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bioRxiv2018

Developmental genetics of corolla tube formation: role of the tasiRNA-ARF pathway

More than 80,000 angiosperm species produce flowers with petals fused into a corolla tube. As an important element of the tremendous diversity of flower morphology, the corolla tube plays a critical role in many specialized interactions between plants and animal pollinators (e.g., beeflies, hawkmoths, hummingbirds, nectar bats), which in turn drives rapid plant speciation. Despite its clear significance in plant reproduction and evolution, the corolla tube remains one of the least understood plant structures from a developmental genetics perspective. Through mutant analyses and transgenic experiments, here we show that the tasiRNA-ARF pathway is required for corolla tube formation in the monkeyflower species Mimulus lewisii. Loss-of-function mutations in the M. lewisii orthologs of ARGONAUTE7 and SUPPRESSOR OF GENE SILENCING 3 cause a dramatic decrease in abundance of TAS3-derived small RNAs and a moderate up-regulation of AUXIN RESPONSE FACTOR 3 (ARF3) and ARF4, which lead to inhibition of lateral expansion of the bases of petal primordia and complete arrest of the upward growth of the inter-primordial regions, resulting in unfused corollas. By using an auxin reporter construct, we discovered that auxin distribution is continuous along the petal primordium base and the inter-primordial region during the critical stage of corolla tube formation in the wild-type, and that this auxin distribution is much weaker and more restricted in the mutant. Together, these results suggest a new conceptual model highlighting the central role of auxin directed synchronized growth of the petal primordium base and the inter-primordial region in corolla tube formation.

plant biology↗

bioRxiv2018

SlARF10, an auxin response factor, is required for chlorophyll and sugar accumulation during tomato fruit development

Tomato green fruits photosynthesis contributes to fruit growth and carbon economy. Tomato auxin response factor 10 (SlARF10) is one of the members of ARF family. Our results showed that SlARF10 locates in the nucleus and has no transcriptional activity. SlARF10 was expressed in various tomato tissues, but highly expressed in green fruit. Up-regulation of SlARF10 produced dark green phenotype of fruits, whereas down-regulation of SlARF10 had light green phenotype. Autofluorescence and chlorophyll content analysis confirmed the phenotypes, which indicated that SlARF10 plays an important role in chlorophyll accumulation in tomato fruits. Up-regulation of SlARF10 increased the photochemical potential in tomato leaves and fruits. Furthermore, the SlARF10 up-regulating lines displayed improved accumulation of starch in fruits, whereas SlARF10 suppressed lines had inhibited starch accumulation. Up-regulation of SlARF10 increased the expression of AGPases, the starch biosynthesis genes. SlARF10 up-regulating lines had increased accumulation of SlGLK1 and SlGLK2 transcripts in fruits. The promoter sequence of SlGLK1 gene had two conserved ARF binding sites. SlARF10 may regulate the expression of SlGLK1, thus controlling chlorophyll accumulation, photosynthesis rates and sugars synthesis in fruits. Our study provided more insight on the link between auxin signaling, chloroplastic activity and sugar metabolism during the development of tomato fruits.\n\nAbbreviations\n\nHighlightSlARF10 played an important role in the chlorophyll accumulation and photosynthesis in tomato fruits. SlARF10 was involved in starch accumulation by controlling the expression of starch synthesis related enzyme genes. SlARF10 may regulate the expression of SlGLK1, thus controlling chlorophyll accumulation, photosynthesis rates and sugars synthesis in tomato fruits.

plant biology↗

bioRxiv2018

PIN7 auxin carrier is a terminator of radial root expansion in Arabidopsis thaliana

Directional growth of lateral roots is critical for radial expansion and soil coverage. Despite its importance, almost nothing is known about its molecular determinants. Initially, young lateral roots (LRs) grow away from the parental root maintaining the angle acquired shortly after emergence. A second downwards bending response to gravity terminates the so-called plateau phase and thereby limits the radial root expansion. Here we show that the exit from the plateau phase correlates with an increase in auxin signalling at the tip of LRs. Moreover, the increase in auxin levels induces the termination of the plateau phase, which requires PIN auxin efflux carriers. Our data suggests that the developmental increase of auxin triggers the preferential de-repression of PIN7 in gravity-sensing columella cells. The subsequent polarization of PIN7 heralds the bending towards gravity and, hence, the exit from the plateau phase. This developmental framework reveals the distinct roles of PIN auxin efflux carriers in controlling the radial growth of root systems.

