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bioRxiv2018

A shared cis-regulatory module activates transcription in the suspensor of plant embryos

The mechanisms controlling the transcription of gene sets in specific regions of a plant embryo shortly after fertilization remain unknown. Previously, we showed that G564 mRNA, encoding a protein of unknown function, accumulates to high levels in the giant suspensor of both Scarlet Runner Bean (SRB) and Common Bean embryos, and a cis-regulatory module containing three unique DNA sequences, designated as the 10-bp, Region 2, and Fifth motifs, is required for G564 suspensor-specific transcription [Henry, K. F. et al., Plant Mol. Biol. 88(3):207-217 (2015); Kawashima, T. et al., Proc. Natl. Acad. Sci USA 106(9):3627-3632 (2009)]. We tested the hypothesis that these motifs are also required for transcription of the SRB GA 20-oxidase gene, which encodes a gibberellic acid hormone biosynthesis enzyme and is co-expressed with G564 at a high level in giant bean suspensors. We used deletion and gain-of-function experiments in transgenic tobacco embryos to show that two GA 20-oxidase DNA regions are required for suspensor-specific transcription - one in the 5 untranslated region (UTR) (+119 to +205) and another in the 5 upstream region (-341 to -316). Mutagenesis of sequences in these two regions determined that the cis-regulatory motifs required for G564 suspensor transcription are also required for GA 20-oxidase transcription within the suspensor, although the motif arrangement differs. Our results demonstrate the flexibility of motif positioning within a cis-regulatory module that activates gene transcription within giant bean suspensors, and suggest that G564 and GA 20-oxidase comprise part of a suspensor gene regulatory network.\n\nSignificanceLittle is known about how genes are expressed in different plant embryo regions. We tested the hypothesis that shared cis-regulatory motifs control the transcription of genes specifically in the suspensor. We carried out functional studies with the Scarlet Runner Bean (SRB) GA 20-oxidase gene that encodes a gibberellic acid (GA) hormone biosynthesis enzyme, and is expressed specifically within the suspensor. We show that cis-regulatory motifs required for GA 20-oxidase transcription within the suspensor are the same as those required for suspensor-specific transcription of the SRB G564 gene, although motif number, spacing and order differ. These cis-elements constitute a control module that is required to activate genes in the SRB suspensor and may form part of a suspensor regulatory network.

plant biology↗

bioRxiv2018

Rhizosphere microbes and host plant genotype influence the plant metabolome and reduce insect herbivory

O_LIRhizosphere microbes affect plant performance, including plant resistance against insect herbivores; yet, the relative influence of rhizosphere microbes vs. plant genotype on herbivory levels and on metabolites related to defense remains unclear.\nC_LIO_LIIn Boechera stricta, we tested the effects of rhizosphere microbes and plant genotype on herbivore resistance, the primary metabolome, and select secondary metabolites.\nC_LIO_LIPlant populations differed significantly in the concentrations of 6 glucosinolates (GLS), secondary metabolites known to provide herbivore resistance in the Brassicaceae, and the population with lower GLS levels experienced ~60% higher levels of aphid (Aphis spp.) attack; no effect was observed of GLS on damage by a second herbivore, flea beetles (Altica spp.). Rhizosphere microbiome (intact vs. disrupted) had no effect on plant GLS concentrations. However, aphid number and flea beetle damage were respectively ~3-fold and 7-fold higher among plants grown in the disrupted rhizosphere microbiome treatment, and distinct (as estimated from 16s rRNA amplicon sequencing) intact native microbiomes also differed in their effects on herbivore damage. These differences may be attributable to shifts in primary metabolic pathways.\nC_LIO_LIThe findings suggest that rhizosphere microbes can play a greater role than plant genotype in defense against insect herbivores, and act through mechanisms independent of plant genotype.\nC_LI

plant biology↗

bioRxiv2018

Nitro-Oleic Acid Induced Reactive Oxygen Species Formation and Plant Defense Signaling in Tomato Cell Suspensions

