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Lipids in salicylic acid-mediated defense in plants: focusing on the roles of phosphatidic acid and phosphatidylinositol 4-phosphate.

Zhang Q, Xiao S - Front Plant Sci (2015)

Bottom Line: Plants have evolved effective defense strategies to protect themselves from various pathogens.While many proteins play essential roles in regulating SA signaling, increasing evidence also supports important roles for signaling phospholipids in this process.In this review, we collate the experimental evidence in support of the regulatory roles of two phospholipids, phosphatidic acid (PA), and phosphatidylinositol 4-phosphate (PI4P), and their metabolizing enzymes in plant defense, and examine the possible mechanistic interaction between phospholipid signaling and SA-dependent immunity with a particular focus on the immunity-stimulated biphasic PA production that is reminiscent of and perhaps mechanistically connected to the biphasic reactive oxygen species (ROS) generation and SA accumulation during defense activation.

View Article: PubMed Central - PubMed

Affiliation: Institute for Bioscience and Biotechnology Research, University of Maryland Rockville, MD, USA.

ABSTRACT
Plants have evolved effective defense strategies to protect themselves from various pathogens. Salicylic acid (SA) is an essential signaling molecule that mediates pathogen-triggered signals perceived by different immune receptors to induce downstream defense responses. While many proteins play essential roles in regulating SA signaling, increasing evidence also supports important roles for signaling phospholipids in this process. In this review, we collate the experimental evidence in support of the regulatory roles of two phospholipids, phosphatidic acid (PA), and phosphatidylinositol 4-phosphate (PI4P), and their metabolizing enzymes in plant defense, and examine the possible mechanistic interaction between phospholipid signaling and SA-dependent immunity with a particular focus on the immunity-stimulated biphasic PA production that is reminiscent of and perhaps mechanistically connected to the biphasic reactive oxygen species (ROS) generation and SA accumulation during defense activation.

No MeSH data available.


Related in: MedlinePlus

A schematic illustration of the regulatory roles of PA and PI4P in SA-dependent plant defense signaling. Plants activate immune responses upon recognition of PAMPs or effectors by PRRs or NB-LRR immune receptors, respectively. Bioactive PA and PI4P play distinct roles in regulating defense signaling. PA production via immunity-activated PLC and/or PLD is required for SA-dependent defense activation and exhibits a biphasic pattern (1° & 2°) that precedes the kinetically similar biphasic ROS generation and SA accumulation. Therefore, we propose that these three signaling molecules are sequentially interconnected with PA most likely being the initial signal of the PA-ROS-SA signaling module. The first wave (1°) of PA-ROS-SA signal amplification (occurring during PTI and ETI) may potentiate the second wave (2°) of PA-ROS-SA signal amplification (occurring mostly during ETI or strengthened PTI), constituting a tunable signaling module for defense in plant cells. PI4P derived from PI4KIIIβ1 and PI4KIIIβ2 functions to maintain the homeostasis of PRRs via facilitating its recycling and/or degradation, thereby preventing inappropriate activation of PTI in the absence of pathogens and allowing measured PTI signaling upon pathogen attack. PAMPs, pathogen-associated molecular patterns; PTI, PAMP-triggered immunity; ETI, effector-triggered immunity; PRR, pattern recognition receptor; NB-LRR, nucleotide binding site leucine-rich-repeats; PA, phosphatidic acid; PI4P, phosphatidylinositol 4-phosphate; TGN, trans-Golgi network; PLC, phospholipase C; PLD, phospholipase D.
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Figure 1: A schematic illustration of the regulatory roles of PA and PI4P in SA-dependent plant defense signaling. Plants activate immune responses upon recognition of PAMPs or effectors by PRRs or NB-LRR immune receptors, respectively. Bioactive PA and PI4P play distinct roles in regulating defense signaling. PA production via immunity-activated PLC and/or PLD is required for SA-dependent defense activation and exhibits a biphasic pattern (1° & 2°) that precedes the kinetically similar biphasic ROS generation and SA accumulation. Therefore, we propose that these three signaling molecules are sequentially interconnected with PA most likely being the initial signal of the PA-ROS-SA signaling module. The first wave (1°) of PA-ROS-SA signal amplification (occurring during PTI and ETI) may potentiate the second wave (2°) of PA-ROS-SA signal amplification (occurring mostly during ETI or strengthened PTI), constituting a tunable signaling module for defense in plant cells. PI4P derived from PI4KIIIβ1 and PI4KIIIβ2 functions to maintain the homeostasis of PRRs via facilitating its recycling and/or degradation, thereby preventing inappropriate activation of PTI in the absence of pathogens and allowing measured PTI signaling upon pathogen attack. PAMPs, pathogen-associated molecular patterns; PTI, PAMP-triggered immunity; ETI, effector-triggered immunity; PRR, pattern recognition receptor; NB-LRR, nucleotide binding site leucine-rich-repeats; PA, phosphatidic acid; PI4P, phosphatidylinositol 4-phosphate; TGN, trans-Golgi network; PLC, phospholipase C; PLD, phospholipase D.

