Plant Developmental Plasticity Research Articles

PARG1 and EXA1 genes as possible components of the facultative epigenetic control of plant development.

Plants are able to adjust their developmental program in response to incremental environmental changes by reprogramming the epigenomes of the cells. This process, known as facultative epigenetic developmental control, underlies plant developmental plasticity and the amazing diversity of morphotypes which arises from the changes in cell fates. How plants determine when epigenome reprogramming should occur is largely unclear. Here, we show that the Arabidopsis PARG1 and EXA1 genes, encoding poly(ADP-ribose) glycohydrolase and GYF domain protein involved in nonsense-mediated mRNA decay, respectively, act synergistically in maintaining leaf cell identity. Loss of their function in Arabidopsis tae mutant triggers autoimmunity and wounding response, alters transcription of a number of epigenetic regulators, initiates the acquisition of pluripotency by cells of the developed leaf and ectopic outgrowths and buds formation. The dependence of the cell fate on the activity level of PARG1 and EXA1 genes indicates that these interacting genes may function as an important regulator of facultative epigenetic control of plant development. This article is protected by copyright. All rights reserved.

Cover Image

The cover image is based on the Advanced Review Alternative splicing: An efficient regulatory approach towards plant developmental plasticity by Sajid Muhammad et al., https://doi.org/10.1002/wrna.1758. Image Credit: Liang Wu.

Recent advances in crop transformation technologies.

Agriculture is experiencing a technological inflection point in its history, while also facing unprecedented challenges posed by human population growth and global climate changes. Key advancements in precise genome editing and new methods for rapid generation of bioengineered crops promise to both revolutionize the speed and breadth of breeding programmes and increase our ability to feed and sustain human population growth. Although genome editing enables targeted and specific modifications of DNA sequences, several existing barriers prevent the widespread adoption of editing technologies for basic and applied research in established and emerging crop species. Inefficient methods for the transformation and regeneration of recalcitrant species and the genotype dependency of the transformation process remain major hurdles. These limitations are frequent in monocotyledonous crops, which alone provide most of the calories consumed by human populations. Somatic embryogenesis and de novo induction of meristems - pluripotent groups of stem cells responsible for plant developmental plasticity - are essential strategies to quickly generate transformed plants. Here we review recent discoveries that are rapidly advancing nuclear transformation technologies and promise to overcome the obstacles that have so far impeded the widespread adoption of genome editing in crop species.

Alternative splicing: An efficient regulatory approach towards plant developmental plasticity.

Alternative splicing (AS) is a gene regulatory mechanism that plants adapt to modulate gene expression (GE) in multiple ways. AS generates alternative isoforms of the same gene following various development and environmental stimuli, increasing transcriptome plasticity and proteome complexity. AS controls the expression levels of certain genes and regulates GE networks that shape plant adaptations through nonsense-mediated decay (NMD). This review intends to discuss AS modulation, from interaction with noncoding RNAs to the established roles of splicing factors (SFs) in response to endogenous and exogenous cues. We aim to gather such studies that highlight the magnitude and impact of AS, which are not always clear from individual articles, when AS is increasing in individual genes and at a global level. This work also anticipates making plant researchers know that AS is likely to occur in their investigations and that dynamic changes in AS and their effects must be frequently considered. We also review our understanding of AS-mediated posttranscriptional modulation of plant stress tolerance and discuss its potential application in crop improvement in the future. This article is categorized under: RNA Processing > Splicing Regulation/Alternative Splicing RNA Processing > Splicing Mechanisms RNA-Based Catalysis > RNA Catalysis in Splicing and Translation.

