The Jasmonate Signal Pathway
Year: 2002
Type: article
Abstract: Plant responses to many biotic and abiotic stresses are orchestrated locally and systemically by signaling molecules known as the jasmonates (JAs). JAs also regulate such diverse processes as pollen maturation and wound responses in Arabidopsis. Here we review recent advances in our understanding of how JA biosynthesis is regulated, the signaling functions of different JAs, and how the JA signal may be transduced via an E3 ubiquitin ligase. We also examine how outputs from the JA, salicylic acid (SA), and ethylene signal pathways are integrated in the regulation of stress response and plant development. We use the term jasmonate to include the biologically active intermediates in the pathway for jasmonic acid biosynthesis, as well as the biologically active derivatives of jasmonic acid. These compounds are widely distributed in plants and affect a variety of processes (Creelman and Mullet, 1997), including fruit ripening, production of viable pollen, root growth, tendril coiling, plant response to wounding and abiotic stress, and defenses against insects and pathogens. The function of JAs in defense was proposed by Farmer and Ryan (Farmer and Ryan, 1992), who provided evidence for a causal link between wounding (as caused by insect herbivores), the formation of JAs, and the induction of genes for proteinase inhibitors that deter insect feeding. In particular, they proposed that wounding caused release of linolenic acid (LA), the presumed precursor of JAs, from membrane lipids. New evidence indicates that JA signaling in plants is generally as proposed by Farmer and Ryan, but more complex than they envisaged. This new evidence indicates that intermediates in JA biosynthesis have distinctive biological activity, that an E3 ubiquitin ligase probably regulates most JA responses in Arabidopsis, and that the JA signaling pathway interacts with other defense signal pathways. A great deal of what we currently know about JA signaling comes from studies on Arabidopsis and tomato. However, there are several discrepancies between the proposed JA signaling pathways of these species, and it is not yet clear whether these reflect gaps in knowledge or reveal fundamental differences in mechanism. For example, Arabidopsis mutants defective in JA biosynthesis or perception are deficient in defense responses and are male sterile (Feys et al., 1994; McConn and Browse, 1996; Vijayan et al., 1998), whereas tomato mutants apparently defective in JA biosynthesis or perception have deficient defenses but are male fertile (Howe et al., 1996; Li et al., 2001). Similarly, the systemic induction of JA responses in tomato is through the well-characterised systemin signal pathway (Constabel et al., 1995; Ryan, 2000; Ryan et al., 2002), but in Arabidopsis there is no evidence for an equivalent pathway, even though systemic signaling can be demonstrated (Kubigsteltig et al., 1999). The JA signal pathway involves several signal transduction events: the perception of the primary wound or stress stimulus and transduction of the signal locally and systemically; the perception of this signal and induction of JA biosynthesis; the perception of JA and induction of responses; and finally, integration of JA signaling with outputs from the SA, ethylene, and other signaling pathways. JA signaling can be induced by a range of abiotic stresses, including osmotic stress (Kramell et al., 1995), wounding, drought, and exposure to “elicitors,” which include chitins, oligosaccharides, oligogalaturonides (Doares et al., 1995), and extracts from yeast (Parchmann et al., 1997; Leon et al., 2001). JA biosynthesis in Arabidopsis is also regulated by cues in the developing stamen, where jasmonic acid is required for pollen development. However, we do not yet know how these stresses or developmental cues are perceived. One approach has been to search for the earliest response to stress, which would therefore be a candidate for a component of the stress perception/signal transduction pathway. Gene Expression in JA Mutants Reveals Interaction between Defense Signal Transduction Pathways. Two μg of total RNA from each sample was analyzed on gel blots on nylon filters. Filters were probed with radiolabeled, polymerase chain reaction–generated DNA fragments from PR1, PDF1.2, Thi2.1, and 18S rRNA genes. (A) Seedlings were grown for 10 days on Murashige and Skoog (MS) agar, then transferred to fresh MS agar (−) or MS agar supplemented with 50 μM SA for 2 further days (+). (B) Seedlings were grown for 12 days on MS agar. (C) Model for positive (arrows) and negative (bars) interactions between the JA, ethylene, and SA signal pathways during response to pathogens, and pests or wounding. Gene symbols (in italics) are defined in the text; proteins are upper case, not italic. Similarly, in Arabidopsis, a mitogen-activated protein kinase named MPK4 is activated 2 to 5 min after wounding (Ichimura et al., 2000). The mpk4 mutant is dwarfed, has elevated levels of SA, and has constitutive