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Plant Cell Advance Publication Papers



The Plant Cell, published by the American Society of Plant Biologists, has the highest impact factor of primary research journals in plant biology.



 









An automated confocal micro-extensometer enables in vivo quantification of mechanical properties with cellular resolution.

2017-11-22T09:48:30-08:00

How complex developmental-genetic networks are translated into organs with specific 3D shapes remains an open question. This question is particularly challenging because the elaboration of specific shapes is in essence a question of mechanics. In plants, this means how the genetic circuitry affects the cell wall. The mechanical properties of the wall and their spatial variation are the key factors controlling morphogenesis in plants. However, these properties are difficult to measure and investigating their relation to genetic regulation is particularly challenging. To measure spatial variation of mechanical properties, one must determine the deformation of a tissue in response to a known force with cellular resolution. Here we present an automated confocal micro-extensometer (ACME), which greatly expands the scope of existing methods for measuring mechanical properties. Unlike classical extensometers, ACME is mounted on a confocal microscope and utilizes confocal images to compute the deformation of the tissue directly from biological markers, thus providing 3D cellular scale information and improved accuracy. Additionally, ACME is suitable for measuring the mechanical responses in live tissue. As a proof of concept, we demonstrate that the plant hormone gibberellic acid induces a spatial gradient in mechanical properties along the length of the Arabidopsis hypocotyl.




MAPKs influence pollen tube growth by controlling the formation of phosphatidylinositol 4,5-bisphosphate in an apical plasma membrane domain

2017-11-22T09:48:30-08:00

An apical plasma membrane domain enriched in the regulatory phospholipid phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P2) is critical for polar tip growth of pollen tubes. How the biosynthesis of PtdIns(4,5)P2 by phosphatidylinositol 4-phosphate 5-kinases (PI4P 5-kinases) is controlled by upstream signaling is currently unknown. The pollen-expressed PI4P 5-kinase PIP5K6 is required for clathrin-mediated endocytosis and polar tip growth in pollen tubes. Here, we identify PIP5K6 as a target of the pollen-expressed mitogen-activated protein kinase MPK6 and characterize the regulatory effects. Based on an untargeted mass spectrometry approach, phosphorylation of purified recombinant PIP5K6 by pollen tube extracts could be attributed to MPK6. Recombinant MPK6 phosphorylated residues T590 and T597 in the variable insert of the catalytic domain of PIP5K6, and this modification inhibited PIP5K6 activity in vitro. PIP5K6 interacted with MPK6 in yeast two-hybrid tests, immuno-pull-down assays, and by bimolecular fluorescence complementation (BiFC) at the apical plasma membrane of pollen tubes. In vivo, MPK6 expression resulted in reduced plasma membrane association of a fluorescent PtdIns(4,5)P2 reporter and decreased endocytosis without impairing membrane association of PIP5K6. Effects of PIP5K6 expression on pollen tube growth and cell morphology were attenuated by coexpression of MPK6 in a phosphosite-dependent manner. Our data indicate that MPK6 controls PtdIns(4,5)P2 production and membrane trafficking in pollen tubes, possibly contributing to directional growth.




The Tomato DELLA Protein PROCERA Acts in Guard Cells to Promote Stomatal Closure

2017-11-17T15:49:54-08:00

Plants employ stomatal closure and reduced growth to avoid water deficiency damage. Reduced levels of the growth-promoting hormone gibberellin (GA) lead to increased tolerance to water deficit, but the underlying mechanism is unknown. Here, we show that the tomato (Solanum lycopersicum) DELLA protein PROCERA (PRO), a negative regulator of GA signaling, acts in guard cells to promote stomatal closure and reduce water loss in response to water deficiency by increasing abscisic acid (ABA) sensitivity. The loss-of-function pro mutant exhibited increased stomatal conductance and rapid wilting under water-deficit stress. Transgenic tomato overexpressing constitutively active stable DELLA proteins (S-della) displayed the opposite phenotype. The effects of S-della on stomatal aperture and water loss were strongly suppressed in the ABA-deficient mutant sitiens (sit), indicating that these effects of S-della are ABA-dependent. While DELLA had no effect on ABA levels, guard cell ABA responsiveness was increased in S-della and reduced in pro plants compared to wild type. Expressing S-della under the control of a guard-cell-specific promoter was sufficient to increase stomatal sensitivity to ABA and to reduce water loss under water-deficit stress but had no effect on leaf size. This result indicates that DELLA promotes stomatal closure independently of its effect on growth.




