Remote-controlled stop of phloem mass flow by biphasic occlusion in Cucurbita maxima

Abstract

The relationships between damage-induced electropotential waves (EPWs), sieve tube occlusion, and stop of mass flow were investigated in intact Cucurbita maxima plants. After burning leaf tips, EPWs propagating along the phloem of the main vein were recorded by extra- and intracellular microelectrodes. The respective EPW profiles (a steep hyperpolarization/depolarization peak followed by a prolonged hyperpolarization/depolarization) probably reflect merged action and variation potentials. A few minutes after passage of the first EPW peak, sieve tubes gradually became occluded by callose, with maximum synthesis occurring ∼10 min after burning. Early stop of mass flow, well before completion of callose deposition, pointed to an occlusion mechanism preceding callose deposition. This obstruction of mass flow was inferred from the halt of carboxyfluorescein movement in sieve tubes and intensified secretion of aqueous saliva by feeding aphids. The early occlusion is probably due to proteins, as indicated by a dramatic drop in soluble sieve element proteins and a simultaneous coagulation of sieve element proteins shortly after the burning stimulus. Mass flow resumed 30–40 min after burning, as demonstrated by carboxyfluorescein movement and aphid activities. Stop of mass flow by Ca2+-dependent occlusion mechanisms is attributed to Ca2+ influx during EPW passage; the reversibility of the occlusion is explained by removal of Ca2+ ions.

ROS, Calcium, and Electric Signals: Key Mediators of Rapid Systemic Signaling in Plants

“…Similar effects of VPs on photosynthesis were found in other species such as Populus trichocarpa and soybean (Glycine max; Gallé et al, 2013). In addition, studies of plant defense against herbivory or pathogen attack indicated that electrical signaling plays an important role in the initiation of systemic reactions such as the activation of various genes (for review, see Davies and Stankovic, 2006;Howe and Jander, 2008), including JA biosynthesis (Mousavi et al, 2013), and sieve tube occlusion (Furch et al, 2010). Recently it was demonstrated that bundle-sheath cells, Ca 2+ -permeable channels, chloroplast ROS, photosynthetic electron transport, and NPQ play an important role in longdistance electrical signaling in plants ( Figs.…”

The Origin and Composition of Cucurbit “Phloem” Exudate

“…The 14 C content of the exudate drops within seconds, suggesting that the phloem involved in long-distance transport of these compounds seals more quickly than the xylem. Initial sealing may be due to the surge of P-protein and ruptured cell contents onto the sieve plates to form slime plugs (Evert et al, 1973;Furch et al, 2010). However, plugging is not immediate.…”

“…However, the sieve tubes do progressively seal. This process is initiated by the formation of slime plugs and callose (Furch et al, 2010). Finally, oxidized P-proteins create an impenetrable barrier over the cut surface, and exudation stops.…”

“…Whereas the circulatory system of animals is easily accessed by venipuncture (the blood flows through extracellular space and is under modest pressure), sieve elements in the phloem are living cells under high turgor (Gould et al, 2004;Turgeon, 2010). Cutting sieve elements results in rapid sealing by several mechanisms: cell contents surge against the sieve plates, callose blocks the pores, phloem proteins coagulate, and, in legumes, forisomes disperse (Furch et al, 2010). This makes it difficult to obtain significant quantities of phloem sap from most plants.…”

Sieve element occlusion(SEO) genes encode structural phloem proteins involved in wound sealing of the phloem

“…Toward the end of sieve element maturation, selective autolysis results in the degradation of the tonoplast, nucleus, and other organelles, whereupon the P-protein bodies disperse into smaller aggregates that move to the periphery of the cell, remaining in this position in the mature, functional sieve tubes (1). There has been much speculation about the function of P-proteins (15), but substantial evidence points toward having a role in rapid phloem wound sealing (2,16). Following injury, conventional P-proteins detach from their parietal position and form plugs at sieve plates to block further translocation (1).…”