expression of systemic acquired resistance (SAR) and the defense-related gene PR1 (Petersen et al., 2000). Dwarfing is reduced and PR1 is not expressed in mpk4 plants containing the nahG transgene encoding a salicylic acid hydroxylase, which reduces salicylic acid level. Significantly, these transgenic plants also fail to express the JA-regulated genes plant defensin 1.2 (PDF1.2) and thionin 2.1 (Thi2.1) after treatment with JA. Assuming that the plants did not contain a low level of SA sufficient to antagonise JA responses (Niki et al., 1998), the result indicates that the MPK4 cascade may simultaneously suppress SA biosynthesis and promote JA perception/response required for induction of PDF1.2 and Thi2.1. Therefore, MPK4 appears to regulate JA perception/response rather than JA biosynthesis, and would therefore act at a different point in the JA pathway than does WIPK (Figure 1). Assuming that the antibody that detects MPK4 identifies the same protein as that defined by mpk4, these results also indicate that the wound-induced activation of MPK4 is probably too rapid for the activating signal to be newly biosynthesised JA. It is therefore more likely that MPK4 is activated by the primary stress perception/transduction signal, or possibly by the rapid release of JA from endogenous stores (Stelmach et al., 2001). A critical question, therefore, is whether MPK4 is activated by a JA signal alone. The Arabidopsis mutant constitutive expression of vegetative storage protein (cev1) was isolated on the basis of constitutive expression of a luciferase reporter for the vegetative storage protein (VSP) promoter. It is dwarfed, has constitutive production of JA and ethylene, constitutive expression of PDF1.2, Thi2.1, and the chitinase CHI, and has enhanced defenses against fungal pathogens (Ellis and Turner, 2001, Figures 1A and 1B) and an insect pest. The cev1 mutant phenotype is partially suppressed in the coronatine insensitive 1 (coi1) and in the ethylene resistant 1 (etr1) mutant backgrounds, and the triple mutant, cev1;coi1;etr1 is wild type except for slightly shorter roots (Ellis et al., 2002). This indicates that cev1 induces biosynthesis of JA and ethylene, and its mutant phenotype is largely determined by responses to these signaling molecules. cev1, therefore, acts at an early step in the stress perception/transduction pathway, before JA and ethylene biosynthesis (Figure 1C). Map-based cloning of CEV1 identified it as the cellulose synthetase gene CESA3. Accordingly, cev1 had reduced cellulose content, and wild-type plants treated with cellulose synthetase inhibitors have enhanced JA responses and exhibit a near- phenocopy of the cev1 mutant. Apparently, alterations in the cell wall can initiate JA signaling (Ellis et al., 2002). When tomato leaves are damaged by herbivores or by simple mechanical wounding, JA signaling and defense gene expression are systemically activated within hours. The systemic signal requires prosystemin, a 200-amino-acid precursor that gives rise to the 18-amino-acid polypeptide systemin by proteolytic processing (Ryan and Pearce, 1998; Ryan et al., 2002). Systemin induces the production of H2O2 and the subsequent biosynthesis of jasmonic acid and induction of defense gene expression (Orozco-Cardenas et al., 2001). Model for the Biosynthesis of JAs. (A) Abbreviations for enzyme names are underlined; abbreviations for names of intermediates are in bold; pathway inputs and outputs are in italic. (B) Structure of sn1-O-(12-oxophytodienoyl)-sn2-O-(hexadecatrienoyl)-monogalactosyl diglyceride, a chloroplast membrane oxylipin containing esterified OPDA. The general pathway for JA biosynthesis presented in Figure 1Aindicates that JAs are biosynthesised from the fatty acid LA (18:3). Apparently they may also be biosynthesised from hexadecatrienoic acid (16:3) (Weber et al., 1997). The biosynthesis of 12-oxo-phytodienoic acid (OPDA) from LA occurs in the chloroplast, which contains an abundance of LA esterified in glycerolipids and phospholipids. By analogy with mammalian eicosanoid biosynthesis, a phospholipase A is expected to be responsible for release of LA from membrane lipids. This has recently been confirmed by characterization of the male-sterile Arabidopsis mutant defective anther dehiscence (dad1) (Ishiguro et al., 2001). dad1 was isolated from a transposon-tagged population on the basis of its male sterility, which could be rescued by LA or jasmonic acid application. The mutation defined an open reading frame, which encodes a lipase that hydrolyses phospholipids in an sn-1-specific manner, that is a phospholipase has an chloroplast and can in The was activated in of to the at which JA is required for of the of pollen and dehiscence of the These therefore, indicate that is required for JA biosynthesis in development. The of in wound-induced JA biosynthesis is expression of transgenic with or that the protein can function in other than The was induced 1 after wounding, but dad1 plants were for wound-induced JA Therefore, is required for regulated production of