Functional diversity of jasmonates in rice
© Liu et al.; licensee Springer. 2015
Received: 5 November 2014
Accepted: 14 January 2015
Published: 29 January 2015
Phytohormone jasmonates (JA) play essential roles in plants, such as regulating development and growth, responding to environmental changes, and resisting abiotic and biotic stresses. During signaling, JA interacts, either synergistically or antagonistically, with other hormones, such as salicylic acid (SA), gibberellin (GA), ethylene (ET), auxin, brassinosteroid (BR), and abscisic acid (ABA), to regulate gene expression in regulatory networks, conferring physiological and metabolic adjustments in plants. As an important staple crop, rice is a major nutritional source for human beings and feeds one third of the world’s population. Recent years have seen significant progress in the understanding of the JA pathway in rice. In this review, we summarize the diverse functions of JA, and discuss the JA interplay with other hormones, as well as light, in this economically important crop. We believe that a better understanding of the JA pathway will lead to practical biotechnological applications in rice breeding and cultivation.
Jasmonates (JA) are a class of polyunsaturated fatty acid-derived phytohormones, playing important roles in plant growth and defense responses. The biosynthesis of JA initiates in chloroplasts, involving the release of α-linolenic acid (α-LeA, 18:3 or 18:2) from the lipid membrane by phospholipases (PLDs). Only α-LeA (18:3) is utilized as a JA precursor through one of the seven distinct branches of the lipoxygenase (LOX) pathway, the allene oxide synthase (AOS) branch. Traditionally, α-LeA (18:3) is oxidized by 13-LOX, an enzyme catalyzing regio- and stereo-specific dioxygenation of polyunsaturated fatty acid at C-13, to specifically form a fatty acid hydroperoxide, 13-HPOT (13S-hydroperoxy-(9Z,11E,15)-octadecatrienoic acid); however, the generation of both 9- and 13-hydroperoxides by OsLOX1 based on a dual C-9 and C-13 specificity was found in rice (Wang et al. 2008). The 13-HPOT then enters the seven enzymatic branches of the LOX pathway, including the oxidation by AOS to form an allene oxide, 12,13-EOT ((9Z,13S,15Z)-12,13-oxido-9,11,15-octadecatrienoic acid). The 12,13-EOT is unstable and can be cyclized by allene oxide cyclase (AOC) to form racemic 12-oxophytodienoic acid (12-OPDA). Subsequently, the cyclized OPDA is transferred from chloroplasts into peroxisomes, where it is reduced by OPDA reductase3 (OPR3) and three further β-oxidation steps are conducted to produce (3R, 7S)-(+)-JA. After being released into the cytosol, it is converted into (3R, 7R)-(−)-JA, which can then be catalyzed by a jasmonate-amido synthase, JASMONATE RESISTANT 1 (JAR1), to form bioactive jasmonate (JA-Ile) by conjugating the amino acid isoleucine to (3R, 7R)-(−)-JA (Lyons et al. 2013; Svyatyna and Riemann 2012; Schaller and Stintzi 2009). Additionally, the hydroperoxy-octadecadienoic acids (HPOTs/HPODs) generated by LOXs can enter the hydroperoxide lyase (HPL) branch of the LOX pathway and are finally converted to green leaf volatiles (GLVs), which are indirectly involved in the defense against herbivores. Thus, the AOS and HPL branches compete for the same substrates and play antagonistic actions in rice (Chehab et al. 2007; Lyons et al. 2013).
Comparison of genes responsible for Jasmonates (JA) biosynthesis and signaling between rice and other plants
Increases contents of JA precursors, resulting in sterility
Liu et al. 2012a
Lipoxygenase, affecting JA signaling in sex determination
Acosta et al. 2009
JA biosynthesis; 1sterility when silenced; 2resistance to Xanthomonas oryzae pv. oryzae (Xoo) and Magnaporthe grisea when overexpressed; 3activated by red and blue light
1JA biosynthesis; 1sterility when mutated; 2susceptible to bacterium Erwinia carotovora ssp. carotovora strain WPP14 (Ecc) when mutated; 3susceptible to Mycosphaerella pinodes when silenced
1JA biosynthesis; sterility complement when expressed in Arabidopsis opr3 mutant; 2activated in response to red light
1JA biosynthesis; 1sterility when mutated; 2susceptible to M. pinodes when silenced
1JA biosynthesis; 1early flowering, elongated sterile lemma and reduced fertility; 1enhanced fungal hyphal growth when mutated; 2involved in light-mediated inhibition of coleoptile elongation
1 P. Patens
1Reduced fertility and altered sporophyte morphology when mutated; 2susceptible to M. pinodes when silenced
1Catalyzing JA-Ile production to resist blast attack; 1coleoptiles grow longer when mutated under FR; 2functioning in JA-light signaling
1Affecting root elongation and seed germination; 2increased susceptibility to the soil fungus Pythium irregulare when mutated; 3hypocotyl growth inhibition when mutated; 4required for shade responses
Promoting production of MeJA
Kim et al. 2009
Promoting production of MeJA; grain yield reduction when overexpressed in rice
Kim et al. 2009
1JA biosynthesis; 2susceptible to rice striped stem borer (SSB) and resistant to rice brown planthopper (BPH) when knocked down
1Contributing to rapid jasmonate synthesis in wounded leaves; 2defense against herbivores
1A JA receptor; 1faster germination when silenced; 2activating JA responsive genes; 3resistance to Xoo
1Male sterility when mutated; resistance to insect herbivory and pathogens; growth inhibition; 2required for light-induced suppression of hypocotyl elongation in response to both R and FR light; 2suppressing chlorophyll biosynthesis
1Functioning in JA signaling; 1regulating JA responsive gene; 2participating in drought resistance; 3 involved in JA-induced resistance to bacterial blight
1functional in shade responses; 2 35S:JAZ1D transgenic plants display male sterility, reduced defense against Pseudomonas syringae, and showing altered JA-mediated root growth inhibition; 3 displaying reduced resistance to the generalist herbivore Spodoptera exigua
1Negatively regulating JA signaling; 1root inhibition when mutated; 2confering resistance to Rice dwarf virus
Yoshii et al. 2008
Positively regulating JA signaling; directing defense against Xoo
Tao et al. 2009
1JA responsive; 2positively regulating Pi uptake
suppressing JA signaling; defense against Xoo and M. grisea
Tao et al. 2009
increased sensitivity to salt and mannitol stresses, increase in lateral roots when overexpressed in Arabidopsis
Zhou et al. 2008
1Activating JA biosynthetic pathway; 1defense against Rhizoctonia Solani and M. Grisea; 2confering drought tolerance
Induced by various pathogens and SA, suppressed by JA
Zheng et al. 2011
1Suppressing JA signaling; 1resisting against SSB when knockdown; 1mediating JA and ET crosstalk; 2mediating JA and SA crosstalk
1Involved in the SA-mediated suppression of JA signaling; 2required for systemic resistance conferred by the Mycorrhizal fungus Piriformospora indica
Causing reduced levels of JA and susceptible to SSB larvae when silenced
Wang et al. 2013
1Positive regulator of ET- and JA-mediated defenses; 2negative regulator of SA-dependent systemic required resistance; 3implicated in responses to abiotic stress
Resistance to SSB infestation; reducing their expression resulted in the reduced elicited levels of linolenic acid, JA, green leaf volatiles, and ethylene
Qi et al. 2011
1mediating wound induction of JA; 2required for high salinity and water deficit tolerance; 3functional in microtubule organization, 4salicylic acid signaling and 5seedling development
Rice growth and development regulated by JA
Flower development and sterility are effected by JA in plants, including Arabidopsis, tomato and maize (Wasternack and Hause 2013). In rice, a mitochondrial proteomic comparison between a sterile line and its fertile near-isogenic line revealed that a sex determination protein TASSELSEED-2 (Os07g46920.1) was significantly up-regulated in the sterile line. At the same time, JA precursors were significantly increased in all of the developmental stages of the reproductive organs in the sterile line, except at the bicellular pollen stage, indicating that the biosynthetic levels of JA may regulate rice sterility (Liu et al. 2012a). The maize homologue of TASSELSEED-1 affects JA signaling, further confirming the effects of JA on rice flower development (Acosta et al. 2009). More direct evidence of JA functioning in rice sterility has been revealed by studying rice genes that are responsible for JA biosynthesis. Similar to the AOS knock-out mutants of Arabidopsis (Park et al. 2002), OsAOS1 and OsAOS2 RNAi-silenced transgenic rice plants show a severe or complete sterility phenotype during the reproductive stage (Bae et al. 2010). The rice OsOPR7 gene that is functionally similar to Arabidopsis opr3, which is involved in JA biosynthesis, is able to complement the male sterility phenotype of Arabidopsis opr3 mutants and restores JA production (Tani et al. 2008). Further, JA-deficient mutants, with a disrupted expression of OsAOC also show typical developmental phenotypes such as early flowering, elongated sterile lemma, and reduced fertility (Riemann et al. 2013). The over-production of JA is also thought to affect rice fertility. The oxylipin pathway contains several competing branch pathways, including allene oxide synthase (AOS) and hydroperoxide lyase (HPL), which are responsible for the production of JAs and aldehydes, respectively. Disruption of the rice HPL pathway by mutations results in a dramatic increase in JA production, leading to a reduced seed-setting ratio and a reduced tiller number due to the interference of pollen fertility (Liu et al. 2012b). These results indicate that JA plays critical roles in rice flower development and fertility.
