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bioRxiv2019

Mapping of transgenic alleles in plants using a Nanopore-based sequencing strategy

Transgenic technology was developed to introduce transgenes into various organisms to validate gene function and add genetic variation for the development of beneficial input or output trait over 40 years ago. However, the identification of the transgene insertion position in the genome, while doable, can be cumbersome in the organisms with complex genomes. Here, we report a Nanopore-based sequencing method to rapidly map transgenic alleles in the soybean genome. This strategy is high-throughput, convenient, reliable, and cost-efficient. The transgenic allele mapping protocol outlined herein can be easily translated to other higher eukaryotes with complex genomes.

plant biology↗

bioRxiv2019

Members of the Arabidopsis auxin receptor gene family are essential early in embryogenesis and have broadly overlapping functions

The TIR1/AFB auxin co-receptors mediate diverse responses to the plant hormone auxin. The Arabidopsis genome encodes six TIR1/AFB proteins representing three of the four clades that were established prior to angiosperm radiation. To determine the role of these proteins in plant development we performed an extensive genetic analysis involving the generation and characterization of all possible multiply mutant lines. We find that loss of all six TIR1/AFB proteins results in defects in embryogenesis as early as the 8-cell stage, and possibly earlier. Mutant embryos progress but exhibit frequent cell division errors followed by proliferation of the suspensor, and eventually seed abortion. Despite this dramatic phenotype, a single wild-type allele of TIR1 or AFB2 is sufficient to support growth throughout plant development. Further, gametophytic expression of the TIR1/AFB genes is not essential for development of the male or female gametophyte. Our analysis reveals extensive functional overlap between even the most distantly related TIR1/AFB genes except for AFB1. Surprisingly, the AFB1 protein has a specialized function in rapid auxin-dependent inhibition of root growth and early phase of root gravitropism. This activity may be related to a difference in subcellular localization compared to the other members of the family.

plant biology↗

bioRxiv2019

tealeaves: an R package for modelling leaf temperature using energy budgets

Plants must regulate leaf temperature to optimize photosynthesis, control water loss, and prevent damage caused by overheating or freezing. Physical models of leaf energy budgets calculate the energy fluxes and leaf temperatures for given a set leaf and environmental parameters. These models can provide deep insight into the variation in leaf form and function, but there are few computational tools available to use these models. Here I introduce a new R package called tealeaves to make complex leaf energy budget models accessible to a broader array of plant scientists. This package enables novice users to start modelling leaf energy budgets quickly while allowing experts customize their parameter settings. The code is open source, freely available, and readily integrates with other R tools for scientific computing. This paper describes the current functionality of tealeaves, but new features will be added in future releases. This software tool will advance new research on leaf thermal physiology to advance our understanding of basic and applied plant science.

plant biology↗

bioRxiv2019

Potential involvement of root auxins in drought tolerance by modulating nocturnal and daytime water use in wheat

The ability of wheat genotypes to save water by reducing their transpiration rate (TR) under times of the day with high vapour pressure deficit (VPD) has been linked to increasing yields in terminal drought environments. Further, recent evidence shows that reducing nocturnal transpiration (TRN) could amplify water-saving. Previous research indicates that such traits involve a root-based hydraulic limitation, but the contribution of hormones, particularly auxin and abscisic acid (ABA) has not been explored to explain the shoot-root link. In this investigation, based on physiological, genetic and molecular evidence gathered on a mapping population, we hypothesized that root auxin accumulation regulates whole-plant water use during both times of the day. Eight double-haploid lines were selected from a mapping population descending from two parents with contrasted water-saving strategies and root hydraulic properties. These spanned the entire range of slopes of TR responses to VPD and TRN encountered in the population. On those lines, we examined daytime/night-time auxin and ABA contents in the roots and the leaves in relation to hydraulic traits that included whole-plant TR, plant hydraulic conductance (KPlant), slopes of TR responses to VPD and leaf-level anatomical traits. Root auxin levels were consistently genotype-dependent in this group irrespective of experiments and times of the day. Daytime root auxin concentrations were found to be strongly and negatively correlated with daytime TR, KPlant and the slope of TR response to VPD. Night-time root auxin levels significantly and negatively correlated with TRN. In addition, daytime and night-time leaf auxin and ABA concentrations did not correlate with any of the examined traits. The above results indicate that accumulation of auxin in the root system reduces daytime and night-time water use and modulates plant hydraulic properties to enable the expression of water-saving traits that have been associated with enhanced yields under drought.