plant biology↗

bioRxiv2018

Paleochronic reversion in Psophocarpus: Dynamics II, rhizogeny on floral anatomic fields

Paleochronic reversion is confirmed in Psophocarpus as a basic floral ground state. That state can expand to include dynamics (T(g,...,h)) of axial expansion (AE) as a permutation (Tx) phase beginning as phyllotactic floral phylloid (Tphyld) and/or axial decompression (TAxl) manifest as linear elongation (TLong) and/or rotation (TRtn) and/or latitudinal (TLat) expansion. Organ regions present a continuum as a vector space [Formula] of floral axial transformation. A generative phase of meristem activity (T(Rz, Sam, Infl)) can follow.\n\nExperiments with 49 phylloid and/or phyllome paleochronically reverted flowers presented varying degrees of phyllotactic permutation involving development of a pericladial stalk (PCL) and/or inter-bracts stem (IBS) and/or activated pedicel (PdcL) and/or gynophore (Gnf), Cupule-like (Gnf)/Cupl-Lk) elongation. A meristem generative function included rhizogeny as root site generation (RSG) at the calyx (Cl), PCL, bracts (Bt), IBS, PdcL and/or Gnf/Cupl-Lk regions manifest as eigenvector functions as RSG whose density of generation was associated with permutation of the ground state. A continuum of pedicel to calyx regions constitutes a subset [Formula] of a linear vector space [Formula] whose extension is defined within the space: [Formula].\n\nThe vector space [Formula] transforms to a master vector field [Formula] of generated Euclidian eigenvectors so that:\n\nO_FD O_INLINEFIG[Formula 1]C_INLINEFIGM_FD(1)C_FD\n\nHighlightsO_LIPaleochronic reversion in plants presents paleo-botanic floral characteristics at a morphologic ground state.\nC_LIO_LIA permutative dynamic can ensue changing floral architecture.\nC_LIO_LIThat dynamic can then transform to meristem generation presenting rhizogenous eigenvectors.\nC_LI

plant biology↗

bioRxiv2018

Dawn and photoperiod sensing by phytochrome A

In plants, light receptors play a pivotal role in photoperiod sensing, enabling them to track seasonal progression. Photoperiod sensing arises from an interaction between the plants endogenous circadian oscillator and external light cues. Here, we characterise the role of phytochrome A (phyA) in photoperiod sensing. Our meta-analysis of functional genomic datasets identified phyA as a principal transcriptional regulator of morning-activated genes, specifically in short photoperiods. We demonstrate that PHYA expression is under the direct control of the PHYTOCHROME INTERACTING FACTOR transcription factors, PIF4 and PIF5. As a result, phyA protein accumulates during the night, especially in short photoperiods. At dawn phyA activation by light results in a burst of gene expression, with consequences for anthocyanin accumulation. The combination of complex regulation of PHYA transcript and the unique molecular properties of phyA protein make this pathway a sensitive detector of both dawn and photoperiod.\n\nSignificance statementThe changing seasons subject plants to a variety of challenging environments. In order to deal with this, many plants have mechanisms for inferring the season by measuring the duration of daylight in a day. A number of well-known seasonal responses such as flowering are responsive to daylength or photoperiod. Here, we describe how the photoreceptor protein phytochrome A senses short photoperiods. This arises from its accumulation during long nights, as happens during winter, and subsequent activation by light at dawn. As a result of this response, the abundance of red anthocyanin pigments is increased in short photoperiods. Thus, we describe a mechanism underlying a novel seasonal phenotype in an important model plant species.

plant biology↗

bioRxiv2018

Engineering Plant Architecture via CRISPR/Cas9-mediated Alteration of Strigolactone Biosynthesis

