Nucleotide-binding domain and leucine-rich repeat proteins (NLRs) are important receptors in plant immunity that allow recognition of pathogen effectors. The rice NLR RGA5 recognizes the Magnaporthe oryzae effector AVR-Pia through direct interaction. Here, we gained detailed insights into the molecular and structural bases of AVR-Pia-RGA5 interaction and the role of the RATX1 decoy domain of RGA5. NMR titration combined with in vitro and in vivo protein-protein interaction analyses identified the AVR-Pia interaction surface that binds to the RATX1 domain. Structure-informed AVR-Pia mutants showed that, although AVR-Pia associates with additional sites in RGA5, binding to the RATX1 domain is necessary for pathogen recognition, but can be of moderate affinity. Therefore, RGA5-mediated resistance is highly resilient to mutations in the effector. We propose a model that explains such robust effector recognition as a consequence, and an advantage, of the combination of integrated decoy domains with additional independent effector-NLR interactions.
Oomycetes, or water moulds, are fungal-like organisms phylogenetically related to algae. They cause devastating diseases in both plants and animals. Here, we describe seven oomycete species that are emerging or re-emerging threats to agriculture, horticulture, aquaculture and natural ecosystems. They include the plant pathogens Phytophthora infestans , Phytophthora palmivora , Phytophthora ramorum , Plasmopara obducens , and the animal pathogens Aphanomyces invadans , Saprolegnia parasitica and Halioticida noduliformans . For each species, we describe its pathology, importance and impact, discuss why it is an emerging threat and briefly review current research activities.
This article is part of the themed issue ‘Tackling emerging fungal threats to animal health, food security and ecosystem resilience’.
We examine recent evidence for ratchet-like genome degradation in mycoheterotrophs, plants that obtain nutrition from fungi. Initial loss of the NADH dehydrogenase-like (NDH) complex may often set off an irreversible evolutionary cascade of photosynthetic gene losses. Genes for plastid-encoded subunits of RNA polymerase and photosynthetic enzymes with secondary functions (Rubisco and ATP synthase) can persist initially, with nonsynchronous and quite broad windows in the relative timing of their loss. Delayed losses of five core nonbioenergetic genes (especially trnE and accD, which respectively code for glutamyl tRNA and a subunit of acetyl-CoA carboxylase) probably explain long-term persistence of heterotrophic plastomes. The observed range of changes of mycoheterotroph plastomes is similar to that of holoparasites, although greater diversity of both probably remains to be discovered. These patterns of gene loss/retention can inform research programs on plastome function.
Organ formation in animals and plants relies on precise control of cell state transitions to turn stem cell daughters into fully differentiated cells. In plants, cells cannot rearrange due to shared cell walls. Thus, differentiation progression and the accompanying cell expansion must be tightly coordinated across tissues. PLETHORA (PLT) transcription factor gradients are unique in their ability to guide the progression of cell differentiation at different positions in the growing Arabidopsis thaliana root, which contrasts with well-described transcription factor gradients in animals specifying distinct cell fates within an essentially static context. To understand the output of the PLT gradient, we studied the gene set transcriptionally controlled by PLTs. Our work reveals how the PLT gradient can regulate cell state by region-specific induction of cell proliferation genes and repression of differentiation. Moreover, PLT targets include major patterning genes and autoregulatory feedback components, enforcing their role as master regulators of organ development.
Cell death and differentiation is a monthly research journal focused on the exciting field of programmed cell death and apoptosis. It provides a single accessible source of information for both scientists and clinicians, keeping them up-to-date with advances in the field. It encompasses programmed cell death, cell death induced by toxic agents, differentiation and the interrelation of these with cell proliferation.
Calcium-dependent protein kinases (CDPKs) are Ca2+-sensors that play pivotal roles in plant development and stress responses. They have the unique ability to directly translate intracellular Ca2+ signals into reversible phosphorylation events of diverse substrates which can mediate interactions with 14-3-3 proteins to modulate protein functions. Recent studies have revealed roles for the coordinated action of CDPKs and 14-3-3s in regulating diverse aspects of plant biology including metabolism, development, and stress responses. We review here the underlying interaction and cross-regulation of the two signaling proteins, and we discuss how this insight has led to the emerging concept of CDPK/14-3-3 signaling modules that could contribute to response specificity.