plant biology↗

bioRxiv2019

Cross-reactivity of a rice NLR immune receptor to distinct effectors from the blast pathogen leads to partial disease resistance

Unconventional integrated domains in plant intracellular immune receptors (NLRs) can directly bind translocated pathogen effector proteins to initiate an immune response. The rice immune receptor pairs Pik-1/Pik-2 and RGA5/RGA4 both use integrated heavy metal-associated (HMA) domains to bind the Magnaporthe oryzae effectors AVR-Pik and AVR-Pia, respectively. These effectors both belong to the MAX effector family and share a core structural fold, despite being divergent in sequence. How integrated domains maintain specificity of recognition, even for structurally similar effectors, has implications for understanding plant immune receptor evolution and function. Here we show that the rice NLR pair Pikp-1/Pikp-2 triggers an immune response leading to partial disease resistance towards the "mismatched" effector AVR-Pia in planta, and that the Pikp-HMA domain binds AVR-Pia in vitro. The HMA domain from another Pik-1 allele, Pikm, is unable to bind AVR-Pia, and does not trigger a response in plants. The crystal structure of Pikp-HMA bound to AVR-Pia reveals a different binding interface compared to AVR-Pik effectors, suggesting plasticity in integrated domain/effector interactions. This work shows how a single NLR can bait multiple pathogen effectors via an integrated domain, and may enable engineering immune receptors with extended disease resistance profiles.

plant biology↗

bioRxiv2019

Mucoromycotina fine root endophyte fungi form nutritional mutualisms with vascular plants.

Fungi and plants have engaged in intimate symbioses that are globally widespread and have driven terrestrial biogeochemical processes since plant terrestrialisation >500 Mya. Recently, hitherto unknown nutritional mutualisms involving ancient lineages of fungi and non-vascular plants have been discovered. However, their extent and functional significance in vascular plants remains uncertain. Here, we provide first evidence of abundant carbon-for-nitrogen exchange between an early-diverging vascular plant (Lycopodiaceae) and Mucoromycotina (Endogonales) fine root endophyte regardless of changes in atmospheric CO2 concentration. Furthermore, we provide evidence that the same fungi also colonize neighbouring non-vascular and flowering plants. These findings fundamentally change our understanding of the evolution, physiology, interrelationships and ecology of underground plant-fungal symbioses in terrestrial ecosystems by revealing an unprecedented nutritional role of Mucoromycotina fungal symbionts in vascular plants.

plant biology↗

bioRxiv2019

A new mechanism for tree mortality due to drought and heatwaves

AO_SCPLOWBSTRACTC_SCPLOWPlants tend to die earlier in hot and drought conditions, but the underlying mechanisms are not yet understood. I propose here a new mechanism by which excessive residual water losses caused by high cuticular permeabilities and a high leaf-to-air vapor pressure deficits would trigger uncontrolled and sudden cavitation events. The combination of heat and drought stresses may therefore lead to an unsuspected risk of hydraulic failure. I explored this hypothesis with a new mechanistic model. The simulations support this hypothesis and highlight the critical role played by the cuticle phase transition temperature. Experiments are now awaited to confirm these predictions.