Differential Regulation of Two-tiered Plant Immunity and Sexual Reproduction by ANXUR Receptor-like Kinases

2017-11-17T15:49:54-08:00

Plants have evolved two tiers of immune receptors to detect infections: cell surface-resident pattern recognition receptors (PRRs) that sense microbial signatures and intracellular nucleotide-binding domain leucine-rich repeat (NLR) proteins that recognize pathogen effectors. How PRRs and NLRs interconnect and activate the specific and overlapping plant immune responses remains elusive. A genetic screen for components controlling plant immunity identified ANXUR1 (ANX1), a malectin-like domain-containing receptor-like kinase, together with its homolog ANX2, as important negative regulators of both PRR- and NLR-mediated immunity in Arabidopsis thaliana. ANX1 constitutively associates with the bacterial flagellin receptor FLAGELLIN-SENSING 2 (FLS2) and its co-receptor BRI1-ASSOCIATED RECEPTOR KINASE 1 (BAK1). Perception of flagellin by FLS2 promotes ANX1 association with BAK1, thereby interfering with FLS2-BAK1 complex formation to attenuate PRR signaling. In addition, ANX1 complexes with the NLR proteins RESISTANT TO PSEUDOMONAS SYRINGAE 2 (RPS2) and RESISTANCE TO P. SYRINGAE PV MACULICOLA 1 (RPM1). ANX1 promotes RPS2 degradation and attenuates RPS2-mediated cell death. Surprisingly, a mutation that affects ANX1 function in plant immunity does not disrupt its function in controlling pollen tube growth during fertilization. Our study thus reveals a molecular link between PRR and NLR protein complexes that both associate with cell surface-resident ANX1 and uncovers uncoupled functions of ANX1 and ANX2 during plant immunity and sexual reproduction.




Canalization of Tomato Fruit Metabolism

2017-11-17T13:26:17-08:00

To explore the genetic robustness (canalization) of metabolism, we examined the levels of fruit metabolites in multiple harvests of a tomato introgression line (IL) population. The IL partitions the whole genome of the wild species Solanum pennellii in the background of the cultivated tomato (Solanum lycopersicum). We identified several metabolite quantitative trait loci that reduce variability for both primary and secondary metabolites, which we named canalization metabolite quantitative trait loci (cmQTL). We validated nine cmQTL using an independent population of backcross inbred lines, derived from the same parents, which allows increased resolution in mapping the QTL previously identified in the ILs. These cmQTL showed little overlap with QTL for the metabolite levels themselves. Moreover, the intervals they mapped to harbored few metabolism-associated genes, suggesting that the canalization of metabolism is largely controlled by regulatory genes.




Arabidopsis Pollen Fertility Requires the Transcription Factors CITF1 and SPL7 that Regulate Copper Delivery to Anthers and Jasmonic Acid Synthesis

2017-11-17T13:26:17-08:00

A deficiency of the micronutrient copper (Cu) leads to infertility and grain/seed yield reduction in plants. How Cu affects fertility, which reproductive structures require Cu, and which transcriptional networks coordinate Cu delivery to reproductive organs is poorly understood. Using RNA-seq analysis, we showed that the expression of a gene encoding a novel transcription factor, CITF1 (Cu-deficiency Induced Transcription Factor 1), was strongly upregulated in Arabidopsis thaliana flowers subjected to Cu deficiency. We demonstrated that CITF1 regulates Cu uptake into roots and delivery to flowers, and is required for normal plant growth under Cu deficiency. CITF1 acts together with a master regulator of copper homeostasis, SPL7 (Squamosa Promoter Binding Protein like7), and the function of both is required for Cu delivery to anthers and pollen fertility. We also found that Cu deficiency upregulates the expression of jasmonic acid (JA) biosynthetic genes in flowers, and increases endogenous JA accumulation in leaves. These effects are controlled in part by CITF1 and SPL7. Finally, we show that JA regulates CITF1 expression and that the JA biosynthetic mutant lacking the CITF1- and SPL7-regulated genes, LOX3 and LOX4, is sensitive to Cu deficiency. Together, our data show that CITF1 and SPL7 regulate Cu uptake and delivery to anthers, thereby influencing fertility, and highlight the relationship between Cu homeostasis, CITF1, SPL7, and the JA metabolic pathway.




Defense Against Reactive Carbonyl Species Involves at Least Three Subcellular Compartments where Individual Components of the System Respond to Cellular Sugar Status

2017-11-17T15:07:08-08:00

Methylglyoxal (MGO) and glyoxal (GO) are toxic reactive carbonyl species generated as by-products of glycolysis. The pre-emption pathway for detoxification of these products, the glyoxalase (GLX) system, involves two consecutive reactions catalyzed by GLXI and GLXII. In Arabidopsis thaliana, the GLX system is encoded by three homologs of GLXI and three homologs of GLXII, from which several predicted GLXI and GLXII isoforms can be derived through alternative splicing. We identified the physiologically relevant splice forms using sequencing data and demonstrated that the resulting isoforms have different subcellular localizations. All three GLXI homologs are functional in vivo, as they complemented a yeast GLXI loss-of-function mutant. Efficient MGO and GO detoxification can be controlled by a switch in metal cofactor usage. MGO formation is closely connected to the flux through glycolysis and through the Calvin Benson cycle; accordingly, expression analysis indicated that GLXI is transcriptionally regulated by endogenous sugar levels. Analyses of Arabidopsis loss-of-function lines revealed that the elimination of toxic reactive carbonyl species during germination and seedling establishment depends on the activity of the cytosolic GLXI;3 isoform. The Arabidopsis GLX system involves the cytosol, chloroplasts, and mitochondria, which harbor individual components that might be utilized at specific developmental stages and respond differentially to cellular sugar status.
