Jasmonates and Histone deacetylase 6 activate Arabidopsis genome-wide histone acetylation and methylation during the early acute stress response

BackgroundJasmonates (JAs) mediate trade-off between responses to both biotic and abiotic stress and growth in plants. The Arabidopsis thaliana HISTONE DEACETYLASE 6 is part of the CORONATINE INSENSITIVE1 receptor complex, co-repressing the HDA6/COI1-dependent acetic acid-JA pathway that confers plant drought tolerance. The decrease in HDA6 binding to target DNA mirrors histone H4 acetylation (H4Ac) changes during JA-mediated drought response, and mutations in HDA6 also cause depletion in the constitutive repressive marker H3 lysine 27 trimethylation (H3K27me3). However, the genome-wide effect of HDA6 on H4Ac and much of the impact of JAs on histone modifications and chromatin remodelling remain elusive.ResultsWe performed high-throughput ChIP-Seq on the HDA6 mutant, axe1-5, and wild-type plants with or without methyl jasmonate (MeJA) treatment to assess changes in active H4ac and repressive H3K27me3 histone markers. Transcriptional regulation was investigated in parallel by microarray analysis in the same conditions. MeJA- and HDA6-dependent histone modifications on genes for specialized metabolism; linolenic acid and phenylpropanoid pathways; and abiotic and biotic stress responses were identified. H4ac and H3K27me3 enrichment also differentially affects JAs and HDA6-mediated genome integrity and gene regulatory networks, substantiating the role of HDA6 interacting with specific families of transposable elements in planta and highlighting further specificity of action as well as novel targets of HDA6 in the context of JA signalling for abiotic and biotic stress responses.ConclusionsThe findings demonstrate functional overlap for MeJA and HDA6 in tuning plant developmental plasticity and response to stress at the histone modification level. MeJA and HDA6, nonetheless, maintain distinct activities on histone modifications to modulate genetic variability and to allow adaptation to environmental challenges.

The molecular function and regulation of Class II TCP transcription factors

<p indent=0mm>TCP transcription factors are a class of plant-specific transcription factors. They extensively participate in developmental processes in multiple stages of various plant species. Among them, Class II TCP subfamily plays pivotal roles in control of leaf development, shoot branch formation and flower organ development. The activity of Class II TCP is tightly regulated at both transcriptional and post-transcriptional levels. They regulate the expression of downstream genes by directly binding to promoters, enhancers, and modifying chromatin structure. These mechanisms make TCP elegantly regulate plant development at specific stages during plant development. This review mainly summarized recent progress with regard to the molecular functions and regulation networks of Class II TCPs, and we try to provide the recent understanding of TCP function in integrating the environmental conditions and internal signals to control plant developmental plasticity.

The microRNA476a‐RFL module regulates adventitious root formation through a mitochondria‐dependent pathway in Populus

For woody plants, clonal propagation efficiency is largely determined by adventitious root (AR) formation at the bases of stem cuttings. However, our understanding of the molecular mechanisms contributing to AR morphogenesis in trees remains limited, despite the importance of vegetative propagation, currently the most common practice for tree breeding and commercialization. Here, we identified Populus-specific miR476a as a regulator of wound-induced adventitious rooting that acts by orchestrating mitochondrial homeostasis. MiR476a exhibited inducible expression during AR formation and directly targeted several Restorer of Fertility like (RFL) genes encoding mitochondrion-localized pentatricopeptide repeat proteins. Genetic modification of miR476a-RFL expression revealed that miR476a/RFL-mediated dynamic regulation of mitochondrial homeostasis influences AR formation in poplar. Mitochondrial perturbation via exogenous application of a chemical inhibitor indicated that miR476a/RFL-directed AR formation depends on mitochondrial regulation that acts via auxin signaling. Our results thus establish a microRNA-directed mitochondrion-auxin signaling cascade required for AR development, providing insights into the role of mitochondrial regulation in the developmental plasticity of plants.

SNF1-related protein kinase 1: the many-faced signaling hub regulating developmental plasticity in plants.

