•Many land plant-like features evolved in freshwater algae.•The cell wall, alternation of division plane and polyplastidy were probably important for terrestrialization.•Phenylpropanoids are ...important protective substances that evolved by gene duplication and retention.•Many gametophytic regulatory pathways have been co-opted for the sporophyte.•Alternation of generations, embryogenesis and mutualistic fungal symbioses are hallmarks of land plants.
500Ma ago the terrestrial habitat was a barren, unwelcoming place for species other than, for example, bacteria or fungi. Most probably, filamentous freshwater algae adapted to aerial conditions and eventually conquered land. Adaptation to a severely different habitat apparently included sturdy cell walls enabling an erect body plan as well as protection against abiotic stresses such as ultraviolet radiation, drought and varying temperature. To thrive on land, plants probably required more elaborate signaling pathways to react to diverse environmental conditions, and phytohormones to control developmental programs. Many such plant-typical features have been studied in flowering plants, but their evolutionary origins were long clouded. With the sequencing of a moss genome a decade ago, inference of ancestral land plant states using comparative genomics, phylogenomics and evolutionary developmental approaches began in earnest. In the past few years, the ever increasing availability of genomic and transcriptomic data of organisms representing the earliest common ancestors of the plant tree of life has much informed our understanding of the conquest of land by plants.
•Whole genome duplications are an important mode of plant evolution.•Plants evolve developmental novelties by retention of duplicated control genes.•Genes controlling transcriptional networks are ...correlated with morphological complexity.•Both ancient and recent paralogs play important roles in the evolution of plant development.
Most duplicated genes (paralogs) are quickly erased during evolution, and only some are retained. Yet, gene and genome duplications are connected to the evolution of genetic and, in turn, morphological complexity. Plants are especially prone to experience polyploidizations and to enhance their gene repertoire after such events. Genes encoding proteins involved in transcriptional regulation are of especial interest since they are correlated with the occurrence of genome duplication events and with the rise of plant morphological complexity. Here, I review what we know about paralog retention as a driver for morphogenetic evolution of plants. The main focus is on the evolution of plant genes controlling development (morphogenetic transcription factors).
Out of a hundred sequenced and published land plant genomes, four are not of flowering plants. This severely skewed taxonomic sampling hinders our comprehension of land plant evolution at large. ...Moreover, most genetically accessible model species are flowering plants as well. If we are to gain a deeper understanding of how plants evolved and still evolve, and which of their developmental patterns are ancestral or derived, we need to study a more diverse set of plants. Here, I thus argue that we need to sequence genomes of so far neglected lineages, and that we need to develop more non-seed plant model species.
Approximately 500 Ma ago, freshwater algae adapted to live on Earth’s surface, subsequently enabling animal life to pursue. Over the last decade, genomes of non-seed plants enabled us to infer trait ...evolution of early land plants. In this issue of Cell, Jiao et al. uncovered another genome, of the streptophyte algae Penium, enhancing our understanding of the water-to-land transition.
Approximately 500 Ma ago, freshwater algae adapted to live on Earth’s surface, subsequently enabling animal life to pursue. Over the last decade, genomes of non-seed plants enabled us to infer trait evolution of early land plants. In this issue of Cell, Jiao et al. uncovered another genome, of the streptophyte algae Penium, enhancing our understanding of the water-to-land transition.
Studies of P. patens, a powerful non-seed plant model system, have made fundamental contributions to diverse fields, including evolutionary developmental and cell biology.
Abstract
Since the ...discovery two decades ago that transgenes are efficiently integrated into the genome of Physcomitrella patens by homologous recombination, this moss has been a premier model system to study evolutionary developmental biology questions, stem cell reprogramming, and the biology of nonvascular plants. P. patens was the first non-seed plant to have its genome sequenced. With this level of genomic information, together with increasing molecular genetic tools, a large number of reverse genetic studies have propelled the use of this model system. A number of technological advances have recently opened the door to forward genetics as well as extremely efficient and precise genome editing in P. patens. Additionally, careful phylogenetic studies with increased resolution have suggested that P. patens emerged from within Physcomitrium. Thus, rather than Physcomitrella patens, the species should be named Physcomitrium patens. Here we review these advances and describe the areas where P. patens has had the most impact on plant biology.