Nitrated fatty acids (NO2-FAs) are formed by the addition reaction of nitric oxide- and nitrite-derived nitrogen dioxide with unsaturated fatty acids. Nitrated fatty acids act as signaling molecules in mammals through the formation of covalent adducts with cellular thiols. The study of NO2-FAs in plant systems constitutes an interesting and emerging area. The presence of NO2-FA has been reported in olives, peas, rice and in Arabidopsis. To gain a better understanding of the role of NO2-FA on plant physiology, we analyzed the effects of exogenous application of nitro-oleic acid (NO2-OA) to tomato cell cultures. We found that NO2-OA induced reactive oxygen species (ROS) production in a dose-dependent manner via activation of NADPH oxidases, which requires calcium entry from the extracellular compartment and protein kinase activation, a mechanism that resembles the plant defense responses. NO2-OA-induced ROS production, expression of plant defense genes and led to cell death. The mechanism of action of NO2-OA involves a reduction in the glutathione cellular pool and covalently addition reactions with protein thiols and reduced glutathione. Altogether, these results indicate that NO2-OA triggers responses associated with plant defense, revealing its possible role as a signal molecule in biotic stress.\n\nAbbreviations

plant biology↗

bioRxiv2018

BED-domain containing immune receptors confer diverse resistance spectra to yellow rust

Introductory paragraph Introductory paragraph Main Methods Author contributions Data availability Competing interests References Crop diseases reduce wheat yields by ~25% globally and thus pose a major threat to global food security1. Genetic resistance can reduce crop losses in the field and can be selected for through the use of molecular markers. However, genetic resistance often breaks down following changes in pathogen virulence, as experienced with the wheat yellow (stripe) rust fungus Puccinia striiformis f. sp. tritici (Pst)2. This highlights the need to (i) identify genes that alone or in combination provide broad-spectrum resistance and (ii) increase our understanding of the underlying molecular mod ...

plant biology↗

bioRxiv2018

Varieties of the plant Ctenante oppenheimiana: A colorful enigma of evolution.

The plant Ctenante oppenheimiana presents an interesting contrast of colors in the abaxial epidermis. A striking feature is that the stomata are green and cover a purple pavement where the pavement cells have green cellular walls. These characteristics have been used in studies about ecophysiology and phenotypic plasticity. However, the existence of a second tricolor variety of the plant make these characteristics even more heterogeneous and introduce new paradigms of the physiological role underlying this morphology. In this work we show by optical microscopy images the striking differences between the varieties bicolor and tricolor of the plant Ctenante oppenheimiana

plant biology↗

bioRxiv2018

Improvements to the rice genome annotation through large-scale analysis of RNA-Seq and proteomics datasets

Rice (Oryza sativa) is one of the most important worldwide crops. The genome has been available for over 10 years and has undergone several rounds of annotation. We created a comprehensive database of transcripts from 29 public RNA sequencing datasets, officially predicted genes from Ensembl plants, and common contaminants in which to search for protein-level evidence. We re-analysed nine publicly accessible rice proteomics datasets. In total, we identified 420K peptide spectrum matches from 47K peptides and 8,187 protein groups. 4168 peptides were initially classed as putative novel peptides (not matching official genes). Following a strict filtration scheme to rule out other possible explanations, we discovered 1,584 high confidence novel peptides. The novel peptides were clustered into 692 genomic loci where our results suggest annotation improvements. 80% of the novel peptides had an ortholog match in the curated protein sequence set from at least one other plant species. For the peptides clustering in intergenic regions (and thus potentially new genes), 101 loci were identified, for which 43 had a high-confidence hit for a protein domain. Our results can be displayed as tracks on the Ensembl genome or other browsers supporting Track Hubs, to support re-annotation of the rice genome.

plant biology↗

bioRxiv2018

Modulation of ACD6 dependent hyperimmunity by natural alleles of an Arabidopsis thaliana NLR resistance gene