Leaf shape varies spectacularly among plants. Leaves are the primary source of photoassimilate in crop plants, and understanding the genetic basis of variation in leaf morphology is critical to improving agricultural productivity. Leaf shape played a unique role in cotton improvement, as breeders have selected for entire and lobed leaf morphs resulting from a single locus, okra (L-D1), which is responsible for the major leaf shapes in cotton. The L-D1 locus is not only of agricultural importance in cotton, but through pioneering chimeric and morphometric studies, it has contributed to fundamental knowledge about leaf development. Here we show that an HD-Zip transcription factor homologous to the LATE MERISTEM IDENTITY1 (LMI1) gene of Arabidopsis is the causal gene underlying the L-D1 locus. The classical okra leaf shape allele has a 133-bp tandem duplication in the promoter, correlated with elevated expression, whereas an 8-bp deletion in the third exon of the presumed wild-type normal allele causes a frame-shifted and truncated coding sequence. Our results indicate that subokra is the ancestral leaf shape of tetraploid cotton that gave rise to the okra allele and that normal is a derived mutant allele that came to predominate and define the leaf shape of cultivated cotton. Virus-induced gene silencing (VIGS) of the LMI1-like gene in an okra variety was sufficient to induce normal leaf formation. The developmental changes in leaves conferred by this gene are associated with a photosynthetic transcriptomic signature, substantiating its use by breeders to produce a superior cotton ideotype.
The environment during seed production has major impacts on the behaviour of progeny seeds. It can be shown that for annual plants temperature perception over the whole life history of the mother can affect the germination rate of progeny, and instances have been documented where these affects cross whole generations. Here we discuss the current state of knowledge of signal transduction pathways controlling environmental responses during seed production, focusing both on events that take place in the mother plant and those that occur directly as a result of environmental responses in the developing zygote. We show that seed production environment effects are complex, involving overlapping gene networks active independently in fruit, seed coat, and zygotic tissues that can be deconstructed using careful physiology alongside molecular and genetic experiments.
The type III secretion (T3S) injectisome is a specialized protein nanomachine that is critical for the pathogenicity of many Gram-negative bacteria, including purveyors of plague, typhoid fever, whooping cough, sexually transmitted infections and major nosocomial infections. This syringe-shaped 3.5-MDa macromolecular assembly spans both bacterial membranes and that of the infected host cell. The internal channel formed by the injectisome allows for the direct delivery of partially unfolded virulence effectors into the host cytoplasm1. The structural foundation of the injectisome is the basal body, a molecular lock-nut structure composed predominantly of three proteins that form highly oligomerized concentric rings spanning the inner and outer membranes2, 3, 4, 5. Here we present the structure of the prototypical Salmonella enterica serovar Typhimurium pathogenicity island 1 basal body, determined using single-particle cryo-electron microscopy, with the inner-membrane-ring and outer-membrane-ring oligomers defined at 4.3 Å and 3.6 Å resolution, respectively. This work presents the first, to our knowledge, high-resolution structural characterization of the major components of the basal body in the assembled state, including that of the widespread class of outer-membrane portals known as secretins.
LOCALIZER is a machine learning method for subcellular localization prediction in plant cells. LOCALIZER has been trained to predict either the localization of plant proteins or the localization of eukaryotic effector proteins to chloroplasts, mitochondria or nuclei in the plant cell.
The localization to chloroplasts and mitochondria is predicted using the presence of transit peptides and the localization to nuclei is predicted using a collection of nuclear localization signals (NLSs).
The oomycete Phytophthora infestans was the causal agent of the Irish Great Famine and is a recurring threat to global food security. The pathogen can reproduce both sexually and asexually, with high potential to adapt to various environments and great risk to break disease resistance genes in potato. As other oomycetes, P. infestans is regarded to be diploid during the vegetative phase of its life cycle, although some studies reported trisomy, and polyploidy. Using microsatellite fingerprinting, genome-wide assessment of SNP polymorphism, nuclear DNA quantification, and microscopic counting of chromosome numbers we assessed the ploidy level of isolates. All progeny from sexual populations of P. infestans in nature were found to be diploid, in contrast nearly all dominant asexual lineages, including the most important pandemic clonal lineages US-1 and 13_A2 were triploid. Such triploids possess significantly more allelic variation than diploids. We observed that triploid genotype can change to a diploid genome constitution when exposed to artificial stress conditions. This study reveals that fluctuations in the ploidy level maybe a key factor in the adaptation process of this notorious plant destroyer and imposes an extra challenge to control this disease.
Bacteria thrive on sugar. So do plant cells. Yamada et al. now show how the fight for sugar plays out in the extracellular spaces around plant cells when pathogenic bacteria are invading the plant (see the Perspective by Dodds and Lagudah). In the model plant Arabidopsis , part of the defense response incited by the presence of pathogenic bacteria includes transcriptional and posttranscriptional regulation of sugar transporters. The resulting uptake of monosaccharides from the extracellular space makes life a little bit more difficult for the invading bacteria.