plant biology↗

bioRxiv2019

GUN1 regulates tetrapyrrole biosynthesis

The biogenesis of the photosynthetic apparatus in developing chloroplasts requires the assembly of proteins encoded on both nuclear and chloroplast genomes1. To co-ordinate this process there needs to be communication between these organelles, and while we have a good understanding of how the nucleus controls chloroplast development, how the chloroplast communicates with the nucleus at this time is still essentially unknown2. What we do know comes from pioneering work in which a series of genomes uncoupled (gun) mutants were identified that show elevated nuclear gene expression after chloroplast damage3. Of the six reported gun mutations, five are in tetrapyrrole biosynthesis proteins4-6 and this has led to the development of a model for chloroplast-to-nucleus retrograde signaling in which ferrochelatase 1 (FC1)-dependent heme synthesis generates a positive signal promoting expression of photosynthesis-related genes6. However, the molecular consequences of the strongest of the gun mutants, gun17, is unknown, preventing the development of a unifying hypothesis for chloroplast-to-nucleus signaling. Here, we show that GUN1 directly binds to heme and other metal-porphyrins, affects flux through the tetrapyrrole biosynthesis pathway and can increase the chelatase activity of FC1. These results raise the possibility that the signaling role of GUN1 may be manifested through changes in tetrapyrrole metabolism and supports a role for tetrapyrroles as mediators of a single biogenic chloroplast-to-nucleus retrograde signaling pathway.

plant biology↗

bioRxiv2019

A plant protein NbP3IP induces autophagy and mediates the autophagic degradation of RSV p3 to inhibit viral infection

In plants, autophagy is involved in responses to viral infection. However, understanding of new host factors mediating autophagic clearance of plant viruses is very limited. We here identified a new host factor NbP3IP participating in autophagy-mediated plant defense against viral infection. NbP3IP interacted with p3, a RNA silencing suppressor encoded by Rice stripe virus (RSV), a negative-strand RNA virus, and mediated its autophagic degradation. NbP3IP could also interact with NbATG8f, which was required for NbP3IP-miediated p3 degradation. Overexpression of NbP3IP induced autophagy and down-regulation of NbP3IP reduced autophagy. Both overexpression of NbP3IP and silencing of GAPC, which also induces autophagy, inhibited RSV infection. In contrast, silencing of ATG7 promoted RSV infection. Thus, through identification of a new potential selective autophagy receptor P3IP, we revealed a new mechanism of autophagy-mediated plant defense against plant viruses and provided the first evidence that plant autophagy can also play an antiviral role against negative-strand RNA viruses.

plant biology↗

bioRxiv2019

Plant growth regulators interact with elevated temperature to alter heat stress signaling via the Unfolded Protein Response

Plants are increasingly exposed to high temperatures, which can cause accumulation of unfolded protein in the endoplasmic reticulum (ER). This condition, known as ER stress, evokes the unfolded protein response (UPR), a cytoprotective signaling pathway. One important branch of the UPR is regulated by splicing of bZIP60 mRNA by the IRE1 stress sensor. There is increasing evidence that commercial plant growth regulators may protect against abiotic stressors including heat stress and drought, but there is very little mechanistic information about these effects or about the regulatory pathways involved. We evaluated evidence in the B73 Zea mays inbred for differences in the activity of the UPR between permissive and elevated temperature in conjunction with plant growth regulator application. Treatment with elevated temperature and plant growth regulators increased UPR activation, as assessed by an increase in splicing of the mRNA of the IRE1 target bZIP60 following paclobutrazol treatment. We propose that plant growth regulator treatment induces bZIP60 mRNA splicing which primes plants for rapid adaptive response to subsequent endoplasmic reticulum-stress inducing conditions.

plant biology↗

bioRxiv2019

Reallocation to lateral and early-emerging axial roots allows maize (Zea mays L.) with reduced nodal root number to more efficiently forage for nitrate

Previous simulations indicated reduced nodal root number (NRN) was promising for maize (Zea mays L.) breeding, and were partially confirmed using variation in NRN among inbreds. However, the exact mechanism was unknown, therefore manipulative experiments were conducted in hydroponics and tall solid-media mesocosms with treatments involving no nodal root excision (0% NRE) or excising either 33% or 67% of the nodal roots (NR) as they emerged under high or low levels of nitrogen (N). Reduced NRN was hypothesized to increase elongation of all remaining root classes, increase N acquisition under low N, and increase shoot mass. In both experiments, plants with 67% NRE had 12% and 19% less root fraction of total biomass, 61% and 91% greater lateral-to-axial root length ratio regardless of N levels; and 61% and 182% greater biomass of embryonic roots under low N, compared to 0% NRE for hydroponics and mesocosms studies, respectively. In hydroponics, regardless of NRE level, specific root respiration under high N was 2.6 times of low N, and was greatest at depth. Under low N in mesocosms, plants with 67% NRE had 52% greater shoot biomass, 450% greater root length at depth, and 232% greater deep-injected 15N content in the shoot relative to 0% NRE, however biomass in hydroponics did not differ based on NRE. These results reveal the mechanism by which plants with fewer nodal roots increase N capture and shoot mass by reallocation of biomass to lateral, embryonic, and first whorl nodal roots that increases foraging efficiency in solid media. SummaryReallocating root biomass from nodal roots to lateral and early-emerging axial roots allows grasses to capture more nitrogen under limiting conditions, including by increasing foraging at depth.