The Snf1-related protein kinase 1 (SnRK1) is the plant homolog of the heterotrimeric AMP-activated protein kinase/sucrose non-fermenting 1 (AMPK/Snf1), which works as a major regulator of growth under nutrient-limiting conditions in eukaryotes. Along with its conserved role as a master regulator of sugar starvation responses, SnRK1 is involved in controlling the developmental plasticity and resilience under diverse environmental conditions in plants. In this review, through mining and analyzing the interactome and phosphoproteome data of SnRK1, we are highlighting its role in fundamental cellular processes such as gene regulation, protein synthesis, primary metabolism, protein trafficking, nutrient homeostasis, and autophagy. Along with the well-characterized molecular interaction in SnRK1 signaling, our analysis highlights several unchartered regions of SnRK1 signaling in plants such as its possible communication with chromatin remodelers, histone modifiers, and inositol phosphate signaling. We also discuss potential reciprocal interactions of SnRK1 signaling with other signaling pathways and cellular processes, which could be involved in maintaining flexibility and homeostasis under different environmental conditions. Overall, this review provides a comprehensive overview of the SnRK1 signaling network in plants and suggests many novel directions for future research.

Leaf vein pattern response to heat and drought requires genes that influence PINFORMED1 localization and is mimicked by ABA treatment

The plasticity of plant development allows acclimation to environmental stresses such as heat and drought. For example, increased vein density with more vein meetings is proposed to provide more efficient and robust water delivery when water availability is reduced. We demonstrate that Arabidopsis leaves respond to short term heat or drought by increasing leaf vein density, which in heat includes a higher density of vein meetings. We find that a set of genes, UNHINGED, FORKED1, FORKED-LIKE1, 2 and 3, which influence PINFORMED1 localization and control vein meeting in developing leaves, is required for the vein pattern response to heat or drought. Comparison of δ13C (‰) and nitrogen (%) under different conditions suggests that while wild type and mutant genotypes enriched δ13C (‰) under drought conditions, only wild type increased total shoot nitrogen suggesting increased photosynthetic assimilation. One explanation is that the mutants’ open vein pattern fails to supply sufficient water to support increased photosynthesis. Finally, treatment with ABA caused changes to leaf vein pattern similar to heat or drought treatment, a response that was eliminated in the abscisic acid insensitive1 but not the forked1 genotype. This suggests that the vein pattern response to reduced water availability may in part be controlled by ABA.

Photoreceptors Regulate Plant Developmental Plasticity through Auxin.

Light absorption by plants changes the composition of light inside vegetation. Blue (B) and red (R) light are used for photosynthesis whereas far-red (FR) and green light are reflected. A combination of UV-B, blue and R:FR-responsive photoreceptors collectively measures the light and temperature environment and adjusts plant development accordingly. This developmental plasticity to photoreceptor signals is largely regulated through the phytohormone auxin. The phytochrome, cryptochrome and UV Resistance Locus 8 (UVR8) photoreceptors are inactivated in shade and/or elevated temperature, which releases their repression of Phytochrome Interacting Factor (PIF) transcription factors. Active PIFs stimulate auxin synthesis and reinforce auxin signalling responses through direct interaction with Auxin Response Factors (ARFs). It was recently discovered that shade-induced hypocotyl elongation and petiole hyponasty depend on long-distance auxin transport towards target cells from the cotyledon and leaf tip, respectively. Other responses, such as phototropic bending, are regulated by auxin transport and signalling across only a few cell layers. In addition, photoreceptors can directly interact with components in the auxin signalling pathway, such as Auxin/Indole Acetic Acids (AUX/IAAs) and ARFs. Here we will discuss the complex interactions between photoreceptor and auxin signalling, addressing both mechanisms and consequences of these highly interconnected pathways.

The Regulation of CIN-like TCP Transcription Factors.

TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR 1 and 2 (TCP) family proteins are the plant-specific transcription factors extensively participating in diverse developmental processes by integrating external cues with internal signals. The roles of CINCINNATA (CIN)-like TCPs are conserved in control of the morphology and size of leaves, petal development, trichome formation and plant flowering. The tight regulation of CIN-like TCP activity at transcriptional and post-transcriptional levels are central for plant developmental plasticity in response to the ever-changing environmental conditions. In this review, we summarize recent progresses with regard to the function and regulation of CIN-like TCPs. CIN-like TCPs are regulated by abiotic and biotic cues including light, temperature and pathogens. They are also finely controlled by microRNA319 (miRNA319), chromatin remodeling complexes and auxin homeostasis. The protein degradation plays critical roles in tightly controlling the activity of CIN-like TCPs as well.

Characterization of indole-3-acetic acid in cambial zone tissue by ultra-performance liquid chromatography-tandem mass spectrometry

The developmental plasticity of plants according to changes in their growth conditions is mediated by signaling molecules called hormones. The major classes of plant hormones are auxin, gibberellins, abscisic acid, and ethylene. Among these, the most important is indole-3-acetic acid (IAA). Quantification of IAA in an extract of approximately 10 mg obtained from the cambial zone of Eucalyptus leaves was performed by ultra-performance liquid chromatography coupled with electrospray ionization tandem mass spectrometry (UPLC/ESI-MS/MS). The leaves were extracted using acetone, and the extract was analyzed using a reverse-phase column (Acquity UPLC BEH C18, 2.1 mm × 100 mm, 1.7 µm) at a flow rate of 0.2 mL/min with gradient elution of an aqueous mobile phase (containing 0.1% formic acid) with methanol. This gradient elution provided an excellent performance in terms of specificity/selectivity, linearity, precision, and ruggedness/stability. In addition, the run time was short (6 min), with excellent linearity (R2 &gt; 0.99) in the range of 10–70 ng/mL. The structure of IAA was elucidated using UPLC/ESIMS/MS, operating and quantifying in multiple reaction monitoring (MRM) mode.

A novel Ca2+-binding protein that can rapidly transduce auxin responses during root growth.

Signaling cross talks between auxin, a regulator of plant development, and Ca2+, a universal second messenger, have been proposed to modulate developmental plasticity in plants. However, the underlying molecular mechanisms are largely unknown. Here, we report that in Arabidopsis roots, auxin elicits specific Ca2+ signaling patterns that spatially coincide with the expression pattern of auxin-regulated genes. We have identified the single EF-hand Ca2+-binding protein Ca2+-dependent modulator of ICR1 (CMI1) as an interactor of the Rho of plants (ROP) effector interactor of constitutively active ROP (ICR1). CMI1 expression is directly up-regulated by auxin, whereas the loss of function of CMI1 associates with the repression of auxin-induced Ca2+ increases in the lateral root cap and vasculature, indicating that CMI1 represses early auxin responses. In agreement, cmi1 mutants display an increased auxin response including shorter primary roots, longer root hairs, longer hypocotyls, and altered lateral root formation. Binding to ICR1 affects subcellular localization of CMI1 and its function. The interaction between CMI1 and ICR1 is Ca2+-dependent and involves a conserved hydrophobic pocket in CMI1 and calmodulin binding-like domain in ICR1. Remarkably, CMI1 is monomeric in solution and in vitro changes its secondary structure at cellular resting Ca2+ concentrations ranging between 10−9 and 10−8 M. Hence, CMI1 is a Ca2+-dependent transducer of auxin-regulated gene expression, which can function in a cell-specific fashion at steady-state as well as at elevated cellular Ca2+ levels to regulate auxin responses.

MADS-Box Genes Are Key Components of Genetic Regulatory Networks Involved in Abiotic Stress and Plastic Developmental Responses in Plants.

