Action of jasmonates in plant stress responses and development — Applied aspects

Biotechnology Advances 32 (2014) 31–39

Contents lists available at ScienceDirect

Biotechnology Advances journal homepage: www.elsevier.com/locate/biotechadv

Research review paper

Action of jasmonates in plant stress responses and development — Applied aspects☆ Claus Wasternack ⁎ Leibniz Institute of Plant Biochemistry, Department of Molecular Signal Processing, Weinberg 3, D-06120 Halle (Saale), Germany

a r t i c l e

i n f o

Available online 2 October 2013 Keywords: Jasmonic acid 12-oxo-phytodienoic acid Necrotrophic pathogens Mycorrhiza Plant growth promoting rhizobacteria Intercropping JA-induced secondary metabolite production Anti-cancer activity

a b s t r a c t Jasmonates (JAs) are lipid-derived compounds acting as key signaling compounds in plant stress responses and development. The JA co-receptor complex and several enzymes of JA biosynthesis have been crystallized, and various JA signal transduction pathways including cross-talk to most of the plant hormones have been intensively studied. Defense to herbivores and necrotrophic pathogens are mediated by JA. Other environmental cues mediated by JA are light, seasonal and circadian rhythms, cold stress, desiccation stress, salt stress and UV stress. During development growth inhibition of roots, shoots and leaves occur by JA, whereas seed germination and flower development are partially affected by its precursor 12-oxo-phytodienoic acid (OPDA). Based on these numerous JA mediated signal transduction pathways active in plant stress responses and development, there is an increasing interest in horticultural and biotechnological applications. Intercropping, the mixed growth of two or more crops, mycorrhization of plants, establishment of induced resistance, priming of plants for enhanced insect resistance as well as pre- and post-harvest application of JA are few examples. Additional sources for horticultural improvement, where JAs might be involved, are defense against nematodes, biocontrol by plant growth promoting rhizobacteria, altered composition of rhizosphere bacterial community, sustained balance between growth and defense, and improved plant immunity in intercropping systems. Finally, biotechnological application for JA-induced production of pharmaceuticals and application of JAs as anti-cancer agents were intensively studied. © 2013 Elsevier Inc. All rights reserved.

Contents 1. 2. 3. 4.

5. 6. 7. 8. 9. 10. 11.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Root nematode defense reactions . . . . . . . . . . . . . . . . . . . . . . . . . . Biotic and abiotic stresses affect crop productivity — the dilemma of growth versus defense JA in mutualistic interactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Arbuscular mycorrhiza . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Root nodule symbiosis of legumes . . . . . . . . . . . . . . . . . . . . . . 4.3. Plant growth promoting rhizobacteria and the biotrophic endophyte P. indica . Trichomes — plant factories for secondary compounds . . . . . . . . . . . . . . . . . Biotechnological application of JA signaling . . . . . . . . . . . . . . . . . . . . . . Tuber formation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Senescence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Intercropping . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pre- and post-harvest effects on crop quality . . . . . . . . . . . . . . . . . . . . . Jasmonates as anti-cancer drugs . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

. . . . . . . . . . . . . .

32 33 34 34 34 34 34 35 35 36 36 36 37 37

Abbreviations: AM, arbuscular mycorrhiza; AOC, allene oxide cyclase; 13-AOS, allene oxide synthase; coi1, coronatine insensitive1; dad1, delayed anther dehiscence1; GA, gibberellic acid; ISR, induced systemic resistance; JA, jasmonic acid; jai1, JA insensitive1; JAR1, JA-amino acid synthetase; JAZ, JASMONATE ZIM DOMAIN PROTEIN; 13-LOX, 13-lipoxygenase; MeJA, JA methyl ester; OPDA, cis-(+)-12-oxo-phytodienoic acid; OPR3, OPDA reductase3; PGPR, plant growth promoting rhizobacteria; PLA1, phospholipase A1; RNS, root nodule symbiosis; SA, salicylic acid; SCF, Skp1/Cullin/F-box complex; TA, tuberonic acid; VOCs, volatile organic compounds. ☆ Invited plenary lecture which was held at the conference “Olomouc Biotech 2013 — Plant Biotechnology: Green for Good II” in Olomouc, Czech Republic, June 17–21; 2013. ⁎ Palacky University & Institute of Experimental Botany ASCR, Laboratory of Growth Regulators, Slechtitelu 11, 783 71 Olomouc, Czech Republic. Tel.: +49 345 5582 1210; fax: +49 345 5582 1219. E-mail address: [email protected]. 0734-9750/$ – see front matter © 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.biotechadv.2013.09.009

32

C. Wasternack / Biotechnology Advances 32 (2014) 31–39

12. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37 Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38

1. Introduction Jasmonates are key signaling compounds in plant responses to biotic and abiotic stresses as well as in development. Jasmonic acid (JA) and its derivatives are synthesized from α-linolenic acid esterified in galactolipids of chloroplast membranes. α-Linolenic acid is released by a phospholipase A1 and oxygenated by a 13-lipoxygenase (13-LOX) to a 13hydroperoxyoctadecatrienoic acid, which is converted by a 13-allene oxide synthase (13-AOS) to a highly unstable epoxide (Fig. 1). This epoxide cyclizes to cis-(+)-12-oxo-phytodienoic acid (OPDA) by the action of an allene oxide cyclase (AOC). The second half of JA biosynthesis takes place in peroxisomes. The final product (+)-7-iso-JA is in equilibrium with (-)-JA and is released into the cytosol. Among numerous metabolic

Fig. 1. Biosynthesis of jasmonic acid (JA) and (+)-7-iso-JA-L-isoleucine takes place in three different compartments of a plant cell. In the chloroplast, α-linolenic acid is released from membranes, oxygenated by a 13-lipoxygenase (13-LOX) to a hydroperoxyoctadecatrienoic acid (13-HPOT), which is converted to an unstable epoxide by a 13-allene oxide synthase (13-AOS) and cyclized by an allene oxide cyclase (AOC) to cis-(+)-12-oxo-phytodienoic acid (OPDA). Upon transport of OPDA into peroxisomes the cyclopentenone ring is reduced by an OPDA reductase3 (OPR3). Subsequently, the fatty acid β-oxidation machinery catalyzes shortening of the carboxylic acid side chain to (+)-7-iso-JA, which is released into the cytosol and epimerizes to (−)-JA. Conjugation with amino acids, such as isoleucine, is catalyzed by jasmonoyl–isoleucine conjugate synthase (JAR1).

