Rhythmic stem extension growth and leaf movements as markers of plant behavior: How endogenous and environmental signals modulate the root-shoot continuum

Abstract

With the short-day plant Chenopodium rubrum and the long-day plantChenopodium murale, growth and behavior have been studied in response to photo-and thermoperiod. With time-lapse photography, rhythmic integration of the plant as a whole could be monitored. Upon photoperiodic flower initiation, rhythmic stem extension rate (SER) and leaf movements (LM) change their phase relationship in a specific way. Flower induction correlates with a threshold value for the ratio between integral growth during the dark-time span and integral growth during the light-time span. This precise output displayed in the growth pattern of the plant is therefore an accurate reflection of all available environmental inputs. Analysis of flower induction in Chenopodium spp. showed that 2 h after the end of the critical dark period, the patterns of cytoplasmic pH and Ca2+ change at the shoot apical meristem (SAM), possibly indicating the arrival of the flower-inducing signal. Changes in LEAFY (a florigenic transcription factor) and aquaporin expression can also be recorded during this phase. The perception of a flower-inducing dark period leads to a change in electrochemical, hydraulic signaling between the leaves and SAM, thereby determining polarity in the whole plant and paving the way for “florigen”. Leaves from flowering plants can be grafted on non-induced plants (short-or long-day species) to induce flowering in the recipient plant. Flowering could even be induced using a different donor and recipient species (inter-species signaling). A rhythmic integration over the whole plant, as seen for SER and LM, most likely involves modulation of turgor pressure via stretch-activated ion channels and concomitant changes in membrane potential, making the plant a hydro-electrochemical signal transducer. Regulation of hydraulics and electrochemistry, two coupled physicochemical processes, was an achievement of early evolution as well as metabolic circadian regulation of transcriptional translational control loops (TTCL). Circadian rhythms (CRs) in energy metabolism are gating inputs and outputs to the TTCL, resulting in a CR of protein synthesis and turnover. Evolution of latitudinal ecotypes with different CR period lengths will depend on specific proteins, as is evident from early crossing experiments. The control of the ionic composition of the cell is crucial for the survival and requires energy to maintain a resting potential of the plasma membrane. This, in turn, enables the generation of action potentials and, hence, a fast systemic communication between plant organs, in particular the root and shoot meristems (RAM and SAM).