Regulation and integration of plant jasmonate signaling: a comparative view of monocot and dicot

The phytohormone jasmonate plays a pivotal role in various aspects of plant life, including developmental programs and defense against pests and pathogens. A large body of knowledge on jasmonate biosynthesis, signal transduction as well as its functions in diverse plant processes has been gained in the past two decades. In addition, there exists extensive crosstalk between jasmonate pathway and other phytohormone pathways, such as salicylic acid(SA) and gibberellin(GA), in co-regulation of plant...     

Abscisic acid negatively modulates plant defence against rice black‐streaked dwarf virus infection by suppressing the jasmonate pathway and regulating reactive oxygen species levels in rice

Abscisic acid (ABA) plays a multifaceted role in plant immunity and can either increase resistance or increase susceptibility to some bacterial and fungal pathogens depending on the pathosystem. ABA is also known to mediate plant defence to some viruses. In this study, the relationship between the ABA pathway and rice black‐streaked dwarf virus (RBSDV) was investigated in rice. The expression of ABA pathway genes was significantly reduced upon RBSDV infection. Application of exogenous hormones and various ABA pathway mutants revealed that the ABA pathway plays a negative role in rice defence against RBSDV. Exogenous hormone treatment and virus inoculation showed that ABA inhibits the jasmonate‐mediated resistance to RBSDV. ABA treatment also suppressed accumulation of reactive oxygen species by inducing the expression of superoxidase dismutases and catalases. Thus, ABA modulates the rice–RBSDV interaction by suppressing the jasmonate pathway and regulating reactive oxygen species levels. This is the first example of ABA increasing susceptibility to a plant virus.     

Jasmonate-dependent induction of indole glucosinolates in Arabidopsis by culture filtrates of the nonspecific pathogen Erwinia carotovora

Elicitors from the plant pathogen Erwinia carotovora trigger coordinate induction of the tryptophan (Trp) biosynthesis pathway and Trp oxidizing genes in Arabidopsis. To elucidate the biological role of such pathogen-induced activation we characterized the production of secondary defense metabolites such as camalexin and indole glucosinolates derived from precursors of this pathway. Elicitor induction was followed by a specific increase in 3-indolylmethylglucosinolate (IGS) content, but only a barely detectable accumulation of the indole-derived phytoalexin camalexin. The response is mediated by jasmonic acid as shown by lack of IGS induction in the jasmonate-insensitive mutant coi1-1. In accordance with this, methyl jasmonate was able to trigger IGS accumulation in Arabidopsis. In contrast, ethylene and salicylic acid seem to play a minor role in the response. They did not trigger alterations in IGS levels, and methyl jasmonate- or elicitor-induced IGS accumulation in NahG and ethylene-insensitive ein2-1 mutant plants was similar as in the wild type. The breakdown products of IGS and other glucosinolates were able to inhibit growth of E. carotovora. The results suggest that IGS is of importance in the defense against bacterial pathogens.     

Heterotrimeric G proteins facilitate Arabidopsis resistance to necrotrophic pathogens and are involved in jasmonate signaling

Heterotrimeric G proteins have been previously linked to plant defense; however a role for the Gbetagamma dimer in defense signaling has not been described to date. Using available Arabidopsis (Arabidopsis thaliana) mutants lacking functional Galpha or Gbeta subunits, we show that defense against the necrotrophic pathogens Alternaria brassicicola and Fusarium oxysporum is impaired in Gbeta-deficient mutants while Galpha-deficient mutants show slightly increased resistance compared to wild-type Columbia ecotype plants. In contrast, responses to virulent (DC3000) and avirulent (JL1065) strains of Pseudomonas syringae appear to be independent of heterotrimeric G proteins. The induction of a number of defense-related genes in Gbeta-deficient mutants were severely reduced in response to A. brassicicola infection. In addition, Gbeta-deficient mutants exhibit decreased sensitivity to a number of methyl jasmonate-induced responses such as induction of the plant defensin gene PDF1.2, inhibition of root elongation, seed germination, and growth of plants in sublethal concentrations of methyl jasmonate. In all cases, the behavior of the Galpha-deficient mutants is coherent with the classic heterotrimeric mechanism of action, indicating that jasmonic acid signaling is influenced by the Gbetagamma functional subunit but not by Galpha. We hypothesize that Gbetagamma acts as a direct or indirect enhancer of the jasmonate signaling pathway in plants.     

