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bioRxiv2019

Natural variation for unusual host responses and flagellin-mediated immunity against Pseudomonas syringae in genetically diverse tomato accessions

The interaction between tomato and Pseudomonas syringae pv. tomato (Pst) is a well-developed model for investigating the molecular basis of the plant immune system. There is extensive natural variation in Solanum lycopersicum (tomato) but it has not been fully leveraged to enhance our understanding of the tomato-Pst pathosystem. We screened 216 genetically diverse accessions of cultivated tomato and a wild tomato species for natural variation in their response to three strains of Pst. The screen uncovered a broad range of previously unseen host symptoms in response to Pst, and one of these, stem galls, was found to be simply inherited. The screen also identified tomato accessions that showed enhanced responses to flagellin in bacterial population assays and in reactive oxygen species assays upon exposure to flagellin-derived peptides, flg22 and flgII-28. Reporter genes confirmed that the host responses were due primarily to pattern recognition receptor-immunity. This study revealed extensive natural variation in tomato for susceptibility and resistance to Pst and will enable elucidation of the molecular mechanisms underlying these host responses.

plant biology↗

bioRxiv2019

Temperature dependence of allelopathy duality and its influence on boreal forest succession-A case analysis of Picea schrenkiana

Global warming in conjunction with various biotic or abiotic interferences has been jeopardizing the ecosystem of boreal forests. By integrating field inspection with experimental simulation, this work comprehensively investigated the allelopathic effects of a key allelochemical 3,4-dihydroxyacetophenone (DHAP) in the exudates of P. schrenkiana needles on its seed and seedling growth, endogenous hormone metabolism and antioxidant enzyme activity, identified the existence of DHAP allelopathy duality at a certain temperature with an inflection concentration point (e.g. about 0.25 mM at dark/light temperature of 4/12 {degrees}C) as the boundary between promotional and inhibitory effect, and verified that the inflection point of DHAP concentration would inevitably shift to a lower level as temperature increased. Consequently, this paper gives a scientific explanation into the intrinsic mechanism of P. schrenkiana degradation due to allelopathy, but also presents a new approach to explore the relationship between forest evolution and global warming.\n\nHighlightA quantitative description on the duality of 3, 4-dihydroxyacetophenone (DHAP) as a promoter or an inhibitor to affect the seed germination, seedling growth and root development of P. schrenkiana, as well as the antioxidant enzyme activities and hormone contents.\n\nThe new findings of DHAP inflection concentration as boundary to divide the promotional and inhibitory effect of allelopathy which would decrease as environment temperatures rise.\n\nAn explanation into the intrinsic mechanism of P. schrenkiana degradation due to allelopathy, and a new approach to explore the relationship between forest evolution and global warming.

plant biology↗

bioRxiv2019

Candidate regulators and target genes of drought stress in needles and roots of Norway spruce

Drought stress impacts on seedling establishment, survival and whole-plant productivity. Drought stress responses have been extensively studied at the physiological and molecular level in angiosperms, particularly in agricultural species and the model Arabidopsis thaliana, with the vast majority of work performed on aboveground tissues. Boreal forests are dominated by coniferous tree species and cover vast areas of the terrestrial surface. These areas are predicted to be particularly influenced by ongoing climate change and will be exposed to more frequent and acute drought. The associated impact at all stages of the forest tree life cycle is expected to have large-scale ecological and economic impacts. To provide a comprehensive understanding of the drought response mechanisms of Picea abies seedlings, we assayed the physiological response of needles and transcriptional responses of roots and needles after exposure to mild and severe drought. Shoots and needles showed extensive reversible plasticity for physiological measures indicative of drought response mechanisms, including stomatal conductance (gs) and shoot water potential. Root and needle transcriptional responses contrasted, with an extensive root-specific down-regulation of growth. When we compared the responses of P. abies with previously-characterised A. thaliana drought response genes, we found that the majority of the genes were conserved across lineages. However, in P. abies, transcription factors (TFs) previously identified as belonging to the ABA-dependent pathway had a more limited role and most differentially expressed genes were specific to the stress response of P. abies. These results highlight the importance of profiling both above- and below-ground tissues and provide a comprehensive framework to advance understanding of the drought response mechanism of P. abies.\n\nOne sentence summaryAnalysis of the drought transcriptome of Norway spruce reveals divergent molecular response pathways in conifers.

