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Three main waves of chromatin dynamics during plant reproduction (Model). Sexual plant reproduction can be seen as a three-step process involving sporogenesis, gametogenesis, and embryogenesis taking place in floral organs. Sporogenesis initiates with the specification of spore mother cells (SMCs) within the sporangium tissues. SMCs are primed toward meiosis while undergoing a somatic-to-reproductive cellular fate transition that generates a pluripotent spore. The spore develops a (male or female) multicellular gametophyte generating distinct cell types: the companion (or accessory) cells and the gametic cells (a schematically reduced form is shown, for more details see Figure 1). Fertilization enables the formation of a totipotent zygote, generating in turn the plant embryo. The acquisition of the SMC fate, the gametic fate and the totipotent zygotic fate is associated with three main waves of chromatin dynamics (I.–III., colored nuclei) comprising large-scale reorganization of the chromatin structure, composition and organization, hence reshaping the epigenetic landscape (as reviewed in the text). Whereas some of those events clearly contribute to cell fate establishment (e.g., I., see the text), the challenge of future investigations is to elucidate the functional role of chromatin dynamics in defining the cells’ potency versus operating cell fate establishment during sexual reproduction.
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Plants have the remarkable ability to establish new cell fates throughout their life cycle, in contrast to most animals that define all cell lineages during embryogenesis. This ability is exemplified during sexual reproduction in flowering plants where novel cell types are generated in floral tissues of the adult plant during sporogenesis, gametoge...
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... Recently, it has been shown that maternally biosynthesized auxin in the fertilized ovules also provides a source of auxin for the early-stage zygotic embryo . However, whether auxin is important directly following fertilization, when the highly specialized, meiotically programmed egg cell is transformed into a totipotent mitotically active embryonic cell (She & Baroux, 2014), is still not known. Similarly, polar auxin transport has been shown to play a vital role in Arabidopsis embryo patterning (i.e. ...
Somatic embryogenesis (SE), or embryo development from in vitro cultured vegetative explants, can be induced in Arabidopsis by the synthetic auxin 2,4-dichlorophenoxyacetic acid (2,4-D) or by overexpression of specific transcription factors, like AT-HOOK MOTIF NUCLEAR LOCALIZED 15 (AHL15). Here we explored the role of endogenous auxin (indole-3-acetic acid or IAA) during 2,4-D and AHL15-induced SE. Using the pWOX2:NLS-YFP reporter we identified three distinct developmental stages for 2,4-D and AHL15-induced SE in Arabidopsis, these being 1) acquisition of embryo identity, 2) formation of pro-embryos and 3) somatic embryo patterning and development. Acquisition of embryo identity coincided with enhanced expression of the IPyA auxin biosynthesis YUCCA genes, resulting in an enhanced pDR5:GFP-reported auxin response in the embryo-forming tissues. Chemical inhibition of the IPyA pathway did not affect the acquisition of embryo identity, but significantly reduced or completely inhibited the formation of pro-embryos. Co-application of IAA with auxin biosynthesis inhibitors in the AHL15-induced SE system rescued differentiated somatic embryo formation, confirming that increased IAA levels are important during the last two stages of SE. Our analyses also showed that polar auxin transport, with AUX/LAX influx and PIN1 efflux carriers as important drivers, is required for the transition of embryonic cells to proembryos and, later, for correct cell fate specification and differentiation. Taken together, our results indicate that endogenous IAA biosynthesis and its polar transport are not required for the acquisition of embryo identity, but rather to maintain embryonic cell identity and for the formation of multicellular proembryos and their development into histodifferentiated embryos.
... Recent studies revealed extensive dynamics in plant nuclear and chromosomal organization [1][2][3]. Plant chromosome and chromatin are very dynamic during sexual reproduction, where different stages are quickly substituted for one another and many events occur in a small number of highly specialized cells [4][5][6]. The process starts with meiosis, continues through gametogenesis and fertilization, and finally seed development. ...
Chromatin-based processes are essential for cellular functions. Structural maintenance of chromosomes (SMCs) are evolutionarily conserved molecular machines that organize chromosomes throughout the cell cycle, mediate chromosome compaction, promote DNA repair, or control sister chromatid attachment. The SMC5/6 complex is known for its pivotal role during the maintenance of genome stability. However, a dozen recent plant studies expanded the repertoire of SMC5/6 complex functions to the entire plant sexual reproductive phase. The SMC5/6 complex is essential in meiosis, where its activity must be precisely regulated to allow for normal meiocyte development. Initially, it is attenuated by the recombinase RAD51 to allow for efficient strand invasion by the meiosis-specific recombinase DMC1. At later stages, it is essential for the normal ratio of interfering and non-interfering crossovers, detoxifying aberrant joint molecules, preventing chromosome fragmentation, and ensuring normal chromosome/sister chromatid segregation. The latter meiotic defects lead to the production of diploid male gametes in Arabidopsis SMC5/6 complex mutants, increased seed abortion, and production of triploid offspring. The SMC5/6 complex is directly involved in controlling normal embryo and endosperm cell divisions, and pioneer studies show that the SMC5/6 complex is also important for seed development and normal plant growth in cereals.
