Transcriptional repression in stochastic gene expression, patterning, and cell fate specification.

Development is often driven by signaling and lineage-specific cues, yielding highly uniform and reproducible outcomes. Development also involves mechanisms that generate noise in gene expression and random patterns across tissues. Cells sometimes randomly choose between two or more cell fates in a mechanism called stochastic cell fate specification. This process diversifies cell types in otherwise homogenous tissues. Stochastic mechanisms have been extensively studied in prokaryotes where noisy gene activation plays a pivotal role in controlling cell fates. In eukaryotes, transcriptional repression stochastically limits gene expression to generate random patterns and specify cell fates. Here, we review our current understanding of repressive mechanisms that produce random patterns of gene expression and cell fates in flies, plants, mice, and humans.

Current Proteomic and Metabolomic Knowledge of Zygotic and Somatic Embryogenesis in Plants.

Embryogenesis is the primary developmental program in plants. The mechanisms that underlie the regulation of embryogenesis are an essential research subject given its potential contribution to mass in vitro propagation of profitable plant species. Somatic embryogenesis (SE) refers to the use of in vitro techniques to mimic the sexual reproduction program known as zygotic embryogenesis (ZE). In this review, we synthesize the current state of research on proteomic and metabolomic studies of SE and ZE in angiosperms (monocots and dicots) and gymnosperms. The most striking finding was the small number of studies addressing ZE. Meanwhile, the research effort focused on SE has been substantial but disjointed. Together, these research gaps may explain why the embryogenic induction stage and the maturation of the somatic embryo continue to be bottlenecks for efficient and large-scale regeneration of plants. Comprehensive and integrative studies of both SE and ZE are needed to provide the molecular foundation of plant embryogenesis, information which is needed to rationally guide experimental strategies to solve SE drawbacks in each species.

Post-Embryonic Phase Transitions Mediated by Polycomb Repressive Complexes in Plants.

Correct timing of developmental phase transitions is critical for the survival and fitness of plants. Developmental phase transitions in plants are partially promoted by controlling relevant genes into active or repressive status. Polycomb Repressive Complex1 (PRC1) and PRC2, originally identified in Drosophila, are essential in initiating and/or maintaining genes in repressive status to mediate developmental phase transitions. Our review summarizes mechanisms in which the embryo-to-seedling transition, the juvenile-to-adult transition, and vegetative-to-reproductive transition in plants are mediated by PRC1 and PRC2, and suggests that PRC1 could act either before or after PRC2, or that they could function independently of each other. Details of the exact components of PRC1 and PRC2 in each developmental phase transitions and how they are recruited or removed will need to be addressed in the future.

From Plant Survival Under Severe Stress to Anti-Viral Human Defense - A Perspective That Calls for Common Efforts.

Reprogramming of primary virus-infected cells is the critical step that turns viral attacks harmful to humans by initiating super-spreading at cell, organism and population levels. To develop early anti-viral therapies and proactive administration, it is important to understand the very first steps of this process. Plant somatic embryogenesis (SE) is the earliest and most studied model for de novo programming upon severe stress that, in contrast to virus attacks, promotes individual cell and organism survival. We argued that transcript level profiles of target genes established from in vitro SE induction as reference compared to virus-induced profiles can identify differential virus traits that link to harmful reprogramming. To validate this hypothesis, we selected a standard set of genes named 'ReprogVirus'. This approach was recently applied and published. It resulted in identifying 'CoV-MAC-TED', a complex trait that is promising to support combating SARS-CoV-2-induced cell reprogramming in primary infected nose and mouth cells. In this perspective, we aim to explain the rationale of our scientific approach. We are highlighting relevant background knowledge on SE, emphasize the role of alternative oxidase in plant reprogramming and resilience as a learning tool for designing human virus-defense strategies and, present the list of selected genes. As an outlook, we announce wider data collection in a 'ReprogVirus Platform' to support anti-viral strategy design through common efforts.

Do Plasmodesmata Play a Prominent Role in Regulation of Auxin-Dependent Genes at Early Stages of Embryogenesis?