plant biology↗

bioRxiv2019

Shoot-to-root translocation of the jasmonate precursor 12-oxo-phytodienoic acid (OPDA) coordinates plant growth responses following tissue damage

Multicellular organisms rely upon the movement of signaling molecules across cells, tissues and organs to communicate among distal sites. In plants, herbivorous insects, necrotrophic pathogens and mechanical wounding stimulate the activation of the jasmonate (JA) pathway, which in turn triggers the transcriptional changes necessary to protect plants against those challenges, often at the expense of growth. Although previous evidence indicated that JA species can translocate from damaged into distal sites, the identity of the mobile compound(s), the tissues through which they translocate and the consequences of their relocation remain unknown. Here, we demonstrated that endogenous JA species generated after shoot injury translocate to unharmed roots via the phloem vascular tissue in Arabidopsis thaliana. By wounding wild-type shoots of chimeric plants and by quantifying the relocating compounds from their JA-deficient roots, we uncovered that the JA-Ile precursor 12-oxo-phytodienoic acid (OPDA) is a mobile JA species. Our data also showed that OPDA is a primary mobile compound relocating to roots where, upon conversion to the bioactive hormone, it induces JA-mediated gene expression and root growth inhibition. Collectively, our findings reveal the existence of long-distance transport of endogenous OPDA which serves as a communication molecule to coordinate shoot-to-root responses, and highlight the importance of a controlled distribution of JA species among organs during plant stress acclimation.

plant biology↗

bioRxiv2019

Environmental and epigenetic regulation of Rider retrotransposons in tomato

Transposable elements in crop plants are the powerful drivers of phenotypic variation that has been selected during domestication and breeding programs. In tomato, transpositions of the LTR (long terminal repeat) retrotransposon family Rider have contributed to various phenotypes of agronomical interest, such as fruit shape and colour. However, the mechanisms regulating Rider activity are largely unknown. We have developed a bioinformatics pipeline for the functional annotation of retrotransposons containing LTRs and defined all full-length Rider elements in the tomato genome. Subsequently, we showed that accumulation of Rider transcripts and transposition intermediates in the form of extrachromosomal DNA is triggered by drought stress and relies on abscisic acid signalling. We provide evidence that residual activity of Rider is controlled by epigenetic mechanisms involving siRNAs and the RNA-dependent DNA methylation pathway. Finally, we demonstrate the broad distribution of Rider-like elements in other plant species, including crops. Thus our work identifies Rider as an environment-responsive element and a potential source of genetic and epigenetic variation in plants.

plant biology↗

bioRxiv2019

Genetic control of pod dehiscence in domesticatedcommon bean: Associations with range expansionand local aridity conditions

SignificancePlant domestication has radically modified crop morphology and development. Nevertheless, many crops continue to display some atavistic characteristics that were advantageous to their wild ancestors, such as pod dehiscence (PD). Domesticated common bean (Phaseolus vulgaris), a nutritional staple for millions of people globally, shows considerable variation in PD. Here, we identified multiple genetic regions controlling PD in common bean grown throughout geographically distributed lineages. For example, on chromosome Pv03, PvPdh1 shows a single base-pair substitution that is strongly associated with decreased PD and expansion of the crop into northern Mexico, where the arid conditions promote PD. The environmental dependency and genetic redundancy explain the maintenance of atavistic traits under domestication. Knowledge of PD genetics will assist in developing aridity-adapted varieties.\n\nAbstractA reduction in pod dehiscence (PD) is an important part of the domestication syndrome in legumes, including common bean. Despite this, many modern dry bean varieties continue to suffer yield reductions due to dehiscence, an atavistic trait, which is particularly problematic in hot, dry environments. To date, the genetic control of this important trait has been only partially resolved. Using QTL mapping and GWAS, we identified major PD QTLs in dry beans on chromosomes Pv03, Pv05, Pv08, and Pv09, three of which had not been described previously. We further determined that the QTL on chromosome Pv03, which is strongly associated with PD in Middle American beans, includes a dirigent-like candidate gene orthologous to Pod dehiscence 1 (Pdh1) of soybean. In this gene, we identified a substitution in a highly conserved amino acid that is unique to PD-resistant varieties. This allele is associated with the expansion of Middle American domesticated common beans into the arid environments of northern Mexico, resulting in a high allelic frequency in the domesticated ecogeographic race Durango. The polygenic redundancy and environmental dependency of PD resistance may explain the maintenance of this atavistic characteristic after domestication. Use of these alleles in breeding will reduce yield losses in arid growing conditions, which are predicted to become more widespread in coming decades.