JA for and may be but is not required wound-induced JA. to have been and or more of these be in wound-induced JA biosynthesis (Ishiguro et al., 2001). A has also been in and JA formation in tomato et al., 1999). However, other evidence that a phospholipase is required for wound-induced JA formation in Arabidopsis and tomato. For example, wounding in and in wild-type whereas transgenic Arabidopsis plants in which is suppressed by a in acid and no in LA et al., 2001). of Arabidopsis by also reduced wound-induced JA and the gene vegetative storage These transgenic plants were male Assuming that the JA of of the transgenic plants was not the results indicate that is required for wound-induced biosynthesis of JA but not for JA biosynthesis in development. However, McConn and that the level of LA for male was than of wild-type Therefore, it is that the JA of was reduced in but not to a level required for male the of fatty to derivatives (Figure in JA biosynthesis include a that a for several including the in JA biosynthesis, 2001). for a that which is apparently in defenses et al., 2001). of an Arabidopsis also suppressed wound-induced JA formation et al., but did not affect male Apparently, therefore, this is required for wound-induced JA but is not required for pollen and development. of the other Arabidopsis genes is required for JA formation in pollen and development. gene in response to JA et al., 1997; et al., 1999). the of acid to an which is to be to by of the of the and are probably and We a mutation in that the function of this gene in defense signaling and in pollen development. However, there is a gene for in the Arabidopsis (Kubigsteltig et al., and we therefore that it functions in wound-induced JA formation and in regulated JA formation required for development. of occurs within 2 after are and occurs in and pollen (Kubigsteltig et al., 1999). The Arabidopsis is activated by a variety of including jasmonic wounding, and SA, that regulation of the expression of the protein a on JA signaling and However, of Arabidopsis in transgenic Arabidopsis and did not the level of jasmonic but the transgenic plants were they a level of jasmonic acid than did plants et al., 2000). In Arabidopsis and in therefore, it appears that wound-induced JA is regulated by the of to rather than by the of In these the release of LA from chloroplast may therefore the step in wound-induced JA By of in transgenic a and the endogenous JA, that in this the for may not JA However, the JA-regulated genes were not in these transgenic plants et al., 1995), that in to JA may be required for the of to acid. DNA gel a as a gene for in tomato. The protein is to the chloroplast by an chloroplast confirmed by et al., 2000). The is expressed at low levels in and with a in and are induced in tomato where it is expressed in the et al., 2000). It may be that the of in plants is at the of release of systemin in et al., where it JA Arabidopsis the of to acid Arabidopsis contains at other named and and the of these is wound induced and protein do not the of et al., 2000). The Arabidopsis mutants and acid different mutant of The plants are deficient in biosynthesis of jasmonic and they et al., 2000; and Browse, 2000). is probably in the and Browse, that its is from the chloroplast to the The mutants are also male and male is by of jasmonic that of the and pollen requires jasmonic acid. Significantly, has JA defense responses against insect pests et al., 2001). Therefore, of jasmonic acid and jasmonate induces of defense genes in Arabidopsis, is sufficient for these This the of which of these JAs the active signal in are induced by jasmonic acid et al., an for regulation of gene expression et al., 2000). Gene expression in plants treated with from that in plants treated with jasmonic acid. For example, jasmonic acid induces expression of for genes including which are not induced by OPDA. genes are regulated by and a of genes is by but not by jasmonic acid. of these genes is and they are therefore not required for defense against insects or pathogens and Browse, 2000). these results for studies et al., that is a signaling in its and has different from that of jasmonic acid. It may therefore be that more than of the in Arabidopsis leaves is as a sn1-O-(12-oxophytodienoyl)-sn2-O-(hexadecatrienoyl)-monogalactosyl (Figure in chloroplast The can be from chloroplast by and this could for the rapid in and jasmonic acid leaves are (Stelmach et al., 2001). The endogenous of this therefore has the to and other JAs for JA of to jasmonic acid. This probably occurs in the where for are known to be However, there is evidence for the of this of the pathway for jasmonic acid which has in recent is a component of plant and is probably by a further of of jasmonic acid. release from plants can be induced by for during insect of the of the responses to which functions as an and as an for insects that on or was also active in the production of compounds that affect plant defense by the of insects et al., 2000). The of jasmonic acid to is by an