Mentions: Based on the evidence from multiple studies described above and summarized in Supplemental Table 1 we propose a model to illustrate biphasic PA-ROS-SA signaling during plant defense activation (Figure 1). The main points of the model are as follows: (i) The first wave is rapid and transient, and is attributable to PTI and/or ETI; whereas the second wave occurs in plant cells undergoing ETI or ectopically strengthened PTI (i.e., suspension-cultured cells treated with high-concentration of PAMPs). (ii) The signaling order is probably from PA (mainly from the PLC-DGK route) to ROS (De Jong et al., 2004; Park et al., 2004), and from ROS to SA (Lamb and Dixon, 1997; Chamnongpol et al., 1998; Mur et al., 2009) in the first wave based on time sequence and some known mechanistic connections. (iii) Elevated SA in the first wave above a threshold level plays an essential role in potentiation (priming) of the second wave of PA (mainly produced by PLDs), ROS and SA production through multi-layered positive feedback amplification circuits where EDS1/PAD4/SAG101 may be essential components required for SA signaling and PTI-ETI connection (Kim et al., 2014; Zhang et al., 2014). Conceivably, the spatiotemporal kinetics and amplitude of the biphasic defense signal amplification may vary under different pathocontexts, which may at least partially account for the discrepancies in the results from different studies (Supplemental Table 1). Nevertheless, the biphasic PA-ROS-SA signal amplification, together with production of other signaling molecules such as nitric oxide and C2H4 (Mur et al., 2008, 2009), likely orchestrates the eventual development of HR and other defense responses in many cases.


Lipids in salicylic acid-mediated defense in plants: focusing on the roles of phosphatidic acid and phosphatidylinositol 4-phosphate.

Zhang Q, Xiao S - Front Plant Sci (2015)

A schematic illustration of the regulatory roles of PA and PI4P in SA-dependent plant defense signaling. Plants activate immune responses upon recognition of PAMPs or effectors by PRRs or NB-LRR immune receptors, respectively. Bioactive PA and PI4P play distinct roles in regulating defense signaling. PA production via immunity-activated PLC and/or PLD is required for SA-dependent defense activation and exhibits a biphasic pattern (1° & 2°) that precedes the kinetically similar biphasic ROS generation and SA accumulation. Therefore, we propose that these three signaling molecules are sequentially interconnected with PA most likely being the initial signal of the PA-ROS-SA signaling module. The first wave (1°) of PA-ROS-SA signal amplification (occurring during PTI and ETI) may potentiate the second wave (2°) of PA-ROS-SA signal amplification (occurring mostly during ETI or strengthened PTI), constituting a tunable signaling module for defense in plant cells. PI4P derived from PI4KIIIβ1 and PI4KIIIβ2 functions to maintain the homeostasis of PRRs via facilitating its recycling and/or degradation, thereby preventing inappropriate activation of PTI in the absence of pathogens and allowing measured PTI signaling upon pathogen attack. PAMPs, pathogen-associated molecular patterns; PTI, PAMP-triggered immunity; ETI, effector-triggered immunity; PRR, pattern recognition receptor; NB-LRR, nucleotide binding site leucine-rich-repeats; PA, phosphatidic acid; PI4P, phosphatidylinositol 4-phosphate; TGN, trans-Golgi network; PLC, phospholipase C; PLD, phospholipase D.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4446532&req=5

