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Poplar stem transcriptome is massively remodelled in response to single or repeated mechanical stimuli

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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]. These alterations of plant architecture are thought to improve plant acclimation to chronic wind regimes [6]. Using continuous monitoring techniques [4, 7], the early kinetics of these plant growth responses were studied in tomato and poplar by applying quantified stem bending. In poplar, 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 finally a relaxation to normal values [4].

To better understand tree acclimation to wind, it is important to first unravel the processes that regulate thigmomorphogenetic syndrome. However, the way plant cells perceive and transduce mechanical signals is still poorly understood. Two major classes of potential mechanosensors are thought to be involved: plant MechanoSensitive (MS) ion channels and Receptor-Like Kinases (RLK) inserted into the cell wall–plasma membrane–cytoskeleton continuum (see [8] for review). Prior to the advent of transcriptomics, studies had identified a handful of mechanoresponsive genes, including TOUCH genes (TCH) that mainly encode calmodulins or calmodulin-like proteins and Xyloglucan endo-Transglycosylase/Hydrolase (XTH) [9], genes encoding protein kinases [10, 11], Transcription Factors (TF) [12], genes involved in Jasmonic Acid (JA) and ethylene synthesis [13, 14], and genes involved in antioxidative responses [15]. In 2005, a transcriptome analysis of touch-stimulated Arabidopsis rosette leaves allowed a more global insight into the molecular functions altered after a touch-stimulus. Over 700 genes presented regulated expression 30 min after the stimulus [16], representing over 2.5% of the genome. Among these genes, the vast majority (589/760) were up-regulated. Analysis of the functional categorization of these up-regulated genes revealed enrichment in genes encoding calcium-binding proteins, cell-wall proteins, disease resistance proteins, kinases and TF, and a decline in genes involved in general metabolism and the ubiquitin/protein degradation pathway. For the down-regulated genes, the “transcription factor” and “cell-wall-associated protein” categories were over-represented. In a subsequent transcriptomic study of the effect of a long-term exposure (8 weeks) to low-speed wind in Populus nigra leaves, Fluch et al. found at least 98 up- and 94 down-regulated genes [17], including genes encoding cell-wall modification proteins, proteins with regulatory roles (e.g. kinases, calmodulin, etc.), Reactive Oxygen Species (ROS) producing or scavenging proteins, or constituents of microtubules. Unfortunately, these two transcriptomic studies concern a unique time-point after stimulation, giving a very static view of the molecular response to mechanical stimulus. In 2004, Kimbrough et al. found 1,691 mechanoresponsive genes on root apices that were transiently (5 s time-lapse) stimulated by moving them back and forth and harvested at different times (0, 2, 5, 15, 30, and 60 min post-stimulation) [18]. To our knowledge, this is the only in-depth kinetic (time-series) study ever made in plants on responses to mechanical stimuli. However, these data cannot be viably extrapolated to the responses of aboveground organs, as the soil and aerial mechanical environments, and the selective pressures they apply to the corresponding organs, are highly distinct.

Despite the tentative general flowchart of physiological and molecular responses to mechanoperception established by Telewski [19], we still have no general understanding of molecular mechanoresponse. The fact is that most molecular thigmomorphogenesis studies were realized on different plant species, submitted to different types of mechanical stimulations, with a huge majority of them using uncontrolled mechanical loadings, all of which makes cross-comparison difficult.

There is an even more striking lack of molecular information for recurring mechanical loads such as wind episodes [6, 20]. In 2010, Martin et al. assessed poplar responses to multiple successive stem bendings mimicking wind, and provided the first evidence of a process of desensitization to mechanical loads at the growth and molecular levels [21]. They found that four early mechanoresponsive genes —encoding two calmodulins, a C2H2 TF, i.e. PtaZFP2, and a XTH, respectively— responded with lower intensity to a second stem bending, applied 24 h after a first one. This phenomenon is now referred to as ‘accommodation’ and is thought to be crucial to avoid over-response to wind [6, 22]. In trees, transcriptomic analysis of transgenic poplars overexpressing PtaZFP2 constituted a first step toward the characterization of this phenomenon at molecular level. This study suggested that part of the accommodation process could be explained by a regulation at transcriptional level [6], thus requiring a more global analysis.

Deciphering the molecular mechanisms driving poplar accommodation to bending stimulation could be crucial to help better understand how trees acclimate to wind. In this study, our aim was to identify new molecular actors involved in mechanoresponse and the accommodation process, and unravel their kinetics of contribution. We thus conducted a time-series search of the transcriptome changes in poplar stem tissue subjected to one or two successive bendings.

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