CORTICAL MICROTUBULE DISORDERING1 is Required for Secondary Cell Wall Patterning in Xylem Vessels

2017-11-13T11:08:49-08:00

Proper patterning of the cell wall is essential for plant cell development. Cortical microtubule arrays direct the deposition patterns of cell walls at the plasma membrane. However, the precise mechanism underlying cortical microtubule organization is not well understood. Here, we show that a microtubule-associated protein, CORD1 (CORTICAL MICROTUBULE DISORDERING 1), is required for the pitted secondary cell wall pattern of metaxylem vessels in Arabidopsis thaliana. Loss of CORD1 and its paralog, CORD2, led to the formation of irregular secondary cell walls with small pits in metaxylem vessels, while overexpressing CORD1 led to the formation of abnormally enlarged secondary cell wall pits. Ectopic expression of CORD1 disturbed the parallel cortical microtubule array by promoting the detachment of microtubules from the plasma membrane. A reconstructive approach revealed that CORD1-induced disorganization of cortical microtubules impairs the boundaries of plasma membrane domains of active ROP11 GTPase, which govern pit formation. Our data suggest that CORD1 promotes cortical microtubule disorganization to regulate secondary cell wall pit formation. The Arabidopsis genome has six CORD1 paralogs that are expressed in various tissues during plant development, suggesting they are important for regulating cortical microtubules during plant development.




Shine-Dalgarno Sequences Play an Essential Role in the Translation of Plastid mRNAs in Tobacco

2017-11-13T11:08:49-08:00

In prokaryotic systems, the translation initiation of many, though not all, mRNAs depends on interaction between a sequence element upstream of the start codon (the Shine-Dalgarno sequence, SD) and a complementary sequence in the 3' end of the 16S ribosomal RNA (anti-Shine-Dalgarno sequence, aSD). Although many chloroplast mRNAs harbor putative SDs in their 5' untranslated regions and the aSD displays strong conservation, the functional relevance of SD-aSD interactions in plastid translation is unclear. Here, by generating transplastomic tobacco (Nicotiana tabacum) mutants with point mutations in the aSD coupled with genome-wide analysis of translation by ribosome profiling, we provide a global picture of SD-dependent translation in plastids. We observed a pronounced correlation between weakened predicted SD-aSD interactions and reduced translation efficiency. However, multiple lines of evidence suggest that the strength of the SD-aSD interaction is not the only determinant of the translational output of many plastid mRNAs. Finally, the translation efficiency of mRNAs with strong secondary structures around the start codon is more dependent on the SD-aSD interaction than weakly structured mRNAs. Thus, our data reveal the importance of the aSD in plastid translation initiation, uncover chloroplast genes whose translation is influenced by SD-aSD interactions, and provide insights into determinants of translation efficiency in plastids.




Dihydrofolate reductase/thymidylate synthase fine-tunes the folate status and controls redox homeostasis in plants

2017-11-13T11:08:49-08:00

Folates (B9 vitamins) are essential cofactors in one-carbon metabolism. Since C1 transfer reactions are involved in synthesis of nucleic acids, proteins, lipids and other biomolecules, as well as in epigenetic control, folates are vital for all living organisms. This work presents the first complete study of a plant DHFR-TS (dihydrofolate reductase-thymidylate synthase) gene family that implements the penultimate step in folate biosynthesis. We demonstrate that one of the DHFR-TS isoforms (THY3) operates as an inhibitor of its two homologs, thus regulating DHFR and TS activities and, as a consequence, folate abundance. In addition, a novel function of folate metabolism in plants is proposed, i.e., maintenance of the redox balance by contributing to NADPH production through the reaction catalysed by methylenetetrahydrofolate dehydrogenase (MTHFD), thus allowing plants to cope with oxidative stress.