Precision plant genome engineering holds much promise for targeted improvement of crop traits via unprecedented single-base level control over the genetic material. Strigolactones (SLs) are a key determinant of plant architecture, known for their role in inhibiting shoot branching (tillering). Here, we used CRISPR/Cas9 in rice (Oryza sativa) for targeted disruption of CAROTENOID CLEAVAGE DIOXYGENASE 7 (CCD7), which controls a key step in SL biosynthesis. The ccd7 mutants exhibited a striking increase in tillering, combined with a dwarf phenotype, which could be rescued by application of the synthetic SL analog GR24. Striga germination assays and liquid chromatography-mass spectrometry analysis showed that root exudates of ccd7 mutants were also SL deficient. Taken together, our results show the power of CRISPR/Cas9 for targeted engineering of plant architecture and for elucidating the molecular underpinnings of architecture-related traits.

plant biology↗

bioRxiv2018

The coming of age of EvoMPMI: evolutionary molecular plant-microbe interactions across multiple timescales

Plant-microbe interactions are great model systems to study co-evolutionary dynamics across multiple timescales, ranging from multimillion year macroevolution to extremely rapid evolutionary adaptations. However, mechanistic research on plant-microbe interactions has often been conducted with little consideration of the insights that can be gained from evolutionary concepts and methods. Conversely, evolutionary research has rarely integrated the diverse range of molecular mechanisms and models that continue to emerge from the molecular plant-microbe interactions field. These trends are changing. In recent years, the incipient field of evolutionary molecular plant-microbe interactions (EvoMPMI) has emerged to bridge the gap between mechanistic molecular research and evolutionary approaches. Here, we report on recent advances in EvoMPMI. In particular, we highlight new systems to study microbe interactions with early diverging land plants, and new findings from studies of adaptive evolution in pathogens and plants. By linking mechanistic and evolutionary research, EvoMPMI promises to add a new dimension to our understanding of plant-microbe interactions.

plant biology↗

bioRxiv2018

FlowPot axenic plant growth system for microbiota research

The presence of resident microbiota on and inside plants is hypothesized to influence many phenotypic attributes of the host. Likewise, host factors and microbe-microbe interactions are believed to influence microbial community assembly. Rigorous testing of these hypotheses necessitates the ability to grow plants in the absence or presence of resident or defined microbiota. To enable such experiments, we developed the scalable and inexpensive FlowPot growth platform. FlowPots have a sterile peat substrate amenable to colonization by microbiota, and the platform supports growth of the model plant Arabidopsis thaliana in the absence or presence of soil-derived microbial communities. Mechanically, the FlowPot system is unique in that it allows for total-saturation of the sterile substrate by \"flushing\" with water and/or nutrient solution via an irrigation port. The irrigation port also facilitates passive drainage of the substrate, preventing root anoxia. Materials to construct an individual FlowPot total [~]$2. A simple experiment with 12 FlowPots requires [~]4.5 h of labor following peat and seed sterilization. Plants are grown on FlowPots within a standard tissue culture microbox after inoculation, thus the Flowpot system is modular and does not require a sterile growth chamber. Here, we provide a detailed assembly and microbiota inoculation protocol for the FlowPot system. Collectively, this standardized suite of tools and colonization protocols empowers the plant microbiome research community to conduct harmonized experiments to elucidate the rules microbial community assembly, the impact of microbiota on host phenotypes, and mechanisms by which host factors influence the structure and function of plant microbiota.

plant biology↗

bioRxiv2018

Rehydration rates and the prevalence of xylem-hydration of flowers

Angiosperm flowers are remarkably diverse anatomically and morphologically, yet they all must satisfy the physiological constraints of supplying sufficient amounts of water and carbon effectively promote pollination. Flowers often occur in the hottest, driest parts of the plant canopy and can face harsh abiotic conditions. Prior evidence suggests that extant species vary dramatically in how water is delivered to flowers, with some evidence that water may be imported into flowers by the phloem. Here we measured midday water potential gradients between flowers, leaves, and stems often phylogenetically diverse species. We further tested the likelihood of xylem-hydration by measuring rates of rehydration after experimentally induced desiccation. There was no significant difference in rehydration rates between leaves and flowers. These results are consistent with xylem-hydration of flowers and suggest that there has been little modification to the mechanisms of water transport despite the diversity of floral form.

