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Oxylipins in moss development and defense.

Ponce de León I, Hamberg M, Castresana C - Front Plant Sci (2015)

Bottom Line: Biochemical characterization of several oxylipin-producing enzymes and oxylipin profiling in P. patens reveal the presence of a wider range of oxylipins compared to flowering plants, including C18 as well as C20-derived oxylipins.Surprisingly, one of the most active oxylipins in plants, JA, is not synthesized in this moss.In this review, we present an overview of oxylipins produced in mosses and discuss the current knowledge related to the involvement of oxylipin-producing enzymes and their products in moss development and defense.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Biología Molecular, Instituto de Investigaciones Biológicas Clemente Estable , Montevideo, Uruguay.

ABSTRACT
Oxylipins are oxygenated fatty acids that participate in plant development and defense against pathogen infection, insects, and wounding. Initial oxygenation of substrate fatty acids is mainly catalyzed by lipoxygenases (LOXs) and α-dioxygenases but can also take place non-enzymatically by autoxidation or singlet oxygen-dependent reactions. The resulting hydroperoxides are further metabolized by secondary enzymes to produce a large variety of compounds, including the hormone jasmonic acid (JA) and short-chain green leaf volatiles. In flowering plants, which lack arachidonic acid, oxylipins are produced mainly from oxidation of polyunsaturated C18 fatty acids, notably linolenic and linoleic acids. Algae and mosses in addition possess polyunsaturated C20 fatty acids including arachidonic and eicosapentaenoic acids, which can also be oxidized by LOXs and transformed into bioactive compounds. Mosses are phylogenetically placed between unicellular green algae and flowering plants, allowing evolutionary studies of the different oxylipin pathways. During the last years the moss Physcomitrella patens has become an attractive model plant for understanding oxylipin biosynthesis and diversity. In addition to the advantageous evolutionary position, functional studies of the different oxylipin-forming enzymes can be performed in this moss by targeted gene disruption or single point mutations by means of homologous recombination. Biochemical characterization of several oxylipin-producing enzymes and oxylipin profiling in P. patens reveal the presence of a wider range of oxylipins compared to flowering plants, including C18 as well as C20-derived oxylipins. Surprisingly, one of the most active oxylipins in plants, JA, is not synthesized in this moss. In this review, we present an overview of oxylipins produced in mosses and discuss the current knowledge related to the involvement of oxylipin-producing enzymes and their products in moss development and defense.

No MeSH data available.


Related in: MedlinePlus

Oxylipin biosynthesis pathways in the moss P. patens. (A) Lipoxygenase-catalyzed oxygenation of arachidonic acid into 12(S)-HPETE and further conversions of this hydroperoxide by allene oxide synthase (PpAOS1-2), allene oxide cyclase (PpAOC2), hydroperoxide lyase (PpHPL), and 12-lipoxygenase (PpLOX1). (B) Oxygenation of linolenic acid into 2(R)-HPOT by Ppα-DOX and by lipoxygenase into 13(S)-HPOT. Breakdown of 2(R)-HPOT into 2(R)-HOT and heptadecatrienal and the further conversions of 13(S)-HPOT by allene oxide synthase (PpAOS1), allene oxide cyclase (PpAOC1-3), and hydroperoxide lyase (PpHPL) are also illustrated.
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Figure 1: Oxylipin biosynthesis pathways in the moss P. patens. (A) Lipoxygenase-catalyzed oxygenation of arachidonic acid into 12(S)-HPETE and further conversions of this hydroperoxide by allene oxide synthase (PpAOS1-2), allene oxide cyclase (PpAOC2), hydroperoxide lyase (PpHPL), and 12-lipoxygenase (PpLOX1). (B) Oxygenation of linolenic acid into 2(R)-HPOT by Ppα-DOX and by lipoxygenase into 13(S)-HPOT. Breakdown of 2(R)-HPOT into 2(R)-HOT and heptadecatrienal and the further conversions of 13(S)-HPOT by allene oxide synthase (PpAOS1), allene oxide cyclase (PpAOC1-3), and hydroperoxide lyase (PpHPL) are also illustrated.