Yeast increases resistance in Arabidopsis against Pseudomonas syringae and Botrytis cinerea by salicylic acid-dependent as well as -independent mechanisms

Cell-wall and glucopeptide components of yeast have been reported to exhibit elicitor activity. The mode of action of defense activation by yeast is not known so far. In this study, we used the model plant Arabidopsis to investigate the activation of defense responses by yeast, the effect on resistance against different pathogens, and the mode of action. Treatment of Arabidopsis plants with an autoclaved yeast suspension induced the expression of systemic acquired resistance-related genes and accumulation of the phytoalexin camalexin. Symptom development and bacterial growth after infection with a virulent strain of the pathogen Pseudomonas syringae was reduced in yeast-pretreated plants. No protection was detectable in mutants affected in the salicylate pathway, while mutants in the jasmonate or camalexin pathway were protected by yeast, indicating that the salicylate pathway is necessary for the yeast-induced resistance against P. syringae. Yeast also reduced symptom development after challenge with Botrytis cinerea. This protection was detectable in all mutants tested, indicating that it is independent of the salicylate, jasmonate, and camalexin pathway.     

GmCOI1, a soybean F-box protein gene, shows ability to mediate jasmonate-regulated plant defense and fertility in Arabidopsis

The F-box protein gene COI1 from Arabidopsis plays a fundamental role in response to jasmonates, which regulate plant root growth, pollen fertility, wounding and healing, and defense against pathogens and insects. Null mutations in COI1 were previously found to abolish all the jasmonate responses, and the Arabidopsis coil-1 mutant is male sterile and susceptible to pathogen infection. In this study, we isolated an F-box protein gene from soybean, which shares significant homology with the Arabidopsis COI1 and similarly contains an F-box motif and leucine rich repeats (LRR), here designated GmCOI1 (Glycine max L. (Merr.) COI1). To test whether the sequence homology and structural similarity are indicative of functional conservation, we expressed GmCOI1 in the Arabidopsis coil-1 mutant. The transgenic coil-1 plants with expression of the GmCOI1 gene were found to exhibit normal jasmonate responses, including jasmonate-regulated plant defense and fertility. In addition, the chimerical proteins with swapped domain of the F-box motif or LRR between GmCOI1 and COI1 were shown to functionally complement the coil-1 mutation. Furthermore, GmCOI1 was found to assemble into the Skpl-Cullin-F-box (SCF) complexes, similar to the formation of the Arabidopsis SCF(COO1). These data demonstrate the soybean F-box protein gene GmCOI1 is able to mediate jasmonate-regulated plant defense and fertility in Arabidopsis, which implies a generic jasmonate pathway with conserved signal components in different plant species.     

外源茉莉酸和茉莉酸甲酯诱导植物抗虫作用及其机理

综述了茉莉酸(jasmonic acid, JA)和茉莉酸甲酯(methyl jasmo nate, MJA)的分子结构和应用其诱导的植物抗虫作用及其机制。植物受外源茉莉酸或茉莉酸甲酯刺激后,一条反应途径是由硬脂酸途径激活防御基因,另一条途径是直接激活防御基因。防御基因激活后导致代谢途径重新配置,并可能诱导植物产生下列4种效应：（1）直接防御,即植物产生对害虫有毒的物质、抗营养和抗消化的酶类,或具驱避性和妨碍行为作用的化合物;（2）间接防御,即产生吸引天敌的挥发物;（3）不防御,即无防御反应;（4）负防御,即产生吸引害虫的挥发物。     

The impact of cytokinin on jasmonate-salicylate antagonism in Arabidopsis immunity against infection with Pst DC3000

Cytokinin has long been shown to be an essential modulator of growth and development in plants. However, its implications in plant immunity have only recently been realized. The interaction between jasmonate and salicylate pathways is regarded as a central backbone of plant immune defense. However, the effect of cytokinin on the jasmonate and salicylate mediated balance in plant immunity is still not known. Here, we analyze the impact of cytokinin on the jasmonate-salicylate antagonism in Arabidopsis immunity regarding infection with hemibiotrophic pathogen Pseudomonas syringae pv tomato DC3000 (Pst DC3000). Systems biology analysis of a refined hormone immune pathway model provides insights into the impact of cytokinin on the balance between jasmonate and salicylic acid pathways in Arabidopsis. Targeted experiments validate model simulations monitoring bacterial growth in wild type plants as well as in jasmonate pathway mutants. An integrated analysis shows that CK promotes the SA pathway of plant immunity and does not promote JA-mediated Arabidopsis susceptibility against infection with Pst DC3000. Finally, we discuss these results in the context of an emerging model of auxin-cytokinin antagonism in plant immunity.     