conversions of JA, such as hydroxylation, O-glucosylation, decarboxylation, carboxylation, methylation, conjugation or sulfation of JA and hydroxylated JA, respectively, the conjugation of JA with amino acids such as L-isoleucine is the most important reaction catalyzed by JAR1 (reviewed in Wasternack, 2007; Wasternack and Hause, 2013). The product (+)-7-iso-JA-L-Ile is the most bioactive JA compound (Fonseca et al., 2009) and is the ligand of the SCFCOI1–JAZ-co-receptor complex (Sheard et al., 2010) (cf. below). All enzymes and proteins involved in JA biosynthesis and perception have been cloned from different plant species and some of them have been crystallized (e.g. 13-LOX, 13-AOS, AOC, ACYL-CoA-OXIDASE1, OPR3, JAR1 and the SCFCOI1–JAZ-co-receptor complex) (Kombrink, 2012; Wasternack and Hause, 2013). Regulation of JA biosynthesis takes places by a positive feedback loop, by substrate availability and by tissue specificity (Wasternack, 2007). The substrate availability is the reason, why constitutive overexpression of genes coding for enzymes of JA biosynthesis such as 13-AOS and AOC did not lead to elevated JA levels (Stenzel et al., 2003). Such transgenic lines produced increased amounts of JA only upon wounding or other environmental stimuli leading to release of α-linolenic acid. The initial rationale behind such transgenic approaches was the expectation to generate plants with increased resistance to herbivores or necrotrophic pathogens. Both responses belong to the well-studied signaling pathways, where JA is involved. Other JA-mediated processes are plant responses to desiccation stress, ozone stress, UV-stress, osmotic stress, cold stress, or light stress, but also formation of secondary metabolites and adaptation to seasonal and circadian rhythm are regulated by JA (Fig. 2). Moreover, jasmonates are involved in the regulation of beneficial plant–microbe interactions, such as interactions with arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria (PGPR). During plant development the following processes are mediated by JA: Male and female organ development, embryo development, sex determination in maize, seed germination, seedling development, root growth, gravitropism, trichome formation, tuber formation, leaf movement, and leaf senescence. Over the last two decades of JA research a remarkable improvement of information accumulated on enzymes and proteins involved in JA biosynthesis and signaling pathways of developmentally regulated processes and of

Fig. 2. Jasmonic acid (JA) and its conjugate with isoleucine are signals in various responses to biotic and abiotic stresses, in developmental processes, but also in applied aspects of agronomical importance such as crop quality, intercropping or defense against necrotrophic pathogens or herbivores. Tumor suppression by JA/JA-Ile might be of importance via pharmaceuticals prepared from plant extracts with high JA/JA-Ile content.

C. Wasternack / Biotechnology Advances 32 (2014) 31–39

different stress responses. The ubiquitin–proteasome system was recognized as the central regulator of JA signaling in 1998, when COI1 (CORONATINE INSENSITIVE1) was identified as an F-box protein (Xie et al., 1998). Here, an Skp1/Cullin/F-box (SCF) complex is a E3 ubiquitin ligase (Fig. 3). The F-box protein recognizes specific target proteins which are subsequently subjected to proteasomal degradation (reviewed in Chini et al., 2009; Kombrink, 2012; Shan et al., 2012). Mechanistic explanations were initiated first in 2007, when a new protein family was identified, called JASMONATE ZIM DOMAIN (JAZ) proteins (Chini et al., 2007; Thines et al., 2007; Yan et al., 2007). These proteins are negative regulators of JA-induced gene expression and can be ubiquitinated via the SCFCOI1 complex. This requires binding of the ligand for COI1–JAZ interaction, a distinct enantiomeric form of jasmonates, the (+)-7-iso-Lisoleucine, which accumulates upon developmental or environmental stimuli (Fonseca et al., 2009); reviewed in (Wasternack and Hause, 2013). Proteasomal degradation of JAZ proteins allows the release of transcription factors, e.g. of the MYC or MYB families, which bind to promoters of JA-responsive genes (Kazan and Manners, 2013; Song et al., 2013). In JA perception and signaling a modular principle occurs consisting of (i) the SCFCOI1-JAZ-co-receptor complex which acts as the JA receptor, of (ii) the JAZ proteins and of (iii) the transcriptions factors such as MYC2. This scenario is active in most of the JA-dependent signaling pathways such as those involved in response to herbivores or pathogens, in trichome development, in formation of glucosinolates, alkaloids or terpenoids, in root growth inhibition, or in anther development. Similar modules exist for perception and signaling of auxins, gibberellic acid (GA) and ethylene (Chini et al., 2009; Kelley and Estelle, 2012). Aspects of biosynthesis, perception and signaling have been repeatedly reviewed including mechanistic explanations on cross-talk to other hormones such as auxin, GA, and salicylic acid (SA) (Kazan and Manners, 2013; Kombrink, 2012; Pieterse et al., 2012; Wasternack, 2007; Wasternack and Hause, 2013; Wasternack and Kombrink, 2010). Simultaneously, however, there was an increasing interest in applied aspects of action of JA. The following paragraphs will give some examples, e.g. of defense against nematodes, growth versus defense, mutualistic interactions such as arbuscular mycorrhiza and growth promotion by rhizobacteria, rhizosphere bacterial community, tuber and trichome formation, senescence, intercropping systems, JA-induced

33

biotechnological processes such as production of secondary compounds, anti-cancer activity of jasmonates and of pre- and postharvest treatments of jasmonates.

2. Root nematode defense reactions Root-knot and cyst nematodes are endoparasites which exhibit a sendentary life-style in roots by reprogramming feeding cells for their own nutrient supply (Gheysen and Mitchum, 2011). The damage in agriculture caused by nematodes is remarkable. There is about 5% crop loss worldwide by root-knot nematodes of the genus Meloidogyne which infects more than 200 mono- and dicotyledonous species. Like bacterial or fungal pathogens, invading nematodes inject effector proteins, which lead to metabolite and transcriptional reprogramming including formation and sustaining homoestasis of plant hormones (Gheysen and Mitchum, 2011). Beside a strong interference with auxin transport in roots, there are clear indications for involvement of JA signaling. In rice, there is a pivotal requirement for the JA-dependent pathway in systemically induced defense against the root-knot nematode Meloidogyne graminicola, whereas ethylene signaling activates the JA pathway in a facultative manner (Nahar et al., 2011). This requirement of JA formation and signaling in root-knot nematode defense reaction of rice is suppressed by brassinosteroids (Nahar et al., 2013). Among the nematode effector proteins are chorismate mutase, cell wall degrading enzymes, spermidin synthase, annexins and several not yet identified proteins, which interfere with the auxin transport or act with plant peptide hormones (Gheysen and Mitchum, 2011). The nematode-induced reprogramming of host cells includes genes involved in remodeling of membranes. Recently, a nematode-induced up-regulation of a wound- and JA-inducible ATPase of Arabidopsis thaliana was found (Ali et al., 2013). This ATPase belongs to a clade of AAA proteins known to alter membrane constituents upon abiotic stress. In nature there is a more complex scenario of systemic responses to root-feeding nematodes due to simultaneously active shoot-feeding insects. The compensatory plant growth response known for herbivory may affect nematode invasion, and root-nematodes can affect positively and negatively shoot herbivorous insects (Wondafrash et al., 2013).