Mentions: Physcomitrella patens is the first moss species with an available sequenced genome (Rensing et al., 2008), and several of the oxylipin-forming enzymes have been identified and biochemically characterized (Figure 1). P. patens has eight genes encoding lipoxygenase of which seven are functionally active in vitro (Anterola et al., 2009). Five are 13-LOXs (PpLOX3–PpLOX7) which use 18:3 as a substrate, while the other two are 12-LOXs (PpLOX1 and PpLOX2) and prefer 20:4 and 20:5 (Anterola et al., 2009). PpLOX3, 4, 6, and 7 can also use 18:2 as a substrate, although the activity is much higher against 18:3 (Anterola et al., 2009). PpLOX1 is an unusual bifunctional LOX that exhibit hydroperoxidase and a fatty acid chain-cleaving lyase activity (Senger et al., 2005; Anterola et al., 2009). In addition, both 12-LOXs accept C18-fatty acids as substrates yielding a broader range of oxylipins (Senger et al., 2005; Wichard et al., 2005; Anterola et al., 2009). LOX-derived 12-hydroperoxy eicosatetraenoic acid (12-HPETE) is further metabolized by the bifunctional LOX, by at least one classical hydroperoxide lyase (PpHPL; Stumpe et al., 2006b), and by two allene oxide synthases (PpAOS; Bandara et al., 2009; Scholz et al., 2012; Figure 1A). From 12-HPETE the unusual PpLOX1 produces C8 volatiles including (2Z)-octen-1-ol and 1-octen-3-ol, and 12-oxo-dodecatrienoic acid (12-ODTE; Senger et al., 2005). PpHPL transforms 12-HPETE into (3Z)-nonenal, which is rapidly isomerized to (2E)-nonenal (Stumpe et al., 2006b; Figure 1A). Experiments with labeled fatty acids in other moss species demonstrated that C8 volatiles are exclusively derived from C20 fatty acids, suggesting a common 12-LOX mediated biosynthetic pathway in mosses (Croisier et al., 2010). These authors have also shown that the biosynthesis of C6 volatiles, i.e., (3Z)-hexenal and hexanal, in different moss species depended on both, C18 and C20 fatty acids (Croisier et al., 2010). PpHPL is an unspecific HPL that metabolizes hydroperoxides derived from both 18:2 and 18:3, but it preferentially uses 9-hydroperoxyoctadecadienoic acid (9-HPOD) as its substrate forming (3Z)-nonenal and 9-oxononanoic acid in vitro (Stumpe et al., 2006b). Interestingly, while in the PpHPL mutant no (3Z)-nonenal is formed, hexanal is still produced, indicating the presence of a hexanal forming enzyme that has not been identified yet (Stumpe et al., 2006b; Scholz et al., 2012). PpAOS1 uses C18-hydroperoxides (Figure 1B) and C20-hydroperoxides (Figure 1A) as substrates yielding 12,13-epoxy-octadecatrienoic acid (12,13-EOT) or 11,12-epoxy-eicosatetraenoic acid (11,12-EETE) when 13-HPOT or 12-HPETE are metabolized, respectively, while PpAOS2 prefers C20-hydroperoxides (Bandara et al., 2009; Scholz et al., 2012). PpAOS1 can also use 9- and 13-LOX-derived hydroperoxides from 18:2 (Scholz et al., 2012). In the absence of allene oxide cyclase activity, the unstable allene oxides are further converted to ketols and racemic cyclopentenones (Stumpe et al., 2010; Hashimoto et al., 2011; Neumann et al., 2012). In the presence of PpAOC2, 11,12-EETE formed the cyclopentenone 11-oxo-5,9,14-prostatrienoic acid (11-OPTA), whereas PpAOC1, PpAOC2, and PpAOC3 metabolized 12,13-EOT into OPDA, the precursor of JA (Stumpe et al., 2010; Hashimoto et al., 2011; Scholz et al., 2012; Figure 1). Individual P. patens mutants lacking either PpAOC1 or PpAOC2 have similar OPDA contents compared to wild-type plants (Stumpe et al., 2010), while in the PpAOS1 mutant the synthesis of OPDA is highly impaired, indicating that PpAOS1 plays a major role in OPDA formation (Scholz et al., 2012). P. patens contains several putative 12-oxophytodienoic acid reductases (OPR; Breithaupt et al., 2009; Li et al., 2009), however, JA is not synthesized in this moss. It seems likely that the enzyme OPR3 responsible for JA biosynthesis is missing; indicating that only the plastidic part of the LOX pathway is present in this moss (Stumpe et al., 2010; Ponce de León et al., 2012). This is further supported by the plastidic localization of all PpLOXs, PpAOCs, and PpAOS2 (Stumpe et al., 2010; Hashimoto et al., 2011; Scholz et al., 2012). The lack of JA is not limited to P. patens since the liverwort Marchantia polymorpha (M. polymorpha) does not synthesize JA (Yamamoto et al., 2015), suggesting that this hormone appeared later in plant evolution. Interestingly, P. patens respond to JA by altering moss development (Ponce de León et al., 2012), suggesting that the downstream components are already present in basal land plants like mosses. P. patens contains six putative genes encoding the JA-isoleucine receptor coronatine insensitive (COI; Chico et al., 2008). It is tempting to speculate that the different P. patens COI-like proteins may recognize, in addition to JA, other oxylipins allowing the binding of a broader range of ligands. However, further studies are needed to understand how JA is perceived in this moss.