... 2) with strong expression differences between males, females, and androhermaphrodites suggests that these genes may have a role in regulation of several pathways related to sex expression differences in S. latifolia. These genes may, among other functions, have a role in flower development as shown in other plant species (Vanyushin and Ashapkin, 2011;She and Baroux, 2014). Further, DNA damage-and stressrelated homologous genes, which were previously shown to be expressed in Arabidopsis as responsive to chemical treatment Nowicka et al., 2020), were expressed only in NT males compared with females and androhermaphrodites (i.e. ...
Dioecious plants possess diverse sex determination systems and unique mechanisms of reproductive organ development; however, little is known about how sex-linked genes shape the expression of regulatory cascades that lead to developmental differences between sexes. In Silene latifolia, a dioecious plant with stable dimorphism in floral traits, early experiments suggested that female-regulator genes act on the factors that determine the boundaries of the flower whorls. To identify these regulators, we sequenced the transcriptome of male flowers with fully developed gynoecia, induced by rapid demethylation in the parental generation. Eight candidates were found to have a positive role in gynoecium promotion, floral organ size, whorl boundary, and affect the expression of class B MADS-box flower genes. To complement our transcriptome analysis, we closely examined the floral organs in their native state using a field emission environmental scanning electron microscopy, and examined the differences between females and androhermaphrodites in their placenta and ovule organization. Our results reveal the regulatory pathways potentially involved in sex-specific flower development in the classical model of dioecy, S. latifolia. These pathways include previously hypothesized and unknown female-regulator genes that act on the factors that determine the flower boundaries, and negative regulator of anther development, SUPERMAN-like (SlSUP).
... During plant sexual reproduction, a variety of epigenetic memories and chromatin modifications acquired in response to both developmental and environmental cues before the establishment of reproductive lineage need to be reprogrammed to ensure the integrity of genetic information between generations (Borg et al., 2020;Ono and Kinoshita, 2021). Reprogramming of histone methylation during plant sexual reproduction has been shown to be required for resetting the chromatin status toward pluri-or totipotency in gametes and the zygote, thus ensuring to establish new cell fates during plant sexual reproduction (Feng et al., 2010;Gutierrez-Marcos and Dickinson, 2012;Kawashima and Berger, 2014;She and Baroux, 2014;Borg et al., 2020). ...
... Gametophyte generation, including sporogenesis and gametogenesis, involves a series of cell division and differentiation, and the consequent zygote resulted from fertilization has the totipotency to develop into a future seedling. Consequently, plants undergo global chromatin re-organization during sexual reproduction to develop into highly distinct cell types and establish cell pluri-or totipotency, in which the reprogramming of histone modifications plays a vital role (Kawashima and Berger, 2014;She and Baroux, 2014). ...
... Plant sexual reproduction consists of three different phases: sporogenesis, gametogenesis, embryo-and endosperm-genesis. Plant reproduction initiates with sporogenesis, and it is characterized by the generation of meiotic-competent spore mother cells (SMCs), namely SMC differentiation (Kawashima and Berger, 2014;She and Baroux, 2014). The male SMCs, also known as pollen mother cells (PMCs) (2n), are differentiated in the sporangium and formed in the anther locule, then undergo meiosis to give rise to four haploid microspores (1n). ...
Plants undergo extensive reprogramming of chromatin status during sexual reproduction, a process vital to cell specification and pluri- or totipotency establishment. As a crucial way to regulate chromatin organization and transcriptional activity, histone modification can be reprogrammed during sporogenesis, gametogenesis, and embryogenesis in flowering plants. In this review, we first introduce enzymes required for writing, recognizing, and removing methylation marks on lysine residues in histone H3 tails, and describe their differential expression patterns in reproductive tissues, then we summarize their functions in the reprogramming of H3 lysine methylation and the corresponding chromatin re-organization during sexual reproduction in Arabidopsis, and finally we discuss the molecular significance of histone reprogramming in maintaining the pluri- or totipotency of gametes and the zygote, and in establishing novel cell fates throughout the plant life cycle. Despite rapid achievements in understanding the molecular mechanism and function of the reprogramming of chromatin status in plant development, the research in this area still remains a challenge. Technological breakthroughs in cell-specific epigenomic profiling in the future will ultimately provide a solution for this challenge.