Fig. 3. Mechanism of jasmonic acid (JA)-induced gene expression following JA perception via the SCFCOI1–JAZ co-receptor complex. At low level of JA/JA-Ile, the promoters of JA-responsive genes are not activated by transcription factors such as MYC2 due to their repression by JAZ proteins. Biotic and abiotic stresses elevate JA/JA-Ile content, which facilitates interaction of JAZ with the F-box protein COI1 within the SCF complex leading to proteasomal degradation of JAZ. The free MYC2 acts on JA-responsive cis-elements (JARE) in JA-responsive promoters and JA-responsive gene expression is switched on. Figure designed by K. Mielke

34

C. Wasternack / Biotechnology Advances 32 (2014) 31–39

3. Biotic and abiotic stresses affect crop productivity — the dilemma of growth versus defense JA is a key player in stress responses against necrotrophic pathogens and herbivores (reviewed in Pieterse et al., 2012; Wasternack and Hause, 2013). Similarly, JA is of central role in abiotic stress responses such as responses to salinity, drought and cold. All of them exhibit negative impact on crop productivity by affecting different levels of cellular integrity and metabolic activity including dramatic reprogramming of gene expression (Tuteja, 2009). Beside the key player in abiotic stresses, ABA, JA has a specific role in regulation of photosynthesis and in crosstalk with ABA signaling. The negative role of JA on photosynthesis became obvious more than 20years ago, when down-regulation of Rubisco by JA was identified (Weidhase et al., 1987b). Meanwhile, Rubisco activase was described as target of the COI1-dependent JA-induced reprogramming of gene expression (Shan et al., 2011; Walia et al., 2007). Effects on stomatal aperture, CO2 mobility and carbon/nitrogen ratio are also involved. Beside the negative role of JA in photosynthesis, an important effect of JA seems to be its growth inhibition through suppression of mitosis and cell proliferation (Noir et al., 2013; Zhang and Turner, 2008). There is a balance of growth and defense, where GA and its negative regulatory proteins DELLAs act antagonistically to JA and its negative regulators JAZs. In the absence of GA and the presence of JA, growth suppression and defense activation takes place (Kazan and Manners, 2012; Wasternack and Hause, 2013). Such costly benefit of defense reaction versus growth was preferentially observed for herbivory. In nature, however, plants are simultaneously exposed to numerous biotic and abiotic stresses. This suggests that in analyses of stress responses combination of stresses is required to cope with field conditions (Mittler, 2006). Interestingly, in many developmental pathways regulating growth and reproduction, signals (hormones, growth regulators) are involved, that are identical to those of stress signaling pathways (Rymen and Sugimoto, 2012). JA is one example. First transcriptome analyses on plants subjected to a combination of stresses revealed that 61% of transcriptome changes upon double stresses could not be predicted from responses to both single stresses (Rasmussen et al., 2013). Obviously, plants have evolved strategies to cope with such stress combinations. The increased possibility to handle genome sequencing functional genomics will lead to crop improvement, functional food design, biofuel development, ecosystem analysis and other aspects where JA is involved (Mittler and Shulaev, 2013). 4. JA in mutualistic interactions Mutualistic interactions between plant roots and microbes are important components of a sustainable agriculture. Growth promotion and crop production can be improved by (i) mycorrhiza, preferentially arbuscular mycorrhiza (AM), by (ii) root nodule symbiosis of legumes (RNS), by (iii) induced systemic resistance (ISR) caused by plant growth promoting rhizobacteria (PGPR) and by (iv) interaction with biotrophic endophytes, such as Piriformospora indica. 4.1. Arbuscular mycorrhiza AM occurs worldwide in about 80% of land plants and is an association of obligate biotrophic fungi of the phylum Glomeromycota (reviewed in Gutjahr and Paszkowski, 2009; Hause and Schaarschmidt, 2009; Wasternack and Hause, 2013). AM leads to enhanced supply of plants with mineral nutrients and water, and is accompanied by an increase in tolerance to abiotic and biotic stresses, such as drought, heavy metals, salt, necrotrophic and biotrophic pathogens as well as chewing herbivorous insects. JA is clearly involved in the establishment and maintenance of AM as evidenced by mutants and transgenic approaches dealing with JA biosynthesis and signaling (Hause and Schaarschmidt, 2009) (Fig. 4). Increased JA levels led to increased AM formation probably mediated

by an enhanced allocation of assimilation products into the roots (Wasternack and Hause, 2013). A role for other phytohormones in regulating AM was also described, but how they affect AM is diverse and depends on the plant–fungus combination analyzed (Foo et al., 2013; Hause et al., 2007). ABA is a positive regulator of AM, whereas ethylene and GA exhibit negative effects on AM formation, since ethylene-insensitive and GA-deficient mutants showed increased AM formation (Foo et al., 2013). Accordingly, in case of GA, AM was reduced in a mutant lacking the GA signaling protein DELLA. Possibly, there is a similar cross-talk between GA and JA by antagonistic action of GA/DELLAs versus JA/JAZ/MYC2 as known for the balance between growth and defense (reviewed in Wasternack and Hause, 2013). 4.2. Root nodule symbiosis of legumes Involvement of JA in RNS of legumes, the nodule formation by nitrogen-fixing rhizobacteria, is controversially discussed. There are data from pharmacological experiments for positive and negative regulation of RNS by JA as well as absence of any effect (Wasternack and Hause, 2013). Most notably, application of JA to roots of Medicago truncatula abolished Nod factor signaling (Sun et al., 2006; Zhang et al., 2012). Even data on shoot-derived JA are controversial in respect to putative role in nodulation. A wound-induced endogenous rise of JA in M. truncatula did not alter nodulation (Landgraf et al., 2012). A metabolomic profiling approach on Nod factor-treated roots of M. truncatula revealed that the oxylipin content was decreased (Zhang et al., 2012), whereas roots exhibiting mature nodules did not show altered JA levels (Zdyb et al., 2011). Modulation of endogenous JA levels by transient expression of AOCsense or AOC-RNAi did not change nodulation of M. truncatula (Zdyb et al., 2011). 4.3. Plant growth promoting rhizobacteria and the biotrophic endophyte P. indica PGPRs such as Pseudomonas fluorescence were initially recognized as agents to enhance defense capacity of above ground parts. This phenomenon was described as induced systemic resistance (ISR). ISR is characterized by priming effects in leaves upon ethylene- and MYB72 dependent generation of a signal in roots, which activates JA and ethylene pathways in a NPR1- and MYC2-dependent manner (reviewed in Pieterse et al., 2012). The interaction between beneficial microbes and plant roots attributes to a broad-spectrum of systemic responses, usually accompanied by callose deposition (Zamioudis and Pieterse, 2012). Initially recognized as potential invaders, PGPRs establish a mutualistic interaction. There are indications that beneficial microbes evolved in a mutualistic interaction with plant roots by rewiring hormone regulated responses (Pieterse et al., 2012). A well-studied example is the biotrophically living root endophyte P. indica, a Basidiomycete (Qiang et al., 2012). P. indica activates the JA pathway leading to an early suppression of SA-dependent defense responses. Moreover, interaction of plants with P. indica results in plant growth promotion and increased phosphate supply, whereas the fungus in turn receives carbohydrates (Pieterse et al., 2012; Qiang et al., 2012). The rhizosphere is of increasing interest to find out plant growth promotion. About 1011 microbial cells per gram roots containing up to 30,000 prokaryotic species occur in the rhizosphere microbiome near the roots (Berendsen et al., 2012). Among the three key components (i) pathogenic microbes, (ii) beneficial microbes and (iii) commensal microbes (without direct effects on pathogens or plants), multifaceted cross-talk takes place. This cross-talk includes damage by infection or toxic compounds in case of pathogens and growth promotion or ISR in case of beneficial microbes. Even the composition of the rhizosphere bacterial communities can alter upon activation of the JA-dependent defense pathways by necrotrophic pathogens or herbivores, presumable