The WOX genes form a plant-specific subclade of the eukaryotic homeobox transcription factor superfamily, which is characterized by the presence of a conserved DNA-binding homeodomain. The analysis ...of WOX gene expression and function shows that WOX family members fulfill specialized functions in key developmental processes in plants, such as embryonic patterning, stem-cell maintenance and organ formation. These functions can be related to either promotion of cell division activity and/or prevention of premature cell differentiation. The phylogenetic tree of the plant WOX proteins can be divided into three clades, termed the WUS, intermediate and ancient clade. WOX proteins of the WUS clade appear to some extent able to functionally complement other members. The specific function of individual WOX-family proteins is most probably determined by their spatiotemporal expression pattern and probably also by their interaction with other proteins, which may repress their transcriptional activity. The prototypic WOX-family member WUS has recently been shown to act as a bifunctional transcription factor, functioning as repressor in stem-cell regulation and as activator in floral patterning. Past research has mainly focused on part of the WOX protein family in some model flowering plants, such as Arabidopsis thaliana (thale cress) or Oryza sativa (rice). Future research, including so-far neglected clades and non-flowering plants, is expected to reveal how these master switches of plant differentiation and embryonic patterning evolved and how they fulfill their function.
The key structures and functions of land plants are most often studied in flowering plant models. However, the evolution of these traits (character states) is often difficult to infer, because we ...lack an accurate phylogenetic frame of reference. The potential branching order of the earliest land plants has now been further condensed, narrowing down potential reference frameworks for comparative studies.
The key structures and functions of land plants are most often studied in flowering plant models. However, the evolution of these traits (character states) is often difficult to infer, because we lack an accurate phylogenetic frame of reference. The potential branching order of the earliest land plants have now been further condensed, narrowing down potential reference frameworks for comparative studies.
Complex multicellular organisms typically possess life cycles in which zygotes (formed by gamete fusion) and meiosis occur. Canonical animal embryogenesis describes development from zygote to birth. ...It involves polarisation of the egg/zygote, asymmetric cell divisions, establishment of axes, symmetry breaking, formation of organs, and parental nutrition (at least in early stages). Similar developmental patterns have independently evolved in other eukaryotic lineages, including land plants and brown algae. The question arises whether embryo-like structures and associated developmental processes recurrently emerge because they are local optima of the evolutionary landscape. To understand which evolutionary principles govern complex multicellularity, we need to analyse why and how similar processes evolve convergently – von Baer's and Haeckel's phylotypic stage revisited in other phyla.
Complex multicellularity evolved several times independently in eukaryotes.
After 150 years we have some molecular evidence for the hourglass pattern described by Haeckel.
Developmental processes akin to animal embryogenesis are also known in land plants and some other lineages.
Although it involves homologous genes, embryogenesis might not be homologous and it is unclear how and why it evolves.
Growing evidence shows that epigenetic mechanisms contribute to complex traits, with implications across many fields of biology. In plant ecology, recent studies have attempted to merge ecological ...experiments with epigenetic analyses to elucidate the contribution of epigenetics to plant phenotypes, stress responses, adaptation to habitat, and range distributions. While there has been some progress in revealing the role of epigenetics in ecological processes, studies with non‐model species have so far been limited to describing broad patterns based on anonymous markers of DNA methylation. In contrast, studies with model species have benefited from powerful genomic resources, which contribute to a more mechanistic understanding but have limited ecological realism. Understanding the significance of epigenetics for plant ecology requires increased transfer of knowledge and methods from model species research to genomes of evolutionarily divergent species, and examination of responses to complex natural environments at a more mechanistic level. This requires transforming genomics tools specifically for studying non‐model species, which is challenging given the large and often polyploid genomes of plants. Collaboration among molecular geneticists, ecologists and bioinformaticians promises to enhance our understanding of the mutual links between genome function and ecological processes.
The maize smut fungus Ustilago maydis is a model organism for elucidating host colonization strategies of biotrophic fungi. Here, we performed an in depth transcriptional profiling of the entire ...plant-associated development of U. maydis wild-type strains. In our analysis, we focused on fungal metabolism, nutritional strategies, secreted effectors, and regulatory networks. Secreted proteins were enriched in three distinct expression modules corresponding to stages on the plant surface, establishment of biotrophy, and induction of tumors. These modules are likely the key determinants for U. maydis virulence. With respect to nutrient utilization, we observed that expression of several nutrient transporters was tied to these virulence modules rather than being controlled by nutrient availability. We show that oligopeptide transporters likely involved in nitrogen assimilation are important virulence factors. By measuring the intramodular connectivity of transcription factors, we identified the potential drivers for the virulence modules. While known components of the b-mating type cascade emerged as inducers for the plant surface and biotrophy module, we identified a set of yet uncharacterized transcription factors as likely responsible for expression of the tumor module. We demonstrate a crucial role for leaf tumor formation and effector gene expression for one of these transcription factors.
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