... One to two microliters of nuclei suspension was used for immunostaining. Immunostaining on isolated nucleus, dissected embryos, and whole-mount ovules was performed according to (69) with minor modifications. Immunostained samples were mounted with ProLong Gold antifade with DAPI (Thermo Fisher Scientific) before imaging. ...
Wide crosses result in postzygotic elimination of one parental chromosome set, but the mechanisms that result in such differential fate are poorly understood. Here, we show that alterations of centromeric histone H3 (CENH3) lead to its selective removal from centromeres of mature Arabidopsis eggs and early zygotes, while wild-type CENH3 persists. In the hybrid zygotes and embryos, CENH3 and essential centromere proteins load preferentially on the CENH3-rich centromeres of the wild-type parent, while CENH3-depleted centromeres fail to reconstitute new CENH3-chromatin and the kinetochore and are frequently lost. Genome elimination is opposed by E3 ubiquitin ligase VIM1. We propose a model based on cooperative binding of CENH3 to chromatin to explain the differential CENH3 loading rates. Thus, parental CENH3 polymorphisms result in epigenetically distinct centromeres that instantiate a strong mating barrier and produce haploids.
... Fruit ripening Recent breakthroughs suggest that the whole process of fruit development starting from seed formation is strictly regulated by genetic and epigenetic mechanisms. Nonetheless, several evidence suggests a complex reprogramming of the chromatin states already in the early stages of the fertilization process, with a global meiocyte chromatin state remodeling, by creating a balance between permissiveassociated marks such as histone 3 lysine 4 trimethylation (H3K4me3) and H3K9ac and repressive-related marks such as H3K27me1, H3K27me3 and H3K9me1 (She et al., 2013;She and Baroux, 2014). In Citrus, epigenetic marks DNA 5mC and histone modifications have been revealed to regulate flowering by the presence of developing fruits that initiated with environmental factors in the previous season (Agustí et al., 2020). ...
Our era has witnessed tremendous technique advances and mechanically epigenetic improvement in plant epige-netics, mainly including histone post-translational modifications (PTMs) and DNA methylation, which have been characterized as playing vital roles in development processes and plant response to environmental factors. Recently , chemical modifications on RNAs like 5-methylcytosine (m 5 C) and N6-methyladenosine (m 6 A) have been revealed as a new layer of epigenetic marks to regulate gene translation efficiency in model plant Arabidopsis thaliana and with later discovery of horticultural species like tomato (Solanum lycopersicum) and poplar (Populus trichocarpa). In model plants, these epigenetic modifications on DNA, RNA, and histone tails largely trigger innumerable studies on how epigenetic mechanisms are involved in gene regulation and biological functions. As an emerging research field in horticultural plants, epigenetic modifications have bloomed in fruit development and ripening, grafting, and bud dormancy. In this Review, we have demonstrated recent advances of high-throughput sequencing methods, summarized epigenetic enzymatic systems to install, remove and recognize epigenetic marks, discussed essential roles of epigenetic regulation, and proposed how innovative computation techniques like machine learning and deep learning are set to understanding epigenetic regulation mechanisms in horticultural plants. We also raise future perspectives on how epigenetic modifications act as new additions for understanding their roles in gene expression that is required for development and environmental adaptation in horticultural plants.
... Late segregation of the germline, common in plants but also found in metazoans such as snails, sea urchins, sponges, and cnidarians [26], results in a long period during which environmentally induced epigenetic changes can be incorporated [16]. DNA methylation and histone modifications are maintained during sexual reproduction in plants, although some reprogramming occurs [27,28]. Thus, late germline segregation should increase the potential for epigenetic inheritance. ...
Epigenetic inheritance is another piece of the puzzle of nongenetic inheritance, although the prevalence, sources, persistence, and phenotypic consequences of heritable epigenetic marks across taxa remain unclear. We systematically reviewed over 500 studies from the past 5 years to identify trends in the frequency of epigenetic inheritance due to differences in reproductive mode and germline development. Genetic, intrinsic (e.g., disease), and extrinsic (e.g., environmental) factors were identified as sources of epigenetic inheritance, with impacts on phenotype and adaptation depending on environmental predictability. Our review shows that multigenerational persistence of epigenomic patterns is common in both plants and animals, but also highlights many knowledge gaps that remain to be filled. We provide a framework to guide future studies towards understanding the generational persistence and eco-evolutionary significance of epigenomic patterns.
... ; https://doi.org/10.1101/2021.08.06.455432 doi: bioRxiv preprint Endogenous auxin in Arabidopsis somatic embryos 4 The first phase of the plant life cycle starts with the fusion of the male and female gametes 105 during fertilization to generate the zygote. This developmental switch, which is defined as 106 gametophyte-to-zygotic transition, coincides with one of the most complex cellular 107 reprogramming events, transforming the highly specialized, meiotically programmed egg cell 108 into a totipotent mitotically active embryonic cell (She and Baroux, 2014) and efflux carriers in controlling embryo development (Robert et al., 2015). 128 ...