Many factors participate in seed germination, including plant hormones, which play critical roles. Gibberellins (GAs), abscisic acid (ABA), auxin, ethylene (ET), cytokinins, and brassinosteroids (BRs) function during seed germination. For example, because of the effects of antagonism between GA and ABA, seeds are released from dormancy (Ye and Zhang 2012). Although no direct effect of auxin on seed germination has been reported, some AUXIN RESPONSE FACTORS are involved in seed germination. It was found that the inhibition of AUXIN RESPONSE FACTOR 10 by microRNA60 is necessary for seed germination (Liu et al. 2007). An increasing amount of ET was also reported during seed germination in different plant species and that ET can release seed dormancy (Borghetti et al. 2002). Cytokinins promote seed germination by alleviating stresses (Miransari and Smith 2014), and seed germination can be enhanced by BR because it offsets the negative effects of ABA on germination (Zhang et al. 2009). JA has long been proposed to inhibit seed germination. Wilen et al. (1991) reported that exogenous applications of JA affected embryo-specific processes in Brassica and Linum oilseeds. In recent years, it was further revealed that OPDA, a key metabolic intermediate during JA biosynthesis, has a synergistic effect with ABA in germination inhibition (Dave et al. 2011). In rice, some evidence indicates that JA also regulates seed germination negatively. The imbibition of a MeJA solution by rice seeds produced a significant inhibition of germination (Tang et al. 2002). The overexpression of pepper MAP kinase, which resulted in a high accumulation of JA, in transgenic rice inhibited seed germination (Lee and Back 2005) and the silencing of the rice Coronatine Insensitive 1 (OsCOI1) gene, a key component of a JA receptor, led to a faster germination compared with wild-type rice plants (Yang et al. 2012). It should be noted that studies on functions of JA during rice seed germination are still preliminary and efforts should be taken to unravel the mechanisms of germination that are regulated by JA in rice.
Root growth inhibition
Auxin plays an essential role during lateral root (LR) development by establishing an auxin gradient mediated by PIN-FORMED2 (PIN2), an auxin efflux transporter (De Smet et al. 2006). However, recent studies revealed that by interacting with auxin and affecting auxin biosynthesis, JA fine-tunes the regulation of LR formation. In fact, an efficient method to identify JA-related mutants in Arabidopsis is by observing the root growth inhibition in JA solutions (Staswick et al. 1992). In general, the regulatory effect of JA through auxin on LR formation is the net result of two competing mechanisms: JA promotes the ANTHRANILATE SYNTHASE ALPHA SUBUNIT 1 (ASA1)-dependent auxin synthesis and JA reduces PIN-dependent auxin transport (Sun et al. 2009). JA is also integrated into auxin-mediated root meristem activity via MYC2/JASMONATE INSENSITIVE1 (MYC2)-dependent repression of PLETHORA (PLT) expression (Chen et al. 2011). Another report, however, suggested that an auxin independent mechanism of the JA regulation of root development exists (Raya-González et al. 2012).
In rice, exogenous applications of MeJA on young seedlings retard the growth of roots and shoots. The lowest concentration of MeJA for the inhibition of rice seedling growth is 0.9 μM (Tsai et al. 1997) and 50% inhibition is observed at 5 μM of JA (Cho et al. 2007). Most differentially regulated proteins in rice roots effected by JA treatments belong to the functional categories of antioxidant, cellular respiration and, defense-related proteins (Cho et al. 2007). RICE SALT SENSITIVE3 (RSS3) was identified as a nuclear factor, which modulates the expression of JA-responsive genes and regulates root cell elongation. In a recent model, RSS3 binds with class-C basic helix-loop-helix (bHLH) transcription factors (TFs) and JASMONATE ZIM-DOMAIN proteins (JAZs) to form a ternary complex, as a result the JA-responsive genes are repressed when JA is absent. In the presence of JA, JAZ was degraded by the 26S proteasome. Thus, an unknown factor binds to the RSS3-bHLH complex, leading to the derepression of the bHLH-mediated transcription (Toda et al. 2013). KCl can partially relieve the MeJA inhibition of root growth because MeJA causes the conspicuous loss of KCl from the cell (Tsai et al. 1997). The JA inhibition of rice root growth can also be demonstrated by an endogenous increase in the JA level. For example, when pepper MAP kinase in rice is overexpressed, the endogenous JA accumulation is increased three times and the phenotype of root inhibition is similar to those of wild-type rice treated with 10 μM JA (Lee and Back 2005). The same phenotype of root growth inhibition is also observed in the rice NAC transcription factor gene rim1 mutant, in which the expression levels of key genes involved in JA biosynthesis, such as LOX, AOS2, and OPR7 are up-regulated because of the change in JA signaling (Yoshii et al. 2010). Additionally, it was found that the rice ROOT MEANDER CURLING (OsRMC) gene in the negative JA signaling pathway is involved in the development of the root system (Jiang et al. 2007).
JA not only plays important roles in sterility, seed germination, and root growth in rice, but it also regulates other rice developmental processes, such as shoot growth, leaf senescence, spikelet development, photomorphogenesis, and gravitropism. For instance, exogenous applications of MeJA inhibit both shoot and root growth in rice (Tsai et al. 1997), the overproduction of JA in rice plants caused the lesion-mimic phenotype on the leaves (Liu et al. 2012b), and the senescence of rice leaves promoted by JA is associated with an increase in ET sensitivity rather than the ET level (Tsai et al. 1996). JA can determine the rice spikelet number and morphology through the JA signaling pathway or by mediating stress signals, subsequently affecting the grain yield (Cai et al. 2014; Kim et al. 2009). JA or its derivatives play an important role in the phytochrome-dependent inhibition of rice coleoptile elongation by light, indicating that JA is one of the hormones that regulate rice photomorphogenesis (Svyatyna and Riemann 2012) (see details in the section “JA-light crosstalk”). JA also modulates gravitropism, in an action mode opposite to that of auxin (Hoffmann et al. 2011; Gutjahr et al. 2005) (see details in the section “JA-auxin crosstalk”).
JA-mediated abiotic stress responses in rice
Abiotic stresses, such as drought, salinity and adverse temperatures, have negative effects on plant growth and reproduction. When responding to these environmental changes, plants adjust the levels of endogenous phytohormones to activate biochemical and physiological pathways for adaptation. For example, ABA is the most studied hormone that responds to various environmental stresses, but other hormones, such as cytokinin, BR, and auxin, also participate in abiotic stress responses (Peleg and Blumwald 2011). Here, we emphasize the role of JA during environmental and abiotic stresses in rice. Under drought, salinity and cold stresses, the expression levels of many genes involved in JA biosynthesis were up-regulated and those genes involved in JA signaling were differentially modulated. At the same time, the JA level in rice was significantly increased compared with the non-stressed control (Moons et al. 1997; Tani et al. 2008; Du et al. 2013). This suggests that JA plays a critical role in regulating the responses and the adaptation of rice to diverse abiotic stresses. However, studies also showed that the JA level was decreased and JA biosynthetic genes were down-regulated under heat stress (Du et al. 2013), implying that different JA-regulating mechanisms may function under different abiotic stresses. There is a correlation between grain yield and MeJA level in rice (Cai et al. 2014; Kim et al. 2009). Increasing the MeJA level by overexpressing Arabidopsis jasmonic acid carboxyl methyltransferase (AtJMT) in rice resulted in a significant reduction in the grain yield. It was postulated that during the early stages of rice flower development under drought conditions, MeJA production is promoted by the induction of OsJMT1, a rice orthologue of AtJMT. The increased accumulation of MeJA activates the expression of OsSDR, which results in the high level of ABA biosynthesis. Drought stress also induces ABA accumulation directly, independently from MeJA. As a result, the accumulation of both MeJA and ABA affects spikelet development and subsequently causes a decrease in grain yield (Kim et al. 2009). Although the increased level of MeJA has a negative effect on rice grain production, JA accumulation may protect rice against salt stress. For example, exogenous applications of JA can ameliorate the performance of salt-stressed rice seedlings. This includes the recovery of many physiological properties, such as leaf water potential, lipopolysaccharide production, maximum quantum yield of Photosystem II, and calcium and magnesium uptake, when applying JA after saline exposure, and this recovery phenomena was more evident in the salt-sensitive cultivar than in the salt-tolerant cultivar (Kang et al. 2005). Additional assays also identified a higher endogenous accumulation of JA in salt-tolerant cultivars of rice than in salt-sensitive rice (Kang et al. 2005), implying that JA is involved in a protective mechanisms against salinity.