Nanopore Sequencing Comes to Plant Genomes

2017-11-07T15:10:10-08:00




EIN3 and PIF3 Form an Interdependent Module that Represses Chloroplast Development in Buried Seedlings

2017-11-07T11:05:50-08:00

In buried seedlings, chloroplasts are arrested at the etioplast stage, but they rapidly mature upon emergence of the seedling. Etioplast-chloroplast differentiation is halted through the integration of soil-induced signals, including pressure and the absence of light, although the details on how this information converges to regulate cellular decisions remain unclear. Here, we identify an interdependent transcription module that integrates the mechanical pressure and darkness signals to control chloroplast development in Arabidopsis thaliana. Mutations of ETHYLENE-INSENSITIVE3 (EIN3), the primary transcription factor in the ethylene signaling pathway that is activated in response to mechanical pressure, cause early development of etioplasts in the dark and severe photobleaching upon light exposure. Genetic studies demonstrate that repression of etioplast differentiation by EIN3 requires PHYTOCHROME INTERACTING FACTOR 3 (PIF3), a darkness-stabilized bHLH transcription factor. EIN3 and PIF3 directly interact and form an interdependent module to repress the expression of most LIGHT HARVESTING COMPLEX (LHC) genes; overexpressing even one LHC could cause premature development of etioplasts. The EIN3-PIF3 transcription module synergistically halts chloroplast development by interdependently co-occupying the promoters of LHC genes. Thus, our results define a transcriptional regulatory module and provide mechanistic insight on the concerted regulation of chloroplast development by multiple soil-induced signals.




Genetic Components of Root Architecture Remodeling in Response to Salt Stress

2017-11-07T11:05:50-08:00

Salinity of the soil is highly detrimental to plant growth. Plants respond by a redistribution of root mass between main and lateral roots, yet the genetic machinery underlying this process is still largely unknown. Here, we describe the natural variation among 347 Arabidopsis thaliana accessions in root system architecture (RSA) and identify the traits with highest natural variation in their response to salt. Salt-induced changes in RSA were associated with 100 genetic loci using genome-wide association studies (GWAS). Two candidate loci associated with lateral root development were validated and further investigated. Changes in CYP79B2 expression in salt stress positively correlated with lateral root development in accessions, and cyp79b2 cyp79b3 double mutants developed fewer and shorter lateral roots under salt stress, but not in control conditions. By contrast, high HKT1 expression in the root repressed lateral root development, which could be partially rescued by addition of potassium. The collected data and Multi-Variate analysis of multiple RSA traits, available through the Salt_NV_Root App, capture root responses to salinity. Together, our results provide a better understanding of effective RSA remodeling responses, and the genetic components involved, for plant performance in stress conditions.




Unexpected Connections between Humidity and Ion TransportDiscovered using a Model to Bridge Guard Cell-to-Leaf Scales

2017-11-01T11:44:16-07:00

Stomatal movements depend on the transport and metabolism of osmotic solutes that drive reversible changes in guard cell volume and turgor. These processes are defined by a deep knowledge of the identities of the key transporters and of their biophysical and regulatory properties, and have been modelled successfully with quantitative kinetic detail at the cellular level. Transpiration of the leaf and canopy, by contrast, is described by quasi-linear, empirical relations for the inputs of atmospheric humidity, CO2, and light, but without connection to guard cell mechanics. Until now, no framework has been available to bridge this gap and provide an understanding of their connections. Here we introduce OnGuard2, a quantitative systems platform that utilizes the molecular mechanics of ion transport, metabolism and signalling of the guard cell to define the water relations and transpiration of the leaf. We show that OnGuard2 faithfully reproduces the kinetics of stomatal conductance in Arabidopsis, its dependence on vapor pressure difference (VPD) and on water feed to the leaf. OnGuard2 also predicted with VPD unexpected alterations in K+ channel activities, and changes in stomatal conductance of the slac1 Cl- channel and ost2 H+-ATPase mutants which we verified experimentally. OnGuard2 thus bridges the micro-macro divide, offering a powerful tool with which to explore the links between guard cell homeostasis, stomatal dynamics and foliar transpiration.




Salt Stress and CTD PHOSPHATASE-LIKE 4 Mediate the Switch Between Production of Small Nuclear RNAs and mRNAs

2017-11-01T13:28:18-07:00

Phosphorylation of the RNA polymerase II (Pol II) C-terminal domain (CTD) regulates transcription of protein-coding mRNAs and non-coding RNAs (ncRNAs). CTD function in transcription of protein-coding RNAs has been studied extensively, but its role in plant ncRNA transcription remains obscure. Here, using Arabidopsis thaliana CTD PHOSPHATASE-LIKE 4 knock-down lines (CPL4RNAi), we showed that CPL4 functions in genome-wide, conditional production of 3'-extensions of small nuclear RNAs (snRNAs) and biogenesis of novel transcripts from protein-coding genes downstream of the snRNAs (snRNA-Downstream Protein-coding Genes, snR-DPGs). Production of snR-DPGs required the Pol II snRNA promoter (PIIsnR), and CPL4RNAi plants showed increased read-through of the snRNA 3'-end processing signal, leading to continuation of transcription downstream of the snRNA gene. We also discovered an unstable, intermediate-length RNA from the SMALL SCP1-LIKE PHOSPHATASE 14 locus (imRNASSP14), whose expression originated from the 5' region of a protein-coding gene. Expression of the imRNASSP14 was driven by a PIIsnR and was conditionally 3'-extended to produce an mRNA. In wild type, salt stress induced the snRNA-to-snR-DPG switch, which was associated with alterations of Pol II-CTD phosphorylation at the target loci. The snR-DPG transcripts occur widely in plants, suggesting that the transcriptional snRNA-to-snR-DPG switch may be a ubiquitous mechanism to regulate plant gene expression in response to environmental stresses.