Plants defend themselves against pathogens by activating an array of immune responses. Unfortunately, immunity programs may also cause unintended collateral damage to the plant itself. The quantitative disease resistance gene ACCELERATED CELL DEATH 6 (ACD6) serves as a nexus for the trade-off between growth and pathogen resistance in wild populations of Arabidopsis thaliana. An autoimmune allele, ACD6-Est, first identified in the natural accession Est-1, is found in over 10% of wild strains, even though it causes a clear fitness penalty under optimal growth conditions. There is, however, extensive variation in the strength of the autoimmune phenotype expressed by strains with an ACD6-Est allele, indicative of genetic modifiers. Quantitative genetic analysis suggests that the population genetic basis of ACD6 modulation is complex, with different strains often carrying different large-effect modifiers. One modifier is SUPPRESSOR OF NPR1-1, CONSTITUTIVE 1 (SNC1), located in a highly polymorphic cluster of nucleotide-binding domain and leucine-rich repeat (NLR) immune receptor genes, which are prototypes for qualitative disease resistance genes. Allelic variation at SNC1 correlates with ACD6-Est activity in multiple accessions, and a common structural variant affecting the NL linker sequence can explain differences in SNC1 activity. Taken together, we find that an NLR gene can mask the activity of an ACD6 autoimmune allele in natural A. thaliana populations, thereby linking different arms of the plant immune system.\n\nAuthor summaryPlants defend themselves against pathogens by activating immune responses. Unfortunately, these can cause unintended collateral damage to the plant itself. Nevertheless, some wild plants have genetic variants that confer a low threshold for the activation of immunity. While these enable a plant to respond particularly quickly to pathogen attack, such variants might be potentially dangerous. We are investigating one such variant of the immune gene ACCELERATED CELL DEATH 6 (ACD6) in the plant Arabidopsis thaliana. We discovered that there are variants at other genetic loci that can mask the effects of an overly active ACD6 gene. One of these genes, SUPPRESSOR OF NPR1-1, CONSTITUTIVE 1 (SNC1), codes for a known immune receptor. The SNC1 variant that attenuates ACD6 activity is rather common in A. thaliana populations, suggesting that new combinations of the hyperactive ACD6 variant and this antagonistic SNC1 variant will often arise by natural crosses. Similarly, because the two genes are unlinked, outcrossing will often lead to the hyperactive ACD6 variants being unmasked again. We propose that allelic diversity at SNC1 contributes to the maintenance of the hyperactive ACD6 variant in natural A. thaliana populations.

plant biology↗

bioRxiv2018

The genetic architecture of shoot and root trait divergence between upland and lowland ecotypes of a perennial grass.

Introduction Introduction Materials and Methods Results Discussion Conclusion Author Contributions: References Adaptation to abiotic stress is an important driver of contemporary evolution in plant populations. Abiotic stressors have been implicated as driving factors in ecological speciation (Stebbins, 1952;Lexer & Fay, 2005), where populations have diverged across a number of traits, exhibit different niche characteristics, and eventually become reproductively isolated (Clausen, 1951; Lowry, 2012; Yardeni et al., 2016). Local adaptation to soil water availability is an especially important driver of plant evolution (Stebbins, 1952; Rajakaruna, 2004; ...

plant biology↗

bioRxiv2018

Exogenous putrescine alleviates photoinhibition caused by salt stress through increasing cyclic electron flow in cucumber

When plants suffer from abiotic stresses, cyclic electron flow (CEF) is induced for photoprotection. Putrescine (Put), a main polyamine in chloroplasts, plays a critical role in stress tolerance. To elucidate the mechanism of Put regulating CEF for salt-tolerance in cucumber leaves, we measured chlorophyll fluorescence, P700 redox state, ATP and NADPH accumulation and so on. The maximum photochemical efficiency of PSII (Fv/Fm) was not influenced by NaCl and/or Put, but the activity of PSI reaction center (P700) was seriously inhibited by NaCl. Salt stress induced high level of CEF, moreover, NaCl and Put treated plants exhibited much higher CEF activity and ATP accumulation than single salt-treated plants to provide adequate ATP/NADPH ratio for plants growth. Furthermore, Put decreased the trans-membrane proton gradient ({Delta}pH), accompanied by reducing the pH-dependent non-photochemical quenching (qE) and increasing efficient quantum yield of PSII (Y(II)). The ratio of NADP+/NADPH in salt stressed leaves was significantly increased by Put, indicating that Put relieved over-reduction pressure at PSI accepter side. Taken together, our results suggest that exogenous Put enhances CEF to supply extra ATP for PSI recovery and CO2 assimilation, decreases {Delta}pH for electron transport related proteins staying active, and enable the non-photochemical quenching transformed into photochemical quenching.

