Recent Advances in Plant Cell Nuclear Signaling

Abstract

In plants, a growing amount of evidence suggests an important role for the nucleus in the establishment of developmental and adaptive processes. Recent years have contributed to an increase in the knowledge about the nuclear compartment that has been considered for a long time as an organelle in which only mechanisms such as transcription and DNA replication occurred. The scenario appears now largely more complicated, in that the nucleus has been shown to harbor a number of partially autonomous regulatory mechanisms, to such an extent that some authors claimed that the nucleus is ‘a cell within a cell’ (Rodrigues et al., 2009Rodrigues M.A Gomes D.A Nathanson M.H Leite M.F Nuclear calcium signaling: a cell within a cell.Braz. J. Med. Biol. Res. 2009; 42: 17-20Crossref PubMed Scopus (29) Google Scholar). In 2010, Molecular Plant published a special issue bringing together a series of articles on the plant nucleus organization and functions (Volume 3, Number 4, 2010). Here, we give a short highlight of these different reviews that we complement with the most recent advances in this fast-moving field. The readers are also invited to refer to the Focus Issue recently published in Plant Physiology (Cheung and Reddy, 2012Cheung A.Y Reddy A.S.N Nuclear architecture and dynamics: territories, nuclear bodies, and nucleocytoplasmic trafficking.Plant Physiol. 2012; 158: 23-25Crossref PubMed Scopus (8) Google Scholar). The nuclear envelope surrounding the nucleoplasm is formed by the inner and outer nuclear membranes, delimiting the perinuclear space. These two distinct membranes are periodically fused at nuclear pore complexes, which are the largest protein assemblies in eukaryotic cells (up to 60 MDa). They are composed of multimers of a set of 30 nucleoporins arranged according to an eightfold radial symmetry. This structure delineates a 9–10-nm-large central pore allowing the selective fluxes of ions and macromolecules such as proteins (<40 KDa), RNAs, and RNA–protein complexes between the cytosol and the nucleoplasm (reviewed by Matzke et al., 2010Matzke A.J.M Weiger T.M Matzke A Ion channels at the nucleus: electrophysiology meets the genome.Mol. Plant. 2010; 3: 642-652Abstract Full Text Full Text PDF PubMed Scopus (46) Google Scholar and Boruc et al., 2012Boruc J Zhou X Meir I Dynamics of the plant nuclear envelope and nuclear pore.Plant Physiol. 2012; 158: 78-86Crossref PubMed Scopus (33) Google Scholar). It is noteworthy that a recent review published in Molecular Plant provides an excellent state of the art on nucleocytoplasmic trafficking of circadian-clock components that are transcriptional regulators involved in the rhythmic oscillations of transcript accumulation during physiological circadian processes (Herrero and Davis, 2012Herrero E Davis S.J Time for nuclear meeting: protein trafficking and chromatin dynamics intersect in the plant circadian system.Mol. Plant. 2012; 5: 554-565Abstract Full Text Full Text PDF PubMed Scopus (34) Google Scholar). Although proteomics analyses of the plant nuclear envelope have not been accomplished yet, genetic, pharmacological, and electrophysiological approaches suggest that both the inner and outer nuclear membranes contain several ion channels and transporters, involved in signal transduction processes. The outer nuclear membrane being continuous with the endoplasmic reticulum, it is supposed that the perinuclear space serves in that case as an internal store for ions (Matzke et al., 2010Matzke A.J.M Weiger T.M Matzke A Ion channels at the nucleus: electrophysiology meets the genome.Mol. Plant. 2010; 3: 642-652Abstract Full Text Full Text PDF PubMed Scopus (46) Google Scholar). The inner nuclear membrane is connected to the nucleoskeleton and peripheral chromatin. While the association of chromatin to the nuclear pore complexes leads to gene activation, interaction of chromatin with the inner nuclear membrane is involved in gene repression (Boruc et al., 2012Boruc J Zhou X Meir I Dynamics of the plant nuclear envelope and nuclear pore.Plant Physiol. 2012; 158: 78-86Crossref PubMed Scopus (33) Google Scholar). Beyond its role as intracellular store, the perinuclear space also contains proteins linking the cytoskeleton to the nucleoplasm, thereby transmitting cellular information more particularly important for chromosome arrangement during cell division (Boruc et al., 2012Boruc J Zhou X Meir I Dynamics of the plant nuclear envelope and nuclear pore.Plant Physiol. 2012; 158: 78-86Crossref PubMed Scopus (33) Google Scholar; Tiang et al., 2012Tiang C.–L He Y Pawlowski W.P Chromosome organization and dynamics during interphase, mitosis, and meiosis in plants.Plant Physiol. 2012; 158: 26-34Crossref PubMed Scopus (81) Google Scholar). Recent advances in cytogenetics techniques, such as fluorescent in situ hybridization and live-cell imaging using fluorescent protein-tagged probes have led these last years to a better understanding of chromosome organization and dynamics in plants (see the recent review by Tiang et al., 2012Tiang C.–L He Y Pawlowski W.P Chromosome organization and dynamics during interphase, mitosis, and meiosis in plants.Plant Physiol. 