A Simple Auxin Transcriptional Response System Regulates Multiple Morphogenetic Processes in the Liverwort Marchantia polymorpha

Abstract

In land plants comparative genomics has revealed that members of basal lineages share a common set of transcription factors with the derived flowering plants, despite sharing few homologous structures. The plant hormone auxin has been implicated in many facets of development in both basal and derived lineages of land plants. We functionally characterized the auxin transcriptional response machinery in the liverwort Marchantia polymorpha, a member of the basal lineage of extant land plants. All components known from flowering plant systems are present in M. polymorpha, but they exist as single orthologs: a single MpTOPLESS (TPL) corepressor, a single MpTRANSPORT INHIBITOR RESPONSE 1 auxin receptor, single orthologs of each class of AUXIN RESPONSE FACTOR (ARF; MpARF1, MpARF2, MpARF3), and a single negative regulator AUXIN/INDOLE-3-ACETIC ACID (MpIAA). Phylogenetic analyses suggest this simple system is the ancestral condition for land plants. We experimentally demonstrate that these genes act in an auxin response pathway — chimeric fusions of the MpTPL corepressor with heterodimerization domains of MpARF1, MpARF2, or their negative regulator, MpIAA, generate auxin insensitive plants that lack the capacity to pattern and transition into mature stages of development. Our results indicate auxin mediated transcriptional regulation acts as a facilitator of branching, differentiation and growth, rather than acting to determine or specify tissues during the haploid stage of the M. polymorpha life cycle. We hypothesize that the ancestral role of auxin is to modulate a balance of differentiated and pluri- or totipotent cell states, whose fates are determined by interactions with combinations of unrelated transcription factors.

Field Guide to Plant Model Systems

“…Furthermore, protocols for efficient Agrobacterium -mediated transformation of spores have been pioneered (Ishizaki et al, 2008), and these may be able to be adapted, with modifications to suit differences in life cycle, to other spore-producing land plants. Studies on the auxin transcriptional response machinery in M. polymorpha have suggested that auxin response modulates, but does not determine cell fates and, furthermore, that it is critical for the transition from 2-dimensional growth to 3-dimensional growth in the haploid generation (Kato et al, 2015; Flores-Sandoval et al, 2015). Gene knockout technologies also enabled the discovery that the molecular mechanism by which plants measure photo-period and control the transition between vegetative growth and reproductive growth is broadly conserved across land plants (Kubota et al, 2014).…”

Mechanisms of auxin signaling

“…Gene expression associated with ARF activation has been implicated in diverse processes in land plants, including tropic responses and the establishment of polarity, as well as embryogenesis and organogenesis in flowering plants, and both gametophyte and sporophyte development in nonflowering plants (De Smet and Jurgens, 2007;Banks, 2009;Moller and Weijers, 2009;Prigge et al, 2010;Vernoux et al, 2010;Bennett et al, 2014;Flores-Sandoval et al, 2015;Kato et al, 2015). At the cellular level, auxin affects all aspects of cellular growth, including cell elongation, cell division and differentiation (Perrot-Rechenmann, 2010;Takatsuka and Umeda, 2014).…”

Primitive Auxin Response without TIR1 and Aux/IAA in the Charophyte Alga Klebsormidium nitens

“…www.plantphysiol.org/cgi/doi/10.1104/pp.17.00274 (Kato et al, 2015), but the M. polymorpha and P. patens genomes contain homologs of the canonical auxin-signaling factors TIR1/AFB, Aux/IAA, and AUXIN RESPONSE FACTOR (ARF; Kato et al, 2015). These auxin-signaling components regulate normal cell elongation and differentiation in M. polymorpha (Flores-Sandoval et al, 2015;Kato et al, 2015). Consequently, auxin-related genes show very few differences between land-plant lineages (Finet and Jaillais, 2012), suggesting that the last common ancestor of land plants had already acquired the core auxin machinery of land plants.…”