JA-mediated rice resistance against pests and pathogens
Many reports indicated that JA plays critical roles in rice immunity against bacterial and fungal infections and damage by herbivores. In bacterial and fungal diseases, such as rice blight caused by Xanthomonas oryzae pv. oryzae (Xoo) and rice blast caused by Magnaporthe grisea, the exogenous application of JA is sufficient to induce rice resistance against infections, effectively reducing lesion symptoms (Yamada et al. 2012; Mei et al. 2006). Molecular assays revealed that the expression levels of several pathogenesis-related (PR) genes, including OsPR1a, OsPR1b, OsPR2, OsPR5, and OsPR10, are up-regulated in rice upon JA treatment (Yang et al. 2013), confirming that JA functions as an important signaling molecule in pathogen resistance. An analysis of transgenic rice plants that could accumulate high levels of endogenous JA through the overexpression of some key JA biosynthetic genes provided direct evidence of its function against microbial diseases. In rice, the overexpression of OsAOS significantly increases the JA level in the transgenic rice lines and the plants show enhanced resistance to the rice blight bacterium Xoo (Liu et al. 2012b) and rice blast fungus M. grisea (Mei et al. 2006). Similarly, the high accumulation of endogenous JA has a positive correlation with the activation of PR genes, such as OsPR1a, OsPR3, and OsPR5, in these transgenic rice plants (Mei et al. 2006). However, when OsAOC, encoding a functional allene oxide cyclase, is impaired in the rice mutants coleoptile photomorphogenesis 2 (cpm2) and hebiba, enhanced fungal hyphal growth is observed compared with on wild-type (Riemann et al. 2013). The functional similarity of AtAOS and OsAOS in resistance mechanisms against pathogens was shown by the Arabidopsis aos mutant, which is more susceptible to the necrotrophic bacterium Erwinia carotovora ssp. carotovora strain WPP14 (Ecc) compared with wild-type and this phenotype can be complemented by potato StAOS2 (Pajerowska-Mukhtar et al. 2008).
WRKY TFs play important roles in modulating JA signaling and many WRKY genes identified are JA responsive in Arabidopsis (Schluttenhofer et al. 2014). In the rice genome there are more than 100 WRKY genes, including OsWRKY03, OsWRKY13, OsWRKY31, OsWRKY53, OsWRKY62, OsWRKY71, OsWRKY89 (Pandey and Somssich 2009), OsWRKY45-1, OsWRKY45-2 (Tao et al. 2009), and OsWRKY30 (Peng et al. 2012) that are associated with pathogen defense. The OsWRKY45-1 and OsWRKY45-2-directed defense against Xoo is accompanied by an increased JA level, even though the molecular mechanisms of the rice-Xoo interactions modulated by these two genes are different (Tao et al. 2009). The expression levels of these two genes are directly regulated by OsWRKY13, which functions as a transcriptional repressor by binding to the promoter regions of the two genes. Thus, OsWRKY13 acts upstream of OsWRKY45s in their pathogen defense signaling pathway (Tao et al. 2009). Indeed, the activation of OsWRKY13 confers rice disease tolerance to Xoo and M. grisea (Qiu et al. 2007). OsWRKY30 also plays critical roles in the JA signaling pathway against rice pathogens. The overexpression of OsWRKY30 in transgenic rice activates some JA biosynthetic genes, increases the JA accumulation level, and strengthens the rice plants ability to resist the rice sheath blight fungus Rhizoctonia solani and the blast fungus M. grisea (Peng et al. 2012).
Jasmonoyl-L-isoleucine (JA-Ile) also plays an important role in JA signaling, and it modulates plant defenses against attacks by pathogens and insects in Arabidopsis and other dicots (Staswick et al. 1998; Kang et al. 2006). In rice, JA-Ile synthases, encoded by OsJAR1 and OsJAR2, catalyze the JA-isoleucine conjugation to form JA-Ile. However, only the expression of OsJAR1, not that of OsJAR2, correlates with JA-Ile accumulation after blast attack (Wakuta et al. 2011), indicating that only OsJAR1 is involved in pathogen defense. JA-Ile, as a primary and bioactive signal, stimulates the COI1 (a component of the E3 ubiquitin ligase SCFCOI1)-mediated JAZ degradation, which is dependent on the 26S proteasome pathway, resulting in the activation of JA responsive genes that confer plant disease resistance (Katsir et al. 2008; Yamada et al. 2012). Indeed, the repression of OsCOI1 expression or the overexpression of OsJAZ8ΔC, in which the Jas domain responsible for JA-dependent OsJAZ8 degradation was deleted, leads to the altered expression of JA-responsive genes and a reduced resistance to Xoo in transgenic rice plants (Yang 2009; Yamada et al. 2012). Additionally, the biosynthetic accumulation of monoterpene linalool is also regulated by OsJAZ8 in a JA-dependent manner, making the rice plants more resistant to Xoo (Taniguchi et al. 2014). These studies demonstrate that JA and JA signaling play critical roles in the regulation of pathogen defenses against bacteria and fungi.
JA or JA signaling also regulates rice plant defenses against some pests, such as nematodes and chewing herbivores. The exogenous treatment of rice shoots with MeJA triggers an intensive systemic defense response and activates the expression of some PR genes, including OsPR1a and OsPR1b, in the roots where the activities of the root knot nematode Meloidogyne graminicola is inhibited (Nahar et al. 2011). Although the mechanism behind how the non-expressor of pathogenesis-related genes1, OsNPR1, regulates JA biosynthesis remains unclear, OsNPR1 knockdown rice plants exhibit enhanced levels of herbivore-mediated JA and JA-dependent resistance against infestation by the rice striped stem borer (SSB) (Li et al. 2013). However, contrasting roles for JA in controlling chewing and phloem-feeding herbivores were revealed by analyzing chloroplast-localized type 2 13-lipoxygenase gene (OsHI-LOX) antisense silenced rice plants (as-lox plants). Although the suppression of OsHI-LOX in rice decreases the SSB-induced JA accumulation and makes the rice more susceptible to SSB larvae, the as-lox rice plants exhibited an enhanced resistance to the rice brown planthopper (BPH) Niaparvata lugens (Zhou et al. 2009). Similar results were also obtained by studying rice mitogen-activated protein kinase (OsMPK) silenced plants. In these rice plants, the reduced elicited level of JA correlates with the improved performance of SSB larvae, but does not produce any positive effects on BPH (Wang et al. 2013), indicating that JA-related defense mechanisms are more complex than expected.
Recently, it was found that Mediator Complex Subunit25 (MED25/PFT1) mediates JA signaling and plays important roles in resistance to necrotrophic fungal pathogens. The Mediator Complex builds a bridge between TFs and RNA Pol II so that RNA Pol II can interact with adjacent TFs. PHYTOCHROME AND FLOWERING TIME1 (PFT1) encodes the MED25 subunit of the plant Mediator. In Arabidopsis, MED25/PFT1 is necessary for JA-related defense gene expression, thus conferring resistance to the leaf-infecting fungi Alternaria brassicicola and Botrytis cinerea. However, pft1 mutant plants show increased resistance to the root infecting hemibiotroph, Fusarium oxysporum, accompanying the significant attenuation of the expression of some JA-responsive genes, suggesting that MED25/PFT1 mediates F. oxysporum-induced disease progression through JA signaling (Kidd et al. 2009). Functions of MED25 may be conserved in monocots as TaPFT1, a wheat homologue of PFT1, is able to complement the pft1/med25 mutation in Arabidopsis (Lyons et al. 2013). However, the role of rice OsPFT1, to our knowledge, is currently unknown. The rice homologue of AtMed25_1 displays similar transcript levels in the reproductive and vegetative stages as found in Arabidopsis (Mathur et al. 2011). Therefore, studies on OsPFT1/MED25 will mark a new insight into JA-related signaling and defense responses in rice.
