Year: 2001
Type: article
Abstract: Polypeptide hormones (extracellular signals) have been recognized for many years as important regulatory molecules in animals and yeast. Beginning with the discovery of insulin in 1922 (Banting and Best, 1922), polypeptides have been established as signals that regulate a broad spectrum of physiological processes. Until 1991, however, plants were not known to utilize polypeptides as regulatory molecules; instead they were thought to use only small organic phytohormones, including auxins, cytokinins, gibberellins, ethylene, abscisic acid (Kende and Zeevaart, 1997), and more recently, brassinolides (Mandava, 1988). The discoveries of polypeptide signals for plant defense, growth, and development over the past decade have heralded the beginning of a new and growing field of polypeptide signaling in plants. Here, we review the currently known polypeptides from plant origins that act as signaling molecules. Where known, the receptor proteins with which the polypeptides interact are discussed, as well as their functional roles in polypeptide/receptor–mediated signaling cascades. This article is not meant to be a comprehensive review of the underlying biology of systems in which polypeptide signaling is found, and our discussion of the relevant research areas emphasizes the biochemical and structural features of polypeptide signals and their receptors. The systemin polypeptide was discovered during a search for the systemic wound signal that regulates the expression of defensive genes in tomato leaves in response to insect attacks or other severe mechanical wounding (Pearce et al., 1991). Several reviews concerning tomato systemin have been written in recent years (Schaller and Ryan, 1995; Ryan, 1998, 2000; Ryan and Pearce, 1998; Schaller, 1999), and the structural and functional data relevant to polypeptide signaling, along with more recent developments, are summarized below. Tomato and potato plants respond to insect attacks by releasing a signal or signals from the wound site that cause the synthesis and accumulation of proteinase inhibitors in both wounded leaves and distal, unwounded leaves (Green and Ryan, 1972). A search for the proteinase inhibitor-inducing factor over the next 20 years led to the isolation of a polypeptide signaling molecule (Pearce et al., 1991; Ryan, 1998). The polypeptide is composed of 18 amino acids with the sequence +AVQSKPPSKRDPPKMQTD−, and because of its association with systemic signaling, it is called systemin. Systemin induces the synthesis of proteinase inhibitors in leaves of young excised tomato plants when supplied at low nanomolar levels through their cut petioles (Pearce et al., 1991). The potency is in the same range as that found for the activity of various polypeptide hormones in animals. A synthetic 14C-labeled systemin was mobile when applied to wound sites, and its movement in the phloem correlates with the movement of the systemic signal that is produced in response to wounding, that is, ∼3 cm/hr (Nelson et al., 1983; Pearce et al., 1991; Narvaez-Vasquez et al., 1995). Prosystemin is found in the vascular bundles of tomato petioles (Jacinto et al., 1997). The mechanism for the movement of systemin in the phloem is not understood, but for systemin to have long-range signaling effects, an amplification of the signal most likely occurs. The presence of prosystemin in phloem parenchyma cells (J. Narvaez-Vasquez and C.A. Ryan, unpublished data) suggests that an interplay between the phloem and its surrounding cells may contribute to the signaling mechanism. Systemin contains several charged amino acids as well as two proline doublets, at positions 6 and 7 and at 12 and 13. Only weak structural features are present in aqueous solutions of systemin, analyzed using nuclear magnetic resonance spectroscopy (Russell et al., 1992), but circular dichroism spectra reveals a poly(l-proline) II, 31 helix secondary structure in the central region of the polypeptide (Toumadje and Johnson, 1995). The polyproline helix is known to provide a kink in proteins (Ferris et al., 2001) and may provide a structure in systemin that is important to its recognition by the systemin receptor (discussed below). Sequential alanine substitution at each of the 18 amino acids of systemin has variable effects on activity. A Thr to Ala substitution at position 17 eliminates activity (Pearce et al., 1993a) and creates a powerful antagonist of native systemin. Removal of the C-terminal Asp of systemin abolishes activity, and this analog is also an antagonist of systemin. Substitution of Pro12 and Pro13 residues with Ala severely reduces the activities of the analogs compared with that of native systemin. The Ala substitution experiments, together with the deletion experiments, indicated that the 14 amino acids at the N terminus are likely involved in receptor binding, whereas the MQTD sequence at the C terminus has a direct role in signaling (Pearce et al., 1993a). This conclusion is supported by