The Biochemical Response of Electrical Signaling in the Reproductive System of Hibiscus Plants

Abstract

Stimulation of the stigma of Hibiscus flowers by pollen, wounding (heat), or cold shock (4°C) evokes electrical potential changes in the style, which propagate toward the ovary with a speed of 1.3 to 3.5 cm s-'. Potential changes were measured intracellularly by microelectrodes inserted i n the style. l h e resting potential ranged from -90 to -112 mV (n = 20) in cells of the vascular tissue and from -1 84 to -220 mV (n = 22) in cells of the pollen-transmitting tissue.The amplitude of the potential changes was between 40 and 150 mV, depending on the kind of stimulus. Self-as well as crosspollination hyperpolarized the resting potential after 50 to 100 s, followed by a series of 10 to 15 action potentials. I n contrast, cooling of the stigma caused a single action potential with a different shape and duration, whereas wounding generated a strong depolarization of the membrane potential with an irregular form and a lower transmission rate. To determine the physiological function of the different signals measured i n the style, the gas exchange and metabolite concentrations were measured in the ovary before and 1 O min after stimulation of the stigma. Self-and cross-pollination caused a transient increase of the ovarian respiration rate by 12%, which was measured 3 to 5 min after the stigma was stimulated. Simultaneously, the levels of ATP, ADP, and starch increased significantly. In contrast, both cold shock and wounding of the stigma caused a spontaneous decrease of the CO, content in the measuring chamber, as well as reduced metabolite concentrations in the ovary. Since the transport of labeled auxin from the top to the base of the style lasts at least 45 min, the influence of a chemical substance transmitted within 10 min is unlikely. lhus, our results strongly support the view that different, stimulus-dependent electrical signals cause specific responses of the ovarian metabolism.Since the last century, electrical signaling in plants has been examined, and comprehensive reviews have been published by Pickard (1973) and Sibaoka (1966). An integral part of the generation of action potentials is based on changes in ion flux, including the efflux of chloride and potassium (Oda, 1976;Fromm and Spanswick, 1993) and the influx of calcium (Williamson and Ashley, 1982; Kikuyama and Tazawa, 1983;Beilby, 1984;Beilby and MacRobbie, 1984). In recent years, evidence was given that action potentials may regulate a wide variety of physiological responses in plants, including elongation growth (Shiina and Tazawa, 1986), respiration (Dziubinska et al., 1989), water uptake (Davies et al., 1991), phloem unloading (Fromm, 1991), activation of proteinase inhibitor genes (Wildon et al., 1992), and gas exchange (Fromm and Eschrich, 1993).With regard to pollination, two different kinds of bioelectric potential changes have been observed in the style of flowers. First, Sinyukhin and Britikov (1967) measured an action potential in the style of Lilium martagon and Incarvillea grandiflora a few minutes after placing pollen on the stigma ...

Reception and learning of electric fields in bees

“…Electric fields induce responses in insects [7,8,28]. A biologically relevant property of body surface charge in pollinating insects was traced to the opposite polarity of their body surface charge to that of flowers, potentially facilitating pollen collection and possibly leaving a cue after electrical neutralization of the flowers' electric field [9][10][11][12]. It has also be noted that charged pollen powder sprayed over flowers leads to fertilization of these flowers [29], and biopesticides may be more effective if electrically charged [30].…”

“…Naturally occurring surface charge is thought to play a role in pollination [9][10][11] reviewed by [12], since flowers were found to be usually negatively charged, whereas the arriving insects appear to carry a positive surface charge. The electric charge that accumulates on the cuticle of flying insects discharges only partially upon landing because of the high contact resistance between legs and ground.…”

Characteristics of Electrical Signals in Poplar and Responses in Photosynthesis

“…Vian et al (1999) induced rapid and systemic accumulation of chloroplast mRNA-binding protein transcripts, in tomato (Lycopersicon esculentum), after flame stimulus. In addition to translation and transcription, evidence exists for a role of electrical signals in many processes of plant life, including respiration (Dziubinska et al, 1989;Filek and Koscielniak, 1997), water uptake (Davies et al, 1991), phloem unloading (Fromm, 1991), and phloem translocation (Fromm and Bauer, 1994) as well as fertilization (Fromm et al, 1995). Recently, this account was extended by a study on the inhibition of photosynthesis in Mimosa pudica (Koziolek et al, 2004) upon flame wounding, which demonstrated that electrical signals triggered transient changes in chlorophyll fluorescence (PSII electron quantum yield) and leaf gas exchange.…”

Ways of signal transmission and physiological role of electrical potentials in plants

“…Electrical potentials generated after depositing an improper pollen on the stigma differed from those induced by a proper pollen. Similar preparation of the ovary for acceptance of the male cell was demonstrated in Hibiscus (Fromm et al 1995). Stimulation of the plant stigma with a compatible pollen induced series of APs, which are propagated along the style to the ovary.…”