Science , this issue p. ; see also p. 
Citrus is a highly valued tree crop worldwide, while, at the same time, citrus production faces many biotic challenges, including bacterial canker and Huanglongbing (HLB). Breeding for disease resistant varieties is the most efficient and sustainable approach to control plant diseases. Traditional breeding of citrus varieties is challenging due to multiple limitations, including polyploidy, polyembryony, extended juvenility, and long crossing cycles. Targeted genome editing technology has the potential to shorten varietal development for some traits, including disease resistance. Here, we used CRISPR/Cas9/sgRNA technology to modify the canker susceptibility gene CsLOB1 in Duncan grapefruit. Six independent lines, DLOB2, DLOB3, DLOB9, DLOB10, DLOB11 and DLOB12, were generated. Targeted next-generation sequencing of the six lines showed the mutation rate was 31.58%, 23.80%, 89.36%, 88.79%, 46.91% and 51.12% for DLOB2, DLOB3, DLOB9, DLOB10, DLOB11, and DLOB12, respectively, of the cells in each line. DLOB2 and DLOB3 showed canker symptoms similar to wild type grapefruit, when inoculated with the pathogen Xanthomonas citri subsp. citri (Xcc). No canker symptoms were observed on DLOB9, DLOB10, DLOB11 and DLOB12 at 4 days post inoculation (DPI) with Xcc. Pustules caused by Xcc were observed on DLOB9, DLOB10, DLOB11 and DLOB12 in later stages, which were much reduced compared to that on wild type grapefruit. The pustules on DLOB9 and DLOB10 did not develop into typical canker symptoms. No side effects and off-target mutations were detected in the mutated plants. This study indicates that genome editing using CRISPR technology will provide a promising pathway to generate disease resistant citrus varieties.
“ A radio series on the history of music called “Composers Datebook” ends each vignette by reminding listeners that “All music was once new.” Well, in evolutionary terms, every tissue and every organ was once an innovation, assembled de novo or from bits and pieces of pre-existing parts. How novelty arises is a fundamental question in the field of developmental evolution. In plants, the legume nodule is a fascinating system for studying the process by which a novel structure evolves and is modified in diverse lineages. ”
Via Jean-Michel Ané, IvanOresnik, Xiefang lab
The extracellular space (apoplast) of plant tissue represents a critical battleground between plants and attacking microbes. Here we show that a pathogen-secreted apoplastic Xyloglucan-specific EndoGlucanase PsXEG1 is a focus of this struggle in the Phytophthora sojae-soybean interaction. We show that soybean produces an apoplastic Glucanase Inhibitor Protein, (GmGIP1), that binds to PsXEG1 to block its contribution to virulence. P. sojae however, secretes a paralogous PsXEG1-Like Protein (PsXLP1) that has lost enzyme activity but binds to GmGIP1 more tightly than does PsXEG1, thus freeing PsXEG1 to support P. sojae infection. The PsXEG1 and PsXLP1gene pair is conserved in many Phytophthora species, and the P. parasitica orthologs PpXEG1 and PpXLP1 have similar functions. Thus this apoplastic decoy strategy maybe widely employed in Phytophthora pathosystems.
The presented review discusses state-of-the-art mass spectrometric methods, which have been developed and applied for investigation of chemical processes in the soil-root interface, the so-called rhizosphere. Rhizosphere soil's physical and chemical characteristics are to a great extent influenced by a complex mixture of compounds released from plant roots, i.e. root exudates, which have a high impact on nutrient and trace element dynamics in the soil-root interface as well as on microbial activities or soil physico-chemical characteristics. Chemical characterization as well as accurate quantification of the compounds present in the rhizosphere is a major prerequisite for a better understanding of rhizosphere processes and requires the development and application of advanced sampling procedures in combination with highly selective and sensitive analytical techniques. During the last years, targeted and non-targeted mass spectrometry-based methods have emerged and their combination with specific separation methods for various elements and compounds of a wide polarity range have been successfully applied in several studies. With this review we critically discuss the work that has been conducted within the last decade in the context of rhizosphere research and elemental or molecular mass spectrometry emphasizing different separation techniques as GC, LC and CE. Moreover, selected applications such as metal detoxification or nutrient acquisition will be discussed regarding the mass spectrometric techniques applied in studies of root exudates in plant-bacteria interactions. Additionally, a more recent isotope probing technique as novel mass spectrometry based application is highlighted.