The Coiled-coil and Nucleotide Binding Domains of BROWN PLANTHOPPER RESISTANCE14 Function in Signaling and Resistance Against Planthopper in Rice

2017-11-01T09:19:24-07:00

BROWN PLANTHOPPER RESISTANCE14 (BPH14), the first planthopper-resistance gene isolated via map-based cloning in rice (Oryza sativa), encodes a coiled-coil-, nucleotide-binding site-, leucine-rich repeat (CC-NB-LRR) protein. Several planthopper and aphid resistance genes encoding proteins with similar structures have recently been identified. Here, we analyzed the functions of the domains of BPH14 to identify molecular mechanisms underpinning BPH14-mediated planthopper resistance. The CC or NB domains alone or in combination (CC-NB [CN]) conferred a similar level of brown planthopper resistance to that of full-length (FL) BPH14. Both domains activated the salicylic acid signaling pathway and defense gene expression. In rice protoplasts and Nicotiana benthamiana leaves, these domains increased reactive oxygen species levels without triggering cell death. Additionally, the resistance domains and FL BPH14 protein formed homo-complexes that interacted with transcription factors WRKY46 and WRKY72. In rice protoplasts, the expression of FL BPH14 or its CC, NB, and CN domains increased the accumulation of WRKY46 and WRKY72 as well as WRKY46- and WRKY72-dependent transactivation activity. WRKY46 and WRKY72 bind to the promoters of the receptor-like cytoplasmic kinase gene RLCK281 and the callose synthase gene LOC_Os01g67364.1, whose transactivation activity is dependent on WRKY46 or WRKY72. These findings shed light on this important insect-resistance mechanism.




MRF Family Genes Are Involved in Protein Translation Control, Especially under Energy-Deficient Conditions, and Their Expression and Functions Are Modulated by the TOR Signaling Pathway

2017-10-30T09:26:09-07:00

Dynamic control of protein translation in response to the environment is essential for the survival of plant cells. Target of rapamycin (TOR) coordinates protein synthesis with cellular energy/nutrient availability through transcriptional modulation and phosphorylation of the translation machinery. However, mechanisms of TOR-mediated translation control are poorly understood in plants. Here, we report that Arabidopsis thaliana MRF (MA3 DOMAIN-CONTAINING TRANSLATION REGULATORY FACTOR) family genes encode translation regulatory factors under TOR control, and their functions are particularly important in energy-deficient conditions. Four MRF family genes (MRF1-MRF4) are transcriptionally induced by dark and starvation (DS). Silencing of multiple MRFs increases susceptibility to DS and treatment with a TOR inhibitor, while MRF1 overexpression decreases susceptibility. MRF proteins interact with eIF4A and co-fractionate with ribosomes. MRF silencing decreases translation activity, while MRF1 overexpression increases it, accompanied by altered ribosome patterns, particularly in DS. Furthermore, MRF deficiency in DS causes altered distribution of mRNAs in sucrose gradient fractions, and accelerates rRNA degradation. MRF1 is phosphorylated in vivo, and phosphorylated by S6 kinases in vitro. MRF expression, and MRF1 ribosome association and phosphorylation are modulated by cellular energy status and TOR activity. We discuss possible mechanisms of the function of MRF family proteins under normal and energy-deficient conditions and their functional link with the TOR pathway.