UVR8 mediates UV-B-induced Arabidopsis defense responses against Botrytis cinerea by controlling sinapate accumulation

Light is emerging as a central regulator of plant immune responses against herbivores and pathogens. Solar UV-B radiation plays an important role as a positive modulator of plant defense. However, since UV-B photons can interact with a wide spectrum of molecular targets in plant tissues, the mechanisms that mediate their effects on plant defense have remained elusive. Here, we show that ecologically meaningful doses of UV-B radiation increase Arabidopsis resistance to the necrotrophic fungus Botrytis cinerea and that this effect is mediated by the photoreceptor UVR8. The UV-B effect on plant resistance was conserved in mutants impaired in jasmonate (JA) signaling (jar1-1 and P35S:JAZ10.4) or metabolism of tryptophan-derived defense compounds (pen2-1, pad3-1, pen2 pad3), suggesting that neither regulation of the JA pathway nor changes in levels of indolic glucosinolates (iGS) or camalexin are involved in this response. UV-B radiation, acting through UVR8, increased the levels of flavonoids and sinapates in leaf tissue. The UV-B effect on pathogen resistance was still detectable in tt4-1, a mutant deficient in chalcone synthase and therefore impaired in the synthesis of flavonoids, but was absent in fah1-7, a mutant deficient in ferulic acid 5-hydroxylase, which is essential for sinapate biosynthesis. Collectively, these results indicate that UVR8 plays an important role in mediating the effects of UV-B radiation on pathogen resistance by controlling the expression of the sinapate biosynthetic pathway.     

The involvement of auxin in the ripening of climacteric fruits comes of age: the hormone plays a role of its own and has an intense interplay with ethylene in ripening peaches

Ethylene has long been regarded as the main regulator of ripening in climacteric fruits. The characterization of a few tomato mutants, unable to produce climacteric ethylene and to ripen their fruits even following treatments with exogenous ethylene, has shown that other factors also play an important role in the control of climacteric fruit ripening. In climacteric peach and tomato fruits it has been shown that, concomitant with ethylene production, increases in the amount of auxin can also be measured. In this work a genomic approach has been used in order to understand if such an auxin increase is functional to an independent role played by the hormone during ripening of the climacteric peach fruits. Besides the already known indirect activity on ripening due to its up-regulation of climacteric ethylene synthesis, it has been possible to show that auxin plays a role of its own during ripening of peaches. In fact, the hormone has shown the ability to regulate the expression of a number of different genes. Moreover, many genes involved in biosynthesis and transport and, in particular, the signalling (receptors, Auxin Response Factors and Aux/IAA) of auxin had increased expression in the mesocarp during ripening, thus strengthening the idea that this hormone is actively involved in the ripening of peaches. This study has also demonstrated the existence of an important cross-talk between auxin and ethylene, with genes in the auxin domain regulated by ethylene and genes in the ethylene domain regulated by auxin.     

Yeast extract and methyl jasmonate-induced silymarin production in cell cultures of Silybum marianum (L.) Gaertn

The biosynthesis of the flavonolignan silymarin, a constitutive compound of the fruits of Silybum marianum with strong antihepatotoxic and hepatoprotective activities, is severely reduced in cell cultures of this species. It is well known that elicitation is one of the strategies employed to increase accumulation of secondary metabolites. Our study here reports on the effect of several compounds on the production of silymarin in S. marianum cultures. Yeast extract (YE), chitin and chitosan were compared with respect to their effects on silymarin accumulation in S. marianum suspensions and only yeast extract stimulated production. Jasmonic acid (JA) potentiated the yeast extract effect. One of the jasmonic acid derivatives, methyl jasmonate (MeJA), strongly promoted the accumulation of silymarin. Methyl jasmonate acted in a number of steps of the metabolic pathway of flavonolignans and its stimulating effect was totally dependent of "de novo" protein synthesis. Chalcone synthase (CHS) activity was enhanced by methyl jasmonate; however there did not appear to be a temporal relationship between silymarin accumulation and increase in enzyme activity. Also, this increase was not blocked by the protein synthesis inhibitor cycloheximide (CH). This study indicates that elicitor treatment promotes secondary metabolite production in S. marianum cultures and that jasmonic acid and its functional analogue plays a critical role in elicitation.     

Carbohydrate sources and sinks in woody plants

Each perennial woody plant is a highly integrated system of competing carbohydrate sinks (utilization sites). Internal competition for carbohydrates is shown by changes in rates of carbohydrate movement from sources to sinks and reversals in direction of carbohydrate transport as the relative sink strengths of various organs change. Most carbohydrates are produced in foliage leaves but some are synthesized in cotyledons, hypocotyls, buds, twigs, stems, flowers, fruits, and strobili. Although the bulk of the carbohydrate pool moves to sinks through the phloem, some carbohydrates are obtained by sinks from the xylem sap. Sugars are actively accumulated in the phloem and move passively to sinks along a concentration gradient. The dry weight of a mature woody plant represents only a small proportion of the photosynthate it produced. This discrepancy results not only from consumption of plant tissues by herbivores and shedding of plant parts, but also from depletion of carbohydrates by respiration, leaching, exudation, secretion, translocation to other plants through root grafts and mycorrhizae and losses to parasites. Large spatial and temporal variations occur in the use of reserve- and currently produced carbohydrates in metabolism and growth of shoots, stems, roots, and reproductive structures. A portion of the carbohydrate pool is diverted for production of chemicals involved in defense against fungi, herbivores, and competing plants. Woody plants accumulate carbohydrates during periods of excess production and deplete carbohydrates when the rate of utilization exceeds the rate of production. Stored carbohydrates play an important role in metabolism, growth, defense, cold hardiness, and postponement or prevention of plant mortality.     