Figure 1: A schematic illustration of the regulatory roles of PA and PI4P in SA-dependent plant defense signaling. Plants activate immune responses upon recognition of PAMPs or effectors by PRRs or NB-LRR immune receptors, respectively. Bioactive PA and PI4P play distinct roles in regulating defense signaling. PA production via immunity-activated PLC and/or PLD is required for SA-dependent defense activation and exhibits a biphasic pattern (1° & 2°) that precedes the kinetically similar biphasic ROS generation and SA accumulation. Therefore, we propose that these three signaling molecules are sequentially interconnected with PA most likely being the initial signal of the PA-ROS-SA signaling module. The first wave (1°) of PA-ROS-SA signal amplification (occurring during PTI and ETI) may potentiate the second wave (2°) of PA-ROS-SA signal amplification (occurring mostly during ETI or strengthened PTI), constituting a tunable signaling module for defense in plant cells. PI4P derived from PI4KIIIβ1 and PI4KIIIβ2 functions to maintain the homeostasis of PRRs via facilitating its recycling and/or degradation, thereby preventing inappropriate activation of PTI in the absence of pathogens and allowing measured PTI signaling upon pathogen attack. PAMPs, pathogen-associated molecular patterns; PTI, PAMP-triggered immunity; ETI, effector-triggered immunity; PRR, pattern recognition receptor; NB-LRR, nucleotide binding site leucine-rich-repeats; PA, phosphatidic acid; PI4P, phosphatidylinositol 4-phosphate; TGN, trans-Golgi network; PLC, phospholipase C; PLD, phospholipase D.
Mentions: Based on the evidence from multiple studies described above and summarized in Supplemental Table 1 we propose a model to illustrate biphasic PA-ROS-SA signaling during plant defense activation (Figure 1). The main points of the model are as follows: (i) The first wave is rapid and transient, and is attributable to PTI and/or ETI; whereas the second wave occurs in plant cells undergoing ETI or ectopically strengthened PTI (i.e., suspension-cultured cells treated with high-concentration of PAMPs). (ii) The signaling order is probably from PA (mainly from the PLC-DGK route) to ROS (De Jong et al., 2004; Park et al., 2004), and from ROS to SA (Lamb and Dixon, 1997; Chamnongpol et al., 1998; Mur et al., 2009) in the first wave based on time sequence and some known mechanistic connections. (iii) Elevated SA in the first wave above a threshold level plays an essential role in potentiation (priming) of the second wave of PA (mainly produced by PLDs), ROS and SA production through multi-layered positive feedback amplification circuits where EDS1/PAD4/SAG101 may be essential components required for SA signaling and PTI-ETI connection (Kim et al., 2014; Zhang et al., 2014). Conceivably, the spatiotemporal kinetics and amplitude of the biphasic defense signal amplification may vary under different pathocontexts, which may at least partially account for the discrepancies in the results from different studies (Supplemental Table 1). Nevertheless, the biphasic PA-ROS-SA signal amplification, together with production of other signaling molecules such as nitric oxide and C2H4 (Mur et al., 2008, 2009), likely orchestrates the eventual development of HR and other defense responses in many cases.

Bottom Line: Plants have evolved effective defense strategies to protect themselves from various pathogens.While many proteins play essential roles in regulating SA signaling, increasing evidence also supports important roles for signaling phospholipids in this process.In this review, we collate the experimental evidence in support of the regulatory roles of two phospholipids, phosphatidic acid (PA), and phosphatidylinositol 4-phosphate (PI4P), and their metabolizing enzymes in plant defense, and examine the possible mechanistic interaction between phospholipid signaling and SA-dependent immunity with a particular focus on the immunity-stimulated biphasic PA production that is reminiscent of and perhaps mechanistically connected to the biphasic reactive oxygen species (ROS) generation and SA accumulation during defense activation.

View Article: PubMed Central - PubMed

Affiliation: Institute for Bioscience and Biotechnology Research, University of Maryland Rockville, MD, USA.

ABSTRACT
Plants have evolved effective defense strategies to protect themselves from various pathogens. Salicylic acid (SA) is an essential signaling molecule that mediates pathogen-triggered signals perceived by different immune receptors to induce downstream defense responses. While many proteins play essential roles in regulating SA signaling, increasing evidence also supports important roles for signaling phospholipids in this process. In this review, we collate the experimental evidence in support of the regulatory roles of two phospholipids, phosphatidic acid (PA), and phosphatidylinositol 4-phosphate (PI4P), and their metabolizing enzymes in plant defense, and examine the possible mechanistic interaction between phospholipid signaling and SA-dependent immunity with a particular focus on the immunity-stimulated biphasic PA production that is reminiscent of and perhaps mechanistically connected to the biphasic reactive oxygen species (ROS) generation and SA accumulation during defense activation.

No MeSH data available.


Related in: MedlinePlus