Plasmodesmata form intercellular channels which ensure the transport of various molecules during embryogenesis and postembryonic growth. However, high permeability of plasmodesmata may interfere with the establishment of auxin maxima, which are required for cellular patterning and the development of distinct tissues. Therefore, diffusion through plasmodesmata is not always desirable and the symplastic continuum must be broken up to induce or accomplish some developmental processes. Many data show the role of auxin maxima in the regulation of auxin-responsive genes and the establishment of various cellular patterns. However, still little is known whether and how these maxima are formed in the embryo proper before 16-cell stage, that is, when there is still a nonpolar distribution of auxin efflux carriers. In this work, we focused on auxin-dependent regulation of plasmodesmata function, which may provide rapid and transient changes of their permeability, and thus take part in the regulation of gene expression.

Ancient noeggerathialean reveals the seed plant sister group diversified alongside the primary seed plant radiation.

Noeggerathiales are enigmatic plants that existed during Carboniferous and Permian times, ∼323 to 252 Mya. Although their morphology, diversity, and distribution are well known, their systematic affinity remained enigmatic because their anatomy was unknown. Here, we report from a 298-My-old volcanic ash deposit, an in situ, complete, anatomically preserved noeggerathialean. The plant resolves the group's affinity and places it in a key evolutionary position within the seed plant sister group. Paratingia wuhaia sp. nov. is a small tree producing gymnospermous wood with a crown of pinnate, compound megaphyllous leaves and fertile shoots each with Ω-shaped vascular bundles. The heterosporous (containing both microspores and megaspores), bisporangiate fertile shoots appear cylindrical and cone-like, but their bilateral vasculature demonstrates that they are complex, three-dimensional sporophylls, representing leaf homologs that are unique to Noeggerathiales. The combination of heterospory and gymnospermous wood confirms that Paratingia, and thus the Noeggerathiales, are progymnosperms. Progymnosperms constitute the seed plant stem group, and Paratingia extends their range 60 My, to the end of the Permian. Cladistic analysis resolves the position of the Noeggerathiales as the most derived members of a heterosporous progymnosperm clade that are the seed plant sister group, altering our understanding of the relationships within the seed plant stem lineage and the transition from pteridophytic spore-based reproduction to the seed. Permian Noeggerathiales show that the heterosporous progymnosperm sister group to seed plants diversified alongside the primary radiation of seed plants for ∼110 My, independently evolving sophisticated cone-like fertile organs from modified leaves.

cROStalk for Life: Uncovering ROS Signaling in Plants and Animal Systems, from Gametogenesis to Early Embryonic Development.

This review explores the role of reactive oxygen species (ROS)/Ca2+ in communication within reproductive structures in plants and animals. Many concepts have been described during the last years regarding how biosynthesis, generation products, antioxidant systems, and signal transduction involve ROS signaling, as well as its possible link with developmental processes and response to biotic and abiotic stresses. In this review, we first addressed classic key concepts in ROS and Ca2+ signaling in plants, both at the subcellular, cellular, and organ level. In the plant science field, during the last decades, new techniques have facilitated the in vivo monitoring of ROS signaling cascades. We will describe these powerful techniques in plants and compare them to those existing in animals. Development of new analytical techniques will facilitate the understanding of ROS signaling and their signal transduction pathways in plants and mammals. Many among those signaling pathways already have been studied in animals; therefore, a specific effort should be made to integrate this knowledge into plant biology. We here discuss examples of how changes in the ROS and Ca2+ signaling pathways can affect differentiation processes in plants, focusing specifically on reproductive processes where the ROS and Ca2+ signaling pathways influence the gametophyte functioning, sexual reproduction, and embryo formation in plants and animals. The study field regarding the role of ROS and Ca2+ in signal transduction is evolving continuously, which is why we reviewed the recent literature and propose here the potential targets affecting ROS in reproductive processes. We discuss the opportunities to integrate comparative developmental studies and experimental approaches into studies on the role of ROS/ Ca2+ in both plant and animal developmental biology studies, to further elucidate these crucial signaling pathways.

ROS and Ions in Cell Signaling during Sexual Plant Reproduction.