acid from Arabidopsis. in vegetative and in developing and locally and systemically are or treated with Arabidopsis jasmonic acid content, the genes for and PDF1.2 and enhanced resistance to by the expression of is sufficient to and can function as an endogenous signal in plant can and to and systemic by including is its production by could and and could also function as an signal and in defense et al., 2001). that of genes to JA are JA biosynthesis the of a positive for JA biosynthesis et al., 2001). This the of that JAs of and et al., 1997; and 1998; et al., 2000; et al., et al., (Figure Significantly, wounding and other stresses that JA responses also these activation of these genes occurs at the of JA JAs therefore to be locally in response to stress cues and developmental and the of this pathway a for of the It is not known whether of JAs between and in Arabidopsis, or whether and systemic signaling involves an signaling such as the systemin from tomato (Ryan and Pearce, It is in our JA biosynthesis and signaling (as defined is to the cell the primary The JA signal is probably transduced by the activation of that these no have been Arabidopsis defense responses are induced by and by jasmonic whereas and are induced by jasmonic acid but not by (Ishiguro et al., et al., 2001). This that in Arabidopsis, at pathways JA for of or jasmonic acid for defense and for of jasmonic but not for development. molecules have been defined by mutants that are insensitive to other signal molecules and 1997). However, mutant for to coronatine of and to et al., et al., and a for mutants that do not express the transgene in the of JA (Ellis and Turner, have identified of the genes and jasmonate resistant This that there is in the of JA or that and function in JA even though is an protein et al., and has to the gene from and protein to plant proteins and 2001). the an open reading as that was isolated as a of constitutive 1 responsible for a in The mutant was isolated in a for Arabidopsis mutants insensitive to by the which is to jasmonic acid (Feys et al., and to et al., The mutants are also to by are male fail to express JA-regulated genes for vegetative storage protein (VSP) et al., 1995), and the plant defensin (PDF1.2) and are to insect and to pathogens et al., 1997; et al., of have also been isolated in for resistance to by jasmonic to the (Ellis and Turner, 2002), and for to et al., 2001). The gene encodes a protein containing an and a et al., proteins in the in from yeast to and function as that proteins as for proteins with and proteins to an E3 ubiquitin ligase known as the complex et al., of how proteins may regulate defenses is by the proteins and which regulate in is an in stress, and developmental to and it in the of induces the of to which is then by the ubiquitin A component is the ubiquitin ligase which contains and the and This complex a protein that other proteins for by the to is then in the and is activated et al., 1998; et al., 1999). of with in Arabidopsis that a E3 JA (A) A protein of or total protein extracts from of transgenic Arabidopsis as or proteins or with antibody with against Arabidopsis Arabidopsis transgenic and (B) A for how may regulate defense responses and and pollen in Arabidopsis, through the E3 ubiquitin of and of these By analogy to for the it is that the of by is required for but apparently not for and pollen development. Therefore, at pathways are regulated by the perception of JAs, that regulates and pollen and requires and that regulates defenses and requires and We therefore that regulates for jasmonic and pollen may to jasmonic acid and and for defenses may in to and we a in Figure for this of JA JA induces biosynthesis of many of in different is a from results in enhanced expression of several genes for biosynthesis and in of and 2000). to and gene expression via a and in the of including the gene of is induced by but is not by also does not of that the JA signal may which then JA responses by with the and 2001). The has to the ethylene response which were isolated as proteins from and Arabidopsis encoding different proteins to activity, and are regulated by ethylene, wounding, or drought, via or pathways. induces of the to to gene expression or et al., 2000). It likely that JA responses in Arabidopsis are regulated by and we that genes that are by JA be candidate and for The JA pathway regulates response to abiotic stress, defenses against insect herbivores and fungal pathogens and defenses against pathogens such as the (Ellis and Turner, it also regulates developmental of plants with a that induces to the of to subsequent SA is for the expression of resistance and including and production of that there is negative between responses to pathogens and responses to wounding. For example, the expression of reduces to but systemic resistance to the insect of but reduces resistance to the insect an between resistance to pathogens and resistance to insect herbivores et al., 1999). This has been in other In Arabidopsis, the enhanced mutation enhanced to by the