•3D growth in plants evolved coincident with the colonization of land.•P. patens is an ideal model organism in which to genetically dissect 3D growth.•2D side branch initials are morphologically ...distinct from 3D side branch initials.•The APB genes are central regulators of the 2D to 3D growth transition.•CESA5, DEK1, NOG1 and CLAVATA genes are important regulators of this transition.
The colonization of land by plants coincided with and was most likely facilitated by the evolution of 3-dimensional (3D) growth. 3D growth is a pivotal feature of all land plants, but most develop in a way that precludes genetic investigation. In the moss Physcomitrella patens, 3D growth (gametophores) is preceded by an extended 2-dimensional (2D) growth phase (protonemata) that can be propagated indefinitely. Studies using P. patens have thus elucidated some of the molecular mechanisms underlying 3D growth regulation. This review summarizes the known molecular mechanisms underlying both the formation of gametophore initial cells and the development of the 3D growth in gametophores.
One of the most transformative events in the history of life on earth was the transition of plants from water to land approximately 470 million years ago. Within the Charophyte green algae, the ...closest living relatives of land plants, body plans have evolved from those that comprise simple unicells to those that are morphologically complex, large and multicellular. The Charophytes developed these broad ranging body plans by exploiting a range of one-dimensional and two-dimensional growth strategies to produce filaments, mats and branches. When plants were confronted with harsh conditions on land, they were required to make significant changes to the way they shaped their body plans. One of the fundamental developmental transitions that occurred was the evolution of three-dimensional growth and the acquisition of apical cells with three or more cutting faces. Plants subsequently developed a range of morphological adaptations (e.g. vasculature, roots, flowers, seeds) that enabled them to colonise progressively drier environments. 3D apical growth also evolved convergently in the brown algae, completely independently of the green lineage. This review summarises the evolving developmental complexities observed in the early divergent Charophytes all the way through to the earliest conquerors of land, and investigates 3D apical growth in the brown algae.
One 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.
•NO GAMETOPHORES 1 (PpNOG1) regulates the 2D to 3D growth transition in P. patens•PpNOG1 acts upstream of 3D-promoting PpAPB transcription factors•PpNOG1 is required for the formation of apical initial cells specified for 3D growth•NOG1 genes are found only in land plants and thus evolved coincident with 3D growth
Moody et al. use forward genetics, somatic hybridization, and genome sequencing to identify NO GAMETOPHORES 1 (PpNOG1), a gene that regulates the two-dimensional (2D) to three-dimensional (3D) growth transition in the moss Physcomitrella patens. PpNOG1 promotes the formation of apical initials that are required for the establishment of 3D growth.
One of the most defining moments in history was the colonization of land by plants approximately 470 million years ago. The transition from water to land was accompanied by significant changes in the ...plant body plan, from those than resembled filamentous representatives of the charophytes, the sister group to land plants, to those that were morphologically complex and capable of colonizing harsher habitats. The moss Physcomitrium patens (also known as Physcomitrella patens) is an extant representative of the bryophytes, the earliest land plant lineage. The protonema of P. patens emerges from spores from a chloronemal initial cell, which can divide to self‐renew to produce filaments of chloronemal cells. A chloronemal initial cell can differentiate into a caulonemal initial cell, which can divide and self‐renew to produce filaments of caulonemal cells, which branch extensively and give rise to three‐dimensional shoots. The process by which a chloronemal initial cell differentiates into a caulonemal initial cell is tightly regulated by auxin‐induced remodeling of the actin cytoskeleton. Studies have revealed that the genetic mechanisms underpinning this transition also regulate tip growth and differentiation in diverse plant taxa. This review summarizes the known cellular and molecular mechanisms underpinning the chloronema to caulonema transition in P. patens.
A proposed model for the chloronema to caulonema transition in P. patens. The differentiation of caulonemata is dependent on the auxin‐induced remodelling of the actin cytoskeleton, but is also underpinned by complex hormone crosstalk that overlaps with light and sugar signaling pathways.
Class I KNOTTED-LIKE HOMEOBOX (KNOX) proteins regulate development of the multi-cellular diploid sporophyte in both mosses and flowering plants; however, the morphological context in which they ...function differs.
In order to determine how Class I KNOX function was modified as land plants evolved, phylogenetic analyses and cross-species complementation assays were performed.
Our data reveal that a duplication within the charophyte sister group to land plants led to distinct Class I and Class II KNOX gene families. Subsequently, Class I sequences diverged substantially in the nonvascular bryophyte groups (liverworts, mosses and hornworts), with moss sequences being most similar to those in vascular plants. Despite this similarity, moss mutants were not complemented by vascular plant KNOX genes. Conversely, the Arabidopsis brevipedicellus (bp-9) mutant was complemented by the PpMKN2 gene from the moss Physcomitrella patens. Lycophyte KNOX genes also complemented bp-9 whereas fern genes only partially complemented the mutant. This lycophyte/fern distinction is mirrored in the phylogeny of KNOX-interacting BELL proteins, in that a gene duplication occurred after divergence of the two groups.
Together, our results imply that the moss MKN2 protein can function in a broader developmental context than vascular plant KNOX proteins, the narrower scope having evolved progressively as lycophytes, ferns and flowering plants diverged.