Pollen grain is a unique haploid organism characterized by two key physiological processes: activation of metabolism upon exiting dormancy and polar tube growth. In gymnosperms and flowering plants, these processes occur in different time frames and exhibit important features; identification of similarities and differences is still in the active phase. In angiosperms, the growth of male gametophyte is directed and controlled by its microenvironment, while in gymnosperms it is relatively autonomous. Recent reviews have detailed aspects of interaction between angiosperm female tissues and pollen such as interactions between peptides and their receptors; however, accumulated evidence suggests low-molecular communication, in particular, through ion exchange and ROS production, equally important for polar growth as well as for pollen germination. Recently, it became clear that ROS and ionic currents form a single regulatory module, since ROS production and the activity of ion transport systems are closely interrelated and form a feedback loop.

Plant Cell and Organism Development.

Plants represent a unique and fascinating group of living organisms [...].

Current Perspectives on the Auxin-Mediated Genetic Network that Controls the Induction of Somatic Embryogenesis in Plants.

Auxin contributes to almost every aspect of plant development and metabolism as well as the transport and signalling of auxin-shaped plant growth and morphogenesis in response to endo- and exogenous signals including stress conditions. Consistently with the common belief that auxin is a central trigger of developmental changes in plants, the auxin treatment of explants was reported to be an indispensable inducer of somatic embryogenesis (SE) in a large number of plant species. Treating in vitro-cultured tissue with auxins (primarily 2,4-dichlorophenoxyacetic acid, which is a synthetic auxin-like plant growth regulator) results in the extensive reprogramming of the somatic cell transcriptome, which involves the modulation of numerous SE-associated transcription factor genes (TFs). A number of SE-modulated TFs that control auxin metabolism and signalling have been identified, and conversely, the regulators of the auxin-signalling pathway seem to control the SE-involved TFs. In turn, the different expression of the genes encoding the core components of the auxin-signalling pathway, the AUXIN/INDOLE-3-ACETIC ACIDs (Aux/IAAs) and AUXIN RESPONSE FACTORs (ARFs), was demonstrated to accompany SE induction. Thus, the extensive crosstalk between the hormones, in particular, auxin and the TFs, was revealed to play a central role in the SE-regulatory network. Accordingly, LEAFY COTYLEDON (LEC1 and LEC2), BABY BOOM (BBM), AGAMOUS-LIKE15 (AGL15) and WUSCHEL (WUS) were found to constitute the central part of the complex regulatory network that directs the somatic plant cell towards embryogenic development in response to auxin. The revealing picture shows a high degree of complexity of the regulatory relationships between the TFs of the SE-regulatory network, which involve direct and indirect interactions and regulatory feedback loops. This review examines the recent advances in studies on the auxin-controlled genetic network, which is involved in the mechanism of SE induction and focuses on the complex regulatory relationships between the down- and up-stream targets of the SE-regulatory TFs. In particular, the outcomes from investigations on Arabidopsis, which became a model plant in research on genetic control of SE, are presented.

The mechanism and function of active DNA demethylation in plants.

DNA methylation is a conserved and important epigenetic mark in both mammals and plants. DNA methylation can be dynamically established, maintained, and removed through different pathways. In plants, active DNA demethylation is initiated by the RELEASE OF SILENCING 1 (ROS1) family of bifunctional DNA glycosylases/lyases. Accumulating evidence suggests that DNA demethylation is important in many processes in plants. In this review, we summarize recent studies on the enzymes and regulatory factors that have been identified in the DNA demethylation pathway. We also review the functions of active DNA demethylation in plant development as well as biotic and abiotic stress responses. Finally, we highlight those aspects of DNA demethylation that require additional research.

The Phloem as a Mediator of Plant Growth Plasticity.

Developmental plasticity, defined as the capacity to respond to changing environmental conditions, is an inherent feature of plant growth. Recent studies have brought the phloem tissue, the quintessential conduit for energy metabolites and inter-organ communication, into focus as an instructive developmental system. Those studies have clarified long-standing questions about essential aspects of phloem development and function, such as the pressure flow hypothesis, mechanisms of phloem unloading, and source-sink relationships. Interestingly, plants with impaired phloem development show characteristic changes in body architecture, thereby highlighting the capacity of the phloem to integrate environmental cues and to fine-tune plant development. Therefore, understanding the plasticity of phloem development provides scenarios of how environmental stimuli are translated into differential plant growth. In this Review, we summarize novel insights into how phloem identity is established and how phloem cells fulfil their core function as transport units. Moreover, we discuss possible interfaces between phloem physiology and development as sites for mediating the plastic growth mode of plants.