Plants, as sessile organisms, adapt to different stressful conditions, such as drought, salinity, extreme temperatures, and nutrient deficiency, via plastic developmental and growth responses. Depending on the intensity and the developmental phase in which it is imposed, a stress condition may lead to a broad range of responses at the morphological, physiological, biochemical, and molecular levels. Transcription factors are key components of regulatory networks that integrate environmental cues and concert responses at the cellular level, including those that imply a stressful condition. Despite the fact that several studies have started to identify various members of the MADS-box gene family as important molecular components involved in different types of stress responses, we still lack an integrated view of their role in these processes. In this review, we analyze the function and regulation of MADS-box gene family members in response to drought, salt, cold, heat, and oxidative stress conditions in different developmental processes of several plants. In addition, we suggest that MADS-box genes are key components of gene regulatory networks involved in plant responses to stress and plant developmental plasticity in response to seasonal changes in environmental conditions.

The Lateral Root Cap Acts as an Auxin Sink that Controls Meristem Size

Plant developmental plasticity relies on the activities of meristems, regions where stem cells continuously produce new cells [1]. The lateral root cap (LRC) is the outermost tissue of the root meristem [1], and it is known to play an important role during root development [2-6]. In particular, it has been shown that mechanical or genetic ablation of LRC cells affect meristem size [7, 8]; however, the molecular mechanisms involved are unknown. Root meristem size and, consequently, root growth depend on the position of the transition zone (TZ), a boundary that separates dividing from differentiating cells [9, 10]. The interaction of two phytohormones, cytokinin and auxin, is fundamental in controlling the position of the TZ [9, 10].Cytokinin via the ARABIDOPSIS RESPONSE REGULATOR 1 (ARR1) control auxin distribution within the meristem, generating an instructive auxin minimum that positions the TZ [10]. We identify a cytokinin-dependent molecular mechanism that acts in the LRC to control the position of the TZ and meristem size. We show that auxin levels within the LRC cells depends on PIN-FORMED 5 (PIN5), a cytokinin-activated intracellular transporter that pumps auxin from the cytoplasm into the endoplasmic reticulum, and on irreversible auxin conjugation mediated by the IAA-amino synthase GRETCHEN HAGEN 3.17 (GH3.17). By titrating auxin in the LRC, the PIN5 and the GH3.17 genes control auxin levels in the entire root meristem. Overall, our results indicate that theLRC serves as an auxin sink that, under the control of cytokinin, regulates meristem size and root growth.

MicroRNAs and Their Regulatory Roles in Plant-Environment Interactions.

MicroRNAs (miRNAs) are 20-24 nucleotide noncoding RNAs abundant in plants and animals. The biogenesis of plant miRNAs involves transcription of miRNA genes, processing of primary miRNA transcripts by DICER-LIKE proteins into mature miRNAs, and loading of mature miRNAs into ARGONAUTE proteins to form miRNA-induced silencing complex (miRISC). By targeting complementary sequences, miRISC negatively regulates gene expression, thereby coordinating plant development and plant-environment interactions. In this review, we present and discuss recent updates on the mechanisms and regulation of miRNA biogenesis, miRISC assembly and actions as well as the regulatory roles of miRNAs in plant developmental plasticity, abiotic/biotic responses, and symbiotic/parasitic interactions. Finally, we suggest future directions for plant miRNA research.

Plant miRNA Conservation and Evolution.

Plant microRNAs do not only perform important roles in development; they also have a fascinating evolutionary dynamics. Their genes appear to originate at quite a high rate during evolution, but most of them evolve initially in an almost neutral way and hence also get lost quite rapidly. Despite the high birth and death rate, a few miRNA-encoding genes got involved in the control of important target genes and thus have been conserved during evolution. This happened obviously at all times and taxonomic levels during land plant evolution. Consequently, the genomes of extant plant species contain a mix of miRNA-encoding genes of different ages, ranging from very young, often even species-specific loci to genes that had already been established in the stem group of extant land plants more than 400 million years ago. It could well be that the evolutionary dynamics of miRNA-encoding genes contributed substantially to the evolution of developmental plasticity in plants.

Mini-Review: Nod Factor Regulation of Phytohormone Signaling and Homeostasis During Rhizobia-Legume Symbiosis.

