Electrifying rhythms in plant cells

Abstract

Physiological oscillations (or rhythms) pervade all spatiotemporal scales of biological organization, either because they perform critical functions or simply because they can arise spontaneously and may be difficult to prevent. Regardless of the case, they reflect regulatory relationships between control points of a given system and offer insights as read-outs of the concerted regulation of a myriad of biological processes. Here we review recent advances in understanding ultradian oscillations (period < 24h) in plant cells, with a special focus on single-cell oscillations. Ion channels are at the center stage due to their involvement in electrical/excitabile phenomena associated with oscillations and cell-cell communication. We highlight the importance of quantitative approaches to measure oscillations in appropriate physiological conditions, which are essential strategies to deal with the complexity of biological rhythms. Future development of optogenetics techniques in plants will further boost research on the role of membrane potential in oscillations and waves across multiple cell types.

Figure 1

Plants generate oscillations in virtually all spatiotemporal scales of biological organization. Archetype of a flowering plant and a moss (drawn on the left) associated with their respective organ/cell/pathway/molecule (zoom on the center) where oscillations of virtually all time scales are generated (traces on the right). The approximate period is shown by the black scale bar, determining the color of the trace (see color code below). From fastest to slowest, it features: femtosecond oscillations in electronic coherence, or “quantum beats,” in the light-harvesting complex II (LHCII) [63] (detrended with loess); root hair [Ca²⁺]_cyt oscillations with period c.a. 30 s [28]; pollen tube growth rate oscillations with period c.a. 50 s in Arabidopsis [15]; Apically-growing Physcomitrium patens protonema tip [Ca²⁺]_cyt oscillations with main periodicity in the 2 min range [19]; microbial symbiosis (Nod/Myc) elicited nuclear Ca²⁺ oscillations in root hairs, a nodulation response with periodicity in the minute range [46]; guard cell [Ca²⁺]_cyt oscillations in response to a CaCl₂ treatment c.a. 3 min [64]; root circumnutation with periodic helical movements of tip position with a period c.a. 1.5 h [51]; lateral root formation by the so-called “root clock” occur with rhythms generated with periodicity c.a. 6 h, showing here by the activity of an auxin reporter (DR5) [48]; the circadian clock is present in most cell types, represented here by gene sets (boxes) peaking at different times of the day (color gradient) in an interlocked transcriptional-translational feedback loops (regulatory interactions). Boxes (from left to right) represent morning (CCA1 and LHY), afternoon (PRRs/RVEs) and evening (LUX, NOX and ELFs) complexes, with a trace of the free-running rhythm of a circadian reporter (CCR2) from [65]; flowering related genes show yearly oscillations, here exemplified with the expression of beta-amylase 5 in a natural environment [66]. This by no means a comprehensive list, lacking examples like metabolic oscillations, other types of circadian oscillators, population dynamics and various other ultradian and infradian rhythms. Illustrated by Joana C. Carvalho.

Figure 2

Varying complexity of oscillatory signatures found in pollen tubes. a. Limit cycle attractor. Top: Synchronized oscillations of tip-pH and growth rate shown in a phase-space plot + time. A limit cycle attractor is evident over time, revealing synchronized oscillations of cytosolic tip pH and growth rate over the course of the cell growth (interval shown c.a. 18 min). Bottom: quantitative spatial profile of cytosolic pH in Arabidopsis pollen tube (after heavy vectorization). Data from [14]. b. Regime transitions. Top: Time series of pollen tube growth rate and cytosolic Ca²⁺ at the tip. Bottom: phase-space plot showing regime “a” —steady growth; regime ”b”—highly synchronized oscillations between growth rate and [Ca²⁺]_cyt; regime “c” —growth arrest and [Ca²⁺]_cyt spiking. Data from [15]. c. Complex oscillations. Top: Time series of an Arabidopsis pollen tube growth rate, cytosolic pH at the tip and shank. Bottom: main periodic components over time found in the synchronized oscillations between tip pH and growth rate, estimated with a cross-wavelet transform. The heatmap indicates the power attributed to each period at every time point, with significant components (p < 0.01) circled in white. The power peaks were marked with a black dot (wavelet ridges), evidencing the drift in the main component as a line (frequency drift), as well as the existence of 2 or 3 parallel components (multiple coexisting frequencies). The pale region indicates the cone of influence, a region where estimates are not reliable. The mean power of each component over time is shown with a curve in the right side of the plot. The peak at 1.35 min does not reflect the almost 2 fold drift in period (from 1 to 2 min oscillations), posing challenges for experimental design and analysis. Data from [14].