plant biology↗

bioRxiv2019

Soybean Haplotype Map (GmHapMap): A Universal Resource for Soybean Translational and Functional Genomics

Here we describe the first worldwide haplotype map for soybean (GmHapMap) constructed using whole-genome sequence data for 1,007 Glycine max accessions and yielding 15 million variants. The number of unique haplotypes plateaued within this collection (4.3 million tag SNPs) suggesting extensive coverage of diversity within the cultivated germplasm. We imputed GmHapMap variants onto 21,618 previously genotyped (50K array/210K GBS) accessions with up to 96% success for common alleles. A GWAS performed with imputed data enabled us to identify a causal SNP residing in the NPC1 gene and to demonstrate its role in controlling seed oil content. We identified 405,101 haplotypes for the 55,589 genes and show that such haplotypes can help define alleles. Finally, we predicted 18,031 putative loss-of-function (LOF) mutations in 10,662 genes and illustrate how such a resource can be used to explore gene function. The GmHapMap provides a unique worldwide resource for soybean genomics and breeding.

plant biology↗

bioRxiv2019

Translational landscape in tomato revealed by transcriptome assembly and ribosome profiling

mRNA translation is a critical step in gene expression, but our understanding of the landscape and control of translation in diverse crops remains lacking. Here, we combined de novo transcriptome assembly and ribosome profiling to study global mRNA translation in tomato roots. Taking advantage of the 3-nucleotide periodicity displayed by translating ribosomes, we identified 354 novel small ORFs (sORFs) translated from previously unannotated transcripts, as well as 1329 upstream ORFs (uORFs) translated within the 5 UTRs of annotated protein-coding genes. Proteomic analysis confirmed that some of these novel uORFs and sORFs generate stable proteins in planta. Compared with the annotated ORFs, the uORFs use more flexible Kozak sequences around translation start sites. Interestingly, uORF-containing genes are enriched for protein phosphorylation/dephosphorylation and signaling transduction pathways, suggesting a regulatory role for uORFs in these processes. We also demonstrated that ribosome profiling is useful to facilitate the annotation of translated ORFs and noncanonical translation initiation sites. In addition to defining the translatome, our results revealed the global control of mRNA translation by uORFs and microRNAs in tomato. In summary, our approach provides a high-throughput method to discover unannotated ORFs, elucidates evolutionarily conserved translational features, and identifies new regulatory mechanisms hidden in a crop genome. SignificanceSeveral studies have shown that altering mRNA translation is a powerful way of improving crop performance. However, due to limited genomic resources and methods, translational regulation remains poorly understood in crops. By leveraging de novo transcriptome assembly and ribosome profiling, we mapped and quantified translating ribosomes across the entire transcriptome in tomato roots. This is the first experiment-based survey to systematically identify actively translated ORFs in a crop. Our results reveal numerous unannotated translation events and uncover new regulatory mechanisms of gene expression in tomato. Our approach not only facilitates our understanding of the tomato translational landscape but also provides a practical strategy to study the translatomes of other species. O_LIThe raw RNA-seq and Ribo-seq data have been deposited in the Gene Expression Omnibus (GEO) database under accession no. GSE124962. C_LIO_LIProteomics raw data files and MaxQuant Search results have been deposited at the MassIVE repository with dataset identifier: MSV000083363. C_LI

plant biology↗

bioRxiv2019

The systemin signaling cascade as derived from phosphorylation time courses under stimulation by systemin and its inactive Thr17Ala (A17) analog

