The shaping of plant axes and crowns through tropisms and elasticity: an example of morphogenetic plasticity beyond the shoot apical meristem

Abstract

Summary Shoot morphogenetic plasticity is crucial to the adaptation of plants to their fluctuating environments. Major insights into shoot morphogenesis have been compiled studying meristems, especially the shoot apical meristem (SAM), through a methodological effort in multiscale systems biology and biophysics. However, morphogenesis at the SAM is robust to environmental changes. Plasticity emerges later on during post‐SAM development. The purpose of this review is to show that multiscale systems biology and biophysics is insightful for the shaping of the whole plant as well. More specifically, we review the shaping of axes and crowns through tropisms and elasticity, combining the recent advances in morphogenetic control using physical cues and by genes. We focus mostly on land angiosperms, but with growth habits ranging from small herbs to big trees. We show that generic (universal) morphogenetic processes have been identified, revealing feedforward and feedback effects of global shape on the local morphogenetic process. In parallel, major advances have been made in the analysis of the major genes involved in shaping axes and crowns, revealing conserved genic networks among angiosperms. Then, we show that these two approaches are now starting to converge, revealing exciting perspectives.

A growing soft robot with climbing plant–inspired adaptive behaviors for navigation in unstructured environments

“…During the apical processing of external signals, cells near the apex develop unevenly and differentially elongate, resulting in environmentally mediated directional growth (tropisms) ( 32 ). Photoreceptors and gravity-sensing cells are distributed throughout the apical shoot and are involved in phototropic ( 33 , 34 ) and gravitropic responses ( 35 , 36 ), respectively. To locate, reach, and interact with obstacles and potential supports, climbing plants produce an initial self-supporting stem whose stiffness and density decrease adaptively after location and attachment to an external support ( 37 , 38 ).…”

Plants sum and subtract stimuli over different timescales

“…Plants, decentralized systems, negotiate fluctuating environments by adapting their morphology advantageously through growth-driven processes called tropisms, whereby organs such as shoots or roots redirect their growth according to directional stimuli, such as gravity or light. The last decade has seen an increasing body of evidence that plants quantify and integrate sensory information about their environment at the tissue level (1)(2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16), detecting and climbing spatial signal gradients despite environmental and 1 B t = 0 h t = 8 h A acclimation stimulus 1 stimulus 2 delay…”

“…Plants, decentralized systems, negotiate fluctuating environments by adapting their morphology advantageously through growth-driven processes called tropisms, whereby organs such as shoots or roots redirect their growth according to directional stimuli, such as gravity or light. The last decade has seen an increasing body of evidence that plants quantify and integrate sensory information about their environment at the tissue level (1)(2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16), detecting and climbing spatial signal gradients despite environmental and internally-driven noise (17). While it is generally accepted that tropic responses are a product of complex computational processes (1,14,(18)(19)(20)(21)(22), attempts to characterize these processes mathematicallythat is, to obtain an understanding of the rules according to which plants quantify and process the sensory information they acquire over time-are limited.…”

Gravity sensing and responses in the coordination of the shoot gravitropic setpoint angle

“…In the roots, water and nutrients also affect growth angles (Kobayashi et al ., 2007 ; Huang et al ., 2018 ; Yamazaki et al ., 2020 ). Environmental cues, including gravity and light, are integrated to optimise plant architecture (Moulia et al ., 2022 ).…”