plant biology↗

bioRxiv2018

Identification and comparison of individual chromosomes of three Hordeum chilense accessions, Hordeum vulgare and Triticum aestivum by FISH

Karyotypes of three accessions of Hordeum chilense (H1, H16 and H7), Hordeum vulgare and Triticum aestivum were characterized by physical mapping of several repetitive sequences. A total of fourteen repetitive sequences were used as probes for fluorescence in situ hybridization (FISH) with the aim of identifying inter- and intra-species polymorphisms. The (AG)12 and 4P6 probes only produced hybridization signals in wheat, the BAC7 probe only hybridized to the centromeric region of H. vulgare, and the pSc119.2 probe hybridized to both wheat and H. chilense, but not to H. vulgare. The remaining repetitive sequences used in this study produced a hybridization signal in all the genotypes. Probes pAs1, pTa535, pTa71, CCS1 and CRW were much conserved, showing no significant polymorphism among the genotypes studied. Probes GAA, (AAC)5, (CTA)5, HvT01 and pTa794 produced the most different hybridization pattern. We identified large polymorphisms in the three accessions of H. chilense studied, supporting the proposal of the existence of different groups inside H. chilense species. The set of probes described in this work allowed the identification of every single chromosome in all three species, providing a complete cytogenetic karyotype of H. chilense, H. vulgare and T. aestivum chromosomes, useful in wheat and tritordeum breeding programs.

plant biology↗

bioRxiv2018

Crop domestication and pathogen virulence: Interactions of tomato and Botrytis genetic diversity

Human selection during crop domestication alters numerous traits, including disease resistance. Studies of qualitative resistance to specialist pathogens typically find decreased resistance in domesticated crops in comparison to their wild relatives. However, less is known about how crop domestication affects quantitative interactions with generalist pathogens. To study how crop domestication impacts plant resistance to generalist pathogens, and correspondingly how this interacts with the pathogens genetics, we infected a collection of wild and domesticated tomato accessions with a genetically diverse population of the generalist pathogen Botrytis cinerea. We quantified variation in lesion size of 97 B. cinerea genotypes (isolates) on 6 domesticated Solanum lycopersicum and 6 wild S. pimpinellifolium genotypes. This showed that lesion size was significantly controlled by plant domestication, plant genetic variation, and the pathogens genotype. Overall, resistance was slightly elevated in the wild germplasm in comparison to domesticated tomato accessions. Genome-wide association (GWA) mapping in B. cinerea identified a highly polygenic collection of genes. This suggests that breeding against this pathogen would need to utilize a diversity of isolates to capture all possible mechanisms. Critically, we identified a discrete subset of B. cinerea genes where the allelic variation was linked to altered virulence against the wild versus domesticated tomato accessions. This indicates that this generalist pathogen already has the necessary allelic variation in place to handle the introgression of wild resistance mechanisms into the domesticated crop. Future studies are needed to assess how these observations extend to other domesticated crops and other generalist pathogens.

plant biology↗

bioRxiv2018

Kinetics of winter deacclimation in response to temperature determines dormancy status and quantifies chilling requirement in grapevines (Vitis spp.)

2.Bud dormancy and cold hardiness are critical adaptations for surviving winter cold stress for temperate perennial plant species, with shifting temperature-based responses during the winter. The objective of this study was to uncover the relationship between dormancy transition (chilling requirement) and temperature on the loss of cold hardiness and budbreak. Dormant cuttings of Vitis vinifera, V. aestivalis, V. amurensis, and V. riparia were examined to determine the relationship between chilling requirement and temperature on rate of deacclimation (kdeacc). Differential thermal analysis was used to determine kdeacc using mean low temperature exotherms. Effect of chill was evaluated as the deacclimation potential ({psi}deacc), which was the change in kdeacc due to chill accumulation. Budbreak was also evaluated in fully chilled buds at different temperatures. Results indicate that {psi}deacc varies dependent on dormancy state, following a logarithmic response to chill accumulation. The effect of temperature on kdeacc was exponential at low and logarithmic at high temperatures. The combination of {psi}deacc and kdeacc resulted in good prediction of deacclimation. Budbreak phenology was also explained by differences in kdeacc. Deacclimation rates can be used as a quantitative determinant of dormancy transition and budbreak, and to refine models predicting effects of climate change.

