Approximate entropy: a promising tool to understand the hidden electrical activity of fruit

Abstract

Fruits, like other parts of the plant, appear to have a rich electrical activity that may contain information. Here, we present data showing differences in the electrome complexity of tomato fruits through ripening and discuss possible physiological processes involved. The complexity of the signals, measured through approximate entropy, varied along the fruit ripening process. When analyzing the fruits individually, a decrease in entropy values was observed when they entered the breaker stage, followed by a tendency to increase again when they entered the light red stage. Consequently, the data obtained showed a decrease in signal complexity in the breaker stage, probably due to some physiological process that ends up predominating to the detriment of others. This result may be linked to processes involved in ripening, such as climacteric. Electrophysiological studies in the reproductive stage of the plant are still scarce, and research in this direction is of paramount importance to understand whether the electrical signals observed can transmit information from reproductive structures to other modules of plants. This work opens the possibility of studying the relationship between the electrical activity and fruit ripening through the analysis of approximate entropy. More studies are necessary to understand whether there is a correlation or a cause-response relationship in the phenomena involved. There is a myriad of possibilities for the applicability of this knowledge to different areas, from understanding the cognitive processes of plants to achieving more accurate and sustainable agriculture.

Keywords: Electrome; fruit herbivory; fruit ripening; machine learning; plant electrophysiology.

Figure 1.

Scheme representing fruit ripening and its different ethylene biosynthesis systems (A, adapted from Liu et al., 2015) and the entropy measures (B). Each line in B represents a repetition of fruit analyzed up to the or stage. CO₂: carbon dioxide; C₂H₄: ethylene; IMG: immature green stage; MG: mature green stage; B: breaker stage; OR: orange red stage; LR: light red stage; A: red stage.

Figure 2.

Summary of physiological and biochemical processes during fruit ripening [33–36]. The average and standard deviation of the days between stages were obtained in our experiment. C₂H₄: Ethylene; ABA: Abscisic acid.

Figure 3.

Scheme representing possible ways of propagating electrical signals from fruit to plant and between cells within the fruit. A: Representation of an action potential generated and transported along phloem cells (adapted from [14]. The curved black arrow on the petiole represents the propagation direction of the fruit-plant electrical signal. The brown structures represent the sieve tube elements, and the orange ones represent the companion cells. The small colored shapes represent ion channels and proton pumps. Thin black arrows on the membrane represent the influx and efflux of ions. Thick black arrows represent the direction of signal passage through phloem cells. B: Representation of cell-to-cell electrical signal transmission within the fruit (adapted from [5]. Components in gray represent ion channels, and those in red represent proton pumps. The small black and blue dots represent ions. The blue arrow represents the influx and efflux of ions and protons. The black dashed arrow demonstrates the direction of propagation of the signal across the membrane, and the solid black arrow through the plasmodesmata. V: vacuole; P: plasmodesmata; PM: plasma membrane; CW: cell wall; H+: proton.