and reduces of SA after The mutation also responses to of that SA with JA signaling et al., 2000). JA regulates wound responses and defense against insect and is in However, of gene expression in wild-type and Arabidopsis plants that were by or to stress a of genes regulated by wounding and by stress, and an different of genes regulated by wounding and by et al., 2000). The results that insect herbivores may the activation of a of defense-related genes. The JA signal pathway also interacts with the ethylene signal pathway in the expression of defense responses and in development. that of are in signaling pathways for ethylene, and salicylic the between JA signaling and other signaling pathways et al., 2001). The cev1 mutant has been to between the JA, ethylene, and SA signal pathways. of cev1 with SA expression of PDF1.2 and expression of PR1, though than in wild-type plants (Figure which are deficient in JA have but PR1 that a signal PR1 in The mutant PDF1.2 Thi2.1, that expression of these genes requires the JA perception/response pathway regulated by (Figure The mutant ethylene resistant 1 (etr1) was to the mutant in which PDF1.2 expression was a for an ethylene signal for PDF1.2 (Ellis and Turner, 2001). is expressed in this mutant, that ethylene signaling the of (Figure These results are in a (Figure that the positive and negative between the JA, SA, and ethylene signal pathways. In to the evidence that JA SA of Arabidopsis mutants with constitutive SA responses a pathway in which JA and ethylene signaling are required for SA The Arabidopsis mutant of PR1 is insensitive to SA, to express and has reduced A for of a mutation named of SA which has constitutive expression of genes and resistance to plants elevated levels of SA but they have constitutive expression of PDF1.2 which is induced by JA and ethylene et al., 1999). The JA of these plants is not and may therefore JA biosynthesis or the JA perception/response pathway. When SA in plants is by the nahG of the are also including the expression of of these plants with which the of SA but is not by salicylic hydroxylase, induces SA responses and induces PDF1.2 expression also et al., 1999). The results indicate that is a negative of SA biosynthesis and also induction of This a induction of PDF1.2 by SA is not in wild-type has to Arabidopsis mutant with constitutive expression of named constitutive 5 The phenotype is suppressed in the mutant, but is partially by the mutant. the phenotype of the whereas This indicates that has an resistance However, the phenotype is also suppressed by the mutation and by the mutation resistance in requires of the JA and the ethylene signal pathways et al., 2000). The and mutants not enhanced resistance but also that also the and ethylene signaling pathways. therefore, these mutant are partially by the fungal which induces cell that requires the JA, ethylene, and SA signaling as by the of cell in and mutants and in plants containing the transgene et al., 2000). The of and on the of Arabidopsis Seedlings Interaction between These Signal in induces a in wild-type but not in the mutant, The mutant constitutive triple response has an even in the of with the in and but not in the mutant cev1 has constitutive JA and signaling Figure and to and responses in cev1 are suppressed in the no Arabidopsis mutants with constitutive JA which yet be in the JA signal pathway, have been isolated In Arabidopsis a of the gene for resistance to the to the of the were and were The named constitutive expression of defined with different including enhanced JA and constitutive activation of JA response genes constitutive activation of SA and JA and et al., 2001). et the mutant constitutive expression 1 which constitutive expression of The mutant phenotype was not suppressed in the mutant that it may a step of In this case, PDF1.2 expression also be but this critical is not yet et al., 2001). of these mutants is likely to reveal of JA The JA signal pathway regulates of and diverse responses to A is to that genes that the primary stress In the primary stress signal is systemically via signal but in Arabidopsis, we do not yet how the systemic wound and stress signal is and of this be a for The of JA is well and may more on the regulation of evidence that JA is not but is at the at which it has indicates that characterization of the that regulate of JA are fundamental to our understanding of the of JA We do not know how JAs are and of the JA therefore a which has and for the JA, SA and ethylene signaling pathways are defined by the signaling molecules they they and in a variety of A is therefore to which of the JA signaling pathway with outputs from the SA and the ethylene signal and understanding of the JA signaling pathway, as it an and the for and of
Source: The Plant Cell
DOI: 10.1105/tpc.000679
Authors: John G. Turner, Christine Ellis, Alessandra Devoto
Institution: University of East Anglia
Language: English
Subfield: Insect Science
Domain: Life Sciences
SDG: Zero hunger
Open Access status: green
OpenAlex ID: W2163581172