experiments in which binding of a systemin analog consisting of only the N-terminal 14 amino acids competes with systemin for binding to Lycopersicon peruvianum cell membranes, while the peptide MQTD does not (Meindl et al., 1998). A cDNA encoding a 200–amino acid systemin precursor called prosystemin contains one copy of the systemin sequence near the C terminus (McGurl et al., 1992), indicating that systemin, like many animal and yeast polypeptide hormones, is proteolytically processed from a larger protein. Prosystemin does not exhibit a signal sequence at its N terminus, nor is it glycosylated (Delano-Frier et al., 1999). The lack of a signal sequence and the absence of any post-translational modification suggest that prosystemin is not synthesized through the secretory pathway but probably on free ribosomes in the cytosol. The transgenic antisense plants with an antisense prosystemin gene, driven by the constitutive 35S promoter (McGurl et al., 1992), exhibit a severely reduced systemic induction of proteinase inhibitors in response to wounding that results in a reduced defense against Manduca sexta larvae attacks (Orozco-Cardenas et al., 1993). On the other hand, plants transformed with a prosystemin cDNA in its sense orientation, driven by the 35S promoter, synthesize defense proteins constitutively, as if they are in a permanently wounded state (McGurl et al., 1994). This phenotype is apparently caused by the expression of the gene in cells throughout the plant in which it is not normally expressed. Grafting wild-type tomato plants to root stocks overexpressing the prosystemin gene causes the wild-type scions to accumulate defense proteins as if they are wounded, suggesting that systemin is from the root to the scions or that it is systemic signal involved in signaling the amplification of systemin or in signaling defense gene plants wild-type not exhibit this response the are wounded (McGurl et al., 1994). experiments provide that systemin is a signal for the systemic wound response to in the Systemin with a with a of (Meindl et al., 1998; and Ryan, 1999). The binding of an analog is found in both and on the of cells of peruvianum (Meindl et al., 1998; and Ryan, 1999). The binding is and and both systemin and the analog as an antagonist of systemin, are powerful of A by is present in the of peruvianum cells and Ryan, 1999), which the same and The receptor has been to from peruvianum cell and as a receptor and Ryan, synthesized with an expression (Delano-Frier et al., and with a cell expression et al., is as as systemin when supplied to young excised tomato plants through their cut the prosystemin is processed or it is processed supplied to the plants has not been A prosystemin the systemin sequence is when supplied to excised tomato plants et al., 1999), indicating that the systemin sequence be present for signaling to of the tomato prosystemin gene are found in and et al., 1998). The exhibit amino acid sequence with tomato prosystemin that range from to the systemin are compared with the tomato systemin they exhibit only two to amino acid with found the C-terminal amino are of the of the is an of defense genes in leaves of young tomato plants when supplied to the plants through their cut systemin was the A of the tomato prosystemin gene not be found in and tomato systemin not defense gene expression in leaves of plants et al., 1998; Pearce et al., however, exhibit a wound response that the synthesis of a of inhibitors that are to tomato (Pearce et al., A to the systemic signal from leaves in the isolation of only of polypeptide signals that structural A was (Pearce et al., on the that systemin caused the of the of tomato cells and 1995). of peruvianum cells with a from from causes the of the cell to when signaling polypeptides are This the isolation of two acid polypeptides from leaves that powerful activities (Pearce et al., are called systemin and systemin in with the of as polypeptides that are from plants at wound and that act or to signaling for defense and Pearce, and are not to each other or to tomato systemin. residues and are glycosylated (Pearce et al., of the polypeptides induces the synthesis of inhibitors when supplied to young excised leaves through their cut and both a when supplied to to the response caused by tomato systemin when it is supplied to tomato plants and Ryan, 1997). A polypeptide is found in and II, and is to for the presence of an at the C of and Tomato of and Tomato Pearce et a cDNA from a cDNA by which a acid precursor of both in the N-terminal region and in the C-terminal This that plant polypeptide signals from a a found in animals and yeast et al., 1991; et al., of and and lack Ala have been at each position in the The analogs were by the in in the at of the to of peruvianum from of and and lack Ala have been at each position in the The analogs were by the in in the at of the to of peruvianum from Tomato systemin is when supplied to indicating that the receptor or other recognition are