Abstract
Key message
We show that in rice, the amino acid-conjugates of JA precursor, OPDA, may function as a non-canonical signal for the production of phytoalexins in coordination with the innate chitin signaling.
Abstract
The core oxylipins, jasmonic acid (JA) and JA-Ile, are well-known as potent regulators of plant defense against necrotrophic pathogens and/or herbivores. However, recent studies also suggest that other oxylipins, including 12-oxo-phytodienoic acid (OPDA), may contribute to plant defense. Here, we used a previously characterized metabolic defense marker, p-coumaroylputrescine (CoP), and fungal elicitor, chitooligosaccharide, to specifically test defense role of various oxylipins in rice (Oryza sativa). While fungal elicitor triggered a rapid production of JA, JA-Ile, and their precursor OPDA, rice cells exogenously treated with the compounds revealed that OPDA, rather than JA-Ile, can stimulate the CoP production. Next, reverse genetic approach and oxylipin-deficient rice mutant (hebiba) were used to uncouple oxylipins from other elicitor-triggered signals. It appeared that, without oxylipins, residual elicitor signaling had only a minimal effect but, in synergy with OPDA, exerted a strong stimulatory activity towards CoP production. Furthermore, as CoP levels were compromised in the OPDA-treated Osjar1 mutant cells impaired in the oxylipin-amino acid conjugation, putative OPDA-amino acid conjugates emerged as hypothetical regulators of CoP biosynthesis. Accordingly, we found several OPDA-amino acid conjugates in rice cells treated with exogenous OPDA, and OPDA-Asp was detected, although in small amounts, in the chitooligosaccharide-treated rice. However, as synthetic OPDA-Asp and OPDA-Ile, so far, failed to induce CoP in cells, it suggests that yet another presumed OPDA-amino acid form(s) could be acting as novel regulator(s) of phytoalexins in rice.
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References
Alamgir KM, Hojo Y, Christeller JT, Fukumoto K, Isshiki R, Shinya T, Baldwin IT, Galis I (2016) Systematic analysis of rice (Oryza sativa) metabolic responses to herbivory. Plant Cell Environ 39:453–466. https://doi.org/10.1111/pce.12640
Arnold MD, Gruber C, Flokova K, Miersch O, Strnad M, Novak O, Wasternack C, Hause B (2016) The recently identified isoleucine conjugate of cis-12-oxo-phytodienoic acid is partially active in cis-12-oxo-phytodienoic acid-specific gene expression of Arabidopsis thaliana. PLoS ONE 11:e0162829. https://doi.org/10.1371/journal.pone.0162829
Bassard JE, Ullmann P, Bernier F, Werck-Reichhart D (2010) Phenolamides: bridging polyamines to the phenolic metabolism. Phytochemistry 71:1808–1824. https://doi.org/10.1016/j.phytochem.2010.08.003
Berens ML, Berry HM, Mine A, Argueso CT, Tsuda K (2017) Evolution of hormone signaling networks in plant defense. Annu Rev Phytopathol 55:401–425. https://doi.org/10.1146/annurev-phyto-080516-035544
Boutrot F, Zipfel C (2017) Function, discovery, and exploitation of plant pattern recognition receptors for broad-spectrum disease resistance. Annu Rev Phytopathol 55:257–286. https://doi.org/10.1146/annurev-phyto-080614-120106