The rhizobia-legume symbiosis is a mutualistic association in which bacteria provide plants with nitrogen compounds and the plant provides bacteria with carbon sources. A successful symbiotic interaction relies on a molecular dialog between the plant and the bacteria, and generally involves rhizobial lipo-chitooligosaccharide signals called Nod factors (NFs). In most cases, specific NF perception is required for rhizobia to enter root cells through newly formed intracellular structures called infection threads (ITs). Concomitantly to IT formation in root hairs, root cortical cells start to divide to create a new root organ called the nodule, which will provide the bacteria with a specific micro-environment required for symbiotic nitrogen fixation. During all these steps of plant–bacteria interaction, new plant cellular compartments and developmental programs are activated. This interaction is costly for the plant that tightly controls symbiosis establishment and functioning. Phytohormones are key regulators of cellular and developmental plasticity in plants, and they are influential endogenous signals that rapidly control plant responses. Although early symbiotic responses were known for decades to be linked to phytohormone-related responses, new data reveal the molecular mechanisms involved and links between phytohormones and the control of early symbiotic events. Reciprocally, NF signaling also targets phytohormone signaling pathways. In this review, we will focus on the emerging notion of NF and phytohormone signaling crosstalk, and how it could contribute to the tight control of symbiosis establishment in legume host plants.

Interactive and noninteractive roles of histone H2B monoubiquitination and H3K36 methylation in the regulation of active gene transcription and control of plant growth and development.

Covalent modifications of histones are essential to control a wide range of processes during development and adaptation to environmental changes. With the establishment of reference epigenomes, patterns of histone modifications were correlated with transcriptionally active or silenced genes. These patterns imply the need for the precise and dynamic coordination of different histone-modifying enzymes to control transcription at a given gene. Classically, the influence of these enzymes on gene expression is examined separately and their interplays rarely established. In Arabidopsis, HISTONE MONOUBIQUITINATION2 (HUB2) mediates H2B monoubiquitination (H2Bub1), whereas SET DOMAIN GROUP8 (SDG8) catalyzes H3 lysine 36 trimethylation (H3K36me3). In this work, we crossed hub2 with sdg8 mutants to elucidate their functional relationships. Despite similar phenotypic defects, sdg8 and hub2 mutations broadly affect genome transcription and plant growth and development synergistically. Also, whereas H3K4 methylation appears largely dependent on H2Bub1, H3K36me3 and H2Bub1 modifications mutually reinforce each other at some flowering time genes. In addition, SDG8 and HUB2 jointly antagonize the increase of the H3K27me3 repressive mark. Collectively, our data provide an important insight into the interplay between histone marks and highlight their interactive complexity in regulating chromatin landscape which might be necessary to fine-tune transcription and ensure plant developmental plasticity.

Emerging Trends in Epigenetic Regulation of Nutrient Deficiency Response in Plants.

Diverse environmental stimuli largely affect the ionic balance of soil, which have a direct effect on growth and crop yield. Details are fast emerging on the genetic/molecular regulators, at whole-genome levels, of plant responses to mineral deficiencies in model and crop plants. These genetic regulators determine the root architecture and physiological adaptations for better uptake and utilization of minerals from soil. Recent evidence also shows the potential roles of epigenetic mechanisms in gene regulation, driven by minerals imbalance. Mineral deficiency or sufficiency leads to developmental plasticity in plants for adaptation, which is preceded by a change in the pattern of gene expression. Notably, such changes at molecular levels are also influenced by altered chromatin structure and methylation patterns, or involvement of other epigenetic components. Interestingly, many of the changes induced by mineral deficiency are also inheritable in the form of epigenetic memory. Unravelling these mechanisms in response to mineral deficiency would further advance our understanding of this complex plant response. Further studies on such approaches may serve as an exciting interaction model of epigenetic and genetic regulations of mineral homeostasis in plants and designing strategies for crop improvement.