C. Wasternack / Biotechnology Advances 32 (2014) 31–39

35

Fig. 4. The role of JA in arbuscular mycorrhization by the fungus Rhizophagus irregularis. Fungal inoculation leads to endogenous rise of jasmonates (JA); mycorrhization is marked by dark roots. Transgenic down-regulation of AOC by expression of an AOC-RNAi construct (MtAOC1-RNAi) leads to decreased JA levels followed by a delayed mycorrhization indicating role of JA in mycorrhization. Modified from Hause and Schaarschmidt (2009).

via carbon containing compounds released by roots (Carvalhais et al., 2013). Flavonoids occurring in root exudates may also affect rhizosphere bacterial as well as fungal communities. The output of all these mutualistic plant–rhizophere interactions is an increased stress tolerance, improved nutrient uptake and decreased pathogen colonization (Berendsen et al., 2012; de Zelicourt et al., 2013). 5. Trichomes — plant factories for secondary compounds Resistance to insects is partially established by formation of terpenoids, flavonoids, alkaloids and defense proteins in glandular trichomes (Tian et al., 2012) (Fig. 5). This cell-type specific formation of secondary compounds is of biotechnological interest. Genetic engineering of the multicellular, glandular trichomes, e.g. of tomato, represent a tool for production of compounds such as terpenoids similar to a biofactory (Tissier, 2012). Trichome formation and the production of secondary

Fig. 5. Scheme on involvement of jasmonic acid (JA) and its conjugate (JA-Ile) in trichome development and production of secondary metabolites in trichomes. Confocal laser scanning micrograph (extended depth of focus) shows trichomes on a vascular bundle of a leaf of Nicotiana benthamiana expressing GFP-KDEL. GFP-KDEL expression was chosen to visualize the trichomes (micrograph and design of the Figure performed by B. Hause).

compounds are JA and COI1-dependent processes, where identical JAZ proteins as well as transcription factors such as MYB75, GL3 and EGL3 are involved. All of them are known to be active in anthocyanin biosynthesis (Qi et al., 2011). Besides the JA-induced formation of secondary compounds, trichomes have a great impact on plant defense against insects under field conditions. Generation of defense proteins such as proteinase inhibitors or secondary compounds such as terpenoids, sesquiterpenes and plant leaf volatiles determine defense reactions including host plant selection by insect larvae, e.g. of the Colorado potato beetle (Meldau et al., 2012). The increased susceptibility of JA signaling mutants such as the tomato mutant jai1, a homolog of coi1 of Arabidopsis, clearly indicates the strict JA dependence of trichome formation and their essential role in plant defense against herbivorous insects (Li et al., 2004). 6. Biotechnological application of JA signaling As described above, trichomes are specialized plant cell factories for secondary compounds. Another tool with long term tradition is a plant cell suspension culture in the biotechnological production of secondary metabolites (Verpoorte et al., 2000). These metabolites are sources for pharmaceuticals, food additives, drugs, dyes, fragrances, or flavors and are formed upon elicitation of plant cell cultures, preferentially by treatment with JA (Zhao et al., 2005). Two decades ago the link between JA and secondary metabolite biosynthesis in cell cultures was shown by detection of endogenous rise of JA upon elicitation of cell suspension cultures of Rauvolfia canescens and Eschscholtzia californica with a yeast elicitor followed by formation of benzo[c]phenanthridine alkaloids (Gundlach et al., 1992). The great effort, however, invested in strategies for JA-induced secondary metabolite formation by cell cultures led only to few successful examples on commercial production (Verpoorte et al., 2000). Among them is the anti-tumor compound taxol (paclitaxel) (Onrubia et al., 2013). Metabolic engineering of plants by introducing genes became the most important strategy upon elucidation of biosynthetic pathways of secondary compounds. Here, engineering of (i) the rate limiting step and/or (ii) handling of regulatory elements such as transcriptions factors (TFs) active in expression of enzymes involved in biosynthetic steps are of special importance. This requires acceptance of genetically modified (GM) plants. Even already 9% of total agricultural land with a global seed value of GM crops of over ten billion US dollar occurred in

36

C. Wasternack / Biotechnology Advances 32 (2014) 31–39

2009, much has to be done for acceptance in the public sector (Van Montagu, 2011). In case of biotechnological formation of plant secondary metabolites by genetic engineering, there are hopeful examples such as glucosinolates, Vitamin A in rice, resveratrol, terpenoid indole alkaloids (Verpoorte et al., 2000) or benzylisoquinoline alkaloids including morphine (Hagel and Facchini, 2013). Manipulation of rate-limiting step has been used in case of benzylisoquinoline alkaloids (Hagel and Facchini, 2013) and nicotine (Dewey and Xie, 2013). There are, however, unexpected drawbacks in respect to the amount of plant-generated alkaloids after stable transformation of plants such as opium poppy even after MeJA treatment. Strong variation in yield of the numerous benzylisoquinoline alkaloids of opium poppy and unexpected switches among the biosynthetic branches are two examples. Cell type specificity of enzyme location, substrate availability, transport of intermediate products and requirements for enzyme complexes are difficulties which have to be bypassed to get high productivity of metabolically engineered opium poppy (Hagel and Facchini, 2013; Memelink, 2004). Besides manipulation of the rate-limiting step of biosynthetic pathways of secondary compounds, TFs are an important tool to engineer production of secondary metabolites (Gantet and Memelink, 2002). Here, advantage can be taken from specificity of TFs for distinct biosynthetic branches. The JA-specific ORCAs (Octadecanoid-responsive Catharanthus AP2-domain proteins) and MYC-type TFs, the key players in JA-induced gene expression, are examples (De Geyter et al., 2012; Gantet and Memelink, 2002; Memelink et al., 2001). ORCAs have been successfully used to manipulate terpenoid indole alkaloids in periwinkle (Pan et al., 2012). MYC2, MYC3, and MYC4 have been shown to regulate glucosinolate biosynthesis (Schweizer et al., 2013). Although these examples illustrate, how JA-signaling can be used for increased production of secondary compounds, there are limitations at commercial level, preferentially by limited productivity of the engineered plants. New tools are under study to get high productivity by synthetic biology and combinatorial biochemistry (Facchini et al., 2012). This includes microbes or yeast as a host, where plant genes combined in a multigene expression construct are used for the following sequence of events: Selection of a plant producing high value metabolites–identification of biosynthesis genes–pathway assembly in yeast–process engineering and fermentation–collection of high value products. Even complex biosynthetic pathways such as that of terpenoids and triterpenoids could be engineered for cheap production of naturally occurring or new, pharmacological relevant terpenoids and triterpenoids (Moses et al., 2013).