in and are both in proteinase synthesis in tomato plants and in of the of tomato cells Pearce and C.A. Ryan, unpublished This that present in tomato cells may the to the same signaling pathway that is by tomato systemin. glycosylated polypeptides of 18 and amino acids in were from tomato leaves that have activity when to tomato or cells Pearce and C.A. Ryan, unpublished the glycosylated are systemic signals has not been nor have their or been the and of the various found throughout the provide a for in other plant for polypeptide wound signals in young using the (Pearce et al., a acid polypeptide was and (Pearce et al., The polypeptide a and more of the of cells the and it is called the (Pearce et al., induces a activity in the The activity of is also more the activities by the between and the various systemin polypeptides in the and is larger the and does not the synthesis of inhibitors in leaves when supplied to young suggesting a signaling role other polypeptides with a amino acid with were from tomato leaves and N-terminal of amino acids of each of the polypeptides were and a search of the of in plant from (Pearce et al., a cDNA with a tomato a cDNA for was that a precursor of amino acids in The contains a acid signal peptide at its N terminus and a acid sequence at its C The of the polypeptide from the precursor the of the by indicating that is proteolytically processed from a larger genes that are present in (Pearce et al., The N-terminal amino acid of each precursor are are the C-terminal encoding the polypeptide (Pearce et al., A structural of precursor proteins is the presence of two residues from the residues are of the recognition site for polypeptide hormones from their The region of the site is in residues that are from as in may be of a recognition site for the Tomato was and were established for that the two that are present in the native The synthetic is as as the native in the whereas a reduced and is with an a binding and a binding (J. Pearce, and C.A. Ryan, The of proteins provide structural of the and of the signaling that of the in by the this the the genes found in the The between the in each the and the from which each is are of the in by the this the the genes found in the The between the in each the and the from which each is are the role of in plants was when of tomato and were and to levels of tomato (Pearce et al., is but the response is and the when the are to and which was in the is in root The cause of the of root by is not known, but of root from that is cell Pearce, and C.A. Ryan, unpublished The tomato in experiments a to the by that was in a root genes are present in and the many are found in and cells of may have a more role in plants. The expression of or of the of the various genes provide their and small polypeptide signals were by and regulate plant cell in The of cell of cells been known for years to be on the cell and low the activity is but if the are with from cell the cells of the known plant hormones for and the of the factor two were from the of cell and of the two that they were both small polypeptides with and and were and The structure of is and of is are found in in animals et al., but to the are the only of post-translational residues in plants. with are present in the of et al., 1997), et al., and et al., and were synthesized and each is as as the native and one or both of the two C-terminal amino acids are compared with native The N-terminal analogs and analogs are suggesting that the N-terminal is the Substitution of with and of Thr with results in an in activity. is thought to be a of the C-terminal likely by of the is processed from the C terminus of a The precursor is synthesized through the secretory pathway the signal sequence is and the are to of the is processed from the C terminus of a The precursor is synthesized through the secretory pathway the signal sequence is and the are to A region of the gene is to the expression of the gene in transformed cells with sense and antisense genes driven by the promoter results in sense with cell two of wild-type and antisense that more the This that the sense is and that the gene expression is reduced by the antisense The expression of the gene is throughout the but in in root and it is likely to have a physiological has been in and cell et al., 2001) and polypeptides have been in cell of and et al., 1997), et al., and et al., polypeptides have not been in expression by the gene promoter in cells is on the presence of both and in the The two hormones together the of activity. The presence of in cells is the and the of the cell et al., The in functional role of in plants has not been but the polypeptide the of cell of et al., and causes in et al., et al., The polypeptide also induces root and in et al., and induces the of on et al., 1998). caused by has an for acid but from in the absence of binding to membranes, with a of and 1999). The binding is and and only analogs with the binding cell are on the that a of been binding is also