Bilin-dependent photoacclimation in Chlamydomonas reinhardtii

2017-10-30T13:10:20-07:00

In land plants, linear tetrapyrrole (bilin)-based phytochrome photosensors optimize photosynthetic light capture by mediating massive reprogramming of gene expression. But, surprisingly, many green algal genomes lack phytochrome genes. Studies of the heme oxygenase mutant (hmox1) of the green alga Chlamydomonas reinhardtii suggest that bilin biosynthesis in plastids is essential for proper regulation of a nuclear gene network implicated in oxygen detoxification during dark-to-light transitions. hmox1 cannot grow photoautotrophically and photoacclimates p oorly to increased illumination. We show that these phenotypes are due to reduced accumulation of photosystem I (PSI) reaction centers, the PSI electron acceptors 5'-monohydroxyphylloquinone and phylloquinone, and the loss of PSI and photosystem II (PSII) antennae complexes during photoacclimation. The hmox1 mutant resembles chlorophyll biosynthesis mutants phenotypically, but can be rescued by exogenous biliverdin IXα, the bilin produced by HMOX1. This rescue is independent of photosynthesis and is strongly dependent on blue light. RNA-Seq comparisons of hmox1, genetically complemented hmox1, and chemically rescued hmox1 reveal that tetrapyrrole biosynthesis, known photoreceptor and photosynthesis-related genes are not impacted in the hmox1 mutant at the transcript level. We propose that a bilin-based, blue-light-sensing system within plastids evolved together with a bilin-based retrograde signaling pathway to ensure that a robust photosynthetic apparatus is sustained in light-grown C. reinhardtii.-




Host-mediated S-nitrosylation disarms the bacterial effector HopAI1 to re-establish immunity

2017-10-30T09:26:09-07:00

Pathogens deliver effectors into plant cells to suppress immunity-related signaling. However, effector recognition by the host elicits a hypersensitive response (HR) that overcomes the inhibition of host signaling networks, restoring disease resistance. Signaling components are shared between the pathogen-associated molecular pattern (PAMP)-triggered immunity and effector-triggered immunity, and it is unclear how plants inactivate these effectors to execute the HR. Here we report that, in Arabidopsis thaliana, during the onset of the HR the bacterial effector HopAI1 is S-nitrosylated and that this modification inhibits its phosphothreonine lyase activity. HopAI1 targets and suppresses mitogen-activated protein kinases (MAPKs). The S nitrosylation of HopAI1 restores MAPK signaling and is required during the HR for activation of the associated cell death. S-nitrosylation is therefore revealed here as a nitric oxide (NO)-dependent host strategy involved in plant immunity that works by directly disarming effector proteins.




Coordinated Functional Divergence of Genes after Genome Duplication in Arabidopsis thaliana

2017-10-26T09:29:02-07:00

Gene and genome duplications have been rampant during the evolution of flowering plants. Unlike small-scale gene duplications, whole-genome duplications (WGDs) copy entire pathways or networks, and as such create the unique situation in which such duplicated pathways or networks could evolve novel functionality through the coordinated sub- or neo-functionalization of its constituent genes. Here, we describe a remarkable case of coordinated gene expression divergence following WGDs in Arabidopsis thaliana. We identified a set of 92 homoeologous gene pairs that all show a similar pattern of tissue-specific gene expression divergence following WGD, with one homoeolog showing predominant expression in aerial tissues and the other homoeolog showing biased expression in tip-growth tissues. We provide evidence that this pattern of gene expression divergence seems to involve genes with a role in cell polarity and that likely function in the maintenance of cell-wall integrity. Following WGD, many of these duplicated genes evolved separate functions through subfunctionalization in growth/development and stress response. Uncoupling these processes through genome duplications likely provided important adaptions with respect to growth and morphogenesis and defense against biotic and abiotic stress.




Light Inhibits COP1-Mediated Degradation of ICE Transcription Factors to Induce Stomatal Development in Arabidopsis

2017-10-25T18:34:39-07:00

Stomata are epidermal openings that facilitate plant-atmosphere gas exchange during photosynthesis, respiration, and water evaporation. Stomatal differentiation and patterning are spatially and temporally regulated by the master regulators SPEECHLESS (SPCH), MUTE, and FAMA, which constitute a central gene regulatory network along with Inducer of CBF Expression (ICE) transcription factors for this developmental process. Stomatal development is also profoundly influenced by environmental conditions, such as light, temperature, and humidity. Light induces stomatal development, and various photoreceptors modulate this response. However, it is unknown how light is functionally linked with the master regulatory network. Here, we demonstrate that, under dark conditions, the E3 ubiquitin ligase CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1) degrades ICE proteins through ubiquitination pathways in leaf abaxial epidermal cells in Arabidopsis. Accordingly, the ICE proteins accumulate in the nuclei of leaf abaxial epidermal cells in COP1-defective mutants, which constitutively produce stomata. Notably, light in the blue, red, and far-red wavelength ranges suppresses the COP1-mediated degradation of the ICE proteins to induce stomatal development. These observations indicate that light is directly linked with the ICE-directed signaling module, via the COP1-mediated protein surveillance system, in the modulation of stomatal development.