The antagonistic functions of the AOS and HPL branches in the oxylipin pathway should also be mentioned. These two branches generate JA and GLVs, respectively. Depletion of the expression of OsHPL3 by mutation leads to the reduced level of E-2-hexenal, but the dramatic overproduction of JA, indicating that the disruption of the HPL pathway channels the substrates toward the JA pathway. This rice plant also showed the activation of JA-mediated defense responses in the resistance to the T1 strain of the bacterial blight Xoo is enhanced (Liu et al. 2012b). Studies on the OsHPL3 rice mutant also revealed the differential defense regulatory roles of JA and GLVs, as the loss of OsHPL3 function confers more resistance to the chewing herbivore SSB but more susceptibility to the phloem-feeding herbivore BPH. Indeed, OsHPL3 provides plants with resistance against BPH; however, it makes plants more susceptible to SSB and Xoo (Tong et al. 2012). Overall, the JA and HPL pathways are competing branches that provide plants with different defensive responses.
JA crosstalk with other hormones in rice
Previously, it was thought that JA and SA acted antagonistically upon pathogen infection and pest invasion throughout the plant kingdom. The antagonistic interaction of these two hormones can also be observed in rice plants. For example, in the OsWRKY13-mediated rice defense against bacterial blight and fungal blast, OsWRKY13 activates the SA-dependent signaling pathway and suppresses the JA-dependent signaling pathway. As a result, the expression of hormone-specific defense-related genes is differentially regulated (Qiu et al. 2007); In Arabidopsis, NPR1 regulates SA and JA antagonistically in response to invasion by Pseudomonas syringae pv tomato DC3000 (Spoel et al. 2003). The same cross-communicating signaling pathway is also conserved in rice plants, as the augmentation of the SA signal transduction pathway by OsNPR1 represses JA signaling pathway (Yuan et al. 2007). Further, JA and SA function antagonistically in OsPLD-mediated defense responses upon a SSB infestation of rice (Qi et al. 2011). However, synergistic JA-SA crosstalk was also found in rice. In the OsHPL3-mediated oxylipin pathway, JA and SA signaling were synergistically augmented in rice defenses against pathogens (Tong et al. 2012), although how SA signaling was activated remains to be elucidated. Therefore, the fine-tuning of overlapping signaling JA and SA pathways may be crucial for plant-specific defense responses.
GA and JA are considered to act antagonistically to adjust the balance of energy allocation between growth and defense. Upon pathogen or insect invasion, JA facilitates the interaction between the JA receptor COI1 and JAZ proteins, the repressors of JA-responsive genes. Consequently, the JAZ proteins are degraded through polyubiquitination, resulting in the initiation of JA defense responses. As JAZ proteins also inhibit DELLA-PIF interactions, a crucial step in GA signaling, the degradation of JAZ repressors strengthens the repression of PIF TFs by DELLA proteins, thus GA-promoted growth is suppressed. However, when JA signaling is down-regulated, JAZ proteins can effectively interfere with the DELLA-PIF interaction, allowing the release of the PIF TFs, which in turn promotes GA-mediated growth (Yang et al. 2012). Indeed, OsCOI1 knocked-down transgenic rice plants exhibit similar phenotypes to rice plants overproducing GA, and MeJA treatment facilitates the rice DELLA protein’s SLR1 accumulation and delays GA-regulated SLR1 degradation in wild-type rice plants (Yang et al. 2012). In addition, GA serves as a virulence factor of Xoo and Magnaporthe oryzae (Mo), and SLR1 is closely related to JA- and SA-dependent disease resistance pathways in rice (Filipe et al. 2014).
However, some preliminary studies revealed that a synergistic regulation by JA and GA in rice may exist. Under salt stress, treatment of rice plants with JA induces a higher accumulation of GA1 than that in the non-JA-treated control (Seo et al. 2005). In rice coleoptiles, there is a temporally high accumulation of thionin transcripts just after germination, followed by a gradual decline, and the level becomes undetectable in 3 days. Interestingly, the expression patterns of thionin genes paralleled those of key genes responsible for the biosynthesis of GA and BR, as was the change in the endogenous JA level. Furthermore, JA treatments exhibited similar effects as GA and BR co-treatments in suppressing the reduction of the thionin transcript level in the post-germination period (Kitanaga et al. 2006). These results strongly suggest that JA and GA act synergistically in rice under specific environmental conditions or at a specific developmental stage.
Generally, it was thought that the JA and ET defense pathways in plants play synergistic functions that counteract invasions by necrotrophic pathogens (Glazebrook 2005) and herbivorous insects (Howe and Jander 2008). However, recent studies revealed that the JA and ET pathways are involved in rice resistance against the obligate biotrophs, root knot nematodes (Nahar et al. 2011). The treatment of rice shoots with exogenous Me-JA and ethephon induced systemic resistance against M. graminicola in roots. Further investigations using ET-insensitive transgenic rice and JA mutant rice plants, in which the JA biosynthetic pathway is disrupted, as well as assays blocking JA or ET biosynthetic pathways through the exogenous application of JA or ET biosynthetic inhibitors, confirmed that ET-mediated systemic defenses to M. graminicola depends on the activation of the JA biosynthetic pathway. Indeed, treatments of rice shoots with ET induce high expression levels of genes responsible for JA biosynthesis and signaling in roots. These all indicate that a synergistic effect of JA and ET against biotrophic pathogens exists. Herbivore infestation experiments further revealed that OsNPR1 plays a negative role in the crosstalk between JA and ET signaling, as knocking down the OsNPR1 gene resulted in increased expression levels of the lipoxygenase gene OsHI-LOX and an ACC synthase gene OsACS2, as well as increased production of JA and ET, conferring rice plants more resistance against SSB (Li et al. 2013). Antagonistic actions between JA and ET, however, may occur when rice plants protect themselves from infection by bacterial Xoo. The knockout of a rice enhanced disease resistance 1 gene, OsEDR1, exhibits reduced expression levels of the ACC synthase gene family, a decreased production of ET, and an enhanced resistance against bacteria. However, the plants show an activation of JA- and SA-associated pathways, suggesting that OsEDR1 regulates the antagonistic interaction between the ET pathway and the JA or SA pathway (Shen et al. 2011).
The interaction between auxin and JA has been well studied in Arabidopsis. It was recognized that auxin promotes plant growth, whereas JA has an opposite function. In general, the interplay of these two hormones occurs at the levels of hormone perception, transport, and homeostasis, or through the interactions of their related regulatory proteins (Perez and Goossens 2013). However, only a few events of JA-auxin crosstalk have been reported in rice. One example is the gravitropism of rice coleoptiles driven by these two hormones. During the gravitropic curvature, a redistribution of auxin occurs, resulting in an auxin gradient, which triggers the differential growth of the upper and lower flanks of coleoptiles. Interestingly, a gradient of JA just opposite to that of auxin is also established and this JA gradient contributes to differential growth inhibition during the tropistic bending, suggesting that JA and auxin function antagonistically in response to gravitational stimulation (Hoffmann et al. 2011; Gutjahr et al. 2005).
As mentioned above, the expression patterns of thionin genes are correlated with GA, BR, and JA in rice coleoptiles just after germination, and BR and GA act synergistically with JA at this specific growth stage (Kitanaga et al. 2006). However, when rice plants are under attack by root-knot nematodes, BR and JA play antagonistic functions in response to the infection. For instance, the activation of the BR pathway in rice root systems makes the plants more susceptible to nematodes, whereas the exogenous foliar application of MeJA strongly suppresses the BR pathway in roots and activates the JA-dependent rice innate immunity against the pathogens. Additionally, the expression of JA biosynthesis and signaling genes are significantly up-regulated in BR-deficient mutants compared with in wild-type, confirming that BR and JA interact negatively in rice roots (Nahar et al. 2013).
The crosstalk between JA and ABA is complex, and either synergistic or antagonistic depending on the different regulatory mechanisms mediated by the two hormones. As mentioned above, when rice plants in the early stage of flowering suffer drought stress, the normal development of the spikelet was affected by the synergistic action between JA and ABA, resulting in a decrease in grain production (Kim et al. 2009). Another example of synergism between these two hormones is that treatment of rice plants with JA and ABA, which leads to similar expression patterns of OsCOI1, a key gene functioning as a JA signaling receptor, implying that the JA and ABA signaling pathways are overlapped. However, when rice plants are under migratory nematode attack or under saline stress, antagonism may occur between ABA and JA. A recent study revealed that the JA pathway is necessary in the rice defense against Hirschmanniella oryzae. However, ABA plays a negative role by antagonizing JA biosynthesis and the signaling pathway, thus making the rice plants more susceptible to the nematode (Nahar et al. 2012). ABA and JA may also interact negatively under saline conditions. It was reported that JA suppresses the ABA-mediated induction of Oslea3 expression, and JA and ABA play antagonistic regulatory effects on the expression of the salt-induced gene salT (Moons et al. 1997).
