Oscillatory signatures underlie growth regimes in Arabidopsis pollen tubes: computational methods to estimate tip location, periodicity, and synchronization in growing cells

Damineli, Daniel Santa Cruz; Portes, Maria Teresa; Feijó, José A.

doi:10.1093/jxb/erx032

“…Nonetheless, the idea of criticality that occurs in a growing plant cell appears to be in line with the detailed explanations that can be found in the literature, which combine growth rate oscillations with synchronised ion fluxes (see Fig. 2D in Damineli et al 2017), where the extracellular H + flux and growth rate curve almost overlap. Summarising, self-organised criticality is a mechanism through which open systems achieve a self-organised statistically stationary state in which they undergo a non-equilibrium phase transition.…”

Section: Introductionsupporting

confidence: 83%

Extracellular ionic fluxes suggest the basis for cellular life at the 1/f ridge of extended criticality

Pietruszka

¹

,

Olszewska

²

2020

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The criticality hypothesis states that a system may be poised in a critical state at the boundary between different types of dynamics. Previous studies have suggested that criticality has been evolutionarily selected, and examples have been found in cortical cell cultures and in the human nervous system. However, no one has yet reported a single-or multi-cell ensemble that was investigated ex vivo and found to be in the critical state. Here, the precise 1/f noise was found for pollen tube cells of optimum growth and for the physiological ("healthy") state of blood cells. We show that the multi-scale processes that arise from the so-called critical phenomena can be a fundamental property of a living cell. Our results reveal that cell life is conducted at the border between order and disorder, and that the dynamics themselves drive a system towards a critical state. Moreover, a temperature-driven re-entrant state transition, manifest in the form of a Lorentz resonance, was found in the fluctuation amplitude of the extracellular ionic fluxes for the ensemble of elongating pollen tubes of Nicotiana tabacum L. or Hyacintus orientalis L. Since this system is fine-tuned for rapid expansion to reach the ovule at a critical temperature which results in fertilisation, the core nature of criticality (long-range coherence) offers an explanation for its potential in cell growth. We suggest that the autonomous organisation of expansive growth is accomplished by self-organised criticality, which is an orchestrated instability that occurs in an evolving cell. "Symbols are very adept at hiding the truth." (Dan Brown)

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“…However, the convolution of acidic pH growth and temperature growth is less shifted away from zero (lag) and is even more pronounced; see also recent outcomes in Pietruszka and Haduch-Sendecka (2016) as well as Olszewska et al (2017Olszewska et al ( , 2018 for cell wall pH (proton efflux rate) and growth rate, which are directly co-regulated in growing shoot tissue, thus strongly supporting the empirical foundations of EWS. Even more supportive for the EWS-model is the result obtained by Damineli et al (2017), where the extracellular H + flux and growth rate curves practically overlap (see Fig. 2d therein); the periods (47.7 ± 3.2 s and 48.7 ± 4.3 s, respectively) for both processes are almost identical within experimental error.…”

Section: Sensing Structural Transitionssupporting

confidence: 66%

“…structurally and temporally organised apical growth, especially since H + usually oscillates with the period similar to growth rate-see Fig. 2d in Damineli et al (2017).…”

Section: Pollen Tube Growth and Oscillationsmentioning

confidence: 97%

Chemical Potential-Induced Wall State Transitions in Plant Cell Growth

Pietruszka

¹

2019

J Plant Growth Regul

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The pH/T duality of acidic pH and temperature (T) action for the growth of grass shoots was examined in order to derive the phenomenological equation of wall properties for living plants. By considering non-meristematic growth as a dynamic series of state transitions (STs) in the extending primary wall, the critical exponents were identified, which exhibit a singular behaviour at a critical temperature, critical pH and critical chemical potential (μ) in the form of four power laws: $$f_{\pi } \left( \tau \right) \propto \left| \tau \right|^{\beta - 1}$$ f π τ ∝ τ β - 1 , $$f_{\tau } (\pi ) \propto \left| \pi \right|^{1 - \alpha }$$ f τ ( π ) ∝ π 1 - α , $$g_{\mu } (\tau ) \propto \left| \tau \right|^{ - 2 - \alpha + 2\beta }$$ g μ ( τ ) ∝ τ - 2 - α + 2 β and $$g_{\tau } (\mu ) \propto \left| \mu \right|^{2 - \alpha }$$ g τ ( μ ) ∝ μ 2 - α . The indices α and β are constants, while π and τ represent a reduced pH and reduced temperature, respectively. The convexity relation α + β ≥ 2 for practical pH-based analysis and β ≡ 2 “mean-field” value in microscopic (μ) representation were derived. In this scenario, the magnitude that is decisive is the chemical potential of the H+ ions, which force subsequent STs and growth. Furthermore, observation that the growth rate is generally proportional to the product of the Euler beta functions of T and pH, allowed to determine the hidden content of the Lockhart constant Ф. It turned out that the pH-dependent time evolution equation explains either the monotonic growth or periodic extension that is usually observed—like the one detected in pollen tubes—in a unified account.

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“…Controlled activation of MS channels from inside a plant cell might be possible through the application of focused ultrasound, as was recently demonstrated for animal TPKs expressed in oocytes [54]. Integration of localized extracellular ion flux measurements with genetically encoded ion or voltage biosensors may allow the study of MS channel function in some cellular contexts, such as pollen tubes [55]. To date, the genetically encoded sensors for transmembrane voltage used extensively in animal systems to monitor ion channel activity in vivo [56] do not yet function well in plants [57].…”

Section: Beyond the Horizon: Innovations In Ms Channel Studiesmentioning

confidence: 99%

Plant mechanosensitive ion channels: an ocean of possibilities

Basu

¹

,

Haswell

²

2017

Current Opinion in Plant Biology

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Mechanosensitive ion channels, transmembrane proteins that directly couple mechanical stimuli to ion flux, serve to sense and respond to changes in membrane tension in all branches of life. In plants, mechanosensitive channels have been implicated in the perception of important mechanical stimuli such as osmotic pressure, touch, gravity, and pathogenic invasion. Indeed, three established families of plant mechanosensitive ion channels play roles in cell and organelle osmoregulation and root mechanosensing—and it is likely that many other channels and functions await discovery. Inspired by recent discoveries in bacterial and animal systems, we are beginning to establish the conserved and the unique ways in which mechanosensitive channels function in plants.

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Oscillatory signatures underlie growth regimes in Arabidopsis pollen tubes: computational methods to estimate tip location, periodicity, and synchronization in growing cells

Abstract: A data analysis pipeline that integrates diverse data sources, detects tip growth in kymographs, and analyses oscillations and synchronization reveales oscillatory signatures underlying distinct growth regimes in Arabidopsis pollen tubes.

Cited by 54 publications

References 52 publications

Extracellular ionic fluxes suggest the basis for cellular life at the 1/f ridge of extended criticality

Extracellular ionic fluxes suggest the basis for cellular life at the 1/f ridge of extended criticality

Chemical Potential-Induced Wall State Transitions in Plant Cell Growth

Plant mechanosensitive ion channels: an ocean of possibilities

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