plant biology↗

bioRxiv2018

Arabidopsis Lunapark proteins are involved in ER cisternae formation

The plant endoplasmic reticulum (ER) is crucial to the maintenance of cellular homeostasis. The ER consists of a dynamic and continuously remodelling network of tubules and cisternae. Several conserved membrane proteins have been implicated in formation and maintenance of the ER network in plants, such as RHD3 and the reticulon family of proteins.\n\nDespite the recent work in mammalian and yeast cells, the detailed molecular mechanisms of ER network organisation in plants still remain largely unknown. Recently novel ER network-shaping proteins called Lunapark have been identified in yeast and mammalian cells.\n\nHere we identify two arabidopsis LNP homologues and investigate their subcellular localisation via confocal microscopy and potential function in shaping the ER network using protein-protein interaction assays and mutant analysis.\n\nWe show that AtLNP1 overexpression in tobacco leaf epidermal cells mainly labels the three-way junctions (trivia) of the ER network whereas AtLNP2 labels the whole ER. Overexpression of LNP proteins results in an increased abundance of ER cisternae and an lnp1lnp2 amiRNA line displays a less structured ER network.\n\nThus, we hypothesize that AtLNP1 and AtLNP2 are involved in determining the dynamic morphology of the plant ER, possibly by regulating the formation of ER cisternae.

plant biology↗

bioRxiv2018

A role for phylloquinone biosynthesis in the plasma membrane as revealed in a non-photosynthetic parasitic plant

Phylloquinone is a lipophilic naphthoquinone found predominantly in chloroplasts and best known for its function in photosystem I electron transport and disulfide bridge formation of photosystem II subunits. Phylloquinone has also been detected in plasma membrane preparations of heterotrophic tissues with potential transmembrane redox function, but the molecular basis for this noncanonical pathway is unknown. Here we provide evidence of plasma membrane phylloquinone biosynthesis in a nonphotosynthetic holoparasite Phelipanche aegyptiaca. A nonphotosynthetic and nonplastidial role for phylloquinone is supported by transcription of phylloquinone biosynthetic genes during seed germination and haustorium development, by plasma membrane-localization of alternative terminal enzymes, and by detection of phylloquinone in germinated seeds. Comparative gene network analysis with photosynthetically competent parasites revealed a bias of Phelipanche phylloquinone genes toward coexpression with oxidoreductases involved in plasma membrane electron transport. Genes encoding the plasma membrane phylloquinone pathway are also present in several photoautotrophic taxa of Asterids, suggesting an ancient origin of multifunctionality. Our findings suggest that nonphotosynthetic holoparasites exploit alternative targeting of phylloquinone for transmembrane redox signaling associated with parasitism.

plant biology↗

bioRxiv2018

Mechanistic analysis of the SERK3 elongated allele defines a role for BIR ectodomains in brassinosteroid signaling

The leucine-rich repeat receptor kinase (LRR-RK) BRI1 requires a shape-complementary SERK co-receptor for brassinosteroid sensing and receptor activation. Interface mutations that weaken the interaction between receptor and co-receptor in vitro reduce brassinosteroid signaling responses. The SERK3 elongated (elg) allele maps to the complex interface and shows enhanced brassinosteroid signaling, but surprisingly no tighter binding to the BRI1 ectodomain in vitro. Here, we report that rather than promoting the interaction with BRI1, the elg mutation disrupts the ability of the co-receptor to interact with the ectodomains of BIR receptor pseudokinases, negative regulators of LRR-RK signaling. A conserved lateral surface patch in BIR LRR domains is required for targeting SERK co-receptors and the elg allele maps to the core of the complex interface in a 1.25 [A] BIR3 - SERK1 structure. Collectively, our structural, quantitative biochemical and genetic analyses suggest that brassinosteroid signaling complex formation is negatively regulated by BIR receptor ectodomains.

