SummaryOne of the most important events in the history of life on earth was the colonization of land by plants; this transition coincided with and was most likely enabled by the evolution of 3-dimensional (3D) growth. Today, the diverse morphologies exhibited across the terrestrial biosphere arise from the differential regulation of 3D growth processes during development. In many plants, 3D growth is initiated during the first few divisions of the zygote, and therefore, the genetic basis cannot be dissected because mutants do not survive. However, in mosses, which are representatives of the earliest land plants, 3D shoot growth is preceded by a 2D filamentous phase that can be maintained indefinitely. Here, we used the moss Physcomitrella patens to identify genetic regulators of the 2D to 3D transition. Mutant screens yielded individuals that could only grow in 2D, and through an innovative strategy that combined somatic hybridization with bulk segregant analysis and genome sequencing, the causative mutation was identified in one of them. The NO GAMETOPHORES 1 (NOG1) gene, which encodes a ubiquitin-associated protein, is present only in land plant genomes. In mutants that lack PpNOG1 function, transcripts encoding 3D-promoting PpAPB transcription factors [1] are significantly reduced, and apical initial cells specified for 3D growth are not formed. PpNOG1 acts at the earliest identified stage of the 2D to 3D transition, possibly through degradation of proteins that suppress 3D growth. The acquisition of NOG1 function in land plants could thus have enabled the evolution and development of 3D morphology.
Summary Dispersal is a key step in land plant life cycles, usually via formation of spores or seeds. Regulation of spore‐ or seed‐germination allows control over the timing of transition from one generation to the next, enabling plant dispersal. A combination of environmental and genetic factors determines when seed germination occurs. Endogenous hormones mediate this decision in response to the environment. Less is known about how spore germination is controlled in earlier‐evolving nonseed plants.Here, we present an in‐depth analysis of the environmental and hormonal regulation of spore germination in the model bryophyte Physcomitrella patens (Aphanoregma patens).Our data suggest that the environmental signals regulating germination are conserved, but also that downstream hormone integration pathways mediating these responses in seeds were acquired after the evolution of the bryophyte lineage. Moreover, the role of abscisic acid and diterpenes (gibberellins) in germination assumed much greater importance as land plant evolution progressed.We conclude that the endogenous hormone signalling networks mediating germination in response to the environment may have evolved independently in spores and seeds. This paves the way for future research about how the mechanisms of plant dispersal on land evolved.
Plant root system plasticity is critical for survival in changing environmental conditions. One important aspect of root architecture is lateral root development, a complex process regulated by hormone, environmental and protein signalling pathways.Here we show, using molecular genetic approaches, that the MYB transcription factor AtMYB93 is a novel negative regulator of lateral root development in Arabidopsis.We identify AtMYB93 as an interaction partner of the lateral-root-promoting ARABIDILLO proteins. Atmyb93 mutants have faster lateral root developmental progression and enhanced lateral root densities, while AtMYB93-overexpressing lines display the opposite phenotype. AtMYB93 is expressed strongly, specifically and transiently in the endodermal cells overlying early lateral root primordia and is additionally induced by auxin in the basal meristem of the primary root. Furthermore, Atmyb93 mutant lateral root development is insensitive to auxin, indicating that AtMYB93 is required for normal auxin responses during lateral root development.We propose that AtMYB93 is part of a novel auxin-induced negative feedback loop stimulated in a select few endodermal cells early during lateral root development, ensuring that lateral roots only develop when absolutely required. Putative AtMYB93 homologues are detected throughout flowering plants and represent promising targets for manipulating root systems in diverse crop species.
ARABIDILLO proteins are F-box-Armadillo (ARM) proteins that regulate root branching in Arabidopsis. Many F-box proteins in plants, yeast and mammals are unstable. In plants, the mechanism for this instability has not been fully investigated. Here, we show that a conserved family of plant ARABIDILLO-related proteins has a unique domain structure consisting of an F-box and leucine-rich repeats (LRRs) followed by ARM-repeats. The LRRs are similar to those found in other plant and animal F-box proteins, including cell cycle proteins and hormone receptors. We demonstrate that the LRRs are required for ARABIDILLO1 function in vivo. ARABIDILLO1 protein is unstable: we show that ARABIDILLO1 protein is associated with ubiquitin and is turned over by the proteasome. Both the F-box and LRR regions of ARABIDILLO1 appear to enable this turnover to occur. Application of known lateral root-regulating signals has no effect on ARABIDILLO1 stability. In addition, plants that lack or overexpress ARABIDILLO proteins respond normally to known lateral root-regulating signals. Thus, we suggest that the signal(s) regulating ARABIDILLO stability in vivo may be either highly specific or novel. The structural conservation between ARABIDILLOs and other plant and animal F-box proteins suggests that the stability of other F-box proteins may be controlled by similar mechanisms.
Highlights d NO GAMETOPHORES 2 (PpNOG2) regulates the 2D to 3D growth transition in P. patens d PpNOG2 regulates gametophore initial cell formation and division plane orientation d PpNOG2 is required for the modulation of the auxin response d PpNOG2 acts upstream of CLAVATA and SCARECROW genes
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