Systemin is a small peptide with important functions in plant wound response signaling. Although transcriptional responses of systemin action are well described, the precise signaling cascades involved in its perception and signal transduction are poorly understood at the protein level. Here we use a phosphoproteomic profiling study involving stimulation time courses with systemin and its inactive analogon A17 to reconstruct a systemin-specific kinase/phosphatase signaling network. The time course analysis of systemin-induced phosphorylation patterns revealed early events at the plasma membrane, such dephosphorylation of H+-ATPase, rapid phosphorylation of NADPH-oxidase and Ca2+-ATPase. Later responses involved transient phosphorylation of small GTPases and vesicle trafficking proteins, as well as transcription factors. Based on a correlation analysis of systemin-specific phosphorylation profiles, we predict substrate candidates for 56 systemin specific kinases and 18 phosphatases. Among the kinases are several systemin-specific receptor kinases as well as kinases with downstream signaling functions, such as MAP-kinases. A regulatory circuit for plasma membrane H+-ATPase was predicted and confirmed by in-vitro activity assays. In this regulatory model we propose that upon systemin treatment, H+-ATPase LHA1 is rapidly de-phosphorylated at its C-terminal regulatory residue T955 by phosphatase PLL5, resulting in the alkalization of the growth medium within 2 minutes of systemin treatment. We further propose that the H+-ATPase LHA1 is re-activated by MAP-Kinase MPK2 later in the systemin response. MPK2 was identified with increased phosphorylation at its activating TEY-motif at 15 minutes of treatment and the predicted interaction with LHA1 was confirmed by in-vitro kinase assays. Our data set provides a valuable resource of proteomic events involved in the systemin signaling cascade with a focus on predictions of substrates to systemin-specific kinases and phosphatases.

plant biology↗

bioRxiv2019

The striking flower-in-flower phenotype of Arabidopsis thaliana Nossen (No-0) is caused by a novel LEAFY allele

SummaryThe transition to reproduction is a crucial step in the life cycle of any organism. In Arabidopsis thaliana the establishment of reproductive growth can be divided into two phases: In the first phase, cauline leaves with axillary meristems are formed and internode elongation begins. In the second phase, lateral meristems develop into flowers with defined organs. Floral shoots are usually determinate and suppress the development of lateral shoots. Here, we describe a Ds transposon insertion mutant in the Nossen (No-0) accession with severe defects in floral development and flower morphology. The most striking aspect is the outgrowth of stems from the axillary bracts of the primary flower carrying terminal secondary flowers. Therefore, we named this mutant flower-in-flower (fif). However, the insertion of the transposon in the annotated gene is not responsible for the fif phenotype. By means of classical and genome sequencing-based mapping, the mutation responsible for the fif phenotype was found to be in the LEAFY (LFY) gene. The mutation, a G-to-A exchange in the second exon of LFY, creates a novel lfy allele and causes a cysteine-to-tyrosine exchange in the 1-helix of the LFY DNA-binding domain. Whereas subcellular localization and homomerization are not affected, the DNA-binding of LFYFIF is abolished. We propose that the amino acid exchange interferes with the cooperative binding of LFY to its target DNA. To generate the strong fif phenotype, LFYFIF may act dominant-negatively by either forming non-binding LFY/LFYFIF heteromers or by titrating out the interaction partners, required for LFY function as transcription factor. Significant StatementThe fif phenotype of Arabidopsis thaliana No-0 is caused by a novel allele of the LEAFY gene

plant biology↗

bioRxiv2019

Maturity2, a novel regulator of flowering time in Sorghum bicolor, increases expression of SbPRR37 and SbCO in long days delaying flowering

