Auxin controls numerous growth processes in land plants through a gene expression system that modulates ARF transcription factor activity 1-3 . Gene duplications in families encoding auxin response components have generated tremendous complexity in most land plants, and neofunctionalization enabled various unique response outputs during development 1,3,4 . However, it is unclear what fundamental biochemical principles underlie this complex response system. By studying the minimal system in Marchantia polymorpha, we derive an intuitive and simple model where a single auxin-dependent A-ARF activates gene expression. It is antagonized by an auxin-independent B-ARF that represses common target genes. The expression patterns of both ARF proteins define developmental zones where auxin response is permitted, quantitatively tuned or prevented. This fundamental design probably represents the ancestral system and formed the basis for inflated, complex systems.The plant hormone auxin controls essentially all aspects of growth and development, and developmental contexts determine its many unique responses 1,2 . TIR1/AFB F-box proteins perceive auxin and promote the ubiquitination and degradation of Aux/IAA transcriptional repressors. Aux/IAAs inhibit DNA-binding ARF transcription factors through direct interaction, and auxin thus releases ARFs from inhibition 3 . Although this signalling module seems simple, each component is encoded by a large gene family in most land plants, particularly in vascular plants 4,5 , allowing overwhelming combinatorial interaction complexity (Fig. 1a; 6 TIR1/AFBs, 29 Aux/IAAs and 23 ARFs; >4,000 combinations in Arabidopsis thaliana). Given different biochemical properties of family members, sets of response components can trigger unique local responses 1,3 , contributing to the paradoxical functional diversity of the chemically simple auxin hormone. Genetic and functional studies in flowering plants suggest functional interactions and trends in diversification among the many ARFs. ARFs are phylogenetically placed into deeply conserved A/B/C classes [4][5][6] . A-ARFs are considered transcriptional activators, and some B-and C-ARFs are considered repressors 7 . Systems-wide interaction analysis among Arabidopsis Aux/IAAs and ARFs suggests more prominent auxin regulation of A-ARFs than B/C-ARFs 8,9 , and individual A-and B-ARFs in the moss Physcomitrella patens can antagonize through competition for DNA sites 10 . However, there are several counterexamples where A-ARFs directly repress targets 11 , Aux/IAAs interact with B/C-ARFs 8,9 and A-and B-ARFs bind different DNA sequences 12 . Because each gene in a multigene family may have sub-or neofunctionalized during evolution, it is entirely unclear what basic biochemical architecture underlies the auxin response system. Recently, we and others have reconstructed the evolutionary history of auxin response components and found that the irreducible complexity in early-diverging land plants encompasses one TIR1/AFB receptor, one Aux/IAA and three ARFs ...
Cell division patterning is important to determine body shape in plants. Nuclear auxin signaling mediated by AUXIN RESPONSE FACTOR (ARF) transcription factors affects plant growth and development through regulation of cell division, elongation and differentiation. The evolutionary origin of the ARF-mediated pathway dates back to at least the common ancestor of bryophytes and other land plants. The liverwort Marchantia polymorpha has three phylogenetically distinct ARFs: MpARF1, the sole 'activator' ARF; and MpARF2 and MpARF3, two 'repressor' ARFs. Genetic screens for auxin-resistant mutants revealed that loss of MpARF1 function conferred auxin insensitivity. Mparf1 mutants showed reduced auxin-inducible gene expression and various developmental defects, including thallus twisting and gemma malformation. We further investigated the role of MpARF1 in gemma development, which is traceable at the cellular level. In wild-type plants, a gemma initial first undergoes several transverse divisions to generate a single-celled stalk and a gemma proper, followed by rather synchronous longitudinal divisions in the latter. Mparf1 mutants often contained multicelled stalks and showed defects in the execution and timing of the longitudinal divisions. While wild-type gemmae finally generate two meristem notches, Mparf1 gemmae displayed various numbers of ectopic meristems. These results suggest that MpARF1 regulates formative cell divisions and axis formation through auxin responses. The mechanism for activator ARF regulation of pattern formation may be shared in land plants and therefore important for the general acquisition of three-dimensional body plans.
Regeneration in land plants is accompanied by the establishment of new stem cells, which often involves reactivation of the cell division potential in differentiated cells. The phytohormone auxin plays pivotal roles in this process. In bryophytes, regeneration is enhanced by removal of the apex and repressed by exogenously applied auxin, which has long been proposed as a form of apical dominance. However, the molecular basis behind these observations remains unexplored. Here, we demonstrate that in the liverwort Marchantia polymorpha, the level of endogenous auxin is transiently decreased in the cut surface of decapitated explants, and identify by transcriptome analysis a key transcription factor gene, LOW AUXIN RESPONSIVE (MpLAXR), which is induced upon auxin reduction. Loss of MpLAXR function resulted in delayed cell cycle reactivation, and transient expression of MpLAXR was sufficient to overcome the inhibition of regeneration by exogenously applied auxin. Furthermore, ectopic expression of MpLAXR caused cell proliferation in normally quiescent tissues. Together, these data indicate that decapitation causes a reduction of auxin level at the cut surface, where, in response, MpLAXR is up-regulated to trigger cellular reprogramming. MpLAXR is an ortholog of Arabidopsis ENHANCER OF SHOOT REGENERATION 1/DORNRÖSCHEN, which has dual functions as a shoot regeneration factor and a regulator of axillary meristem initiation, the latter of which requires a low auxin level. Thus, our findings provide insights into stem cell regulation as well as apical dominance establishment in land plants.
In flowering plants, strigolactones (SLs) have dual functions as hormones that regulate growth and development, and as rhizosphere signaling molecules that induce symbiosis with arbuscular mycorrhizal (AM) fungi. Here, we report the identification of bryosymbiol (BSB), an SL from the bryophyte Marchantia paleacea. BSB is also found in vascular plants, indicating its origin in the common ancestor of land plants. BSB synthesis is enhanced at AM symbiosis permissive conditions and BSB deficient mutants are impaired in AM symbiosis. In contrast, the absence of BSB synthesis has little effect on the growth and gene expression. We show that the introduction of the SL receptor of Arabidopsis renders M. paleacea cells BSB-responsive. These results suggest that BSB is not perceived by M. paleacea cells due to the lack of cognate SL receptors. We propose that SLs originated as AM symbiosis-inducing rhizosphere signaling molecules and were later recruited as plant hormone.
Auxin controls numerous growth processes in land plants through a gene expression system9 that modulates ARF transcription factor activity 1-3 . Gene duplications in families encoding 10 auxin response components have generated tremendous complexity in most land plants, and 11 neofunctionalization enabled various unique response outputs during development 2-4 . 12 However, it is unclear what fundamental biochemical principles underlie this complex 13 response system. By studying the minimal system in Marchantia polymorpha, we derive an 14 intuitive and simple model where a single auxin-dependent A-ARF activates gene expression.15It is antagonized by an auxin-independent B-ARF that represses common target genes. 16
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