Plants not only capture light for photosynthesis, but also perceive specific light qualities and transmit these light signals to modify their growth and development in response to the environment. Light signals are converted to developmental cues mainly through the interactions between light and hormone signals. More and more evidence has revealed that phytohormones, such as auxin, JA, and GA, are involved in light/phytochrome-regulated growth. In recent years, the crosstalk between JA and light has attracted special interest (Kazan and Manners 2011). In Arabidopsis, various components of the JA pathway, such as COI1, JAZ, MYC2, and JAR1, were found to influence light-mediated responses. For instance, JAR1 acts as a jasmonate-conjugating enzyme. The jar1-1 mutant, with the substitution of Phe for the conserved Ser-101 in the open reading frame of JAR1, exhibits a long-hypocotyl phenotype under weak far red light (Wang et al. 2011). Similarly, the coleoptiles of the rice Osjar1 mutant grew longer than those of the wild-type under continuous far red light, indicating that interference of the JA pathway in rice results in an altered sensitivity to far red light (Riemann et al. 2008). Although it has long been recognized that red light induces inhibition of rice coleoptile elongation (Furuya et al. 1969), the elongation of coleoptiles was not inhibited by irradiation with red light in the mutant hebiba in which OsAOC, an early gene in JA biosynthesis pathway, is impaired (Riemann et al. 2003), indicating that JA is involved in the light-mediated inhibition of coleoptile elongation. Another study revealed that the JA content increases and the expression of a key gene responsible for JA synthesis, OsOPR, is activated in response to red light irradiation; however, the red light-induced expression of OsOPR was eliminated in hebiba (Riemann et al. 2003). This implies that the JA deficiency is associated with light-mediated phenotypes in this mutant.
In addition, the transcription of OsAOS1, another key gene in JA biosynthesis, is enhanced by red light in a phytochrome-mediated manner in rice seedlings (Haga and Iino 2004), revealing that phytochromes play key roles in the connection between light and the JA pathway. The involvement of phytochromes, such as PHYA and PHYB, in the JA-light crosstalk can also be demonstrated from the further assays on OsJAR1 since the expression of this gene is down-regulated in both phyA and phyB rice mutants and completely eliminated in the phyA phyB double mutant (Riemann et al. 2008). Another study in hebiba revealed that the photodestruction of phyA is delayed in this mutant; however, exogenous applications of MeJA accelerate the phyA degradation upon light activation (Riemann et al. 2009). A differential display screen between hebiba and wild-type rice also led to the identification of a JA-induced gene, GER1, which is redundantly controlled by PhyA and PhyB under red light (Riemann et al. 2007). Blue light is also thought to interact with the JA pathway since it induces the expression of OsAOS1 in a cryptochrome (Oscry1a and Oscry1b)-mediated manner, resulting in the inhibition of rice coleoptile growth (Hirose et al. 2006).
JA-light crosstalk may also play a role in the JA-mediated defense against blast fungi in rice. Evidence revealed that the phyA phyB phyC triple mutant exhibits an increased susceptibility to M. grisea due to the down-regulation of the JA-responsive defense gene PR1b (Xie et al. 2011).
Although most discoveries concerning the JA pathway and JA functions are from studies of the dicotyledonous model plant A. thaliana, recent endeavors have revealed that the functions of JA in rice, an important crop for human beings, are versatile. In rice, it regulates flower development and fertility, seed germination, root system development, shoot growth, leaf senescence, spikelet development, photomorphogenesis, and gravitropism as well as mediating responses to abiotic and biotic stresses. In general, the JA pathway interacts with the pathways of other hormones to compose a complex regulatory network. Both synergistic and antagonistic crosstalk exists between JA and other hormones, indicating that the fine-tuning of the JA pathway is necessary in rice plants so that the proper physiological activities can be implemented. It should be noted that some of the reports on the JA pathway in rice are still preliminary and efforts should be made to identify new components involved in the JA regulatory pathway.
This work is supported by grants from the Key Bioengineering Discipline of Hebei Province, the Project for Improvement of Integrated Strength of Universities in Central and Western Areas of China (Plant diversity and resources utilization), the Cutting-edge and Characteristic Disciplines of Biology (Botany), the Scientific Research Foundation for the Returned Overseas Chinese Scholars by State Education Ministry of China (No. 2011–1139), National Nature Science Foundation of China (No. 31371693, 31201199 and 30800682), Nature Science Foundation of Shandong Province (No. ZR2013CL013), and the Open Foundation of State Key Laboratory of Rice Biology (No. 120201).
- Acosta IF, Laparra H, Romero SP, Schmelz E, Hamberg M, Mottinger JP, Moreno MA, Dellaporta SL (2009) Tasselseed1 is a lipoxygenase affecting jasmonic acid signaling in sex determination of maize. Science 323:262–265PubMedView ArticleGoogle Scholar
- Bae HK, Kang HG, Kim GJ, Eu HJ, Oh SA, Song JT, Chung IK, Eun MY, Park SK (2010) Transgenic rice plants carrying RNA interference constructs of AOS (allene oxide synthase) genes show severe male sterility. Plant Breeding 129:647–651View ArticleGoogle Scholar
- Bargmann BOR, Laxalt AM, ter Riet B, van Schooten B, Merquiol E, Testerink C, Haring MA, Bartels D, Munnik T (2009) Multiple PLDs required for high salinity and water deficit tolerance in plants. Plant Cell Physiol 50:78–89PubMed CentralPubMedView ArticleGoogle Scholar
- Borghetti F, Noda FN, de Sa CM (2002) Possible involvement of proteasome activity in ethylene-induced germination of dormant sunflower embryos. Braz J Plant Physiol 14:125–131View ArticleGoogle Scholar
- Brodersen P, Petersen M, Bjørn Nielsen H, Zhu S, Newman MA, Shokat KM, Rietz S, Parker J, Mundy J (2006) Arabidopsis MAP kinase 4 regulates salicylic acid- and jasmonic acid/ethylene-dependent responses via EDS1 and PAD4. Plant J 47:532–546PubMedView ArticleGoogle Scholar
- Browse J (2009a) Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol 60:183–205PubMedView ArticleGoogle Scholar
- Browse J (2009b) The power of mutants for investigating jasmonate biosynthesis and signaling. Phytochemistry 70:1539–1546PubMedView ArticleGoogle Scholar
- Cai Q, Yuan Z, Chen M, Yin C, Luo Z, Zhao X, Liang W, Hu J, Zhang D (2014) Jasmonic acid regulates spikelet development in rice. Nat Commun 5:3476, Doi: 10.1038/ncomms4476PubMedGoogle Scholar
- Chauvin A (2014) A 13-LOX hierarchy for defence in Arabidopsis thaliana. Dissertation. Genève, Switzerland: University of GenèveGoogle Scholar
- Chauvin A, Caldelari D, Wolfender JL, Farmer EE (2013) Four 13-lipoxygenases contribute to rapid jasmonate synthesis in wounded Arabidopsis thaliana leaves: a role for lipoxygenase 6 in responses to long-distance wound signals. 197:566–575Google Scholar
- Chehab EW, Perea JV, Gopalan B, Theg S, Dehesh K (2007) Oxylipin pathway in rice and Arabidopsis. J Integr Plant Biol 49:43–51View ArticleGoogle Scholar
- Chen IC, Huang IC, Liu MJ, Wang ZG, Chung SS, Hsieh HL (2007) Glutathione S-transferase interacting with far-red insensitive 219 is involved in phytochrome A-mediated signaling in Arabidopsis. Plant Physiol 143:1189–1202PubMed CentralPubMedView ArticleGoogle Scholar