Sorghum bicolor is a drought-resilient facultative short-day C4 grass that is grown for grain, forage, and biomass. Adaptation of sorghum for grain production in temperate regions resulted in the selection of mutations in Maturity loci (Ma1 - Ma6) that reduced photoperiod sensitivity and resulted in earlier flowering in long days. Prior studies identified the genes associated with Ma1 (PRR37), Ma3 (PHYB), Ma5 (PHYC) and Ma6 (GHD7) and characterized their role in the flowering time regulatory pathway. The current study focused on understanding the function and identity of Ma2. Ma2 delayed flowering in long days by selectively enhancing the expression of SbPRR37 (Ma1) and SbCO, genes that co-repress the expression of SbCN12, a source of florigen. Genetic analysis identified epistatic interactions between Ma2 and Ma4 and located QTL corresponding to Ma2 on SBI02 and Ma4 on SBI10. Positional cloning and whole genome sequencing identified a candidate gene for Ma2, Sobic.002G302700, which encodes a SET and MYND (SYMD) domain lysine methyltransferase. Nine sorghum genotypes previously identified as recessive for Ma2 contained the mutated version of Sobic.002G302700 present in 80M (ma2).

plant biology↗

bioRxiv2019

\"Low-cost\" initial burst of root development in whole Fagus crenata seedlings: The key to survival?

Terrestrial plants are rooted in one place, and therefore their metabolism must be flexible to adapt to continuously changing environments. This flexibility is probably influenced by the divergent metabolic traits of plant organs. However, direct measurements on organ-specific metabolic rates are particularly scarce and little is known about their roles in determining whole-individual meatabolism. To reveal this on seedlings of Fagus crenata, which is one of the most widespread dominant genus in temperate deciduous broad leaf forests in the circum-polar Northern Hemisphere, we measured respiration, fresh mass and surface area for total leaves, stems and roots of 55 individuals in two years from germination and analyzed their relationships with individual metabolism. Proportion of roots to whole plant in mass increased from approximately 17% to 74%, and that in surface area increased from about 11% to 82% in the two years. Nonetheless, the increment of the proportion of root respiration to whole-plant respiration was from 9.2% to only 40%, revealing that the increment in mass and surface area of roots was much larger than the increment in energetic cost. As a result, only the roots showed a substantial decline in both respiration/surface area and respiration/mass among the three organs; roots had about 90% decline in their respiration/surface area, and 84% decline in their respiration/mass, while those in leaves and stems were relatively constant. The low-cost and rapid root development is specific to the two years after germination and would be effective for avoiding water and nutrient deficit, and possibly helps seedling survival. This drastic shift in structure and function with efficient energy use in developmental change from seeds to seedlings may underpin the establishment of F. crenata forests. We discuss significance of lowering energetic cost for various individual organisms to effectively acquire resources from a wide perspective of view.

plant biology↗

bioRxiv2019

Genome-Wide Association Study and Pathway-Level Analysis of Kernel Color in Maize

Rapid development and adoption of biofortified, provitamin A-dense orange maize (Zea mays L.) varieties could be facilitated by a greater understanding of the natural variation underlying kernel color, including as relates to carotenoid biosynthesis and retention in maize grain. Greater abundance of carotenoids in maize kernels is generally accompanied by deeper orange color, useful for distinguishing provitamin A-dense varieties to consumers. While kernel color can be scored and selected with high-throughput, low-cost phenotypic methods within breeding selection programs, it remains to be well established as to what would be the logical genetic loci to target for selection for kernel color. We conducted a genome-wide association study of maize kernel color, as determined by colorimetry, in 1,651 yellow and orange inbreds from the Ames maize inbred panel. Associations were found with y1, encoding the first committed step in carotenoid biosynthesis, and with dxs2, which encodes the enzyme responsible for the first committed step in the biosynthesis of the isoprenoid precursors of carotenoids. These genes logically could contribute to overall carotenoid abundance and thus kernel color. The lcyE and zep1 genes, which can affect carotenoid composition, were also found to be associated with colorimeter values. A pathway-level analysis, focused on genes with a priori evidence of involvement in carotenoid biosynthesis and retention, revealed associations for dxs3 and dmes1, involved in isoprenoid biosynthesis; ps1 and vp5, within the core carotenoid pathway; and vp14, involved in cleavage of carotenoids. Collectively, these identified genes appear relevant to the accumulation of kernel color.

plant biology↗