Bozsoki Z, Gysel K, Hansen SB, Lironi D, Kronauer C, Feng F, de Jong N, Vinther M, Kamble M, Thygesen MB, Engholm E, Kofoed C, Fort S, Sullivan JT, Ronson CW, Jensen KJ, Blaise M, Oldroyd G, Stougaard J, Andersen KR, Radutoiu S (2020) Ligand-recognizing motifs in plant LysM receptors are major determinants of specificity. Science 369:663–670. https://doi.org/10.1126/science.abb3377
Breithaupt C, Kurzbauer R, Schaller F, Stintzi A, Schaller A, Huber R, Macheroux P, Clausen T (2009) Structural basis of substrate specificity of plant 12-oxophytodienoate reductases. J Mol Biol 392:1266–1277. https://doi.org/10.1016/j.jmb.2009.07.087
Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671. https://doi.org/10.1038/nature06006
Chini A, Monte I, Zamarreno AM, Hamberg M, Lassueur S, Reymond P, Weiss S, Stintzi A, Schaller A, Porzel A, Garcia-Mina JM, Solano R (2018) An OPR3-independent pathway uses 4,5-didehydrojasmonate for jasmonate synthesis. Nat Chem Biol 14:171–178. https://doi.org/10.1038/NCHEMBIO.2540
Christeller JT, Galis I (2014) α-Linolenic acid concentration and not wounding per se is the key regulator of octadecanoid (oxylipin) pathway activity in rice (Oryza sativa L.) leaves. Plant Physiol Biochem 83:117–125. https://doi.org/10.1016/j.plaphy.2014.07.013
Dave A, Graham IA (2012) Oxylipin signaling: a distinct role for the jasmonic acid precursor cis-(+)-12-oxo-phytodienoic acid (cis-OPDA). Front Plant Sci 3:42. https://doi.org/10.3389/fpls.2012.00042
Dave A, Hernandez ML, He ZS, Andriotis VME, Vaistij FE, Larson TR, Graham IA (2011) 12-Oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis. Plant Cell 23:583–599. https://doi.org/10.1105/tpc.110.081489
Desaki Y, Kohari M, Shibuya N, Kaku H (2019) MAMP-triggered plant immunity mediated by the LysM-receptor kinase CERK1. J Gen Plant Pathol 85:1–11. https://doi.org/10.1007/s10327-018-0828-x
Dhakarey R, Peethambaran PK, Riemann M (2016) Functional analysis of jasmonates in rice through mutant approaches. Plants 5:15. https://doi.org/10.3390/plants5010015
Edreva AM, Velikova VB, Tsonev TD (2007) Phenylamides in plants. Russ J Plant Physiol 54:287–301. https://doi.org/10.1134/S1021443707030016
Erb M, Reymond P (2019) Molecular interactions between plants and insect herbivores. Annu Rev Plant Biol 70:527–557. https://doi.org/10.1146/annurev-arplant-050718-095910
Farmer EE, Davoine C (2007) Reactive electrophile species. Curr Opin Plant Biol 10:380–386. https://doi.org/10.1016/j.pbi.2007.04.019
Flokova K, Feussner K, Herrfurth C, Miersch O, Mik V, Tarkowska D, Strnad M, Feussner I, Wasternack C, Novak O (2016) A previously undescribed jasmonate compound in flowering Arabidopsis thaliana: the identification of cis-(+)-OPDA-Ile. Phytochemistry 122:230–237. https://doi.org/10.1016/j.phytochem.2015.11.012
Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009) (+)-7-iso-Jasmonoyl-l-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5:344–350. https://doi.org/10.1038/nchembio.161
Fukumoto K, Alamgir KM, Yamashita Y, Mori I, Matsuura H, Galis I (2013) Response of rice to insect elicitors and the role of OsJAR1 in wound and herbivory-induced JA-Ile accumulation. J Integr Plant Biol 55:775–784. https://doi.org/10.1111/jipb.12057
Gleason C, Leelarasamee N, Meldau D, Feussner I (2016) OPDA has key role in regulating plant susceptibility to the root-knot nematode Meloidogyne hapla in Arabidopsis. Front Plant Sci 7:1565. https://doi.org/10.3389/fpls.2016.01565