plant biology↗

bioRxiv2018

Long non-coding RNAs in wild wheat progenitors

Triticum urartu and Aegilops tauschii are the diploid progenitors of the hexaploid Triticum aestivum (AuAuBBDD), donors of the Au and D genome respectively. In this work we investigate the long noncoding RNAs (lncRNAs) component of the genomes of these two wild wheat relatives. Sixty-eight RNA-seq libraries generated from several organs and conditions were retrieved from public databases. We annotated and characterized 14,515 T. urartu and 20,908 Ae. tauschii bona-fide lncRNA transcripts that show features similar to those of other plant and animal counterparts. Thousands of lncRNAs were found significantly modulated in different organs and exhibited organ specific expression, with a predominant accumulation in the spike, fostering the hypothesis of their crucial role in reproductive organs. Most of the organ-specific lncRNAs were found associated with transposable elements (TEs), indicating the possible role of TEs in lncRNA origin, differentiation and function. The majority of T. urartu and Ae. tauschii lncRNAs appear to be species-specific; nevertheless, we found some lncRNAs conserved between the two wheat progenitors, highlighting the presence and conservation of exonic splicing enhancers sites in multi-exon conserved lncRNAs. In addition, we found cases of lncRNA conservation and their cis regulatory regions spanning the wheat pre-domestication and post-domestication period. Altogether, these results represent the first comprehensive genome-wide encyclopedia of lncRNAs in wild wheat relatives, and they provide clues as to the hidden regulatory pathway mediated by long noncoding RNAs in these largely unexplored wheat progenitors.

plant biology↗

bioRxiv2018

Structural insights into DNA sequence recognition by Arabidopsis ETHYLENE RESPONSE FACTOR 96

The phytohormone ethylene is widely involved in many developmental processes and is a crucial regulator of defense responses against biotic and abiotic stresses in plants. Ethylene-responsive element binding protein (EREBP), a member of the APETALA2/ethylene response factor (AP2/ERF) superfamily, is a transcription factor that regulates stress-responsive genes by recognizing a specific cis-acting element of target DNA. A previous study showed only the NMR structure of the AP2/ERF domain of AtERF100 in complex with a GCC box DNA motif. In this report, we determined the crystal structure of AtERF96 in complex with a GCC box at atomic resolution. We analyzed the binding residues of the conserved AP2/ERF domain in the DNA recognition sequence. In addition to the AP2/ERF domain, an N-terminal -helix of AtERF96 participates in DNA interaction in the flanking region. We also demonstrated the structure of AtERF96 EDLL motif, a unique conserved motif in the group IX of AP2/ERF family, is critical for the transactivation of defense-related genes. Our study establishes the structural basis of the AtERF96 transcription factor in complex with the GCC box, as well as the DNA binding mechanisms of the N-terminal -helix and AP2/ERF domain.

plant biology↗

bioRxiv2018

Cell type identity determines transcriptomic immune responses in Arabidopsis thaliana roots.

Root pathogens are a major threat in global crop production and protection strategies are required to sustainably enhance the efficiency of root immunity. Our understanding of root immunity is still limited relative to our knowledge of immune responses in leaves. In an effort to reveal the organisation of immunity in roots, we undertook a cell type-specific transcriptome analysis to identify gene networks activated in epidermis, cortex and pericycle cells of Arabidopsis roots upon treatment with two immunity elicitors, the bacterial microbe-associated molecular pattern flagellin, and the endogenous damage-associated molecular pattern Pep1. Our analyses revealed that both elicitors induced immunity gene networks in a cell type-specific manner. Interestingly, both elicitors did not alter cell identity-determining gene networks. Using sophisticated paired motif promoter analyses, we identified key transcription factor pairs involved in the regulation of cell type-specific immunity networks. In addition, our data show that cell identity networks integrate with cell immunity networks to activate cell type-specific immune response according to the functional capabilities of each cell type.\n\nMaterial Distribution FootnoteThe author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) is: Patrick Schafer (p.schafer@warwick.ac.uk).

plant biology↗

bioRxiv2018

Nuclear import of Arabidopsis POLY(ADP-RIBOSE) POLYMERASE 2 is mediated by importin-α and a nuclear localization sequence located between the predicted SAP domains