ZEITLUPE Contributes to a Thermoresponsive Protein Quality Control System in Arabidopsis

2017-10-23T13:15:55-07:00

Cellular proteins undergo denaturation and oxidative damage under heat stress, forming insoluble aggregates that are toxic to cells. Plants possess versatile mechanisms to deal with insoluble protein aggregates. Denatured proteins are either renatured to their native conformations or removed from cellular compartments; these processes are often referred to as protein quality control. Heat shock proteins (HSPs) act as molecular chaperones that assist in the renaturation-degradation process. However, how protein aggregates are cleared from cells in plants is largely unknown. Here, we demonstrate that heat-induced protein aggregates are removed by a protein quality control system that includes the ZEITLUPE (ZTL) E3 ubiquitin ligase, a central circadian clock component in Arabidopsis thaliana. ZTL mediates the polyubiquitination of aggregated proteins, which leads to proteasomal degradation and enhances the thermotolerance of plants growing at high temperatures. The ZTL-defective ztl-105 mutant exhibited reduced thermotolerance, which was accompanied a decline in polyubiquitination but an increase in protein aggregate formation. ZTL and its interacting partner HSP90 were cofractionated with insoluble aggregates under heat stress, indicating that ZTL contributes to the thermoresponsive protein quality control machinery. Notably, the circadian clock was hypersensitive to heat in ztl-105. We propose that ZTL-mediated protein quality control contributes to the thermal stability of the circadian clock.




A Tripartite Amplification Loop Involving the Transcription Factor WRKY75, Salicylic Acid, and Reactive Oxygen Species Accelerates Leaf Senescence

2017-10-23T13:15:55-07:00

Leaf senescence is a highly coordinated, complicated process involving the integration of numerous internal and environmental signals. Salicylic acid (SA) and reactive oxygen species (ROS) are two well-defined inducers of leaf senescence whose contents progressively and inter-dependently increase during leaf senescence via an unknown mechanism. Here, we characterized the transcription factor WRKY75 as a positive regulator of leaf senescence in Arabidopsis thaliana. Knock-down or knock-out of WRKY75 delayed age-dependent leaf senescence, while over-expression of WRKY75 accelerated this process. WRKY75 transcription is induced by age, SA, H2O2, and multiple plant hormones. Meanwhile, WRKY75 promotes SA production by inducing the transcription of SA INDUCTION-DEFICIENT2 (SID2) and suppresses H2O2 scavenging, partly by repressing the transcription of CATALASE2 (CAT2). Genetic analysis revealed that the mutation of SID2 or an increase in catalase activity rescued the precocious leaf senescence phenotype evoked by WRKY75 over-expression. Based on these results, we propose a tripartite amplification loop model in which WRKY75, SA, and ROS undergo a gradual but self-sustained rise driven by three interlinking positive feedback loops. This tripartite amplification loop provides a molecular framework connecting upstream signals, such as age and plant hormones, to the downstream regulatory network executed by SA- and H2O2-responsive transcription factors during leaf senescence.




Reciprocally Retained Genes in the Angiosperm Lineage Show the Hallmarks of Dosage Balance Sensitivity

2017-10-23T13:15:55-07:00

In several organisms, particular functional categories of genes, such as regulatory and complex-forming genes, are preferentially retained after whole-genome multiplications but rarely duplicate through small-scale duplication, a pattern referred to as reciprocal retention. This peculiar duplication behavior is hypothesized to stem from constraints on the dosage balance between the genes concerned and their interaction context. However, the evidence for a relationship between reciprocal retention and dosage balance sensitivity remains fragmentary. Here, we identified which gene families are most strongly reciprocally retained in the angiosperm lineage and studied their functional and evolutionary characteristics. Reciprocally retained gene families exhibit stronger sequence divergence constraints and lower rates of functional and expression divergence than other gene families, suggesting that dosage balance sensitivity is a general characteristic of reciprocally retained genes. Gene families functioning in regulatory and signaling processes were much more strongly represented at the top of the reciprocal retention ranking than those functioning in multiprotein complexes, suggesting that regulatory imbalances may lead to stronger fitness effects than classical stoichiometric protein complex imbalances. Finally, reciprocally retained duplicates are often subject to dosage balance constraints for prolonged evolutionary times, which may have repercussions for the ease with which genome multiplications can engender evolutionary innovation.




Antagonistic Transcription Factor Complexes Modulate the Floral Transition in Rice

2017-10-17T09:49:34-07:00

Plants measure day or night lengths to coordinate specific developmental changes with a favorable season. In rice (Oryza sativa), the reproductive phase is initiated by exposure to short days when expression of HEADING DATE 3a (Hd3a) and RICE FLOWERING LOCUS T 1 (RFT1) is induced in leaves. The cognate proteins are components of the florigenic signal, and move systemically through the phloem to reach the shoot apical meristem (SAM). In the SAM, they form a transcriptional activation complex with the bZIP transcription factor OsFD1, to start panicle development. Here, we show that Hd3a and RFT1 can form transcriptional activation or repression complexes also in leaves, and feed-back to regulate their own transcription. Activation complexes depend upon OsFD1 to promote flowering. However, additional bZIPs, including Hd3a BINDING REPRESSOR FACTOR 1 (HBF1) and HBF2 form repressor complexes that reduce Hd3a and RFT1 expression to delay flowering. We propose that Hd3a and RFT1 are also active locally in leaves to fine-tune photoperiodic flowering responses.