Background. Plant-pathogenic oomycetes are responsible for economically important losses on crops worldwide. Phytophthora palmivora, a broad-host-range tropical relative of the potato late blight pathogen, causes rotting diseases in many important tropical crops including papaya, cocoa, oil palm, black pepper, rubber, coconut, durian, mango, cassava and citrus. Transcriptomics have helped to identify repertoires of host-translocated microbial effector proteins which counteract defenses and reprogram the host in support of infection. As such, these studies have helped understanding of how pathogens cause diseases. Despite the importance of P. palmivora diseases, genetic resources to allow for disease resistance breeding and identification of microbial effectors are scarce. Results. We employed the model plant Nicotiana benthamiana to study the P. palmivora root infections at the cellular and molecular level. Time-resolved dual transcriptomics revealed different pathogen and host transcriptome dynamics. De novo assembly of P. palmivora transcriptome and semi-automated prediction and annotation of the secretome enabled robust identification of conserved infection-promoting effectors. We show that one of them, REX3, suppresses plant secretion processes. In a survey for early transcriptionally activated plant genes we identified a N. benthamiana gene specifically induced at infected root tips that encodes a peptide with danger-associated molecular features. Conclusions. These results constitute a major advance in our understanding of P. palmivora diseases and establish extensive resources for P. palmivora pathogenomics, effector-aided resistance breeding and the generation of induced resistance to Phytophthora root infections. Furthermore, our approach to find infection relevant secreted genes is transferable to other pathogen-host interactions and not restricted to plants.
"Notably, all required functional components were identified by metagenomics, enabling validation of robust in vivo RNA-guided DNA interference activity in E. coli. Interrogation of environmental microbial communities combined with in vivo experiments allows access to an unprecedented diversity of genomes whose content will expand the repertoire of microbe-based biotechnologies"...
Plants are energy storage factories. Photosynthetic cells convert energy from sunlight to sugars that are transported to growing tissues via both extracellular and intercellular trafficking pathways. Many pathogens have evolved mechanisms to infect the nutrient-rich niche of plant tissues and exploit these sugar pipelines. Some pathogens manipulate sugar transport to enhance their access to carbohydrate. For example, Xanthomonas bacteria deliver transcriptionactivator–like effector proteins into leaf cells. These proteins induce expression of SWEET family sugar transporters to release sucrose into the apoplastic (extracellular) space where the bacteria grow ( 1 ). On page 1427 of this issue, Yamada et al. ( 2 ) show that, in return, plants can also regulate sugar transporters, to redistribute the sugars away from the infection niche, removing the pathogens' energy source and limiting their proliferation.
The study of leaf functional trait relationships, the so-called leaf economics spectrum1,2, is based on the assumption of high-light conditions (as experienced by sunlit leaves). Owing to the exponential decrease of light availability through canopies, however, the vast majority of the world's vegetation exists in at least partial shade. Plant functional traits vary in direct dependence of light availability3, with different traits varying to different degrees, sometimes in conflict with expectations from the economic spectrum3. This means that the derived trait relationships of the global leaf economic spectrum are probably dependent on the extent to which observed data in existing large-scale plant databases represent high-light conditions. Here, using an extensive worldwide database of within-canopy gradients of key physiological, structural and chemical traits3, along with three different global trait databases4,5, we show that: (1) accounting for light-driven trait plasticity can reveal novel trait relationships, particularly for highly plastic traits (for example, the relationship between net assimilation rate per area (Aa) and leaf mass per area (LMA)); and (2) a large proportion of leaf traits in current global plant databases reported as measured in full sun were probably measured in the shade. The results show that even though the majority of leaves exist in the shade, along with a large proportion of observations, our current understanding is too focused on conditions in the sun.
The pressing global issue of food insecurity due to population growth, diminishing land and variable climate can only be addressed in agriculture by improving both maximum crop yield potential and resilience1, 2. Genetic modification is one potential solution, but has yet to achieve worldwide acceptance, particularly for crops such as wheat3. Trehalose-6-phosphate (T6P), a central sugar signal in plants, regulates sucrose use and allocation, underpinning crop growth and development4, 5. Here we show that application of a chemical intervention strategy directly modulates T6P levels in planta. Plant-permeable analogues of T6P were designed and constructed based on a ‘signalling-precursor’ concept for permeability, ready uptake and sunlight-triggered release of T6P in planta. We show that chemical intervention in a potent sugar signal increases grain yield, whereas application to vegetative tissue improves recovery and resurrection from drought. This technology offers a means to combine increases in yield with crop stress resilience. Given the generality of the T6P pathway in plants and other small-molecule signals in biology, these studies suggest that suitable synthetic exogenous small-molecule signal precursors can be used to directly enhance plant performance and perhaps other organism function.
