX2 genes is land plant universal The evolution of vasculature paved the way for land plants to colonize a vast array of terrestrial habitats. Dierschke et al. demonstrate that maternally expressed Marchantia polymorpha Class II KNOX controls sporophyte capsule secondary cell wall and pectin biosynthesis during sporogenesis, a function conserved throughout land plant evolution.