Cross-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites

Plants are often attacked by many herbivorous insects and pathogens at the same time. Two important suites of responses to attack are mediated by plant hormones, jasmonate and salicylate, which independently provide resistance to herbivorous insects and pathogens, respectively. Several lines of evidence suggest that there is negative cross-talk between the jasmonate and salicylate response pathways. This biochemical link between general plant defense strategies means that deploying defenses against one attacker can positively or negatively affect other attackers. In this study, we tested for cross-talk in the jasmonate and salicylate signaling pathways in a wild tomato and examined the effects of cross-talk on an array of herbivores of cultivated tomato plants. In the wild cultivar, induction of defenses signaled by salicylate reduced biochemical expression of the jasmonate pathway but did not influence performance of S. exigua caterpillars. This indicates that the signal interaction is not a result of agricultural selection. In cultivated tomato, biochemical attenuation of the activity of a defense protein (polyphenol oxidase) in dual-elicited plants resulted in increased of performance of cabbage looper caterpillars, but not thrips, spider mites, hornworm caterpillars or the bacteria Pseudomonas syringae pv. tomato. In addition, we tested the effects of jasmonate-induced resistance on the ability of thrips to vector tomato spotted wilt virus. Although thrips fed less on induced plants, this did not affect the level of disease. Thus, the negative interaction between jasmonate and salicylate signaling had biological consequences for two lepidopteran larvae but not for several other herbivores tested or on the spread of a disease.     

OsJAR1 Contributes Mainly to Biosynthesis of the Stress-Induced Jasmonoyl-Isoleucine Involved in Defense Responses in Rice

Jasmonate plays key roles in plant growth and stress responses, as in defense against pathogen attack. Jasmonoyl-isoleucine (JA-Ile), a major active form of jasmonates, is thought to play a pivotal role in plant defense responses, but the involvement of JA-Ile in rice defense responses, including phytoalexin production, remains largely unknown. Here we found that OsJAR1 contributes mainly to stress-induced JA-Ile production by the use of an osjar1 Tos17 mutant. The osjar1 mutant was impaired in JA-induced expression of JA-responsive genes and phytoalexin production, and these defects were restored genetically. Endogenous JA-Ile was indispensable to the production of a flavonoid phytoalexin, sakuranetin, but not to that of diterpenoid phytoalexins in response to heavy metal stress and the rice blast fungus. The osjar1 mutant was also found to be more susceptible to the blast fungus than the parental wild type. These results suggest that JA-Ile production makes a contribution to rice defense responses with a great impact on stress-induced sakuranetin production.     

Non-host defense response in a novel Arabidopsis-Xanthomonas citri subsp. citri pathosystem

Citrus canker, caused by Xanthomonas citri subsp. citri (Xcc), is one of the most destructive diseases of citrus. Progress of breeding citrus canker-resistant varieties is modest due to limited resistant germplasm resources and lack of candidate genes for genetic manipulation. The objective of this study is to establish a novel heterologous pathosystem between Xcc and the well-established model plant Arabidopsis thaliana for defense mechanism dissection and resistance gene identification. Our results indicate that Xcc bacteria neither grow nor decline in Arabidopsis, but induce multiple defense responses including callose deposition, reactive oxygen species and salicylic aicd (SA) production, and defense gene expression, indicating that Xcc activates non-host resistance in Arabidopsis. Moreover, Xcc-induced defense gene expression is suppressed or attenuated in several well-characterized SA signaling mutants including eds1, pad4, eds5, sid2, and npr1. Interestingly, resistance to Xcc is compromised only in eds1, pad4, and eds5, but not in sid2 and npr1. However, combining sid2 and npr1 in the sid2npr1 double mutant compromises resistance to Xcc, suggesting genetic interactions likely exist between SID2 and NPR1 in the non-host resistance against Xcc in Arabidopsis. These results demonstrate that the SA signaling pathway plays a critical role in regulating non-host defense against Xcc in Arabidopsis and suggest that the SA signaling pathway genes may hold great potential for breeding citrus canker-resistant varieties through modern gene transfer technology.