Systemin triggers an increase of cytoplasmic calcium in tomato mesophyll cells: Ca²⁺ mobilization from intra‐ and extracellular compartments

Abstract

Key-words: Lycopersicon esculentum; aequorin; calcium; channels; systemin; tomato; wound response. INTRODUCTION Synthesis and accumulation of proteinase inhibitors (PIs)is one of the responses induced in plants by wounding. This response occurs both in the wounded leaf and in distal unwounded leaves within a few hours of the initial damages (Pearce et al. 1991;O'Donnell 1995). This implies the systemic propagation of a signal from the injury site to distal tissues. Putative chemical messengers for this systemic wound signal include systemin. Systemin is an 18 amino acid polypeptide which was originally isolated from tomato (Lycopersicon esculentum) leaves and which, like wounding itself, elicits the systemic synthesis of PIs in tomato plants (Pearce et al. 1991). Systemin was named after its property of being systemically mobile in the phloem (Pearce et al. 1991). Following its application to wound sites on leaves, the polypeptide moves throughout the leaf and is found within 1-2 h in the phloem exudate (Pearce et al. 1991;Narvaez-Vasquez et al. 1995). Systemin, the first plant polypeptide hormone, behaves in a strikingly similar manner to polypeptide hormones in animal and yeast cells . However, until now the initial stages in stimulus-response coupling at the plasma membrane have not been clear. The signal transduction pathway is thought to involve the binding of systemin to a membrane receptor (Farmer & Ryan 1992) which has not yet been clearly identified. Schaller & Ryan (1994) found a 50 kDa plasma membrane protein which binds systemin. However, this proteolytic protein does not appear to be a receptor, but has the properties of a furinlike proteinase able to cleave systemin to smaller polypeptides (Schaller & Ryan 1994).The binding of systemin to a plasma membrane receptor would lead to the activation of a lipase and then to a subsequent intracellular release of linolenic acid and synthesis of methyl jasmonate (Farmer & Ryan 1990. These two components of the octadecanoid signal transduction pathway are known to have a powerful ability to induce Pin II gene expression (Farmer & Ryan 1990. Systemin and jasmonic acid (JA) have also now been shown to trigger other cell responses such as synthesis of woundinducible polyphenol oxidase (Constabel, Bergey & Ryan 1995) and aspartic protease [Schaller & Ryan 1996; see also ]. Moyen & Johannes (1996) recently showed that some of the early events triggered by systemin within a few minutes of application on Lycopersicon esculentum mesophyll tissue are a depolarization of the plasma membrane and a transient H + efflux followed by a longer lasting H + influx. Moreover, systemin also triggers an increase of extracellular K + par- 1101alleled by an alkalization in the extracellular medium of suspension-cultured cells of Lycopersicon peruvianum (Felix & Boller 1995). Systemin-induced ion fluxes are affected in the presence of fusicoccin, which has been shown to antagonize the PI synthesis induced by systemin (O'Donnell 1995) and by oligogalacturonides (OG) (Doherty & Bowle...

The Tomato Suppressor of prosystemin-mediated responses2 Gene Encodes a Fatty Acid Desaturase Required for the Biosynthesis of Jasmonic Acid and the Production of a Systemic Wound Signal for Defense Gene Expression

“…The systemin/jasmonate signaling pathway is initiated upon the binding of systemin to a 160-kD plasma membrane-bound receptor (SR160) that was identified recently as a member of the Leu-rich repeat receptor-like kinase family of proteins (Meindl et al, 1998;Ryan, 1999, 2002). Binding of systemin to the cell surface is associated with several rapid signaling events, including increased cytosolic Ca 2 ϩ levels, membrane depolarization, inhibition of a plasma membrane proton ATPase, and activation of a mitogen-activated protein kinase activity (Felix and Boller, 1995;Moyen and Johannes, 1996;Stratmann and Ryan, 1997;Moyen et al, 1998;Schaller and Oecking, 1999).…”

Positional Specificity of a Phospholipase A Activity Induced by Wounding, Systemin, and Oligosaccharide Elicitors in Tomato Leaves

“…Both wounding and systemin also have been shown to cause a rapid and transient increase in the concentration of intracellular Ca 2ϩ (Knight et al, 1991;Moyen et al, 1998). Accordingly, specific inhibitors of protein kinases and Ca 2ϩ channel blockers can inhibit both the wound-and the systemin-induced MAPK and PLA activation and the accumulation of defense proteins (Seo et al, 1995(Seo et al, , 1999Romeis et al, 1999;Schaller and Oecking, 1999; J. Narváez-Vásquez and C.A.…”

“…In this pathway, linolenic acid (LA), released from membrane phospholipids by a phospholipase, is converted to 12-oxophytodienoic acid (PDA) and jasmonic acid (JA), which are powerful inducers of defense gene transcription (Farmer and Ryan, 1992;Blechert et al, 1995). The activation of the phospholipase may be preceded or mediated by phosphorylation events (Farmer et al, 1991;Seo et al, 1995;Stratmann and Ryan, 1997) and by transient increases in cytosolic Ca 2 ϩ (Knight et al, 1991;Moyen et al, 1998) and ion fluxes (Thain et al, 1990;Felix et al, 1993;Felix and Boller, 1995;Moyen and Johannes, 1996;Schaller and Oecking, 1999).…”

Signaling in Plant Resistance Responses: Divergence and Cross-Talk of Defense Pathways

“…Changes in plasma membrane permeability are among the earliest cellular responses to treatment with systemin and oligogalacturonide elicitors of the wound response. The influx of calcium and protons and the efflux of potassium and chloride ions lead to an increase in the cytoplasmic free calcium concentration, intracellular acidification, depolarization of the plasma membrane, and alkalinization of the apoplast (Felix and Boller, 1995;Thain et al, 1995;Moyen and Johannes, 1996;Moyen et al, 1998;Schaller, 1998). These early events are essentially indistinguishable from those triggered in plant cells after pathogen recognition or elicitation (Conrath et al, 1991;Ebel and Mithöfer, 1998;Scheel, 1998;Katz et al, 2002).…”