plant biology↗

bioRxiv2018

Dissection of the microProtein miP1 floral repressor complex in Arabidopsis

MicroProteins have emerged as potent regulators of transcription factor activity. Here we use a combination of forward genetics and proteomics to dissect the miP1a/b microProtein complex that acts to delay the floral transition in Arabidopsis. The microProteins miP1a and miP1b can bridge an interaction between the flowering promoting factor CONSTANS (CO) and the TOPLESS (TPL) co-repressor protein to represses flowering. We find that the JUMONJI14 (JMJ14) histone demethylase is part of this repressor complex that can initiate chromatin changes in FLOWERING LOCUS T (FT) gene, the direct target of CO. Plants with mutations in JMJ14 exhibit an early flowering phenotype that is largely dependent on the activity of CO, supporting a role for CO in this repressive complex. When mis-expressed at the shoot apex, CO can induce early flowering only in the jmj14 background. Our results indicate that the repressor acts in the shoot apical meristem to keep it in an undifferentiated state until the leaf-derived florigen signal induces the conversion into a floral meristem.

plant biology↗

bioRxiv2018

Sent to the Corner: xylem vessel anatomy not surface area determines megaphyll hydraulics in Cecropia obtusa Trecul (Urticaceae)

Corners rule predicts a positive correlation between leaf dimensions and the cross-sectional area of the primary stem. Although this relationship is usually explained by hydraulic and mechanical requirements, these hypotheses have never been tested empirically. However, Corners rule is tricky to investigate since rapid secondary growth of the stem prevents a rigorous link being established between a given leaf and the supporting stem. We chose a twig-like leaf model since petiole anatomy is only linked to the attached lamina. We tested the hypothesis that anatomical adjustments to hydraulic requirements related to vessel size enable reduced investment in tissue in the framework of Corners rule. We conducted a functional, mechanistic and intraspecific investigation of Cecropia obtusa Trecul, a Neotropical pioneer tree, by integrating morphological, anatomical and theoretical hydraulic traits around the lamina-petiole size relationship. The twig-like structure of the leaf and the strong lamina-petiole correlation of this model tree species made it possible to use the leaf-level model for a rigorous investigation of the functional implications of Corners rule. We found a positive correlation between petiole size, lamina size, the ratio of mean vessel area to vessel frequency in the petiole xylem and theoretical specific conductivity in the petiole xylem. Hydraulic function supports Corners rule to a lesser extent than previously thought. Variations in vessel dimensions mainly drive xylem hydraulic performances and avoid disproportionate petiole cross-sections to answer to hydraulic requirements associated with lamina size.

plant biology↗

bioRxiv2018

Blue light advances bud burst in branches of three temperate deciduous tree species under short-day conditions

During spring, utilising multiple cues allow temperate tree species to coordinate their bud burst and leaf out, at the right moment to capitalise on favourable conditions for photosynthesis. Whilst the effect of blue light (400-500nm) has been shown to increase percentage bud burst of axillary shoots of Rosa sp, the effects of blue light on spring-time bud burst of temperate deciduous tree species has not previously been reported. We tested the hypotheses that blue light would advance spring bud burst in temperate tree species, and that late-successional species would respond more than early-successional species, whos bud burst is primarily determined by temperature. The bud development of Alnus glutinosa, Betula pendula, and Quercus robur branches, cut from dormant trees, was monitored under two light treatments of equal photosynthetically active radiation (PAR, 400-700 nm) and temperature, either with or without blue light, under controlled environmental conditions. In the presence of blue light, the mean time required to reach 50% bud burst was reduced by 3.3 days in Betula pendula, 6 days in Alnus glutinosa, and 6.3 days in Quercus robur. This result highlights the potential of the blue region of the solar spectrum to be used as an extra cue that could help plants to regulate their spring phenology, alongside photoperiod and temperature. Understanding how plants combine photoreceptor-mediated cues with other environmental cues such as temperature to control phenology is essential if we are to accurately predict how tree species might respond to climate change.\n\nKey MessageAn LED spectrum containing blue light advanced bud burst in branches of Betula pendula, Alnus glutinosa and Quercus robur compared with a spectrum without blue light in a controlled environment.

plant biology↗