Abstract
BackgroundTrees experience mechanical stimuli -like wind- that trigger thigmomorphogenetic syndrome, leading to modifications of plant growth and wood quality. This syndrome affects tree productivity but is also believed to improve tree acclimation to chronic wind. Wind is particularly challenging for trees, because of their stature and perenniality. Climate change forecasts are predicting that the occurrence of high wind will worsen, making it increasingly vital to understand the mechanisms regulating thigmomorphogenesis, especially in perennial plants. By extension, this also implies factoring in the recurring nature of wind episodes. However, data on the molecular processes underpinning mechanoperception and transduction of mechanical signals, and their dynamics, are still dramatically lacking in trees.ResultsHere we performed a genome-wide and time-series analysis of poplar transcriptional responsiveness to transitory and recurring controlled stem bending, mimicking wind. The study revealed that 6% of the poplar genome is differentially expressed after a single transient bending. The combination of clustering, Gene Ontology categorization and time-series expression approaches revealed the diversity of gene expression patterns and biological processes affected by stem bending. Short-term transcriptomic responses entailed a rapid stimulation of plant defence and abiotic stress signalling pathways, including ethylene and jasmonic acid signalling but also photosynthesis process regulation. Late transcriptomic responses affected genes involved in cell wall organization and/or wood development. An analysis of the molecular impact of recurring bending found that the vast majority (96%) of the genes differentially expressed after a first bending presented reduced or even net-zero amplitude regulation after the second exposure to bending.ConclusionThis study constitutes the first dynamic characterization of the molecular processes affected by single or repeated stem bending in poplar. Moreover, the global attenuation of the transcriptional responses, observed from as early as after a second bending, indicates the existence of a mechanism governing a fine tuning of plant responsiveness. This points toward several mechanistic pathways that can now be targeted to elucidate the complex dynamics of wind acclimation.
Highlights
Trees experience mechanical stimuli -like wind- that trigger thigmomorphogenetic syndrome, leading to modifications of plant growth and wood quality
This study suggested that part of the accommodation process could be explained by a regulation at transcriptional level [6], requiring a more global analysis
Statistical analysis revealed 2,663 genes differentially expressed along the time-course (Fig. 1; Additional file 1). These Differentially Expressed Genes (DEG) represented 6% of the whole poplar genome, and 75.6% of them were regulated at just 0.5 h or 2 h post-bending (0.5 h PB or 2 h PB)
Summary
Trees experience mechanical stimuli -like wind- that trigger thigmomorphogenetic syndrome, leading to modifications of plant growth and wood quality. Data on the molecular processes underpinning mechanoperception and transduction of mechanical signals, and their dynamics, are still dramatically lacking in trees In their fluctuating environment, plants are constantly exposed to abiotic stimuli to which they are sensitive and responsive. Some of these stimuli, such as wind exposure, count a strong mechanical component that has a major influence on plant growth and development Exposure to such mechanical stimulations results in the so-called thigmomorphogenetic syndrome characterized by a reduction in stem elongation [1, 2], local stimulation of radial growth [3, 4], and modification of the stem’s mechanical properties [5]. A single transitory stem bending led first to a short period of secondary growth inhibition (4 h) followed by a massive stimulation of the growth rate over 3 days, and a relaxation to normal values [4]
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