Somatic embryogenesis (SE) is the process by which embryos develop from in vitro cultured vegetative tissue explants. The synthetic auxin 2,4-dichlorophenoxyacetic acid (2,4-D) is widely used for SE induction, but SE can also be induced by overexpression of specific transcription factors, such as AT-HOOK MOTIF NUCLEAR LOCALIZED 15 (AHL15). 2,4-D and AHL15 both trigger the biosynthesis of the natural auxin indole-3-acetic acid (IAA). However, the role of this endogenously produced auxin in SE is yet not well understood. In this study we show that the induction of embryonic stem cells from explants does not require IAA biosynthesis, whereas an increase in IAA levels is essential to maintain embryo identity and for embryo formation from these stem cells. Further analysis showed that YUCCA ( YUC ) genes involved in the IPyA auxin biosynthesis pathway are up-regulated in embryo-forming tissues. Chemical inhibition of the IPyA pathway significantly reduced or completely inhibited the formation of somatic embryos in both 2,4-D-and AHL15-dependent systems. In the latter system, SE could be restored by exogenous IAA application, confirming that the biosynthesis-mediated increase in IAA levels is important. Our analyses also showed that PIN1 and AUX1 are the major auxin carriers that determine respectively auxin efflux and influx during SE. This auxin transport machinery is required for the proper transition of embryonic cells to proembryos and, later, for correct cell fate specification and differentiation. Taken together, our results indicate that auxin biosynthesis in conjunction with its polar transport are required during SE for multicellular somatic proembryo development and differentiation.
One sentence summary
Somatic embryogenesis in Arabidopsis requires auxin biosynthesis and polar auxin transport only after the acquisition of embryonic competence for somatic proembryo development and differentiation.
... A cell lineage committed to producing gametes (the germline sensu stricto) is specified late in sporophyte development. However, whether the plant germline initiates with spore mother cell formation (Grossniklaus, 2011;She and Baroux, 2014), or with the mature gametophyte (Berger and Twell, 2011), is still a matter of debate. It is also unclear when exactly plant germline is separated from somatic lineages (Lanfear, 2018). ...
A genetic continuity of living organisms relies on the germline which is a specialized cell lineage producing gametes. Essential in the germline functioning is the protection of genetic information that is subjected to spontaneous mutations. Due to indeterminate growth, late specification of the germline, and unique longevity, plants are expected to accumulate somatic mutations during their lifetime that leads to decrease in individual and population fitness. However, protective mechanisms, similar to those in animals, exist in plant shoot apical meristem (SAM) allowing plants to reduce the accumulation and transmission of mutations. This review describes cellular- and tissue-level mechanisms related to spatio-temporal distribution of cell divisions, organization of stem cell lineages, and cell fate specification to argue that the SAM functions analogous to animal germline.
... DNA methylation plays important roles in regulating genome imprinting and gene expression in plant sexual reproduction (Jullien and Berger, 2010;She and Baroux, 2014). It is hypothesized that DNA methylation reprogramming in the zygote and early stage of embryos after fertilization is important to maintain genome integrity in the embryos (Kawashima and Berger, 2014). ...
Orchids have evolved a specialized reproductive program. During embryogenesis, the zygote undergoes programmed cell division and produces a tubular-shaped embryo that does not undergo organogenesis and fails to form an embryogenic leaf (cotyledon) or root apical meristem. Upon germination, the tubular embryo emerges and grows into a structure that is referred to as the protocorm. Despite the absence of a pre-established body plan, the anterior end of the protocorm becomes active and forms shoot apical meristems after germination. However, the molecular mechanisms that have evolved to establish the unique structures and unparalleled developmental programs are largely unclear. Recently, we conducted a comparative transcriptomic study to capture the dynamic gene expression profiles of reproductive tissues at different developmental stages in Phalaenopsis aphrodite. Our data provide evidence suggesting that the distinct molecular signatures are associated with different reproductive tissues. These experiments demonstrate that comparative genome-wide gene expression study is a powerful approach to molecularly characterize tissues or organs whose molecular identity is unclear. Importantly, our data provide crucial evidence that the protocorm and protocorm-like body (PLB) share similar transcriptome dynamics but are molecularly distinct from zygotic embryonic tissues. This study challenges the previous understanding that PLBs are of embryonic origin. Moreover, we hypothesize that SHOOT MERISTEMLESS, a class I KNOTTED-LIKE HOMEOBOX gene, may play a role during PLB regeneration. In this chapter, I summarize the specialized reproductive development of orchids and delineate recent progress in deciphering the molecular mechanisms of reproductive development of P. aphrodite. I also discuss the developmental origin of the PLB and its difference from that of the protocorm and somatic embryo.