plant biology↗

bioRxiv2019

Bacterially produced spermidine induces plant systemic susceptibility to pathogens

Plant root-associated microbes promote plant growth and induce systemic resistance (ISR) to foliar pathogens. In an attempt to find novel growth-promoting and ISR-inducing strains, we previously identified strains of root-associated Pseudomonas spp. that promote plant growth but unexpectedly induced systemic susceptibility (ISS) rather than ISR to foliar pathogens. Here we demonstrate that the ISS-inducing phenotype is common among root-associated Pseudomonas spp. Using comparative genomics, we identified a single P. fluorescens locus that is unique to ISS strains. We generated a clean deletion of the 11-gene ISS locus and found that it is necessary for the ISS phenotype. Although the functions of the predicted genes in the locus are not apparent based on similarity to genes of known function, the ISS locus is present in diverse bacteria and a subset of the genes have previously been implicated in pathogenesis in animals. Collectively these data show that a single bacterial locus contributes to modulation of systemic plant immunity. ImportanceMicrobiome-associated bacteria can have diverse effects on health of their hosts, yet the genetic and molecular basis of these effects have largely remained elusive. This work demonstrates that a novel bacterial locus can modulate systemic plant immunity. Additionally, this work demonstrates that growth promoting strains may have unanticipated consequences on plant immunity and this is critical to consider when engineering the plant microbiome for agronomic improvement.

plant biology↗

bioRxiv2019

Loss of a glutaredoxin gene underlies parallel evolution of trichome patter in Antirrhinum

Most angiosperms produce trichomes--epidermal hairs that have protective or more specialised roles. In almost all species trichomes are multicellular and, in the majority, secretory. Despite the importance of multicellular trichomes for plant protection and as a source of high-value products, little is known about the mechanisms that control their development. Here we use natural variation between Antirrhinum (snapdragon) species to examine how trichome distribution is regulated and has evolved. We show that a single gene, Hairy (H), which is needed to repress trichome fate, underlies variation in trichome distribution patterns between all Antirrhinum species except one. H encodes an epidermis-specific glutaredoxin and trichome distribution within individual plants reflects the location of H expression. Gene phylogenies and functional tests suggest that H gained its trichome-repressing role late in eudicot evolution and that Antirrhinum species with widespread trichomes evolved multiple times from a largely bald ancestor though independent losses of H activity. We also find evidence for an evolutionary reversal involving a suppressor mutation, and for a pleiotropic effect of H that might constrain the evolution of trichome patterns.

plant biology↗

bioRxiv2019

Molecular framework for TIR1/AFB-Aux/IAA-dependent auxin sensing controlling adventitious rooting in Arabidopsis