Oxylipins in moss development and defense.

Ponce de León I, Hamberg M, Castresana C - Front Plant Sci (2015)

Oxylipin biosynthesis pathways in the moss P. patens. (A) Lipoxygenase-catalyzed oxygenation of arachidonic acid into 12(S)-HPETE and further conversions of this hydroperoxide by allene oxide synthase (PpAOS1-2), allene oxide cyclase (PpAOC2), hydroperoxide lyase (PpHPL), and 12-lipoxygenase (PpLOX1). (B) Oxygenation of linolenic acid into 2(R)-HPOT by Ppα-DOX and by lipoxygenase into 13(S)-HPOT. Breakdown of 2(R)-HPOT into 2(R)-HOT and heptadecatrienal and the further conversions of 13(S)-HPOT by allene oxide synthase (PpAOS1), allene oxide cyclase (PpAOC1-3), and hydroperoxide lyase (PpHPL) are also illustrated.
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Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4490225&req=5

Figure 1: Oxylipin biosynthesis pathways in the moss P. patens. (A) Lipoxygenase-catalyzed oxygenation of arachidonic acid into 12(S)-HPETE and further conversions of this hydroperoxide by allene oxide synthase (PpAOS1-2), allene oxide cyclase (PpAOC2), hydroperoxide lyase (PpHPL), and 12-lipoxygenase (PpLOX1). (B) Oxygenation of linolenic acid into 2(R)-HPOT by Ppα-DOX and by lipoxygenase into 13(S)-HPOT. Breakdown of 2(R)-HPOT into 2(R)-HOT and heptadecatrienal and the further conversions of 13(S)-HPOT by allene oxide synthase (PpAOS1), allene oxide cyclase (PpAOC1-3), and hydroperoxide lyase (PpHPL) are also illustrated.
Mentions: Physcomitrella patens is the first moss species with an available sequenced genome (Rensing et al., 2008), and several of the oxylipin-forming enzymes have been identified and biochemically characterized (Figure 1). P. patens has eight genes encoding lipoxygenase of which seven are functionally active in vitro (Anterola et al., 2009). Five are 13-LOXs (PpLOX3–PpLOX7) which use 18:3 as a substrate, while the other two are 12-LOXs (PpLOX1 and PpLOX2) and prefer 20:4 and 20:5 (Anterola et al., 2009). PpLOX3, 4, 6, and 7 can also use 18:2 as a substrate, although the activity is much higher against 18:3 (Anterola et al., 2009). PpLOX1 is an unusual bifunctional LOX that exhibit hydroperoxidase and a fatty acid chain-cleaving lyase activity (Senger et al., 2005; Anterola et al., 2009). In addition, both 12-LOXs accept C18-fatty acids as substrates yielding a broader range of oxylipins (Senger et al., 2005; Wichard et al., 2005; Anterola et al., 2009). LOX-derived 12-hydroperoxy eicosatetraenoic acid (12-HPETE) is further metabolized by the bifunctional LOX, by at least one classical hydroperoxide lyase (PpHPL; Stumpe et al., 2006b), and by two allene oxide synthases (PpAOS; Bandara et al., 2009; Scholz et al., 2012; Figure 1A). From 12-HPETE the unusual PpLOX1 produces C8 volatiles including (2Z)-octen-1-ol and 1-octen-3-ol, and 12-oxo-dodecatrienoic acid (12-ODTE; Senger et al., 2005). PpHPL transforms 12-HPETE into (3Z)-nonenal, which is rapidly isomerized to (2E)-nonenal (Stumpe et al., 2006b; Figure 1A). Experiments with labeled fatty acids in other moss species demonstrated that C8 volatiles are exclusively derived from C20 fatty acids, suggesting a common 12-LOX mediated biosynthetic pathway in mosses (Croisier et al., 2010). These authors have also shown that the biosynthesis of C6 volatiles, i.e., (3Z)-hexenal and hexanal, in different moss species depended on both, C18 and C20 fatty acids (Croisier et al., 2010). PpHPL is an unspecific HPL that metabolizes hydroperoxides derived from both 18:2 and 18:3, but it preferentially uses 9-hydroperoxyoctadecadienoic acid (9-HPOD) as its substrate forming (3Z)-nonenal and 9-oxononanoic acid in vitro (Stumpe et al., 2006b). Interestingly, while in the PpHPL mutant no (3Z)-nonenal is formed, hexanal is still produced, indicating the presence of a hexanal forming enzyme that has not been identified yet (Stumpe et al., 2006b; Scholz et al., 2012). PpAOS1 uses C18-hydroperoxides (Figure 1B) and C20-hydroperoxides (Figure 1A) as substrates yielding 12,13-epoxy-octadecatrienoic acid (12,13-EOT) or 11,12-epoxy-eicosatetraenoic acid (11,12-EETE) when 13-HPOT or 12-HPETE are metabolized, respectively, while PpAOS2 prefers C20-hydroperoxides (Bandara et al., 2009; Scholz et al., 2012). PpAOS1 can also use 9- and 13-LOX-derived hydroperoxides from 18:2 (Scholz et al., 2012). In the absence of allene oxide cyclase activity, the unstable allene oxides are further converted to ketols and racemic cyclopentenones (Stumpe et al., 2010; Hashimoto et al., 2011; Neumann et al., 2012). In the presence of PpAOC2, 11,12-EETE formed the cyclopentenone 11-oxo-5,9,14-prostatrienoic acid (11-OPTA), whereas PpAOC1, PpAOC2, and PpAOC3 metabolized 12,13-EOT into OPDA, the precursor of JA (Stumpe et al., 2010; Hashimoto et al., 2011; Scholz et al., 2012; Figure 1). Individual P. patens mutants lacking either PpAOC1 or PpAOC2 have similar OPDA contents compared to wild-type plants (Stumpe et al., 2010), while in the PpAOS1 mutant the synthesis of OPDA is highly impaired, indicating that PpAOS1 plays a major role in OPDA formation (Scholz et al., 2012). P. patens contains several putative 12-oxophytodienoic acid reductases (OPR; Breithaupt et al., 2009; Li et al., 2009), however, JA is not synthesized in this moss. It seems likely that the enzyme OPR3 responsible for JA biosynthesis is missing; indicating that only the plastidic part of the LOX pathway is present in this moss (Stumpe et al., 2010; Ponce de León et al., 2012). This is further supported by the plastidic localization of all PpLOXs, PpAOCs, and PpAOS2 (Stumpe et al., 2010; Hashimoto et al., 2011; Scholz et al., 2012). The lack of JA is not limited to P. patens since the liverwort Marchantia polymorpha (M. polymorpha) does not synthesize JA (Yamamoto et al., 2015), suggesting that this hormone appeared later in plant evolution. Interestingly, P. patens respond to JA by altering moss development (Ponce de León et al., 2012), suggesting that the downstream components are already present in basal land plants like mosses. P. patens contains six putative genes encoding the JA-isoleucine receptor coronatine insensitive (COI; Chico et al., 2008). It is tempting to speculate that the different P. patens COI-like proteins may recognize, in addition to JA, other oxylipins allowing the binding of a broader range of ligands. However, further studies are needed to understand how JA is perceived in this moss.