ITHACA, NY–Researchers have sequenced the genome of the whitefly (Bemisia tabici), an invasive insect responsible for spreading plant viruses worldwide, causing billions of dollars in crop losses each year.
The genome study, led by Associate Professor Zhangjun Fei of the Boyce Thompson Institute (BTI), offers many clues to the insect's remarkable ability to resist pesticides, transmit more than 300 plant viruses, and to feed on at least 1,000 different plant species. Published today in the journal BMC Biology, the study will serve as a foundation for future work to combat this global pest.
"Whitefly is an economically important pest for agriculture crops. It causes direct damage and also is a major vector for viruses, like Tomato yellow leaf curl virus, Cassava mosaic virus and Cassava brown streak virus, so it creates huge crop losses and poses serious threats to food security, especially in Africa and other parts of the developing world," said Fei.
In collaboration with a group of international colleagues, BTI researchers created a high-quality draft genome sequence of the whitefly and identified genes that code for proteins. The genome sequence can be accessed at the whitefly genome database developed by the Fei lab.
An analysis showed that, compared to related species, the whitefly has expanded families of detoxification genes. It also has extra genes that code for proteins related to virus acquisition and transmission, as well as insecticide resistance.
In an impressive example of horizontal gene transfer, the whitefly has acquired 142 genes from bacteria or fungi, including some coding for enzymes that break down foreign chemicals. These genes likely allow the whitefly to feed on diverse types of plants and to rapidly evolve resistance to insecticides.
Because pesticides are ineffective at keeping whitefly populations in check, collaborators at USDA plan to use the genome sequence to develop a control strategy using RNA interference (RNAi). Once scientists pinpoint the genes necessary for virus transmission and survival in the whitefly genome, they can develop new varieties of crops that will produce RNA molecules that block the expression of those necessary genes, killing the whitefly or preventing it from spreading the virus .
Throughout evolution, a wide number of organisms specialized in parasitizing plants. Plants are not exceptions; certain plant species evolved as parasites of their own kind. Parasitic angiosperms evolved at least 12 times and show various lifestyles. For example, facultative parasitic plants can complete their life cycle and produce seeds without hosts, whereas obligate parasitic plants totally rely on their hosts. Some obligate parasitic plants, such as broomrapes (Orobanche spp.), witchweeds (Striga spp.), and dodders (Cuscuta spp.), are major crop pathogens that cause severe and persistent damage in agriculture. During parasitism, series of molecular signals are emitted by nearby plants and perceived by parasitic plants. These stimuli are often essential for parasitic plants to germinate and/or undergo parasitic stages in the right place and at the right time. On the other hand, a growing body of evidence supports the idea that plant immunity programs can be activated by detection of molecules derived from parasitic plants. Here, we summarize the molecular interactions between parasitic plants and host plants, mainly obtained from studies on Orobanchaceae parasitic plants
The ability to edit plant genomes through gene targeting (GT) requires efficient methods to deliver both sequence-specific nucleases (SSNs) and repair templates to plant cells. This is typically achieved using Agrobacterium T-DNA, biolistics or by stably integrating nuclease-encoding cassettes and repair templates into the plant genome. In dicotyledonous plants, such as tobacco and tomato, greater than 10-fold enhancements in GT frequencies have been achieved using DNA virus-based replicons. These replicons transiently amplify to high copy numbers in plant cells to deliver abundant SSNs and repair templates to achieve targeted gene modification. In the present work, we developed a replicon-based system for genome engineering of cereal crops using a deconstructed version of the wheat dwarf virus (WDV). In wheat cells, the replicons achieve a 110-fold increase in expression of a reporter gene relative to non-replicating controls. Further, replicons carrying CRISPR/Cas9 nucleases and repair templates achieved GT at an endogenous ubiquitin locus at frequencies 12-fold greater than non-viral delivery methods. The use of a strong promoter to express Cas9 was critical to attain these high GT frequencies. We also demonstrate gene targeted integration by HR in all the three homoeoalleles (A, B, and D) of the hexaploid wheat genome, and we show that with the WDV replicons, multiplexed GT within the same wheat cell can be achieved at frequencies of ~1%. In conclusion, high frequencies of GT using WDV-based DNA replicons will make it possible to edit complex cereal genomes without the need to integrate GT reagents into the genome.
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