Class 1 KNOX genes are not involved in shoot development in the moss Physcomitrella patens but do function in sporophyte development

Abstract

SUMMARY Although the number and form of metazoan organs are determined in the embryo, plants continuously form organs via pluripotent stem cells contained within the meristem. Flowering plants have an indeterminate meristem in their diploid generation, whereas the common ancestor of land plants is inferred to have formed an indeterminate meristem in its haploid generation, as observed in the extant basal land plants, bryophytes, including mosses. It is hypothesized that the underlying gene networks for the diploid meristem were initially present in the haploid generation of the basal land plants and were eventually co-opted for expression in the diploid generation. In flowering plants, the class 1 KNOTTED1-LIKE HOMEOBOX (KNOX) transcription factors are essential for the function of the indeterminate apical meristem. Here, we show that the class 1 KNOX orthologs function in the diploid organ, with determinate growth in the moss Physcomitrella patens, but do not function in the haploid indeterminate meristem. We propose that the genetic networks governing the indeterminate meristem in land plants are variable, and the networks governing the diploid indeterminate meristem with the class 1 KNOX genes likely evolved de novo in the flowering plant lineage.

The Gibberellin perception system evolved to regulate a pre-existing GAMYB-mediated system during land plant evolution

“…Similar to the ancestors of land plants, P. patens, which develops a parasitic sporophyte on the gametophyte, has a gametophyte-dominant life cycle, whereas vascular plants, including S. moellendorffii, have a sporophyte-dominant life cycle 29 . The evolutional transition from a gametophyte-to a sporophyte-dominant life cycle and the subsequent adaptation to the land environment have increased the complexity of the sexual reproduction system: for example, the transition from spore sac cells to tapetal cells, and the transition from homospory to heterospory.…”

“…4a,b). P. patens develops protonemata colony from spores, and then differentiates gametophores with haploid leafy shoots and root-like rhizoids from a fraction of the protonema 29 ( Fig. 4c and Supplementary Fig.…”

“…4d,e), which contain an egg and sperm cells, respectively, develop, and an egg cell is fertilized by a sperm cell 29 . Finally, the resulting zygote develops a sporophyte that contains a spore-producing tissue, the sporangium 29 (Fig. 4f).…”

“…In contrast, the transcripts of PpGAMYB2 and PpCYP703B2, the predominantly expressed genes, co-localized in spore sac cells of the sporangium (Supplementary Fig. S5c,d; insets), which correspond to tapetal cells in flowering plants 29 .…”

KNOX genes: versatile regulators of plant development and diversity

“…5). Given the role of KNOX genes in shoot development, it was surprising to find that Class I and II KNOX genes are neither expressed nor functional in the moss gametophyte, acting instead during sporophyte development (Sakakibara et al, 2008;Singer and Ashton, 2007). Genetic control of the shoot system in haploid moss and in diploid flowering plants might, therefore, represent convergent evolution (see Glossary, Box 1).…”