Bottom Line: Biochemical characterization of several oxylipin-producing enzymes and oxylipin profiling in P. patens reveal the presence of a wider range of oxylipins compared to flowering plants, including C18 as well as C20-derived oxylipins.Surprisingly, one of the most active oxylipins in plants, JA, is not synthesized in this moss.In this review, we present an overview of oxylipins produced in mosses and discuss the current knowledge related to the involvement of oxylipin-producing enzymes and their products in moss development and defense.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Biología Molecular, Instituto de Investigaciones Biológicas Clemente Estable , Montevideo, Uruguay.

ABSTRACT
Oxylipins are oxygenated fatty acids that participate in plant development and defense against pathogen infection, insects, and wounding. Initial oxygenation of substrate fatty acids is mainly catalyzed by lipoxygenases (LOXs) and α-dioxygenases but can also take place non-enzymatically by autoxidation or singlet oxygen-dependent reactions. The resulting hydroperoxides are further metabolized by secondary enzymes to produce a large variety of compounds, including the hormone jasmonic acid (JA) and short-chain green leaf volatiles. In flowering plants, which lack arachidonic acid, oxylipins are produced mainly from oxidation of polyunsaturated C18 fatty acids, notably linolenic and linoleic acids. Algae and mosses in addition possess polyunsaturated C20 fatty acids including arachidonic and eicosapentaenoic acids, which can also be oxidized by LOXs and transformed into bioactive compounds. Mosses are phylogenetically placed between unicellular green algae and flowering plants, allowing evolutionary studies of the different oxylipin pathways. During the last years the moss Physcomitrella patens has become an attractive model plant for understanding oxylipin biosynthesis and diversity. In addition to the advantageous evolutionary position, functional studies of the different oxylipin-forming enzymes can be performed in this moss by targeted gene disruption or single point mutations by means of homologous recombination. Biochemical characterization of several oxylipin-producing enzymes and oxylipin profiling in P. patens reveal the presence of a wider range of oxylipins compared to flowering plants, including C18 as well as C20-derived oxylipins. Surprisingly, one of the most active oxylipins in plants, JA, is not synthesized in this moss. In this review, we present an overview of oxylipins produced in mosses and discuss the current knowledge related to the involvement of oxylipin-producing enzymes and their products in moss development and defense.

No MeSH data available.


Related in: MedlinePlus