Fluctuations shape plants through proprioception

Abstract

Plant proprioception Plants are battered inside and out by mechanical forces such as gravity, wind, or a passerby plucking a flower. Moulia et al. review what is known about how plants sense and interpret mechanical forces to guide growth and development. Minute fluctuations in mechanical cues form the basis of a developmental proprioception system that ensures steady growth despite variable environments. Science, this issue p. eabc6868 BACKGROUND Plants constantly experience fluctuating internal and external mechanical cues, ranging from nanoscale deformation of wall components, cell growth variability, nutating stems, and fluttering leaves to stem flexion under tree weight and wind drag. The plants’ reactions seem ambivalent. Indeed, fluctuations may appear as noise that may confuse any sensing pathway, jeopardize the reproducibility of plant morphogenesis and development, or even result in mechanical hazards (e.g., stem windbreaks or growth cracks resulting from mechanical conflicts between differentially growing cells). At the same time, plants seem to enhance and even generate some fluctuations to remodel their structure (from the subcellular to the tissue scale), prime their morphogenesis, and control its outcome. ADVANCES In this Review, we explore the instructive role of fluctuations. At the organ scale, stems and leaves are one-dimensional (1D) or 2D thin structures embedded in a 3D space, and they display a continuous active degree of freedom along their growing tissues. They display large rotations during growth (e.g., tropism, primordia emergence, hook formation, etc.), bringing geometric nonlinearities and even mechanical elastic instabilities (buckling) or mechanical hazards caused by large bending and possible resonance under the drag of turbulent wind flow. At the cellular level, cells are also endowed with continuous growth that leads to many possibilities of mechanical conflicts with neighboring cells caused by differential growth and possible buckling out-of-plane instabilities. Finally, at the intracellular level, the cytoskeleton is made of thin microtubules and actin filaments, which undergo an autonomous dynamic of assembly-disassembly, leading to larger self-organized behaviors and instabilities. Thus, plant morphogenesis is the outcome of highly nonlinear, dissipative processes at all scales. At first sight, this may make the effect of fluctuation even worse. However, developing plants use such fluctuations to monitor and channel their own shape and growth, through a form of proprioception. Proprioception (from the Latin words proprius, meaning own, and capere, meaning to take or to feel) is a sensory mechanism that involves the perception of cell- and tissue-shape changes linked to changes in body configuration and involves the sense of tension and deformation. We present evidence of proprioception in plants, and we show that this perception can feedback on growth control, allowing it to dampen the noisy effect of external and internal fluctuations. This is illustrated at the organ or global scale in stem and leaf tropisms and at the cellular or local scale in the control of cell growth heterogeneities in meristems and sepals. Fluctuations in mechanical cues may also be actively enhanced, producing oscillating behavior in tissues. For example, proprioception through leaf nastic movements and active leaf fluttering may promote organ flattening. Because certain shapes are more amenable to fluctuations, proprioception may also help plant shapes to reach self-organized criticality to support such adaptability. OUTLOOK Fluctuations in plant shape should thus not be disregarded as noise with respect to the display of a genetic program. Instead, fluctuations promote proprioception at all scales. It follows that plants, like all living organisms, should be considered to be like active and self-sensing materials and structures: They perceive the fluctuations in their own shape originating from external or internal sources to monitor and channel their growth. Moreover, proprioception can be tuned flexibly to either dampen or enhance fluctuations, channeling shape reproducibility or, instead, priming symmetry breaking. The latter is made easier for highly symmetric shapes, and hence dynamically critical shapes, such as the ones that are reached through proprioceptive dampening. At such critical points, fluctuations occur at all scales. Coarser-grained fluctuations even span the whole system and trigger global changes and thus further morphogenetic steps. The balance between dampening and priming proprioception and the interplay between internal and external fluctuations is a target for further inquiries. Fluctuation-based plant morphogenesis. Exogenous and endogenous fluctuations in curvature and growth are perceived at organ and cellular scales. Such proprioception can be ambivalent, either dampening or enhancing fluctuations, channeling shape reproducibility, or instead priming symmetry breaking. Proprioception may channel the formation of organs with shapes at critical points, which are also more amenable to fluctuations, thereby enhancing proprioception in a positive feedback loop. PHOTO CREDIT: JULIEN DERR AND RENAUD BASTIEN, LABORATOIRE MATIÈRES ET SYSTÈMES COMPLEXES Plants constantly experience fluctuating internal and external mechanical cues, ranging from nanoscale deformation of wall components, cell growth variability, nutating stems, and fluttering leaves to stem flexion under tree weight and wind drag. Developing plants use such fluctuations to monitor and channel their own shape and growth through a form of proprioception. Fluctuations in mechanical cues may also be actively enhanced, producing oscillating behaviors in tissues. For example, proprioception through leaf nastic movements may promote organ flattening. We propose that fluctuation-enhanced proprioception allows plant organs to sense their own shapes and behave like active materials with adaptable outputs to face variable environments, whether internal or external. Because certain shapes are more amenable to fluctuations, proprioception may also help plant shapes to reach self-organized criticality to support such adaptability.