- Chen Q, Sun J, Zhai Q, Zhou W, Qi L, Xu L, Wang B, Chen R, Jiang H, Qi J, Li X, Palme K, Li C (2011) The basic helix-loop-helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis. Plant Cell 23:3335–3352PubMed CentralPubMedView ArticleGoogle Scholar
- Cho K, Agrawal GK, Shibato J, Jung YH, Kim YK, Nahm BH, Jwa NS, Tamogami S, Han O, Kohda K, Iwahashi H, Rakwal R (2007) Survey of differentially expressed proteins and genes in jasmonic acid treated rice seedling shoot and root at the proteomics and transcriptomics levels. J Proteome Res 6:3581–3603PubMedView ArticleGoogle Scholar
- Chung HS, Koo AJK, Gao X, Jayanty S, Thines B, Jones AD, Howe GA (2008) Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory. Plant Physiol 146:952–964PubMed CentralPubMedView ArticleGoogle Scholar
- Dave A, Hernandez ML, He Z, Andriotis VM, Vaistij FE, Larson TR, Graham IA (2011) 12-oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis. Plant Cell 23:583–599PubMed CentralPubMedView ArticleGoogle Scholar
- De Smet I, Vanneste S, Inze D, Beeckman T (2006) Lateral root initiation or the birth of a new meristem. Plant Mol Biol 60:871–887PubMedView ArticleGoogle Scholar
- Du H, Liu H, Xiong L (2013) Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice. Front Plant Sci 4:397PubMed CentralPubMedView ArticleGoogle Scholar
- Filipe O, Seifi HS, Hofte M, Vleesschauwer DD (2014) The rice DELLA protein SLR1 integrates and amplifies salicylic acid- and jasmonic acid-dependent immunity. In: Abstracts of the XVI International Congress on Molecular Plant-Microbe Interactions, Rhodes, Greece, 6–10 July 2014Google Scholar
- Furuya M, Pjon CJ, Fujii T, Ito M (1969) Phytochrome action in Oryza sativa L. III. the separation of photoperceptive site and growing zone in coleoptiles, and auxin transport as effector system. Dev Growth Differ 11:62–76PubMedView ArticleGoogle Scholar
- Gardiner J, Collings DA, Harper JD, Marc J (2003) The effects of the phospholipase D-antagonist 1-butanol on seedling development and microtubule organisation in Arabidopsis. Plant Cell Physiol 44:687–696PubMedView ArticleGoogle Scholar
- Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227PubMedView ArticleGoogle Scholar
- Gutjahr C, Riemann M, Muller A, Duchting P, Weiler EW, Nick P (2005) Cholodny-Went revisited: a role for jasmonate in gravitropism of rice coleoptiles. Planta 222:575–585PubMedView ArticleGoogle Scholar
- Haga K, Iino M (2004) Phytochrome-mediated transcriptional up-regulation of ALLENE OXIDE SYNTHASE in rice seedlings. Plant Cell Physiol 45:119–128PubMedView ArticleGoogle Scholar
- Hirose F, Shinomura T, Tanabata T, Shimada H, Takano M (2006) Involvement of rice cryptochromes in de-etiolation responses and flowering. Plant Cell Physiol 47:915–925PubMedView ArticleGoogle Scholar
- Hoffmann M, Hentrich M, Pollmann S (2011) Auxin-oxylipin crosstalk: relationship of antagonists. J Integr Plant Biol 53:429–445PubMedView ArticleGoogle Scholar
- Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66PubMedView ArticleGoogle Scholar
- Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K (2000) Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J 24:655–665PubMedView ArticleGoogle Scholar
- Jiang J, Li J, Xu Y, Han Y, Bai Y, Zhou G, Lou Y, Xu Z, Chong K (2007) RNAi knockdown of Oryza sativa root meander curling gene led to altered root development and coiling which were mediated by jasmonic acid signalling in rice. Plant Cell Environ 30:690–699PubMedView ArticleGoogle Scholar
- Kang DJ, Seo YJ, Lee JD, Ishii R, Kim KU, Shin DH, Park SK, Jang SW, Lee IJ (2005) Jasmonic acid differentially affects growth, ion uptake and abscisic acid concentration in salt-tolerant and salt-sensitive rice cultivars. J Agron Crop Sci 191:273–282View ArticleGoogle Scholar
- Kang JH, Wang L, Giri A, Baldwin IT (2006) Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairs jasmonic acid–isoleucine-mediated defenses against Manduca sexta. Plant Cell 18:3303–3320PubMed CentralPubMedView ArticleGoogle Scholar
- Katsir L, Chung HS, Koo AJ, Howe GA (2008) Jasmonate signaling: a conserved mechanism of hormone sensing. Curr Opin Plant Biol 11:428–435PubMed CentralPubMedView ArticleGoogle Scholar
- Kazan K, Manners JM (2011) The interplay between light and jasmonate signaling during defence and development. J Exp Bot 62:4087–4100PubMedView ArticleGoogle Scholar
- Kidd BN, Edgar CI, Kumar KK, Aitken EA, Schenk PM, Manners JM, Kazan K (2009) The mediator complex subunit PFT1 is a key regulator of jasmonate-dependent defense in Arabidopsis. Plant Cell 21:2237–2252PubMed CentralPubMedView ArticleGoogle Scholar
- Kim EH, Kim YS, Park SH, Koo YJ, Choi YD, Chung YY, Lee IJ, Kim JK (2009) Methyl jasmonate reduces grain yield by mediating stress signals to alter spikelet development in rice. Plant Physiol 149:1751–1760PubMed CentralPubMedView ArticleGoogle Scholar
- Kitanaga Y, Jian C, Hasegawa M, Yazaki J, Kishimoto N, Kikuchi S, Nakamura H, Ichikawa H, Asami T, Yoshida S, Yamaguchi I, Suzuki Y (2006) Sequential regulation of gibberellin, brassinosteroid, and jasmonic acid biosynthesis occurs in rice coleoptiles to control the transcript levels of anti-microbial thionin genes. Biosci Biotechnol Biochem 70:2410–2419PubMedView ArticleGoogle Scholar
- Krinke O, Flemr M, Vergnolle C, Collin S, Renou JP, Taconnat L, Yu A, Burketová L, Valentová O, Zachowski A, Ruelland E (2009) Phospholipase D activation is an early component of the salicylic acid signaling pathway in Arabidopsis cell suspensions. Plant Physiol 150:424–436PubMed CentralPubMedView ArticleGoogle Scholar
- Lee DE, Back K (2005) Ectopic expression of MAP kinase inhibits germination and seedling growth in transgenic rice. Plant Growth Regul 45:251–257View ArticleGoogle Scholar
- Li R, Afsheen S, Xin Z, Han X, Lou Y (2013) OsNPR1 negatively regulates herbivore-induced JA and ethylene signaling and plant resistance to a chewing herbivore in rice. Physiol Plant 147:340–351PubMedView ArticleGoogle Scholar
- Liu PP, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52:133–146PubMedView ArticleGoogle Scholar
- Liu G, Tian H, Huang YQ, Hu J, Ji YX, Li SQ, Guo L, Feng YQ, Zhu YG (2012a) Alterations of mitochondrial protein assembly and jasmonic acid biosynthesis pathway in Honglian (HL)-type cytoplasmic male sterility rice. J Bio Chem 287:40051–40060View ArticleGoogle Scholar
- Liu X, Li F, Tang J, Wang W, Zhang F, Wang G, Chu J, Yan C, Wang T, Chu C, Li C (2012b) Activation of the jasmonic acid pathway by depletion of the hydroperoxide lyase OsHPL3 reveals crosstalk between the HPL and AOS branches of the oxylipin pathway in rice. PLoS One 7(11):e50089PubMed CentralPubMedView ArticleGoogle Scholar
- Lyons R, Manners JM, Kazan K (2013) Jasmonate biosynthesis and signaling in monocots: a comparative overview. Plant Cell Rep 32:815–827PubMedView ArticleGoogle Scholar
- Mathur S, Vyas S, Kapoor S, Tyagi AK (2011) The mediator complex in plants: structure, phylogeny, and expression profiling of representative genes in a dicot (Arabidopsis) and a monocot (rice) during reproduction and abiotic stress. Plant Physiol 157:1609–1627PubMed CentralPubMedView ArticleGoogle Scholar
- Mei C, Qi M, Sheng G, Yang Y (2006) Inducible overexpression of a rice allene oxide synthase gene increases the endogenous jasmonic acid level, PR gene expression, and host resistance to fungal infection. Mol Plant Microbe Interact 19:1127–1137PubMedView ArticleGoogle Scholar
- Melotto M, Mecey C, Niu Y, Chung HS, Katsir L, Yao J, Zeng W, Thines B, Staswick P, Browse J, Howe GA, He SY (2008) A critical role of two positively charged amino acids in the Jas motif of Arabidopsis JAZ proteins in mediating coronatine- and jasmonoyl isoleucine-dependent interactions with the COI1 F-box protein. Plant J 55:979–988PubMed CentralPubMedView ArticleGoogle Scholar