2012; 158: 26-34Crossref PubMed Scopus (81) Google Scholar). Thus, it appears that, during interphase, chromatin is highly organized within the nuclear space, in sub-nuclear domains called chromosome territories. This spatial organization is dependent on genetic factors and environmental conditions, and controls gene expression during plant growth and development and in response to stresses as reviewed by Sáez–Vásquez and Gadal, 2010Sáez–Vásquez J Gadal O Genome organization and function: a view from yeast and Arabidopsis.Mol. Plant. 2010; 3: 678-690Abstract Full Text Full Text PDF PubMed Scopus (22) Google Scholar. Particularly, the authors compared the spatial genome organization of yeast and Arabidopsis and highlighted the mutual benefit of this comparison to better understand the consequences of this organization on eukaryotic physiology. More recently, Tiang and his colleagues discuss in more detail the chromosome dynamics and their functional significance on chromatin remodeling (Tiang et al., 2012Tiang C.–L He Y Pawlowski W.P Chromosome organization and dynamics during interphase, mitosis, and meiosis in plants.Plant Physiol. 2012; 158: 26-34Crossref PubMed Scopus (81) Google Scholar). In addition, it is noteworthy that the concentration of genes, specific protein factors, and RNAs in particular nuclear structures such as nuclear bodies or perinuclear domains as well as the association of transcriptional and RNA-processing factors in large ribonucleoprotein complexes contribute to an optimal and coordinated gene expression (Sáez–Vásquez and Gadal, 2010Sáez–Vásquez J Gadal O Genome organization and function: a view from yeast and Arabidopsis.Mol. Plant. 2010; 3: 678-690Abstract Full Text Full Text PDF PubMed Scopus (22) Google Scholar; Cheung and Reddy, 2012Cheung A.Y Reddy A.S.N Nuclear architecture and dynamics: territories, nuclear bodies, and nucleocytoplasmic trafficking.Plant Physiol. 2012; 158: 23-25Crossref PubMed Scopus (8) Google Scholar). As nicely reviewed by Charon et al., 2010Charon C Beatriz–Moreno A Bardou F Crespi M Non-protein-coding RNAs and their interacting-binding proteins in plant cell nucleus.Mol. Plant. 2010; 3: 729-739Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar, part of the regulation of gene expression occurs via transcriptional and post-transcriptional processes in the nucleus. These processes involve non-protein-coding RNAs (npcRNAs) such as small interfering RNAs (siRNAs), microRNAs (miRNAs), or natural antisens RNAs which in fine induce messenger RNA cleavage and translational inhibition or transcriptional gene silencing. Therefore, npcRNAs have been implicated in the regulation of a number of developmental processes and in plant responses to both biotic and abiotic stresses. Generally, npcRNAs exert their actions through association with RNA-binding proteins within ribonucleoprotein complexes (Charon et al., 2010Charon C Beatriz–Moreno A Bardou F Crespi M Non-protein-coding RNAs and their interacting-binding proteins in plant cell nucleus.Mol. Plant. 2010; 3: 729-739Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar). Among the nuclear proteins subjected to posttranslational regulation, histones are certainly the most studied. Histones are small basic proteins which associate with DNA to form chromatin. They can be posttranslationally modified by either acetylation/deacetylation, methylation/demethylation, phosphorylation, or ubiquitinylation. With chromatin remodeling processes, these posttranslational modifications are part of the epigenetic regulatory mechanisms involved in the control of gene expression. Numerous studies report histone modifications during plant developmental pathways as diverse as flowering time, cell differentiation, and in response to changes in environmental conditions such as cold or light (reviewed by Ahmad et al., 2010Ahmad A Zhang Y Cao X.F Decoding the epigenetic language of plant development.Mol. Plant. 2010; 3: 719-728Abstract Full Text Full Text PDF PubMed Scopus (70) Google Scholar and Dahan et al., 2011Dahan J Koen E Dutartre A Lamotte O Bourque S Post-translational modifications of nuclear proteins in the response of plant cells to abiotic stresses.in: Shanker A.K. Venkateswarlu B. Abiotic Stress Response in Plants: Physiological, Biochemical and Genetic Perspectives. InTech, Rijeka, Croatia2011: 77-112Crossref Google Scholar). A nice example is the studies reviewed by Dao-Xiu Zhou and his colleagues (Servet et al., 2010Servet C Conde e Silva N Zhou D.–X Histone acetyltransferase AtGCN5/HAG1 is a versatile regulator of developmental and inducible gene expression in Arabidopsis.Mol. Plant. 2010; 3: 670-677Abstract Full Text Full Text PDF PubMed Scopus (133) Google Scholar) focusing on the histone acetyltransferase AtGCN5/HAG1 in Arabidopsis, which is essential for regulating gene expression in response to environmental stresses and during many plant development processes. Besides acetylation of histones, it is now clear that deacetylation of nuclear proteins is also an important mechanism involved in plant cell physiology. Thus, recently, it has been shown in Nicotiana tabacum that type-2 histone deacetylases (NtHD2a and NtHD2b) play a key role as negative regulators of programmed cell death induced by the defense elicitor cryptogein (Bourque et al., 2011Bourque S Dutartre A Hammoudi V Blanc S Dahan J Jeandroz S Pichereraux C Rossignol M Wendehenne D Type-2 histone deacetylases as new regulators of elicitor-induced cell death in plants.New Phytol. 