Plastic Transcriptomes Stabilize Immunity to Pathogen Diversity: The Jasmonic Acid and Salicylic Acid Networks Within the Arabidopsis/Botrytis Pathosystem

2017-10-17T08:50:49-07:00

To respond to pathogen attack, selection and associated evolution has led to the creation of plant immune system that are a highly effective and inducible defense system. Central to this system are the plant defense hormones jasmonic acid (JA) and salicylic acid (SA) and crosstalk between the two, which may play an important role in defense responses to specific pathogens or even genotypes. Here, we used the Arabidopsis-B. cinerea pathosystem to test how the host's defense system functions against genetic variation in a pathogen. We measured defense-related phenotypes and transcriptomic responses in Arabidopsis wild-type Col-0 and JA- and SA-signaling mutants, coi1-1 and npr1-1, individually challenged with 96 diverse B. cinerea isolates. Those data showed genetic variation in the pathogen influences on all components within the plant defense system at the transcriptional level. We identified four gene co-expression networks and two vectors of defense variation triggered by genetic variation in B. cinerea. This showed that the JA and SA signaling pathways functioned to constrain/canalize the range of virulence in the pathogen population, but the underlying transcriptomic response was highly plastic. These data showed that plants utilize major defense hormone pathways to buffer disease resistance, but not the metabolic or transcriptional responses to genetic variation within a pathogen.







The Plastid and Mitochondrial Peptidase Network in Arabidopsis thaliana: A Foundation for Testing Genetic Interactions and Functions in Organellar Proteostasis

2017-09-25T11:17:55-07:00

Plant plastids and mitochondria have dynamic proteomes. Protein homeostasis in these organelles is maintained by a proteostasis network containing protein chaperones, peptidases and their substrate recognition factors. However, many peptidases, as well as their functional connections and substrates, are poorly characterized. This review provides a systematic insight into the organellar peptidase network in Arabidopsis. We present a compendium of known and putative Arabidopsis peptidases and inhibitors, and compare the distribution of plastid and mitochondrial peptidases to the total peptidase complement. This comparison shows striking biases, such as the (near) absence of cysteine and aspartic peptidases and peptidase inhibitors, whereas other peptidase families were exclusively organellar; reasons for such biases are discussed. A genome-wide mRNA-based co-expression data set was generated based on quality controlled and normalized public data, and used to infer additional plastid peptidases, and to generate a co-expression network for 97 organellar peptidase baits (1742 genes, making 2544 edges). The graphical network includes 10 modules with specialized/enriched functions, such as mitochondrial protein maturation, thermotolerance, senescence, or enriched subcellular locations such as the thylakoid lumen or chloroplast envelope. The peptidase compendium, including the autophagy and proteosomal systems, and the annotation based on the MEROPS nomenclature of peptidase clans and families, is incorporated into the Plant Proteome Database (PPDB).




S-type Anion Channels SLAC1 and SLAH3 Function as Essential Negative Regulators of Inward K+ Channels and Stomatal Opening in Arabidopsis

2016-03-24T11:37:57-07:00

Drought stress induces stomatal closure and inhibits stomatal opening simultaneously. However, the underlying molecular mechanism is still largely unknown. Here we show that S-type anion channels SLAC1 and SLAH3 mainly inhibit inward K+ (K+in) channel KAT1 by protein-protein interaction, and consequently prevent stomatal opening in Arabidopsis. Voltage-clamp results demonstrated that SLAC1 inhibited KAT1 dramatically, but did not inhibit KAT2. SLAH3 inhibited KAT1 to a weaker degree relative to SLAC1. Both the N terminus and the C terminuses of SLAC1 inhibited KAT1, but the inhibition by the N terminus was stronger. The C terminus was essential for the inhibition of KAT1 by SLAC1. Furthermore, drought stress strongly up-regulated the expression of SLAC1 and SLAH3 in Arabidopsis guard cells, and the over-expression of wild type and truncated SLAC1 dramatically impaired K+in currents of guard cells and light-induced stomatal opening. Additionally, the inhibition of KAT1 by SLAC1 and KC1 only partially overlapped, suggesting that SLAC1 and KC1 inhibited K+in channels using different molecular mechanisms. Taken together, we discovered a novel regulatory mechanism for stomatal movement, in which singling pathways for stomatal closure and opening are directly coupled together by protein-protein interaction between SLAC1/SLAH3 and KAT1 in Arabidopsis.