- Miransari M, Smith DL (2014) Plant hormones and seed germination. Environ Exp Bot 99:110–121View ArticleGoogle Scholar
- Moons A, Prinsen E, Bauw G, Van Montagu M (1997) Antagonistic effects of abscisic acid and jasmonates on salt stress inducible transcripts in rice roots. Plant Cell 9:2243–2259PubMed CentralPubMedView ArticleGoogle Scholar
- Motes CM, Pechter P, Yoo CM, Wang YS, Chapman KD, Blancaflor EB (2005) Differential effects of two phospholipase D inhibitors, 1-butanol and N-acylethanolamine, on in vivo cytoskeletal organization and Arabidopsis seedling growth. Protoplasma 226:109–123PubMedView ArticleGoogle Scholar
- Nahar K, Kyndt T, De Vleesschauwer D, Hofte M, Gheysen G (2011) The jasmonate pathway is a key player in systemically induced defense against root knot nematodes in rice. Plant Physiol 157:305–316PubMed CentralPubMedView ArticleGoogle Scholar
- Nahar K, Kyndt T, Nzogela YB, Gheysen G (2012) Abscisic acid interacts antagonistically with classical defense pathways in rice-migratory nematode interaction. New Phytol 196:901–913PubMedView ArticleGoogle Scholar
- Nahar K, Kyndt T, Hause B, Höfte M, Gheysen G (2013) Brassinosteroids suppress rice defense against root-knot nematodes through antagonism with the jasmonate pathway. Mol Plant Microbe Interact 26:106–115PubMedView ArticleGoogle Scholar
- Pajerowska-Mukhtar KM, Mukhtar MS, Guex N, Halim VA, Rosahl S, Somssich IE, Gebhardt C (2008) Natural variation of potato allene oxide synthase 2 causes differential levels of jasmonates and pathogen resistance in Arabidopsis. Planta 228:293–306PubMed CentralPubMedView ArticleGoogle Scholar
- Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655PubMed CentralPubMedView ArticleGoogle Scholar
- Park JH, Halitschke R, Kim HB, Baldwin IT, Feldmann KA, Feyereisen R (2002) A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant J 31:1–12PubMedView ArticleGoogle Scholar
- Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295PubMedView ArticleGoogle Scholar
- Peng X, Hu Y, Tang X, Zhou P, Deng X, Wang H, Guo Z (2012) Constitutive expression of rice WRKY30 gene increases the endogenous jasmonic acid accumulation, PR gene expression and resistance to fungal pathogens in rice. Planta 236:1485–1498PubMedView ArticleGoogle Scholar
- Perez AC, Goossens A (2013) Jasmonate signalling: a copycat of auxin signalling? Plant Cell Environ 36:2071–2084PubMedView ArticleGoogle Scholar
- Petersen M, Brodersen P, Naested H, Andreasson E, Lindhart U, Johansen B, Nielsen HB, Lacy M, Austin MJ, Parker JE, Sharma SB, Klessig DF, Martienssen R, Mattsson O, Jensen AB, Mundy J (2000) Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell 103:1111–1120PubMedView ArticleGoogle Scholar
- Qi J, Zhou G, Yang L, Erb M, Lu Y, Sun X, Cheng J, Lou Y (2011) The chloroplast-localized phospholipases D α4 and α5 regulate herbivore-induced direct and indirect defenses in rice. Plant Physiol 157:1987–1999PubMed CentralPubMedView ArticleGoogle Scholar
- Qiu D, Xiao J, Ding X, Xiong M, Cai M, Cao Y, Li X, Xu C, Wang S (2007) OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. Mol Plant Microbe Interact 20:492–499PubMedView ArticleGoogle Scholar
- Raya-González J, Pelagio-Flores R, López-Bucio J (2012) The jasmonate receptor COI1 plays a role in jasmonate-induced lateral root formation and lateral root positioning in Arabidopsis thaliana. J Plant Physiol 169:1348–1358PubMedView ArticleGoogle Scholar
- Riemann M, Muller A, Korte A, Furuya M, Weiler EW, Nick P (2003) Impaired induction of the jasmonate pathway in the rice mutant hebiba. Plant Physiol 133:1820–1830PubMed CentralPubMedView ArticleGoogle Scholar
- Riemann M, Gutjahr C, Korte A, Riemann M, Danger B, Muramatsu T, Bayer U, Waller F, Furuya M, Nick P (2007) GER1, a GDSL motif-encoding gene from rice is a novel early light- and jasmonate-induced gene. Plant Biol 9:32–40PubMedView ArticleGoogle Scholar
- Riemann M, Riemann M, Takano M (2008) Rice JASMONATE RESISTANT 1 is involved in phytochrome and jasmonate signalling. Plant Cell Environ 31:783–792PubMedView ArticleGoogle Scholar
- Riemann M, Bouyer D, Hisada A, Müller A, Yatou O, Weiler EW, Takano M, Furuya M, Nick P (2009) Phytochrome A requires jasmonate for photodestruction. Planta 229:1035–1045PubMedView ArticleGoogle Scholar
- Riemann M, Haga K, Shimizu T, Okada K, Ando S, Mochizuki S, Nishizawa Y, Yamanouchi U, Nick P, Yano M, Minami E, Takano M, Yamane H, Iino M (2013) Identification of rice Allene Oxide Cyclase mutants and the function of jasmonate for defence against Magnaporthe oryzae. Plant J 74:226–238PubMedView ArticleGoogle Scholar
- Robson F, Okamota H, Patrick E, Harris SR, Wasternack C, Brearley C, Turner JG (2010) Jasmonate and phytochrome A signaling in Arabidopsis wound and shade responses are integrated through JAZ1 stability. Plant Cell 22:1143–1160PubMed CentralPubMedView ArticleGoogle Scholar
- Santino A, Taurino M, De Nomenico S, Bonsegna S, Poltronieri P, Pastor V, Flors V (2013) Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. Plant Cell Rep 32:1085–1098PubMedView ArticleGoogle Scholar
- Schaller A, Stintzi A (2009) Enzymes in jasmonate biosynthesis - structure, function, regulation. Phytochemistry 70:1532–1538PubMedView ArticleGoogle Scholar
- Schluttenhofer C, Pattanaik S, Patra B, Yuan L (2014) Analyses of Catharanthus roseus and Arabidopsis thaliana WRKY transcription factors reveal involvement in jasmonate signaling. BMC Genomics 15:502PubMed CentralPubMedView ArticleGoogle Scholar
- Seo HS, Kim SK, Jang SW, Choo YS, Sohn EY, Lee IJ (2005) Effect of jasmonic acid on endogenous gibberellins and abscisic acid in rice under NaCl stress. Biol Plantarum 49:447–450View ArticleGoogle Scholar
- Seo JS, Joo J, Kim MJ, Kim YK, Nahm BH, Song SI, Cheong JJ, Lee JS, Kim JK, Choi YD (2011) OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J 65:907–921PubMedView ArticleGoogle Scholar
- Shen X, Liu H, Yuan B, Li X, Xu C, Wang S (2011) OsEDR1 negatively regulates rice bacterial resistance via activation of ethylene biosynthesis. Plant Cell Environ 34:179–191PubMedView ArticleGoogle Scholar
- Shen H, Liu C, Zhang Y, Meng X, Zhou X, Chu C, Wang X (2012) OsWRKY30 is activated by MAP kinases to confer drought tolerance in rice. Plant Mol Biol 80:241–253PubMedView ArticleGoogle Scholar
- Spoel SH, Koornneef A, Claessens SM, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Metraux JP, Brown R, Kazan K, Van Loon LC, Dong XN, Pieterse CM (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770PubMed CentralPubMedView ArticleGoogle Scholar
- Staswick PE, Su W, Howell SH (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci U S A 89:6837–6840PubMed CentralPubMedView ArticleGoogle Scholar
- Staswick PE, Yuen GY, Lehman CC (1998) Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare. Plant J 15:747–754PubMedView ArticleGoogle Scholar
- Stein E, Molitor A, Kogel KH, Waller F (2008) Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1. Plant Cell Physiol 49:1747–1751PubMedView ArticleGoogle Scholar
- Stumpe M, Göbel C, Faltin B, Beike AK, Hause B, Himmelsbach K, Bode J, Kramell R, Wasternack C, Frank W, Reski R, Feussner I (2010) The moss Physcomitrella patens contains cyclopentenones but no jasmonates: mutations in allene oxide cyclase lead to reduced fertility and altered sporophyte morphology. New Phytol 188:740–749PubMedView ArticleGoogle Scholar
- Sun J, Xu Y, Ye S, Jiang H, Chen Q, Liu F, Zhou W, Chen R, Li X, Tietz O, Wu X, Cohen JD, Palme K, Li C (2009) Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation. Plant Cell 21:1495–1511PubMed CentralPubMedView ArticleGoogle Scholar