In Arabidopsis thaliana, canonical auxin-dependent gene regulation is mediated by 23 transcription factors from the AUXIN RESPONSE FACTOR (ARF) family, most of which interact with 29 auxin/indole acetic acid (Aux/IAA) repressors, themselves forming, in the presence of auxin, coreceptor complexes with one of six TRANSPORT INHIBITOR1/AUXIN-SIGNALLING F-BOX PROTEINS (TIR1/AFB). Different combinations of co-receptors drive specific sensing outputs, allowing auxin to control a myriad of processes. Considerable efforts have been made to discern the temporal and spatial specificity of auxin action. However, owing to a lack of obvious phenotype in single loss-of-function mutants in Aux/IAA genes, most genetic studies have relied on gain-of-function mutants, which are highly pleiotropic. In this article, we describe a molecular framework for the role of several members of the auxin sensing machinery. Using loss-of-function mutants, we demonstrate that TIR1 and AFB2 are positive regulators, whereas IAA6, IAA9 and IAA17 are negative regulators of adventitious root (AR) formation. The three Aux/IAA proteins interact with ARF6 and/or ARF8, which we have previously shown to be positive regulators of AR formation upstream of jasmonate, and likely repress their activity. Our data also suggest a dual role for TIR1 in the control of JA biosynthesis and conjugation, as revealed by upregulation of several JA biosynthesis genes in the tir1-1 mutant. In conclusion, we propose that in the presence of auxin, TIR1 and AFB2 form specific sensing complexes with IAA6, IAA9 and/or IAA17 that modulate JA homeostasis to control AR initiation.\n\nSignificanceAdventitious root (AR) formation is a quantitative trait with high phenotypic plasticity and auxin plays a major role in its control. In previous studies, we have shown that, in Arabidopsis hypocotyls, AR formation is negatively regulated by jasmonate, whose homeostasis is controlled by a regulatory module composed of three AUXIN RESPONSE FACTORS (ARF), two of which are positive regulators of three auxin inducible Gretchen Hagen3 (GH3) genes. The present work demonstrates that the two F-box proteins, i.e., TIR1 and AFB2, together with at least three Aux/IAA proteins are likely to interact in a combinatorial manner to control the activity of the two activator ARFs upstream of JA biosynthesis and/or homeostasis, thereby controlling AR initiation in Arabidopsis hypocotyls.

plant biology↗

bioRxiv2019

The Ptr1 locus of Solanum lycopersicoides confers resistance to race 1 strains of Pseudomonas syringae pv. tomato and to Ralstonia pseudosolanacearum by recognizing the type III effectors AvrRpt2/RipBN

Race 1 strains of Pseudomonas syringae pv. tomato, which causes bacterial speck disease of tomato, are becoming increasingly common and no simply-inherited genetic resistance to such strains is known. We discovered that a locus in Solanum lycopersicoides, termed Pseudomonas tomato race 1 (Ptr1), confers resistance to race 1 Pst strains by recognizing the type III effector AvrRpt2. In Arabidopsis, AvrRpt2 degrades the RIN4 protein thereby activating RPS2-mediated immunity. Ptr1 also recognized homologs of AvrRpt2 from diverse bacteria including one in Ralstonia pseudosolanacearum and this correlated with the ability of AvrRpt2 to degrade RIN4. Using site-directed mutagenesis of AvrRpt2 we found that Ptr1 and RPS2 recognize identical features of AvrRpt2. However, the genome sequence of S. lycopersicoides revealed no RPS2 homolog in the Ptr1 region. Ptr1 could play an important role in controlling bacterial speck disease and its future cloning may shed light on an example of convergent evolution for recognition of a widespread type III effector.

plant biology↗

bioRxiv2019

PHYSIOLOGICAL GROWTH INDICES OF MAIZE (Zea mays L.) GENOTYPES IN SYLHET

Maize (Zea mays L.) is an important food and feed crop in Bangladesh as well as in the world. But its cultivation is limited in the soils of Sylhet, Bangladesh. To study the physiological growth indices of maize genotypes an experiment was carried out at the experimental field of Sylhet Agricultural University (SAU), Bangladesh during December 2014 to May 2015. The maize genotypes as the experimental materials were ZM 0001, ZM 0002, ZM 0003, ZM 0004, ZM 0005, ZM 0006 ZM 0007 and BARI Maize 6. The experiment was laid out in a Randomized Complete Block Design (RCBD) with three replications. Seeds were sown on 26 December 2014. Proper cultural management practices were followed as and when necessary during the growing period of the crop. Data were recorded on dry matter partitioning, different growth rate parameters and dry matter production of different plant parts at 30 days interval. The results indicated significant variations in almost all of the growth indices. Dry matter accumulation continued to increase from seedling to harvesting. The highest root dry matter was found in ZM 0007 (36.03 g) whereas the highest shoot and leaf dry matter was found in BARI Maize 6 (254.6 and 45.99 g, respectively) at harvest. The highest total dry matter (TDM) was produced in BARI Maize 6 at harvest (287.5 g) and AGR and CGR value was also highest in BARI Maize 6 (5.686 g day-1 and 45.48 g m-2 day-1) but at 60-90 days after germination (DAG). The highest RGR value was in ZM 0001 at seedling stage (114.1 mg g-1 day-1). A zigzag pattern graph was observed in all genotypes for RSR, RWR and SWR at different growth stages but a declining trend from seedling to harvesting was observed for LWR. Correlation between the growth rate parameters and kernel yield showed that shoot, leaf, total dry weight, AGR, CGR, RGR and SWR had significant positive correlation with yield.

plant biology↗

bioRxiv2019

Comparative Population Genomics of Bread Wheat (Triticum aestivum) Reveals Its Cultivation and Breeding History in China

The evolution of bread wheat (Triticum aestivum) is distinctive in that domestication, natural hybridization, and allopolyploid speciation have all had significant effects on the diversification of its genome. Wheat was spread around the world by humans and has been cultivated in China for ~4,600 years. Here, we report a comprehensive assessment of the evolution of wheat based on the genome-wide resequencing of 120 representative landraces and elite wheat accessions from China and other representative regions. We found substantially higher genetic diversity in the A and B subgenomes than in the D subgenome. Notably, the A and B subgenomes of the modern Chinese elite cultivars were mainly derived from European landraces, while Chinese landraces had a greater contribution to their D subgenomes. The duplicated copies of homoeologous genes from the A, B, and D subgenomes were commonly found to be under different levels of selection. Our genome-wide assessment of the genetic changes associated with wheat breeding in China provides new strategies and practical targets for future breeding.

plant biology↗

bioRxiv2019

Foliar fungi alter reproductive timing and allocation in Arabidopsis under normal and water-stressed conditions

Microbes influence plant phenotypes but most known examples of this are from the study of below-ground microbes and plant disease modification. To examine the potential importance of phyllosphere microbes on non-disease related plant traits, we used sterile Arabidopsis clones to test the effects of foliar fungi on flowering phenology and reproductive allocation under conditions of varying water stress. We inoculated the sterile plants with fully-factorial combinations of four fungal isolates, then measured flowering time and reproductive allocation for each treatment group under normal and water-stressed conditions. All plants inoculated with foliar fungi had significantly later flowering and greater seed mass than the sterile control groups. The magnitude of this effect depended on the specific fungi present, but individual fungal effects diminished as inoculum richness increased. Above-ground microbes likely influence other plant traits as well and should be considered in any study measuring plant phenotypes.

plant biology↗

bioRxiv2019

A natural, conditional gene drive in plants

A new class of gene drive in plant populations with herbicide resistance is described; a conditional gene drive that operates following herbicide application. Screening progeny from controlled crosses of Brassica napus heterozygous for a dominant allele conferring chlorsulfuron resistance, demonstrated that the herbicide imposes in planta gametic selection against pollen and ovules with the recessive allele for herbicide susceptibility, as well as embryonic selection against embryos homozygous for the susceptible allele. We postulate that natural gene drives are common in plant populations and can operate in a conditional manner resulting in non-Mendelian inheritance in response to abiotic and biotic stresses.

plant biology↗

bioRxiv2019

Assessing the remarkable morphological diversity and transcriptomic basis of leaf shape in Ipomoea batatas (sweetpotato)

O_LILeaf shape, a spectacularly diverse plant trait, varies across taxonomic levels, geography, and in response to environmental differences. However, comprehensive intraspecific analyses of leaf shape variation across variable environments is surprisingly absent. Here, we perform a multi-level analysis of leaf shape using diverse accessions of sweetpotato (Ipomoea batatas), and uncover the role of genetics, environment, and GxE on this important trait.\nC_LIO_LIWe examine leaf shape using a variety of morphometric analyses, and complement this with a transcriptomic survey to identify gene expression changes associated with shape variation. Additionally, we examine the role of genetics and environment on leaf shape by performing field studies in two geographically separate common gardens.\nC_LIO_LIWe show that extensive leaf shape variation exists within I. batatas, and identify promising candidate genes underlying this variation. Interestingly, when considering traditional measures, we find that genetic factors are largely responsible for most of leaf shape variation, but that the environment is highly influential when using more quantitative measures via leaf outlines.\nC_LIO_LIThis extensive and multi-level examination of leaf shape shows an important role of genetics underlying a potentially important agronomic trait, and highlights that the environment can be a strong influence when using more quantitative measures of leaf shape.\nC_LI

plant biology↗

bioRxiv2019

Identification of the Calmodulin-dependent NAD+ kinase sustaining the elicitor-induced oxidative burst in plants