nutrient remobilization (Wu et al., 2012). Senescence promotion by JA was one of the two first physiological effects observed for JA (Ueda and Kato, 1980). Later on, JA-induced senescence was described for barley as a process which includes down-regulation of RUBISCO and accumulation of JA-induced proteins (JIPs). It was the first described JA-induced alteration of gene expression (Weidhase et al., 1987a). Meanwhile, senescence associated genes (SAGs), such as SAG12, SAG 13, SAG 113, and TFs, such as WRKY6, WRKY43, or WRKY75, have been identified as key components of senescence promotion (reviewed in Li et al., 2012; Reinbothe et al., 2009; Wu et al., 2012). The dramatic reprogramming of gene expression during senescence was documented by several microarray analyses and establishment of the leaf senescence data base (Buchanan-Wollaston et al., 2005; Liu et al., 2011). Here, involvement of JA became obvious. Numerous genes identified in microarray analyses of JA-treated tissues were also found among senescence-induced genes. Many of them belong to photosynthesis, primary metabolism and cellular redox machinery. Altered gene expression upon JA-induced senescence corresponds to altered gene expression upon endogenously increased levels of hormones such as ethylene or JA (Navabpour et al., 2003), thereby supporting involvement of these hormones. Key components of JA-induced senescence are (i) chlorophyll-breakdown by JAinducible chlorophyllase1, (ii) degradation of gene products involved in photosynthesis such as large and small subunit of RUBISCO or chlorophyll a/b binding proteins and (iii) accumulation of JA-induced proteins (JIPs), which are partially involved in JA synthesis such as LOX2 (Reinbothe et al., 2009; Seltmann et al., 2010). 9. Intercropping There is worldwide an increasing interest in intercropping, the mixed growth of two or more crops. This may originate from the numerous disadvantages occurring by growth of plants in monocultures. In China, intercropping reached already more than 28 million hectares (Xiong et al., 2013). Improved crop productivity by intercropping is mainly caused by more effective utilization of soil nutrients, increased root development and root interaction. An example is the peanut/maize intercropping which improves the iron (Fe) content of peanuts in calcerous soils (Fig. 6). A recent proteomic approach revealed an improved ecological adaptation of both plants (Xiong et al., 2013). In both species increased stress resistant ability occurs as indicated by down-regulation of various families of stress-related proteins. In

7. Tuber formation Potato is one of the most important crops. For a long time, JA was thought to be involved in tuber formation due to tuber-inducing activity of jasmonate compounds applied to potato stolons. Among them were 12-hydroxy-JA, called tuberonic acid (TA), and its glucoside (Koda, 1992). Recent work clearly indicates a control by light, temperature and GA. The homeobox gene BEL1 is expressed in leaves in a photoperioddependent manner including CONSTANS and FLOWERING LOCUS T. BEL1 mRNA accumulates under short day condition and low temperature. Subsequently, BEL1 mRNA is transported via the phloem to the stolon tip, where a BEL1-dependent activation of GA biosynthesis finally initiates tuber formation (Lin et al., 2013). Obviously, the initially observed role of JA compounds in potato tuber formation seems to be indirect and occurs via cross-talk between GA and JA (Wasternack and Hause, 2013). 8. Senescence Besides plant damage by pathogens or herbivores, senescence is among the most prominent negative regulators of plant growth and development. Senescence is a genetically programmed process which affects crop production by negative regulation of photosynthesis and

Fig. 6. Improved ecological adaption of intercropping peanut and maize. Mixed growth of maize and peanut plants leads to down-regulation of stress-related proteins, increased photosynthetic activity, and up-regulation of JA biosynthesis genes. Intercropping increases Fe availability in the rhizosphere and improves Fe nutrition of peanuts accompanied by a positive effect on carbon and nitrogen metabolism. Modified from Xiong et al. (2013), source of pictures: maize: anno82; http://piqs.de/fotos/ 80063.html; peanut: 2008 NC State University.

C. Wasternack / Biotechnology Advances 32 (2014) 31–39

maize up-regulation of several JA biosynthesis genes under conditions of intercropping may attribute to the stress resistance ability in peanuts through rhizosphere interactions (Fig. 6). Possibly, interaction between both plants is mediated by root exudates and/or volatile JA compounds such as JA methyl ester (MeJA) and cis-jasmone. Besides MeJA, cisjasmone is well-known as an airborne signal in plant–insect interactions, thereby affecting plant stress tolerance in agro-ecosystems (Pickett, 2012). Chemical ecology tells us, how plant secondary metabolites can attribute to pest control. Preferentially volatile organic compounds (VOCs), usually induced by JA, are generated in intercropping plants. VOCs greatly influence plant–insect interactions (Poveda and Kessler, 2012). Maize plants intercropped with legumes or grasses are much less damaged by repelling (pushing) the adult stem borer moth out of the field via JA-induced VOCs, whereas Napier grass grown at the boarder of the maize field can attract (pull) gravid females away from maize (Hassanali et al., 2008). This push–pull approach in nature has great impact on a pesticide-free management of agro-ecosystems (Poveda and Kessler, 2012). Besides plant–plant and plant–insect communications in intercropping systems, there is a role of the airborne signal methanol. Production of methanol is induced by wounding and JA and is involved in the establishment of antibacterial resistance as well as in the increased gating capacity of plasmodesmata in neighboring plants (Dorokhov et al., 2012). In intercropping systems the release of volatiles is an important determinant. Interestingly, increased production of allelopathic compounds, e.g. by Solidago altissima during herbivore exclusion, has a positive effect on its competitive ability suggesting an evolutionary advantage via a shift in resource allocation (Uesugi and Kessler, 2013).

10. Pre- and post-harvest effects on crop quality Numerous application experiments, preferentially with MeJA, revealed for monocotyledonous and dicotyledonous plants great benefit of pre- and post-harvest treatments mainly due to increased postharvest decease resistance against infection by Botrytis or green mold (Rohwer and Erwin, 2008). Even the well-established link between JA-mediated defense and plant circadian clock (Goodspeed et al., 2012) can be of advantage in post-harvest (Goodspeed et al., 2013). The circadian clock is retrained in post-harvest by light–dark cycles and attributes to enhanced herbivore resistance and improved nutritional value of the cabbage (Goodspeed et al., 2013). The post-harvest quality is not diminished by a pre-harvest MeJA treatment (Ku et al., 2013). Beneficial volatiles are also often involved in the establishment of resistance after post-harvest treatments. Similarly, chilling injury may occur during post-harvest storage. Application of MeJA can reduce the negative impact of chilling injury, and this effect is strengthened by chilling (e.g. for about one week) at about 5 °C (Rohwer and Erwin, 2008). Crop quality can be greatly improved by MeJA treatment including partial benefits for human health. Prominent examples are (i) the JAinduced accumulation of the “healthy” compound resveratrol in Vitis vinifera (Ahuja et al., 2012; Verpoorte et al., 2000), (ii) the JA-induced glucosinolate formation in cruciferous vegetables (Grubb and Abel, 2006), (iii) the JA-induced accumulation of anthocyanins and antioxidant compounds in fruits and vegetables (Wang and Zheng, 2005) and (iv) the JA-induced formation of alkaloids, taxol, saponins and other groups of compounds being of pharmaceutical interest or being of healthy value in diets. The latter aspects are linked to hydrophilic and lipophilic antioxidants (Martin et al., 2013). Many of the hydrophilic antioxidants such as anthocyanins, flavonols, isoflavonoids or chlorogenic acid and the lipophilic antioxidants such as lycopene or vitamin E are formed in JA-inducible pathways, but occur at low levels in crop plants or medicinal plants. Therefore, remarkable effort has been done to increase their content by transgenic approaches or biotechnological production of individual compounds (Gantet and Memelink,