in from cells of and and 1999). acid to the of proteins of and and that to be of a receptor of the with to by and of causes a of for each of the and which suggests that they are The data that has a role to cell and but its mechanism of its signaling its to other hormones, and its role in to be is an signaling polypeptide of amino acids in that is involved in the of cell in the of The of position and in plants is and established in 1997), a between the of cells and the cells be as the plant The cells while the surrounding cells more and et al., 1995; and present in are to the of cells in each in or in which many more cells are found in both and are found in of wild-type plants 1997). exhibit the same as plants with et al., that both and are of a signaling was using two by a and which from the of the et al., 1999). The gene contains and two small that a of amino acids an acid N-terminal The processed polypeptide is composed of amino is that any of of the signal but a acid in the C terminus of polypeptides et al., and 2001) and in the C terminus of polypeptides and which with a or a The that residues are for to a of small polypeptides that may have a role in signaling are found in cells of the and in the central of et al., 1999). The gene is in the most cells near the The polypeptide synthesized from is to be from cell in the central region of the with a et al., in underlying the of the with a of the cell et al., 1999). The amino acid sequence of suggests that it is a consisting of a a of and is thought to be with a acid a to a et al., 1999). The association is thought to be through et al., 1999). and are in the central of the and are of a larger that a et al., in the same as and a called et al., 1999). which has and is to a both and was with that two proteins interact in et al., 1998). is present in two one of and one of et al., 1999). The two are present in and the the of in their structural is present in both while is only found in the against proteins were found only in the the and are of the signaling The is thought to be a composed of and and the composed of the and and proteins et al., 1999). has been to to various et al., and regulates signaling et al., et al., by binding to plants overexpressing of the of the to with and in plants in which is that expression to cell the copy of the of plants does not cause in or of signaling is a of the expression of which cell and of cells in a in the and to the genes et al., The and between genes and the for cell both and et al., has not been found to root for the and with the Polypeptide A for the receptor and its with the polypeptide which regulates the of cell and in the and of binding of to the receptor the to the of and signaling pathway from et al., for the and with the Polypeptide A for the receptor and its with the polypeptide which regulates the of cell and in the and of binding of to the receptor the to the of and signaling pathway from et al., The signaling pathway has an signaling for are in by a polypeptide signal and its receptor may be a for many of and and of other in and in plants. A of signaling polypeptides of to amino acids in called proteins or et al., et al., a central role in in the the the and between and in is by genes at the when the in with the of the a that the et al., The response to of the with a role in et al., and is composed of a of small proteins of to amino including their signal et al., 2000; polypeptide contains The amino acid of the signal are but the processed polypeptide while at the exhibit weak at other The the and not the polypeptides is in to most proteins in which the amino acids in signal are are the The of the suggests that the polypeptides may that are not from and The of the polypeptides are with their roles as signals that when recognized by the The polypeptides are from in the and to the et al., and 2000; et al., cell of the cells at the a to et al., et al., 2000; interact with an receptor on the cell of The has a functional at its C terminus and and with a region in the and an at its region et al., 1991). to be with with present in a and both and sequence that are involved in and is and may interact with to the of levels that be functional et al., by to et al., 1999). is not to cause and et al., 2000; et al., and in one of the gene is et al., 1999). gene have been from yeast that interact with the of and they to have roles in the signaling by the This is composed of an with in yeast et al., and two proteins that have been in the of by et al., recent that may not in the of by et al., 2001) but may of in the absence of et al., with its not interact with but to cells of the and to from the experiments using and indicated that and may a receptor on the et al., and the of binding between the two signaling was et al., et al., direct for the that regulates a does not have in its the genes and et al., the has been to a of genes for polypeptides with to and proteins et al., of this are in recent review et al., 2000; and 2000; and in a article in this