NADP(H) is an essential cofactor ofmultiple metabolic processes in all living organisms. While NADP+ production in plants has long been known to involve a Calmodulin (CaM)/Ca2+-dependent NAD+ kinase, the nature of the enzyme catalyzing this activity has remained enigmatic, as well as its role in plant physiology. Here, we identify an Arabidopsis P-loop ATPase (Atlg04280) with a bacterial type II zeta toxin domain, that catalyzes NADP+ production upon binding of CaM/Ca2+ to a domain located in its N-terminal region. The encoded protein (NADKc-1) is associated with the mitochondria and amplifies the elicitor-induced oxidative burst in Arabidopsis leaves representing the missing link between calcium signalling and metabolism in the response to pathogen elicitor. By analysis of various plants and algae, we show that NADKc is well conserved in the plant lineage and present in basal plants. Our data allows proposing that the CaM-dependent NAD kinase activity is only found in photosynthetic species carrying NADKc-1 related proteins, which would represent the only proteins harboring CaM-dependent NAD kinase activity in plants and algae.

plant biology↗

bioRxiv2019

Plant seeds are primed by herbivore-induced plant volatiles

Mature plants can detect and respond to herbivore-induced plant volatiles (HIPVs) by priming or directly activating defenses against future herbivores. Whether other plant life stages can respond to HIPVs in similar manners is poorly understood. For example, seeds are known to respond to a variety of environment cues that are essential for proper germination timing and survival. Seeds may also be exposed to HIPVs prior to germination, and such exposure may affect the growth, development, and defense profiles when the seeds grow into mature plants. Here, we investigated the effect of seed exposure to common HIPVs on growth, reproduction and defense characteristics in the model plants Arabidopsis thaliana and Medicago truncatula. Of all the HIPVs tested, indole specifically reduced both beet armyworm growth on A. thaliana and pea 33 aphid fecundity on M. truncatula. Induction of defense genes was not affected by seed exposure to indole in either plant species, suggesting that seed priming operates independently of induced resistance. Moreover, neither species showed any negative effect of seed exposure to HIPVs on vegetative and reproductive growth. Rather, M. truncatula plants derived from seeds exposed to z-3-hexanol and z-3-hexenyl acetate grew faster and produced larger leaves compared to controls. Our results indicate that seeds are sensitive to specific HIPVs, which represents a novel ecological mechanism of plant-to-plant communication.

plant biology↗

bioRxiv2019

Systemic signalling through TCTP1 controls lateral root formation in Arabidopsis

As in animals, the plant body plan and primary organs are established during embryogenesis. However, plants have the ability to generate new organs and functional units throughout their whole life. These are produced through the specification, initiation and differentiation of secondary meristems, governed by the intrinsic genetic program and cues from the environment. They give plants an extraordinary developmental plasticity to modulate their size and architecture according to environmental constraints and opportunities. How this plasticity is regulated at the whole organism level is still largely elusive. In particular the mechanisms regulating the iterative formation of lateral roots along the primary root remain little known. A pivotal role of auxin is well established and recently the role of local mechanical signals and oscillations in transcriptional activity has emerged. Here we provide evidence for a role of Translationally Controlled Tumor Protein (TCTP), a vital ubiquitous protein in eukaryotes. We show that Arabidopsis AtTCTP1 controls root system architecture through a dual function: as a general constitutive growth promoter locally, and as a systemic signalling agent via mobility from the shoot. Our data indicate that this signalling function is specifically targeted to the pericycle and modulates the frequency of lateral root initiation and emergence sites along the primary root, and the compromise between branching and elongating, independent of shoot size. Plant TCTP genes show high similarity among species. TCTP messengers and proteins have been detected in the vasculature of diverse species. This suggests that the mobility and extracellular signalling function of AtTCTP1 to control root organogenesis might be widely conserved within the plant kingdom, and highly relevant to a better understanding of post-embryonic formation of lateral organs in plants, and the elusive coordination of shoot and root morphogenesis.

plant biology↗