37

2002; Verpoorte et al., 2000; Zhao et al., 2005) (cf. Section 6, Biotechnological Aspects). 11. Jasmonates as anti-cancer drugs Jasmonates do not occur in human tissues. After a decade of speculative suggestions, however, now clear evidence is available on anticancer activity of jasmonates at least for several human cell lines (reviewed in Cohen and Flescher, 2009). The anti-cancer activity takes place by direct cell death induction via interference with energy metabolism, mitochondrial perturbation and production of reactive oxygen species. Additionally, jasmonates lead to cell cycle arrest and re-differentiation and exert anti-inflammatory properties (Cohen and Flescher, 2009; Raviv et al., 2013). Chemical synthesis of jasmonates, design of new JA compounds and increase in pharmaco-kinetic stability are strategies in anti-cancer therapy with jasmonates. Among jasmonates with anticancer activity are JA, MeJA, and the decarboxylated form cis-jasmone. JA-rich plants were proposed to function as a useful tool in anti-cancer therapy. The pharmaceutical industry already took advantage of this for a long time by production of pharmaceuticals prepared with extracts from plants such as mistletoe (Viscum album), even a putative explanation was given more recently: Such plants carry a JA content of about four orders of magnitude higher levels than wounded tomato or tobacco leaves (Miersch and Wasternack, unpublished). There are numerous other plants with high MeJA content such as Jasminum, Chloranthus, Cymbidium, Rosmarinus, Lonicera or Artemisia, and for some of them anti-cancer activity of ethanolic extracts has been shown (Cohen and Flescher, 2009). Furthermore, algae extracts carrying high jasmonate content exert anti-cancer activity in prostate cancer (Farooqi et al., 2012). Another line of JA-mediated anti-cancer activity is given by its induction of biosynthesis of glucosinolates occurring in cruciferous vegetables, particular broccoli, cauliflower or kale. The cancer preventive effect of these vegetables is known for a long time (van Poppel et al., 1999), and JA-induced glucosinolate formation is well-documented (Grubb and Abel, 2006). Pre-harvest MeJA-treatment of cauliflower under field conditions increased glucosinolate levels up to 5-fold and increased marker enzymes of anti-cancer bioactivity (Ku et al., 2013). 12. Conclusions The initial observations on the role of JA in plant defense were done two decades ago and led to studies on putative applications in agriculture. These studies were based preferentially on treatment with jasmonates. Meanwhile, there is a large body of information on JA biosynthesis and signaling in plant responses to biotic and abiotic stresses as well as during development. Mechanistic insights were found by biochemical, molecular and cell-biological studies for herbivory, responses to necrotrophic pathogens, induced systemic resistance, trichome development and senescence. Main components of JA biosynthesis, perception and signaling could be identified showing the similar modular principle as the signaling components of other plant hormones. This allowed increasing insight into the cross-talk of JA with other hormones. Consequently, growing interest in applied aspects of JA and JA signaling became obvious. Here, increase in crop productivity, in resistance to pathogens, herbivores and other stresses or in delayed senescence are some challenges of agro-economic impact. Mycorrhiza, PGPR and intercropping may lead to agro-cultural improvement. The complexity in nature, however, requires new methods and tools to find out strategies for agricultural improvement via hormone research such as that on JA. System biology and combinatorial biochemistry approaches are already used to get insights in responses to simultaneously applied different stresses, or biotechnological production of JA-induced compounds of pharmaceutical or medicinal interest. Other areas of interest with economical impact are the interaction between bacterial and fungal soil communities with plant roots, the interaction between different but simultaneously active insect communities and growth/defense of