- Svyatyna K, Riemann M (2012) Light-dependent regulation of the jasmonate pathway. Protoplasma 249(Suppl 2):S137–S145PubMedView ArticleGoogle Scholar
- Tang RS, Wang H, Cao XZ (2002) Effects of methyl jasmonate on the seed germinating and the growth of rice seedling. Acta Agronomic Sinica 28:333–338Google Scholar
- Tani T, Sobajima H, Okada K, Chujo T, Arimura S, Tsutsumi N, Nishimura M, Seto H, Nojiri H, Yamane H (2008) Identification of the OsOPR7 gene encoding 12-oxophytodienoate reductase involved in the biosynthesis of jasmonic acid in rice. Planta 227:517–526PubMedView ArticleGoogle Scholar
- Taniguchi S, Hosokawa-Shinonaga Y, Tamaoki D, Yamada S, Akimitsu K, Gomi K (2014) Jasmonate induction of the monoterpene linalool confers resistance to rice bacterial blight and its biosynthesis is regulated by JAZ protein in rice. Plant Cell Environ 37:451–461PubMedView ArticleGoogle Scholar
- Tao Z, Liu H, Qiu D, Zhou Y, Li X, Xu C, Wang S (2009) A pair of allelic WRKY genes play opposite roles in rice-bacteria interactions. Plant Physiol 151:936–948PubMed CentralPubMedView ArticleGoogle Scholar
- Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during JA signalling. Nature 448:661–665PubMedView ArticleGoogle Scholar
- Toda Y, Tanaka M, Ogawa D, Kurata K, Kurotani K, Habu Y, Ando T, Sugimoto K, Mitsuda N, Katoh E, Abe K, Miyao A, Hirochika H, Hattori T, Takeda S (2013) Rice salt sensitive3 forms a ternary complex with JAZ and class-C bHLH factors and regulates jasmonate-induced gene expression and root cell elongation. Plant Cell 25:1709–1725PubMed CentralPubMedView ArticleGoogle Scholar
- Tong X, Qi J, Zhu X, Mao B, Zeng L, Wang B, Li Q, Zhou G, Xu X, Lou Y, He Z (2012) The rice hydroperoxide lyase OsHPL3 functions in defense responses by modulating the oxylipin pathway. Plant J 71:763–775PubMedView ArticleGoogle Scholar
- Toyoda K, Kawanishi Y, Kawamoto Y, Kurihara C, Yamagishi N, Tamura A, Yoshikawa N, Inagaki Y, Ichinose Y, Shiraishi T (2013) Suppression of mRNAs for lipoxygenase (LOX), allene oxide synthase (AOS), allene oxide cyclase (AOC) and 12-oxo-phytodienoic acid reductase (OPR) in pea reduces sensitivity to the phytotoxin coronatine and disease development by Mycosphaerella pinodes. J Gen Plant Pathol 79:321–334View ArticleGoogle Scholar
- Tsai FY, Hung KT, Kao CH (1996) An increase in ethylene sensitivity is associated with jasmonate-promoted senescence of detached rice leaves. J Plant Growth Regul 15:197–200View ArticleGoogle Scholar
- Tsai FY, Lin CC, Kao CH (1997) A comparative study of the effects of abscisic acid and methyl jasmonate on seedling growth of rice. Plant Growth Regul 21:37–42View ArticleGoogle Scholar
- Vleesschauwer DD, Gheysen G, Hofte M (2013) Hormone defense networking in rice: tales from a different world. Trends Plant Sci 18:555–565PubMedView ArticleGoogle Scholar
- Wakuta S, Suzuki E, Saburi W, Matsuura H, Nabeta K, Imai R, Matsui H (2011) OsJAR1 and OsJAR2 are jasmonyl-L-isoleucine synthases involved in wound- and pathogen-induced jasmonic acid signalling. Biochem Biophys Res Commun 409:634–639PubMedView ArticleGoogle Scholar
- Wang C, Zien CA, Afitlhile M, Welti R, Hildebrand DF, Wang X (2000) Involvement of phospholipase D in wound-induced accumulation of jasmonic acid in arabidopsis. Plant Cell 12:2237–2246PubMed CentralPubMedView ArticleGoogle Scholar
- Wang R, Shen W, Liu L, Jiang L, Liu Y, Su N, Wan J (2008) A novel lipoxygenase gene from developing rice seeds confers dual position specificity and responds to wounding and insect attack. Plant Mol Biol 66:401–414PubMedView ArticleGoogle Scholar
- Wang JG, Chen CH, Chien CT, Hsieh HL (2011) FAR-RED INSENSITIVE219 modulates CONSTITUTIVE PHOTOMORPHOGENIC1 activity via physical interaction to regulate hypocotyl elongation in Arabidopsis. Plant Physiol 156:631–646PubMed CentralPubMedView ArticleGoogle Scholar
- Wang Q, Li J, Hu L, Zhang T, Zhang G, Lou Y (2013) OsMPK3 positively regulates the JA signaling pathway and plant resistance to a chewing herbivore in rice. Plant Cell Rep 32:1075–1084PubMedView ArticleGoogle Scholar
- Wang H, Xu Q, Kong YH, Chen Y, Duan JY, Wu WH, Chen YF (2014) Arabidopsis WRKY45 transcription factor activates phosphate transporter1;1 expression in response to phosphate starvation. Plant Physiol 164:2020–2029PubMed CentralPubMedView ArticleGoogle Scholar
- Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. an update to the 2007 review in annals of botany. Ann Bot 111:1021–1058PubMed CentralPubMedView ArticleGoogle Scholar
- Wilen RW, van Rooijen GJ, Pearce DW, Pharis RP, Holbrook LA, Moloney MM (1991) Effects of jasmonic acid on embryo-specific processes in Brassica and Linum oilseeds. Plant Physiol 95:399–405PubMed CentralPubMedView ArticleGoogle Scholar
- Xie XZ, Xue YJ, Zhou JJ, Zhang B, Chang H, Takano M (2011) Phytochromes regulate SA and JA signaling pathways in rice and are required for developmentally controlled resistance to Magnaporthe grisea. Mol Plant 4:688–696PubMedView ArticleGoogle Scholar
- Yamada S, Kano A, Tamaoki D, Miyamoto A, Shishido H, Miyoshi S, Taniguchi S, Akimitsu K, Gomi K (2012) Involvement of OsJAZ8 in jasmonate-induced resistance to bacterial blight in rice. Plant Cell Physiol 53:2060–2072PubMedView ArticleGoogle Scholar
- Yang DL (2009) The phytohormonal signaling pathways in rice immune responses and Jasmonate signaling pathway represses gibberellin signaling pathway. Dissertation. Beijing, China: Chinese Academy of SciencesGoogle Scholar
- Yang DL, Yao J, Mei CS, Tong XH, Zeng LJ, Li Q, Xiao LT, Sun TP, Li J, Deng XW, Lee CM, Thomashow MF, Yang Y, He Z, He SY (2012) Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc Natl Acad Sci U S A 109:E1192–E1200PubMed CentralPubMedView ArticleGoogle Scholar
- Yang DL, Yang Y, He Z (2013) Roles of plant hormones and their interplay in rice immunity. Mol Plant 6:675–685PubMedView ArticleGoogle Scholar
- Ye N, Zhang J (2012) Antagonism between abscisic acid and gibberellins is partially mediated by ascorbic acid during seed germination in rice. Plant Signal Behav 7:563–565PubMed CentralPubMedView ArticleGoogle Scholar
- Yoshii M, Shimizu T, Yamazaki M, Higashi T, Miyao A, Hirochika H, Omura T (2008) Disruption of a novel gene for a NAC-domain protein in rice confers resistance to Rice dwarf virus. Plant J 57:615–625PubMedView ArticleGoogle Scholar
- Yoshii M, Yamazaki M, Rakwal R, Kishi-Kaboshi M, Miyao A, Hirochika H (2010) The NAC transcription factor RIM1 of rice is a new regulator of jasmonate signaling. Plant J 61:804–815PubMedView ArticleGoogle Scholar
- Yuan Y, Zhong S, Li Q, Zhu Z, Lou Y, Wang L, Wang J, Wang M, Li Q, Yang D, He Z (2007) Functional analysis of rice NPR1-like genes reveals that OsNPR1/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility. Plant Biotechnol J 5:313–324PubMedView ArticleGoogle Scholar
- Zhang S, Cai Z, Wang X (2009) The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling. Proc Natl Acad Sci U S A 1106:4543–4548View ArticleGoogle Scholar
- Zheng J, Zou X, Mao Z, Xie B (2011) A novel pepper (Capsicum annuum L.) WRKY gene, CaWRKY30, is involved in pathogen stress responses. J Plant Biol 54:329–337View ArticleGoogle Scholar
- Zhou QY, Tian AG, Zou HF, Xie ZM, Lei G, Huang J, Wang CM, Wang HW, Zhang JS, Chen SY (2008) Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnol J 6:486–503PubMedView ArticleGoogle Scholar
- Zhou G, Qi J, Ren N, Cheng J, Erb M, Mao B, Lou Y (2009) Silencing OsHI-LOX makes rice more susceptible to chewing herbivores, but enhances resistance to a phloem feeder. Plant J 60:638–648PubMedView ArticleGoogle Scholar
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited.