Dataset Information

Jasmonate Signalling Contributes to Primary Root Inhibition Upon Oxygen Deficiency in Arabidopsis thaliana.

ABSTRACT: Plants, including most crops, are intolerant to waterlogging, a stressful condition that limits the oxygen available for roots, thereby inhibiting their growth and functionality. Whether root growth inhibition represents a preventive measure to save energy or is rather a consequence of reduced metabolic rates has yet to be elucidated. In the present study, we gathered evidence for hypoxic repression of root meristem regulators that leads to root growth inhibition. We also explored the contribution of the hormone jasmonic acid (JA) to this process in Arabidopsis thaliana. Analysis of transcriptomic profiles, visualisation of fluorescent reporters and direct hormone quantification confirmed the activation of JA signalling under hypoxia in the roots. Further, root growth assessment in JA-related mutants in aerobic and anaerobic conditions indicated that JA signalling components contribute to active root inhibition under hypoxia. Finally, we show that the oxygen-sensing transcription factor (TF) RAP2.12 can directly induce Jasmonate Zinc-finger proteins (JAZs), repressors of JA signalling, to establish feedback inhibition. In summary, our study sheds new light on active root growth restriction under hypoxic conditions and on the involvement of the JA hormone in this process and its cross talk with the oxygen sensing machinery of higher plants.

SUBMITTER: Shukla V

PROVIDER: S-EPMC7464498 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Publications

Jasmonate Signalling Contributes to Primary Root Inhibition Upon Oxygen Deficiency in <i>Arabidopsis thaliana</i>.

Shukla Vinay V Lombardi Lara L Pencik Ales A Novak Ondrej O Weits Daan A DA Loreti Elena E Perata Pierdomenico P Giuntoli Beatrice B Licausi Francesco F

Plants (Basel, Switzerland) 20200817 8

Plants, including most crops, are intolerant to waterlogging, a stressful condition that limits the oxygen available for roots, thereby inhibiting their growth and functionality. Whether root growth inhibition represents a preventive measure to save energy or is rather a consequence of reduced metabolic rates has yet to be elucidated. In the present study, we gathered evidence for hypoxic repression of root meristem regulators that leads to root growth inhibition. We also explored the contributi ...[more]

PMID: 32824502

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Project description:An original approach to develop sustainable agriculture with less nitrogen fertilizer inputs is to tackle the cross-talk between nitrogen nutrition and plant growth regulators. In particular the gaseous hormone, ethylene, is a prime target for that purpose. The variation of ethylene production in natural accessions of the model species Arabidopsis thaliana was explored in response to the nitrate supply. Ethylene was measured with a laser-based photoacoustic detector. First, experimental conditions were established with Columbia-0 (Col-0) accession, which was grown in vitro on horizontal plates across a range of five nitrate concentrations (0.5, 1, 2.5, 5, or 10 mM). The concentrations of 1 and 10 mM nitrate were retained for further characterization. Along with a decrease of total dry biomass and higher biomass allocation to the roots, the ethylene production was 50% more important at 1 mM than at 10 mM nitrate. The total transcript levels of 1-AMINOCYCLOPROPANE-1-CARBOXYLIC ACID SYNTHASES (ACS) in roots and those of ACC OXIDASES (ACO) in shoots increased by 100% between the same treatments. This was mainly due to higher transcript levels of ACS6 and of ACO2 and ACO4 respectively. The assumption was that during nitrogen deficiency, the greater biomass allocation in favor of the roots was controlled by ethylene being released in the shoots after conversion of ACC originating from the roots. Second, biomass and ethylene productions were measured in 20 additional accessions. Across all accessions, the total dry biomass and ethylene production were correlated negatively at 1 mM but positively at 10 mM nitrate. Furthermore, polymorphism was surveyed in ACC and ethylene biosynthesis genes and gene products among accessions. Very few substitutions modifying the amino acids properties in conserved motifs of the enzymes were found in the accessions. Natural variation of ethylene production could be further explored to improve Nitrogen Use Efficiency (NUE), in particular by manipulating features like the biomass production and the timing of senescence upon nitrogen limitation.

Project description:Physical damage can strongly affect plant growth, reducing the biomass of developing organs situated at a distance from wounds. These effects, previously studied in leaves, require the activation of jasmonate (JA) signalling. Using a novel assay involving repetitive cotyledon wounding in Arabidopsis seedlings, we uncovered a function of JA in suppressing cell division and elongation in roots. Regulatory JA signalling components were then manipulated to delineate their relative impacts on root growth. The new transcription factor mutant myc2-322B was isolated. In vitro transcription assays and whole-plant approaches revealed that myc2-322B is a dosage-dependent gain-of-function mutant that can amplify JA growth responses. Moreover, myc2-322B displayed extreme hypersensitivity to JA that totally suppressed root elongation. The mutation weakly reduced root growth in undamaged plants but, when the upstream negative regulator NINJA was genetically removed, myc2-322B powerfully repressed root growth through its effects on cell division and cell elongation. Furthermore, in a JA-deficient mutant background, ninja1 myc2-322B still repressed root elongation, indicating that it is possible to generate JA-responses in the absence of JA. We show that NINJA forms a broadly expressed regulatory layer that is required to inhibit JA signalling in the apex of roots grown under basal conditions. By contrast, MYC2, MYC3 and MYC4 displayed cell layer-specific localisations and MYC3 and MYC4 were expressed in mutually exclusive regions. In nature, growing roots are likely subjected to constant mechanical stress during soil penetration that could lead to JA production and subsequent detrimental effects on growth. Our data reveal how distinct negative regulatory layers, including both NINJA-dependent and -independent mechanisms, restrain JA responses to allow normal root growth. Mechanistic insights from this work underline the importance of mapping JA signalling components to specific cell types in order to understand and potentially engineer the growth reduction that follows physical damage.

Dataset Information

Jasmonate Signalling Contributes to Primary Root Inhibition Upon Oxygen Deficiency in Arabidopsis thaliana.

Publications

Jasmonate Signalling Contributes to Primary Root Inhibition Upon Oxygen Deficiency in <i>Arabidopsis thaliana</i>.

Similar Datasets

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