38

C. Wasternack / Biotechnology Advances 32 (2014) 31–39

plants. Finally, additional facets of the plant life cycle in its natural environment will become important for potential application in agriculture. Acknowledgments The preparation of the manuscript was funded by the Region HANA for Biotechnological and Agricultural Research, Czech Republic (grant no. ED0007/01/01). I thank Prof. B. Hause (Halle/Saale) for critical reading of the manuscript and for help in preparing some figures. I thank K. Mielke (Halle/Saale) for the design of Fig. 3. References Ahuja I, Kissen R, Bones AM. Phytoalexins in defense against pathogens. Trends Plant Sci 2012;17:73–90. Ali MA, Plattner S, Radakovic Z, Wieczorek K, Elashry A, Grundler FMW, et al. An Arabidopsis ATPase gene involved in nematode-induced syncytium development and abiotic stress responses. Plant J 2013;74:852–66. Berendsen RL, Pieterse CMJ, Bakker PAHM. The rhizosphere microbiome and plant health. Trends Plant Sci 2012;17:478–86. Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, et al. Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 2005;42:567–85. Carvalhais LC, Dennis PG, Badri DV, Tyson GW, Vivanco JM, Schenk PM. Activation of the jasmonic acid plant defence pathway alters the composition of rhizosphere bacterial communities. PLoS One 2013;8:e56457. Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, et al. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 2007;448:666–71. Chini A, Boter M, Solano R. Plant oxylipins: COI1/JAZs/MYC2 as the core jasmonic acid-signalling module. FEBS J 2009;276:4682–92. Cohen S, Flescher E. Methyl jasmonate: a plant stress hormone as an anti-cancer drug. Phytochemistry 2009;70:1600–9. De Geyter N, Gholami A, Goormachtig S, Goossens A. Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci 2012;17:349–59. de Zelicourt A, Al-Yousif M, Hirt H. Rhizosphere microbes as essential partners for plant stress tolerance. Mol Plant 2013;6:242–5. Dewey RE, Xie J. Molecular genetics of alkaloid biosynthesis in Nicotiana tabacum. Phytochemistry 2013;94:10–27. Dorokhov YL, Komarova TV, Petrunia IV, Frolova OY, Pozdyshev DV, Gleba YY. Airborne signals from a wounded leaf facilitate viral spreading and induce antibacterial resistance in neighboring plants. PLoS Pathog 2012;8:e1002640. Facchini PJ, Bohlmann J, Covello PS, De Luca V, Mahadevan R, Page JE, et al. Synthetic biosystems for the production of high-value plant metabolites. Trends Biotechnol 2012;30:127–31. Farooqi AA, Butt G, Razzaq Z. Algae extracts and methyl jasmonate anti-cancer activities in prostate cancer: choreographers of ‘the dance macabre’. Cancer Cell Intern 2012;12:50. Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, et al. (+)-7-isojasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nature. Chem Biol 2009;5:344–50. Foo E, Ross JJ, Jones WT, Reid JB. Plant hormones in arbuscular mycorrhizal symbioses: an emerging role for gibberellins. Ann Bot 2013;111:769–79. Gantet P, Memelink J. Transcription factors: tools to engineer the production of pharmacologically active plant metabolites. Trends Pharmacol Sci 2002;23:563–9. Gheysen G, Mitchum MG. How nematodes manipulate plant development pathways for infection. Curr Opin Plant Biol 2011;14:415–21. Goodspeed D, Chehab EW, Min-Venditti A, Braam J, Covington MF. Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior. Proc Natl Acad Sci U S A 2012;109:4674–7. Goodspeed D, Liu John D, Chehab EW, Sheng Z, Francisco M, Kliebenstein Daniel J, et al. Postharvest circadian entrainment enhances crop pest resistance and phytochemical cycling. Curr Biol 2013;23:1235–41. Grubb CD, Abel S. Glucosinolate metabolism and its control. Trends Plant Sci 2006;11: 89–100. Gundlach H, Müller M, Kutchan T, Zenk M. Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc Natl Acad Sci U S A 1992;89:2389–93. Gutjahr C, Paszkowski U. Weights in the balance: jasmonic acid and salicylic acid signaling in root-biotroph interactions. Mol Plant-Microbe Interact 2009;22:763–72. Hagel JM, Facchini PJ. Benzylisoquinoline alkaloid metabolism: a century of discovery and a brave new world. Plant Cell Physiol 2013;54:647–72. Hassanali A, Herren H, Khan ZR, Pickett JA, Woodcock CM. Integrated pest management: the push–pull approach for controlling insect pests and weeds of cereals, and its potential for other agricultural systems including animal husbandry. Philos Trans R Soc Lond B Biol Sci 2008;363:611–21. Hause B, Schaarschmidt S. The role of jasmonates in mutualistic symbioses between plants and soil-born microorganisms. Phytochemistry 2009;70:1589–99. Hause B, Mrosk C, Isayenkov S, Strack D. Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 2007;68:101–10. Kazan K, Manners JM. JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci 2012;17:22–31. Kazan K, Manners JM. MYC2: the master in action. Mol Plant 2013;6:686–703.

Kelley DR, Estelle M. Ubiquitin-mediated control of plant hormone signaling. Plant Physiol 2012;160:47–55. Koda Y. The role of jasmonic acid and related compounds in the regulation of plant development. Int Rev Cytol 1992;135:155–99. Kombrink E. Chemical and genetic exploration of jasmonate biosynthesis and signaling paths. Planta 2012;236:1351–66. Ku K, Choi J-H, Kushad M, Jeffery E, Juvik J. Pre-harvest methyl jasmonate treatment enhances cauliflower chemoprotective attributes without a loss in postharvest quality. Plant Foods Hum Nutr 2013;68:113–7. Landgraf R, Schaarschmidt S, Hause B. Repeated leaf wounding alters the colonization of Medicago truncatula roots by beneficial and pathogenic microorganisms. Plant Cell Environ 2012;35:1344–57. Li L, McCaig B, Wingerd B, Wang J, Whaton M, Pichersky E, et al. The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 2004;16:126–43. Li Z, Peng J, Wen X, Guo H. Gene network analysis and functional studies of senescence-associated genes reveal novel regulators of Arabidopsis leaf senescence. J Integr Plant Biol 2012;54:526–39. Lin T, Sharma P, Gonzalez DH, Viola IL, Hannapel DJ. The impact of the long-distance transport of a BEL1-like messenger RNA on development. Plant Physiol 2013;161:760–72. Liu X, Li Z, Jiang Z, Zhao Y, Peng J, Jin J, et al. LSD: a leaf senescence database. Nucl Acid Res 2011;39:D1103–7. Martin C, Zhang Y, Tonelli C, Petroni K. Plants, diet, and health. Annu Rev Plant Biol 2013;64:19–46. Meldau S, Erb M, Baldwin IT. Defence on demand: mechanisms behind optimal defence patterns. Ann Bot 2012;110:1503–14. Memelink J. Putting the opium in poppy to sleep. Nat Biotechnol 2004;22:1526–7. Memelink J, Verpoorte R, Kijne J. ORCAnization of jasmonate-responsive gene expression in alkaloid metabolism. Trends Plant Sci 2001;6:212–9. Mittler R. Abiotic stress, the field environment and stress combination. Trends Plant Sci 2006;11:15–9. Mittler R, Shulaev V. Functional genomics, challenges and perspectives for the future. Physiol Plant 2013;148:317–21. Moses T, Pollier J, Thevelein JM, Goossens A. Bioengineering of plant (tri)terpenoids: from metabolic engineering of plants to synthetic biology in vivo and in vitro. New Phytol 2013;200:27–43. Nahar K, Kyndt T, De Vleesschauwer D, Höfte M, Gheysen G. The jasmonate pathway is a key player in systemically induced defense against root knot nematodes in rice. Plant Physiol 2011;157:305–16. Nahar K, Kyndt T, Hause B, Höfte M, Gheysen G. Brassinosteroids suppress rice defense against root-knot nematodes through antagonism with the jasmonate pathway. Mol Plant-Microbe Interact 2013;26:106–15. Navabpour S, Morris K, Allen R, Harrison E, A-H-Mackerness S, Buchanan-Wollaston V. Expression of senescence-enhanced genes in response to oxidative stress. J Exp Bot 2003;54:2285–92. Noir S, Bömer M, Takahashi N, Ishida T, Tsui T-L, Balbi V, et al. Jasmonate controls leaf growth by repressing cell proliferation and the onset of endoreduplication while maintaining a potential stand-by mode. Plant Physiol 2013;161:1930–51. Onrubia M, Cusidó R, Ramirez K, Hernández-Vázquez L, Moyano E, Bonfill M, et al. Bioprocessing of plant in vitro systems for the mass production of pharmaceutically important metabolites: paclitaxel and its derivatives. Curr Med Chem 2013;20: 880–91. Pan Q, Wang Q, Yuan F, Xing S, Zhao J, Choi YH, et al. Overexpression of ORCA3 and G10H in Catharanthus roseus plants regulated alkaloid biosynthesis and metabolism revealed by NMR-metabolomics. PLoS One 2012;7:e43038. Pickett JA. New synthesis: chemical ecology and sustainable food production. J Chem Ecol 2012;38. (1071-). Pieterse CMJ, van der Does D, Zamioudis C, Leon-Reyes A, van Wees SCM. Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 2012;28:489–521. Poveda K, Kessler A. New synthesis: plant volatiles as functional cues in intercropping systems. J Chem Ecol 2012;38. (1341-). Qi T, Song S, Ren Q, Wu D, Huang H, Chen Y, et al. The jasmonate-ZIM-domain proteins interact with the WD-Repeat/bHLH/MYB complexes to regulate jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana. Plant Cell 2011;23:1795–814. Qiang X, Weiss M, Kogel K-H, Schäfer P. Piriformospora indica — a mutualistic basidiomycete with an exceptionally large plant host range. Mol Plant Pathol 2012;13:508–18. Rasmussen S, Barah P, Suarez-Rodriguez MC, Bressendorff S, Friis P, Costantino P, et al. Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiol 2013;161:1783–94. Raviv Z, Cohen S, Reischer-Pelech D. The anti-cancer activities of jasmonates. Cancer Chemother Pharmacol 2013;71:275–85. Reinbothe C, Springer A, Samol I, Reinbothe S. Plant oxylipins: role of jasmonic acid during programmed cell death, defence and leaf senescence. FEBS J 2009;276:4666–81. Rohwer C, Erwin J. Horticultural applications of jasmonates: a review. J Horticult Sci Biotechnol 2008;83:283–304. Rymen B, Sugimoto K. Tuning growth to the environmental demands. Curr Opin Plant Biol 2012;15:683–90. Schweizer F, Fernández-Calvo P, Zander M, Diez-Diaz M, Fonseca S, Glauser G, et al. Arabidopsis basic helix–loop–helix transcription factors MYC2, MYC3, and MYC4 regulate glucosinolate biosynthesis, insect performance, and feeding behavior. Plant Cell 2013. http://dx.doi.org/10.1105/tpc.113.115139. Seltmann MA, Stingl NE, Lautenschlaeger JK, Krischke M, Mueller MJ, Berger S. Differential impact of lipoxygenase 2 and jasmonates on natural and stress-induced senescence in Arabidopsis. Plant Physiol 2010;152:1940–50.