BABY BOOM (BBM): a candidate transcription factor gene in plant biotechnology.

Plants have evolved a number of transcription factors, many of which are implicated in signaling pathways as well as regulating diverse cellular functions. BABY BOOM (BBM), transcription factors of the AP2/ERF family are key regulators of plant cell totipotency. Ectopic expression of the BBM gene, originally identified in Brassica napus, has diverse functions in plant cell proliferation, growth and development without exogenous growth regulators. The BBM gene has been implicated to play an important role as a gene marker in multiple signaling developmental pathways in plant development. This review focuses on recent advances in our understanding of a member of the AP2 family of transcription factor BBM in plant biotechnology including plant embryogenesis, cell proliferation, regeneration, plant transformation and apogamy. Recent discoveries about the BBM gene will inevitably help to unlock the long-standing mysteries of different biological mechanisms of plant cells.

The Dead Can Nurture: Novel Insights into the Function of Dead Organs Enclosing Embryos.

Plants have evolved a variety of dispersal units whereby the embryo is enclosed by various dead protective layers derived from maternal organs of the reproductive system including seed coats (integuments), pericarps (ovary wall, e.g., indehiscent dry fruits) as well as floral bracts (e.g., glumes) in grasses. Commonly, dead organs enclosing embryos (DOEEs) are assumed to provide a physical shield for embryo protection and means for dispersal in the ecosystem. In this review article, we highlight recent studies showing that DOEEs of various species across families also have the capability for long-term storage of various substances including active proteins (hydrolases and ROS detoxifying enzymes), nutrients and metabolites that have the potential to support the embryo during storage in the soil and assist in germination and seedling establishment. We discuss a possible role for DOEEs as natural coatings capable of "engineering" the seed microenvironment for the benefit of the embryo, the seedling and the growing plant.

Analysis of microRNA reveals cleistogamous and chasmogamous floret divergence in dimorphic plant.

Cleistogenes songorica, a grass species that exhibits two spatially different type of inflorescence, chastogamy (CH), flowers localized at the top, and cleistogamy (CL) flowers embedded in leaf sheath. This study aimed at dissecting reasons underlying these distinct floral development patterns at morphological and microRNA level. Phenotyping for CH and CL was conducted and four small RNA libraries were constructed from the CH and CL flowers for high-throughput sequencing to identify the differentiated miRNAs. As results, spikelet, stigma, anther, lemma and lodicule length of CH flowers were found larger than that of CL, and so was seed setting. Also, 17 flower-related differential expression miRNAs were identified which were associated with floral organ development and morphogenesis, and the flower development. Further results showed that miR159a.1-CL3996.Contig2 pair was related to anther development, miR156a-5p-CL1954.Contig2 was linked to response to high light intensity, miR408-3p/miR408d-Unigene429 was related to pollination and Unigene429 positively regulated flower development. To our knowledge, this is the first study on differential miRNA accumulation between CH and CL flowers and our study serves as a foundation to the future elucidation of regulatory mechanisms of miRNAs in the divergent development of CL and CH flowers in a single plant.

The suspensor as a model system to study the mechanism of cell fate specification during early embryogenesis.

KEY MESSAGE: The advances in the suspensor. During early embryogenesis, the proembryo consists of two domains, the embryo proper and the suspensor. Unlike the embryo proper, which has been investigated extensively, research on the suspensor has been limited in past decades. Recent studies have revealed that the suspensor plays an important role in early embryogenesis and the process of suspensor formation and degeneration may provide a unique model for studies on cell division pattern, cell fate determination, and cell death. In this review, we briefly summarize the advances in research on the suspensor, which provide new insight in our understanding of the mechanism of early embryogenesis and show great potential for a unique model for future investigations.

Insights from Proteomic Studies into Plant Somatic Embryogenesis.