The colonization of land by plants was one of the most transformative events in the history of life on Earth. The transition from water, which coincided with and was likely facilitated by the ...evolution of three-dimensional (3D) growth, enabled the generation of morphological diversity on land. In many plants, the transition from two-dimensional (2D) to 3D growth occurs during embryo development. However, in the early divergent moss Physcomitrella patens, 3D growth is preceded by an extended filamentous phase that can be maintained indefinitely. Here, we describe the identification of the cytokinin-responsive NO GAMETOPHORES 2 (PpNOG2) gene, which encodes a shikimate o-hydroxycinnamoyltransferase. In mutants lacking PpNOG2 function, transcript levels of CLAVATA and SCARECROW genes are significantly reduced, excessive gametophore initial cells are produced, and buds undergo premature developmental arrest. Mutants also exhibit misregulation of auxin-responsive genes. Our results suggest that PpNOG2 functions in the ascorbic acid pathway leading to cuticle formation and that NOG2-related genes were co-opted into the lignin biosynthesis pathway after the divergence of bryophytes and vascular plants. We present a revised model of 3D growth in which PpNOG2 comprises part of a feedback mechanism that is required for the modulation of gametophore initial cell frequency. We also propose that the 2D to 3D growth transition in P. patens is underpinned by complex auxin-cytokinin crosstalk that is regulated, at least in part, by changes in flavonoid metabolism.
•NO GAMETOPHORES 2 (PpNOG2) regulates the 2D to 3D growth transition in P. patens•PpNOG2 regulates gametophore initial cell formation and division plane orientation•PpNOG2 is required for the modulation of the auxin response•PpNOG2 acts upstream of CLAVATA and SCARECROW genes
Moody et al. use forward genetics to identify NO GAMETOPHORES 2 (PpNOG2), a gene that regulates the two-dimensional (2D) to three-dimensional (3D) growth transition in the moss Physcomitrella patens. PpNOG2 is required to modulate gametophore initial cell frequency and cell division plane orientation during the establishment of 3D growth.
The perinatal period is a window of heightened plasticity that lays the groundwork for future anatomic, physiologic, and behavioral outcomes. During this time, maternal diet plays a pivotal role in ...the maturation of vital organs and the establishment of neuronal connections. However, when perinatal nutrition is either lacking in specific micro- and macronutrients or overloaded with excess calories, the consequences can be devastating and long lasting. The brain is particularly sensitive to perinatal insults, with several neurologic and psychiatric disorders having been linked to a poor in utero environment. Diseases characterized by learning and memory impairments, such as autism, schizophrenia, and Alzheimer disease, are hypothesized to be attributed in part to environmental factors, and evidence suggests that the etiology of these conditions may date back to very early life. In this review, we discuss the role of the early-life diet in shaping cognitive outcomes in offspring. We explore the endocrine and immune mechanisms responsible for these phenotypes and discuss how these systemic factors converge to change the brain's epigenetic landscape and regulate learning and memory across the lifespan. Through understanding the maternal programming of cognition, critical steps may be taken toward preventing and treating diseases that compromise learning and memory.
Forward genetics is now straightforward in the moss Physcomitrella patens, and large mutant populations can be screened relatively easily. However, perturbation of development before the formation of ...gametes currently leaves no route to gene discovery.
Somatic hybridization has previously been used to rescue sterile mutants and to assign P. patens mutations to complementation groups, but the cellular basis of the fusion process could not be monitored, and there was no tractable way to identify causative mutations.
Here we use fluorescently tagged lines to generate somatic hybrids between Gransden (Gd) and Villersexel (Vx) strains of P. patens, and show that hybridization produces fertile diploid gametophytes that form phenotypically normal tetraploid sporophytes. Quantification of genetic variation between the two parental strains reveals single nucleotide polymorphisms at a frequency of 1/286 bp.
Given that the genetic distinction between Gd and Vx strains exceeds that found between pairs of strains that are commonly used for genetic mapping in other plant species, the spore populations derived from hybrid sporophytes provide suitable material for bulk segregant analysis and gene identification by genome sequencing.
Carnitine palmitoyltransferase 1 (Cpt1a) is a rate-limiting enzyme that mediates the transport of fatty acids into the mitochondria for subsequent beta-oxidation. The objective of this study was to ...uncover how diet mediates the transcriptional regulation of Cpt1a. Pregnant Sprague Dawley rats were exposed to either a high-fat (HF) or low-fat control diet during gestation and lactation. At weaning, male offspring received either a HF or control diet, creating 4 groups: lifelong control diet (C/C; n = 12), perinatal HF diet (HF/C; n = 9), post-weaning HF diet (C/HF; n = 10), and lifelong HF diet (HF/HF; n = 10). Only HF/HF animals had higher hepatic Cpt1a mRNA expression than C/C. Epigenetic analysis revealed reduced DNA methylation (DNAMe) and increased histone 3 lysine 4 dimethylation (H3K4Me2) upstream and within the promoter of Cpt1a in the HF/HF group. This was accompanied by increased peroxisome proliferator activated receptor alpha (PPARα) and CCAAT/enhancer binding protein beta (C/EBPβ) binding directly downstream of the Cpt1a transcription start site within the first intron. Findings were confirmed in rat hepatoma H4IIEC3 cells treated with non-esterified fatty acid (NEFA). After 12 h of NEFA treatment, there was an enrichment of SWI/SNF related matrix associated actin dependent regulator of chromatin subfamily D member 1 (BAF60a or SMARCD1) in the first intron of Cpt1a. We conclude that dietary fat elevates hepatic Cpt1a expression via a highly coordinated transcriptional mechanism involving increased H3K4Me2, reduced DNAMe, and recruitment of C/EBPβ, PPARα, PGC1α, and BAF60a to the gene.
•Cpt1a gene is responsive to dietary high fat at transcription level;•Persistent perturbation of genomic structure by dietary fat occurs through reduced DNA methylation at Cpt1a gene;•Histones were also modified by dietary fat to demonstrate a landscape shift at genomic regions;•Epigenetic modifications are associated with recruitment of a milieu of transcription factors and co-factors.
PDF