Proteins of the poly(ADP-ribose) polymerase (PARP) family modify target proteins by covalent attachment of ADP-ribose moieties onto amino acid side chains. In Arabidopsis, PARP proteins contribute to repair of DNA lesions and modulate plant responses to various abiotic and biotic stressors. Arabidopsis PARP1 and PARP2 are nuclear proteins and given that their molecular weights exceed the diffusion limit of nuclear pore complexes, an active import mechanism into the nucleus is likely. Here we use confocal microscopy of fluorescent protein-tagged Arabidopsis PARP2 and PARP2 deletion constructs in combination with site-directed mutagenesis to identify a nuclear localization sequence in PARP2 that is required for nuclear import. We report that in co-immunoprecipitation assays PARP2 interacts with several isoforms of the importin- group of nuclear transport adapters and that PARP2 binding to IMPORTIN-2 is mediated by the identified nuclear localization sequence. Our results demonstrate that PARP2 is a cargo protein of the canonical importin-/{beta} nuclear import pathway.

plant biology↗

bioRxiv2018

Robust predictions of specialized metabolism genes through machine learning

Plant specialized metabolism (SM) enzymes produce lineage-specific metabolites with important ecological, evolutionary, and biotechnological implications. Using Arabidopsis thaliana as a model, we identified distinguishing characteristics of SM and GM (general metabolism, traditionally referred to as primary metabolism) genes through a detailed study of features including duplication pattern, sequence conservation, transcription, protein domain content, and gene network properties. Analysis of multiple sets of benchmark genes revealed that SM genes tend to be tandemly duplicated, co-expressed with their paralogs, narrowly expressed at lower levels, less conserved, and less well connected in gene networks relative to GM genes. Although the values of each of these features significantly differed between SM and GM genes, any single feature was ineffective at predicting SM from GM genes. Using machine learning methods to integrate all features, a well performing prediction model was established with a true positive rate of 0.87 and a true negative rate of 0.71. In addition, 86% of known SM genes not used to create the machine learning model were predicted as SM genes, further demonstrating its accuracy. We also demonstrated that the model could be further improved when we distinguished between SM, GM, and junction genes responsible for reactions shared by SM and GM pathways. Application of the prediction model led to the identification of 1,217 A. thaliana genes with previously unknown functions, providing a global, high-confidence estimate of SM gene content in a plant genome.\n\nSignificanceSpecialized metabolites are critical for plant-environment interactions, e.g., attracting pollinators or defending against herbivores, and are important sources of plant-based pharmaceuticals. However, it is unclear what proportion of enzyme-encoding genes play roles in specialized metabolism (SM) as opposed to general metabolism (GM) in any plant species. This is because of the diversity of specialized metabolites and the considerable number of incompletely characterized pathways responsible for their production. In addition, SM gene ancestors frequently played roles in GM. We evaluate features distinguishing SM and GM genes and build a computational model that accurately predicts SM genes. Our predictions provide candidates for experimental studies, and our modeling approach can be applied to other species that produce medicinally or industrially useful compounds.

plant biology↗

bioRxiv2018

Geminivirus Replication Protein impairs SUMO conjugation of PCNA at two acceptor sites

Geminiviruses are DNA viruses that replicate in nuclei of infected plant cells using the plant DNA replication machinery, including PCNA (Proliferating cellular nuclear antigen), a cofactor that orchestrates genome duplication and maintenance by recruiting crucial players to replication forks. These viruses encode a multifunctional protein, Rep, which is essential for viral replication, induces the accumulation of the host replication machinery and interacts with several host proteins, including PCNA and the SUMO E2 conjugation enzyme (SCE1). Post-translational modification of PCNA by ubiquitin or SUMO plays an essential role in the switching of PCNA between interacting partners during DNA metabolism processes (e.g. replication, recombination, repair, etc.). In yeast, PCNA sumoylation has been associated to DNA repair involving homologous recombination (HR). Previously, we reported that ectopic Rep expression results in very specific changes in the sumoylation pattern of plant cells. In this work, we show, using a reconstituted sumoylation system in Escherichia coli, that tomato PCNA is sumoylated at two residues, K254 and K164, and that co-expression of the geminivirus protein Rep suppresses sumoylation at these lysines. Finally, we confirm that PCNA is sumoylated in planta and that Rep also interferes with PCNA sumoylation in plant cells.\n\nImportanceSUMO adducts have a key role in regulating the activity of animal and yeast PCNA on DNA repair and replication. Our work demonstrates for the first time that sumoylation of plant PCNA occurs in plant cells and that a plant virus interferes with this modification. This work marks the importance of sumoylation in allowing viral infection and replication in plants. Moreover, it constitutes a prime example of viral proteins interfering with post-translational modifications of selected host factors to create a proper environment for infection.

plant biology↗

bioRxiv2018

Expression of a glucomannan mannosyltransferase gene (GMMT) from Aloe vera is induced by water deficit and abscisic acid.