of The et al., in is a for the of signaling in and in with the of the the polypeptide with the receptor to a signaling that to the The results in the of the receptor and the of which may to the of to the of to the in is a for the of signaling in and in with the of the the polypeptide with the receptor to a signaling that to the The results in the of the receptor and the of which may to the of to the of to the from the from and a acid polypeptide and a acid polypeptide are from amino from the from and a acid polypeptide and a acid polypeptide are from amino The search for the role of polypeptides has more with the that a of amino acids the acid of the gene et al., The acid polypeptide but not the acid polypeptide was in using however, to a that was as a of The that the two polypeptides may a regulatory role in from the by activity or by the to The of have not been for a regulatory The data the that of as well as the presence of the are important for and that they likely an important role in if the are only in the cells in which they are they not be signals that the of hormones but roles as of a new of of the signaling that regulate cell in the Several other polypeptides have been to be signaling molecules in plants with various roles to growth, and A small gene, called is in and root and is for and signaling during root The gene a that has an encoding a acid but its role in signaling is is of that and are with of root and Several have for of animal polypeptide hormones in plants. A polypeptide called et al., was that caused the of a that of an insulin has been for the polypeptide or the and the of this polypeptide in the insulin is an role in plants is with the polypeptide the a a was from using with an et al., The and of a from A polypeptide has been from that has the structure as insulin et al., 1999), but activity in plants has been with the nor has an insulin gene been from plants. A of polypeptides from called in animals as of and and a of to polypeptides be from helix with peptide 1999). The caused effects in including in levels and in plant have been and nor have the or genes that polypeptides been Polypeptide signaling has been known for more years to be of in a spectrum of physiological in and research over the past decade has their in plants. Polypeptide signaling may have its origins in that plants and a for the of polypeptide signaling in polypeptide hormones two hormones et al., and and 1993). The polypeptide hormones, and are synthesized as in the secretory pathway of cells and are processed and in in response to physiological The hormones are to or they are recognized by to signaling are insulin and Polypeptide hormones are from that are to amino acids in et al., of polypeptides are produced as a copy from a as but several of the as while other are processed to hormones physiological as The of structural is for the of receptor binding that of polypeptide of polypeptide hormones from larger in is by of the of are and at the C terminus of the This of is found in both animals and and have been in known have been (Schaller and Ryan, and of amino acids that are for are found in et al., in of the precursor proteins (Pearce et al., in of precursor proteins et al., and in 20 of precursor proteins and the amino acids may be of and the in other polypeptide signals to the of polypeptide signals or to to be A for polypeptide synthesis and is found with factor and 1993). factor amino acids from a acid factor amino acids from a acid and factor amino acids from a acid The of most of this of polypeptides are between to amino acids in are are synthesized through the secretory the however, are not processed in but are in The with the of the the polypeptide to the are that the which be recognized by their receptors. Several plant polypeptide hormones in this review are synthesized as apparently through the secretory and the and to be to interact with their to be in that it is synthesized in the to the and to the receptors. The of tomato prosystemin and of not have signal and are apparently synthesized in the on free a not found with animal polypeptide systemin be to the wounding, it interact with its receptor on cell does not to the of polypeptide hormones, as an the for polypeptide hormones to be and the systemin or receptor and currently as the receptor and the provide systems for structural to and to the plant to only a small of plant polypeptide signals and their have been polypeptide signaling in plants has a new for research in this are to a of the of polypeptide signaling in plants and of the of and the that their signaling of plant and plant defense, and plant to the This research for new plant biology as well as for the of and from the of and and the is
Source: The Plant Cell
DOI: 10.1105/tpc.010484
Authors: Clarence A. Ryan, Gregory Pearce, Justin Scheer, Daniel S. Moura
Institution: Washington State University
Language: English
Subfield: Plant Science
Domain: Life Sciences
Open Access status: bronze
OpenAlex ID: W2347055016