Goetz S, Hellwege A, Stenzel I, Kutter C, Hauptmann V, Forner S, McCaig B, Hause G, Miersch O, Wasternack C, Hause B (2012) Role of cis-12-oxo-phytodienoic acid in tomato embryo development. Plant Physiol 158:1715–1727. https://doi.org/10.1104/pp.111.192658
Guo HM, Li HC, Zhou SR, Xue HW, Miao XX (2014) Cis-12-oxo-phytodienoic acid stimulates rice defense response to a piercing-sucking insect. Mol Plant 7:1683–1692. https://doi.org/10.1093/mp/ssu098
Gust AA, Pruitt R, Nürnberger T (2017) Sensing danger: key to activating plant immunity. Trends Plant Sci 22:779–791. https://doi.org/10.1016/j.tplants.2017.07.005
Hasegawa M, Mitsuhara I, Seo S, Imai T, Koga J, Okada K, Yamane H, Ohashi Y (2010) Phytoalexin accumulation in the interaction between rice and the blast fungus. Mol Plant Microbe Interact 23:1000–1011. https://doi.org/10.1094/MPMI-23-8-1000
Hayafune M, Berisio R, Marchetti R, Silipo A, Kayama M, Desaki Y, Arima S, Squeglia F, Ruggiero A, Tokuyasu K, Molinaro A, Kaku H, Shibuya N (2014) Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proc Natl Acad Sci USA 111:E404–E413. https://doi.org/10.1073/pnas.1312099111
Heitz T, Widemann E, Lugan R, Miesch L, Ullmann P, Désaubry L, Holder E, Grausem B, Kandel S, Miesch M, Werck-Reichhart D, Pinot F (2012) Cytochromes P450 CYP94C1 and CYP94B3 catalyze two successive oxidation steps of plant hormone jasmonoyl-isoleucine for catabolic turnover. J Biol Chem 287:6296–6306. https://doi.org/10.1074/jbc.M111.316364
Howe GA, Major IT, Koo AJ (2018) Modularity in jasmonate signaling for multistress resilience. Annu Rev Plant Biol 69:387–415. https://doi.org/10.1146/annurev-arplant-042817-040047
Jikumaru Y, Asami T, Seto H, Yoshida S, Yokoyama T, Obara N, Hasegawa M, Kodama O, Nishiyama M, Okada K, Nojiri H, Yamane H (2004) Preparation and biological activity of molecular probes to identify and analyze jasmonic acid-binding proteins. Biosci Biotechnol Biochem 68:1461–1466. https://doi.org/10.1271/bbb.68.1461
Jimenez-Aleman GH, Almeida-Trapp M, Fernandez-Barbero G, Gimenez-Ibanez S, Reichelt M, Vadassery J, Mithofer A, Caballero J, Boland W, Solano R (2019) Omega hydroxylated JA-Ile is an endogenous bioactive jasmonate that signals through the canonical jasmonate signaling pathway. Biochim Biophys Acta Mol Cell Biol Lipids 1864:158520. https://doi.org/10.1016/j.bbalip.2019.158520
Kajiwara A, Abe T, Hashimoto T, Matsuura H, Takahashi K (2012) Efficient synthesis of (+)-cis-12-oxo-phytodienoic acid by an in vitro enzymatic reaction. Biosci Biotechnol Biochem 76:2325–2328. https://doi.org/10.1271/bbb.120506
Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, Minami E, Shibuya N (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci USA 103:11086–11091. https://doi.org/10.1073/pnas.0508882103
Kaur H, Heinzel N, Schöttner M, Baldwin IT, Galis I (2010) R2R3-NaMYB8 regulates the accumulation of phenylpropanoid-polyamine conjugates, which are essential for local and systemic defense against insect herbivores in Nicotiana attenuata. Plant Physiol 152:1731–1747. https://doi.org/10.1104/pp.109.151738
Koo AJK, Cooke TF, Howe GA (2011) Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-l-isoleucine. Proc Natl Acad Sci USA 108:9298–9303. https://doi.org/10.1073/pnas.1103542108