Somatic embryogenesis is a biotechnological approach mainly used for the clonal propagation of different plants worldwide. In somatic embryogenesis, embryos arise from somatic cells under appropriate culture conditions. This plasticity in plants is a demonstration of true cellular totipotency and is the best approach among the genetic transformation protocols used for plant regeneration. Despite the importance of somatic embryogenesis, knowledge regarding the control of the somatic embryogenesis process is limited. Therefore, the elucidation of both the biochemical and molecular processes is important for understanding the mechanisms by which a single somatic cell becomes a whole plant. Modern proteomic techniques rely on an alternative method for the identification and quantification of proteins with different abundances in embryogenic cell cultures or somatic embryos and enable the identification of specific proteins related to somatic embryogenesis development. This review focuses on somatic embryogenesis studies that use gel-free shotgun proteomic analyses to categorize proteins that could enhance our understanding of particular aspects of the somatic embryogenesis process and identify possible targets for future studies.

Plant embryogenesis.

Land plants are called 'embryophytes' and thus, their collective name is defined by their ability to form embryos. Indeed, embryogenesis is a widespread phenomenon in plants, and much of our diet is composed of embryos (just think of grains, beans or nuts; Figure 1). However, in addition to embryos as a source of nutrition, they are also a fascinating study object. Some of the most fundamental decisions on fate and identity, as well as patterning and morphogenesis, are taken during the first days of plant life. Yet, embryos are diverse in structure and function, and embryogenesis in plants is by no means restricted to the zygote - the product of fertilization. In this Primer, we discuss the adventures of the young plant. We will consider what it means to be a plant embryo and how to become one. We will next highlight how the study of early embryogenesis can reveal principles underlying oriented cell division and developmental pattern formation in plants.

Functions of IQD proteins as hubs in cellular calcium and auxin signaling: A toolbox for shape formation and tissue-specification in plants?

Calcium (Ca2+) ions play pivotal roles as second messengers in intracellular signal transduction, and coordinate many biological processes. Changes in intracellular Ca2+ levels are perceived by Ca2+ sensors such as calmodulin (CaM) and CaM-like (CML) proteins, which transduce Ca2+ signals into cellular responses by regulation of diverse target proteins. Insights into molecular functions of CaM targets are thus essential to understand the molecular and cellular basis of Ca2+ signaling. During the last decade, IQ67-domain (IQD) proteins emerged as the largest class of CaM targets in plants with mostly unknown functions. In the March issue of Plant Physiology, we presented the first comprehensive characterization of the 33-membered IQD family in Arabidopsis thaliana. We showed, by analysis of the subcellular localization of translational green fluorescent protein (GFP) fusion proteins, that most IQD members label microtubules (MTs), and additionally often localize to the cell nucleus or to membranes, where they recruit CaM Ca2+ sensors. Important functions at MTs are supported by altered MT organization and plant growth in IQD gain-of-function lines. Because IQD proteins share structural hallmarks of scaffold proteins, we propose roles of IQDs in the assembly of macromolecular complexes to orchestrate Ca2+ CaM signaling from membranes to the nucleus. Interestingly, expression of several IQDs is regulated by auxin, which suggests functions of IQDs as hubs in cellular auxin and calcium signaling to regulate plant growth and development.

Regulation of Plant Cellular and Organismal Development by SUMO.

This chapter clearly demonstrates the breadth and spectrum of the processes that SUMO regulates during plant development. The gross phenotypes observed in mutants of the SUMO conjugation and deconjugation enzymes reflect these essential roles, and detailed analyses of these mutants under different growth conditions revealed roles in biotic and abiotic stress responses, phosphate starvation, nitrate and sulphur metabolism, freezing and drought tolerance and response to excess copper. SUMO functions also intersect with those regulated by several hormones such as salicylic acid , abscisic acid , gibberellins and auxin, and detailed studies provide mechanistic clues of how sumoylation may regulate these processes. The regulation of COP1 and PhyB functions by sumoylation provides very strong evidence that SUMO is heavily involved in the regulation of light signaling in plants. At the cellular and subcellular levels, SUMO regulates meristem architecture, the switch from the mitotic cycle into the endocycle, meiosis, centromere decondensation and exit from mitosis, transcriptional control, and release from transcriptional silencing. Most of these advances in our understanding of SUMO functions during plant development emerged over the past 6-7 years, and they may only predict a prominent rise of SUMO as a major regulator of eukaryotic cellular and organismal growth and development.