C. Wasternack / Biotechnology Advances 32 (2014) 31–39 Shan X, Wang J, Chua L, Jiang D, Peng W, Xie D. The role of Arabidopsis rubisco activase in jasmonate-induced leaf senescence. Plant Physiol 2011;155:751–64. Shan X, Yan J, Xie D. Comparison of phytohormone signaling mechanisms. Curr Opin Plant Biol 2012;15:84–91. Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR, et al. Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 2010;468:400–5. Song S, Qi T, Huang H, Xie D. Regulation of stamen development by coordinated actions of jasmonate, auxin, and gibberellin in Arabidopsis. Mol Plant 2013;6:1065–73. Stenzel I, Hause B, Maucher H, Pitzschke A, Miersch O, Ziegler J, et al. Allene oxide cyclase dependence of the wound response and vascular bundle-specific generation of jasmonates in tomato — amplification in wound signaling. Plant J 2003;33: 577–89. Sun J, Cardoza V, Mitchell DM, Bright L, Oldroyd G, Harris JM. Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation. Plant J 2006;46:961–70. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, et al. JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 2007;448:661–5. Tian D, Tooker J, Peiffer M, Chung S, Felton G. Role of trichomes in defense against herbivores: comparison of herbivore response to woolly and hairless trichome mutants in tomato (Solanum lycopersicum). Planta 2012;236:1053–66. Tissier A. Glandular trichomes: what comes after expressed sequence tags? Plant J 2012;70: 51–68. Tuteja N. Cold, salinity and drought stress. In: Hirt H, editor. Plant stress biology. Weinheim: Wiley-Blackwell; 2009. p. 137–59. Ueda J, Kato J. Isolation and identification of a senescence-promoting substance from wormwood (Artemisia absinthium L.). Plant Physiol 1980;66:246–9. Uesugi A, Kessler A. Herbivore exclusion drives the evolution of plant competitiveness via increased allelopathy. New Phytol 2013;198:916–24. Van Montagu M. It is a long way to GM agriculture. Annu Rev Plant Biol 2011;62:1–23. van Poppel G, Verhoeven D, Verhagen H, Goldbohm R. Brassica vegetables and cancer prevention. Epidemiology and mechanisms. Adv Exp Med Biol 1999;472:159–68. Verpoorte R, van der Heijden R, Memelink J. Engeneering the plant cell factory for secondary metabolite production. Transgen Res 2000;9:323–43. Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Close TJ. Large-scale expression profiling and physiological characterization of jasmonic acid-mediated adaptation of barley to salinity stress. Plant Cell Environ 2007;30:410–21. Wang SY, Zheng W. Preharvest application of methyl jasmonate increases fruit quality and antioxidant capacity in raspberries. Int J Food Sci Technol 2005;40:187–95.

39

Wasternack C. Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 2007;100:681–97. Wasternack C, Hause B. 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 2013;111:1021–58. Wasternack C, Kombrink E. Jasmonates: structural requirements for lipid-derived signals active in plant stress responses and development. ACS Chem Biol 2010;5:63–77. Weidhase R, Kramell H-M, Lehmann J, Liebisch H-W, Lerbs W, Parthier B. Methyljasmonate-induced changes in the polypeptide pattern of senescing barley leaf segments. Plant Sci 1987a;51:177–86. Weidhase R, Lehmann J, Kramell H-M, Sembdner G, Parthier B. Degradation of ribulose1,5-bisphosphate carboxylase and chlorophyll in senescing barley leaf segments triggered by jasmonic acid methylester, and counteraction by cytokinins. Physiol Plant 1987b;69:161–6. Wondafrash M, Van Dam NM, Tytgat TOG. Plant systemic induced responses mediate interactions between root parasitic nematodes and aboveground herbivorous insects. Front Plant Sci 2013:4. Wu X-Y, Kuai B-K, Jia J-Z, Jing H-C. Regulation of leaf senescence and crop genetic improvement. J Integr Plant Biol 2012;54:936–52. Xie D-X, Feys B, James S, Nieto-Rostro M, Turner J. COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 1998;280:1091–4. Xiong H, Shen H, Zhang L, Zhang Y, Guo X, Wang P, et al. Comparative proteomic analysis for assessment of the ecological significance of maize and peanut intercropping. J Proteome 2013;78:447–60. Yan Y, Stolz S, Chetelat A, Reymond P, Pagni M, Dubugnon L, et al. A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell 2007;19:2470–83. Zamioudis C, Pieterse CMJ. Modulation of host immunity by beneficial microbes. Mol Plant-Microbe Interact 2012;25:139–50. Zdyb A, Demchenko K, Heumann J, Mrosk C, Grzeganek P, Göbel C, et al. Jasmonate biosynthesis in legume and actinorhizal nodules. New Phytol 2011;189:568–79. Zhang Y, Turner JG. Wound-induced endogenous jasmonates stunt plant growth by inhibiting mitosis. PLoS One 2008;3:e3699. Zhang N, Venkateshwaran M, Boersma M, Harms A, Howes-Podoll M, den Os D, et al. Metabolomic profiling reveals suppression of oxylipin biosynthesis during the early stages of legume–rhizobia symbiosis. FEBS Lett 2012;586:3150–8. Zhao J, Davis LC, Verpoorte R. Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 2005;23:283–333.