HighlightGMMT (a possible CSLA9) from Aloe vera is upregulated during water stress. Aloe vera GMMT expression is also induced by exogenous application of the plant stress hormone abscisic acid (ABA) in non-water-stressed plants.\n\nSummaryIn Aloe barbadensis Miller (Aloe vera), a xerophytic crassulacean acid metabolism (CAM) plant, the main polysaccharide of the gel present in the leaves is an acetylated glucomannan named acemannan. This polysaccharide is responsible for the plant succulence, helping it to retain water. In this study we determined using polysaccharide analysis by carbohydrate gel electrophoresis (PACE) that the acemannan is a glucomannan without galactose side branches. We also investigated the expression of the gene responsible for acemannan backbone synthesis, encoding a glucomannan mannosyltransferase (GMMT). It was found by in silico analyses that the GMMT gene belongs to the cellulose synthase like A type-9 (CSLA9) subfamily. Using RT-qPCR it was found that the expression of GMMT increased in Aloe vera plants subjected to water stress. This expression correlates with an increase of endogenous ABA levels, suggesting that the gene expression could be regulated by ABA. To corroborate this hypothesis, exogenous ABA was applied to non-water-stressed plants, increasing the expression of GMMT significantly 48 h after ABA treatment.

plant biology↗

bioRxiv2018

Vacuolar iron stores gated by NRAMP3 and NRAMP4 are the primary source of iron in germinating seeds

During seed germination, iron (Fe) stored in vacuoles is exported by the redundant NRAMP3 and NRAMP4 transporter proteins. A double nramp3 nramp4 mutant is unable to mobilize Fe stores and does not develop in the absence of external Fe. We used RNA sequencing to compare gene expression in nramp3 nramp4 and wild type during germination and early seedling development. Even though sufficient Fe was supplied, the Fe-responsive transcription factors bHLH38, 39, 100 and 101 and their downstream targets FRO2 and IRT1 mediating Fe uptake were strongly upregulated in the nramp3 nramp4 mutant. Activation of the Fe deficiency response was confirmed by increased ferric chelate reductase activity in the mutant. At early stages, genes important for chloroplast redox control (FSD1, SAPX), Fe homeostasis (FER1, SUFB) and chlorophyll metabolism (HEMA1, NYC1) were downregulated, indicating limited Fe availability in plastids. In contrast, expression of FRO3, encoding a ferric reductase involved in Fe import into the mitochondria, was maintained and Fe-dependent enzymes in the mitochondria were unaffected in nramp3 nramp4. Together these data show that a failure to mobilize Fe stores during germination triggered Fe deficiency responses and strongly affected plastids but not mitochondria.

plant biology↗

bioRxiv2018

DET1-mediated degradation of a SAGA-like deubiquitination module controls H2Bub homeostasis

DE-ETIOLATED 1 (DET1) is an evolutionarily conserved component of the ubiquitination machinery that mediates the destabilization of key regulators of cell differentiation and proliferation in multicellular organisms. In this study, we provide evidence from Arabidopsis that DET1 is essential for the regulation of histone H2B monoubiquitination (H2Bub) over most genes by controlling the stability of a plant deubiquitination module (DUBm). In contrast with yeast and metazoan DUB modules that are associated with the large SAGA complex, the Arabidopsis DUBm only comprises three proteins (hereafter named SGF11, ENY2 and UBP22) and appears to act independently as a major H2Bub deubiquitinase activity. Our study further unveils that DET1-DDB1-Associated-1 (DDA1) protein interacts with SGF11 in vivo, linking the DET1 complex to light-dependent ubiquitin-mediated proteolytic degradation of the DUBm. Collectively, these findings uncover a signaling path controlling DUBm availability, potentially adjusting H2Bub turnover capacity to the cell transcriptional status.

plant biology↗