2011; 192: 127-139Crossref PubMed Scopus (54) Google Scholar). It is well known that, in mammalian and yeast cells, phosphoinositides such as inositol phosphates and inositol phospholipids are able to regulate different nuclear functions including cell cycle, DNA synthesis, RNA-processing, and chromatin remodeling. In this frame, Dieck and his colleagues recently gave an exhaustive overview of still largely uncharacterized roles of different actors of the phosphoinositide pathway in the plant nucleus (Dieck et al., 2012Dieck C.B Boss W.F Perera I.Y A role for phophoinositides in regulating plant nuclear functions.Front. Plant Sci. 2012; 3: 50Crossref PubMed Scopus (28) Google Scholar). Interestingly, the authors discussed these different putative functions in the context of plant development and stress responses as well as plant hormone regulation. Calcium (Ca2+) is now largely recognized as an important second messenger that plays key roles in many developmental and stress-responsive processes in plants. It is also now clear that Ca2+-dependent processes take place not only in the cytosol, but in other organelles as well. Concerning the nucleus, recent studies have shown that plant cell nuclei possess their own Ca2+ stores and signaling machinery. This allows the nucleus to control its own Ca2+ homeostasis, leading to the notion of ‘nuclear autonomy’ (for review, see Mazars et al., 2011Mazars C Brière C Bourque S Thuleau P Nuclear calcium signaling: an emerging topic in plants.Biochimie. 2011; 93: 2068-2074Crossref PubMed Scopus (20) Google Scholar). Thus, the concept of Ca2+ signature, initially proposed for cytosolic Ca2+ signals, can be extended to nuclear calcium signals, which, by themselves or in association with other messengers (Mazars et al., 2010Mazars C Thuleau P Lamotte O Bourque S Cross-talk between ROS and calcium in regulation of nuclear activities.Mol. Plant. 2010; 3: 706-718Abstract Full Text Full Text PDF PubMed Scopus (92) Google Scholar), can modulate the activity of nuclear proteins, and thus regulate transcription and expression of specific genes. For instance, it has been shown recently that nuclear calcium variation was a key step in the signaling pathway leading to sphingolipid-induced programmed cell death in tobacco (Lachaud, 2010Lachaud C et al.Nuclear calcium controls the apoptotic-like cell death induced by d-erythro-sphinganine in tobacco cells.Cell Calcium. 2010; 47: 92-100Crossref PubMed Scopus (62) Google Scholar). Calcium-dependent gene regulation results from the interaction of Ca2+ with Ca2+-sensors, either in the nucleus or in the cytoplasm, depending on physiological conditions, which may inhibit or enhance their binding to target proteins, like transcription factors (CAMTAs, GTLs, MYBs, WRKYs, …), or by modulation of transcriptional activity through Ca2+-dependent phosphorylation/dephosphorylation, as reviewed by Galon et al., 2010Galon Y Finkler A Fromm H Calcium-regulated transcription in plants.Mol. Plant. 2010; 3: 653-659Abstract Full Text Full Text PDF PubMed Scopus (135) Google Scholar. In particular, recent progress in this area has emphasized the role of Ca2+- and Ca2+/CaM-regulated transcription in plant cell response to stresses (for review, see Reddy et al., 2011Reddy A.S.N Ali G.S Celesnik H Day I.S Coping with stresses: roles of calcium and calcium/calmodulin-regulated gene expression.Plant Cell. 2011; 23: 2010-2032Crossref PubMed Scopus (524) Google Scholar). For instance, activated Ca2+-sensors can directly bind to cis-elements in the promoters of specific genes to induce or repress their transcription. Ca2+ can also bind directly to transcription factors to modulate their activity. In a recent work, transcriptomic and bioinformatic analysis has revealed a total of 269 genes up-regulated by Ca2+ in Arabidopsis and identified three new promoter motifs (CR/DRE, Site II, and CAM box, in addition to ABRE) that are Ca2+-dependent (Whalley et al., 2011Whalley H.J Sargeant A.W Steele J.F.C Lacoere T Lamb R Saunders N.J Knight H Knight M.R Transcriptomic analysis reveals calcium regulation of specific promoter motifs in Arabidopsis.Plant Cell. 2011; 23: 4079-4095Crossref PubMed Scopus (79) Google Scholar). The different authors cited in the present highlight have already exhaustively described perspectives and future challenges in their respective field of investigation. From that, it emerges that, despite many breakthroughs made during recent years on the knowledge of nuclear functions, a number of unsolved questions remain to be investigated. Nevertheless, from recent developments of high spatiotemporal resolution imaging techniques and systematic quantitative high-throughput studies combined with genetic, biochemical, proteomic, and bioinformatic approaches, it can clearly be expected that, in the near future, we should gain a better understanding of the 4D nuclear organization, dynamics, and signaling and of how they affect gene expression and in fine plant development and adaptive responses to the environment.