Kramell R, Schmidt J, Schneider G, Sembdner G, Schreiber K (1988) Synthesis of N-(jasmonyl) amino acid conjugates. Tetrahedron 44:5791–5807. https://doi.org/10.1016/S0040-4020(01)81437-X
Lee HY, Seo JS, Cho JH, Jung H, Kim JK, Lee JS, Rhee S, Choi YD (2013) Oryza sativa COI homologues restore jasmonate signal transduction in Arabidopsis coi1-1 mutants. PLoS ONE 8:e52802. https://doi.org/10.1371/journal.pone.0052802
Liu W, Park SW (2021) 2-oxo-Phytodienoic acid: a fuse and/or switch of plant growth and defense responses? Front Plant Sci 12:7240793. https://doi.org/10.3389/fpls.2021.724079
Liu H, Li X, Xiao J, Wang S (2012) A convenient method for simultaneous quantification of multiple phytohormones and metabolites: application in study of rice-bacterium interaction. Plant Methods 8:2. https://doi.org/10.1186/1746-4811-8-2
Maynard D, Groger H, Dierks T, Dietz KJ (2018) The function of the oxylipin 12-oxophytodienoic acid in cell signaling, stress acclimation, and development. J Exp Bot 69:5341–5354. https://doi.org/10.1093/jxb/ery316
Monte I, Kneeshaw S, Franco-Zorrilla JM, Chini A, Zamarreno AM, Garcia-Mina JM, Solano R (2020) An ancient COI1-independent function for reactive electrophilic oxylipins in thermotolerance. Curr Biol 30:962–971. https://doi.org/10.1016/j.cub.2020.01.023
Morimoto N, Ueno K, Teraishi M, Okumoto Y, Mori N, Ishihara A (2018) Induced phenylamide accumulation in response to pathogen infection and hormone treatment in rice (Oryza sativa). Biosci Biotechnol Biochem 82:407–416. https://doi.org/10.1080/09168451.2018.1429889
Mueller S, Hilbert B, Dueckershoff K, Roitsch T, Krischke M, Mueller MJ, Berger S (2008) General detoxification and stress responses are mediated by oxidized lipids through TGA transcription factors in Arabidopsis. Plant Cell 20:768–785. https://doi.org/10.1105/tpc.107.054809
Muench M, Hsin CH, Ferber E, Berger S, Mueller MJ (2016) Reactive electrophilic oxylipins trigger a heat stress-like response through HSFA1 transcription factors. J Exp Bot 67:6139–6148. https://doi.org/10.1093/jxb/erw376
Nojiri H, Sugimori M, Yamane H, Nishimura Y, Yamada A, Shibuya N, Kodama O, Murofushi N, Omori T (1996) Involvement of jasmonic acid in elicitor-induced phytoalexin production in suspension-cultured rice cells. Plant Physiol 110:387–392. https://doi.org/10.1104/pp.110.2.387
Okada K, Abe H, Arimura G (2015) Jasmonates induce both defense responses and communication in monocotyledonous and dicotyledonous plants. Plant Cell Physiol 56:16–27. https://doi.org/10.1093/pcp/pcu158
Ohkama-Ohtsu N, Sasaki-Sekimoto Y, Oikawa A, Jikumaru Y, Shinoda S, Inoue E, Kamide Y, Yokoyama T, Hirai M, Shirasu K, Kamiya Y, Oliver DJ, Saito K (2011) 12-Oxo-phytodienoic acid-glutathione conjugate is transported into the vacuole in Arabidopsis. Plant Cell Physiol 52:205–209. https://doi.org/10.1093/pcp/pcq181
Park SW, Li W, Viehhauser A, He B, Kim S, Nilsson AK, Andersson MX, Kittle JD, Ambavaram MMR, Luan S, Esker AR, Tholl D, Cimini D, Ellerstrom M, Coaker G, Mitchell TK, Pereira A, Dietz KJ, Lawrence CB (2013) Cyclophilin 20–3 relays a 12-oxo-phytodienoic acid signal during stress responsive regulation of cellular redox homeostasis. Proc Natl Acad Sci USA 110:9559–9564. https://doi.org/10.1073/pnas.1218872110
Ponce De León I, Schmelz EA, Gaggero C, Castro A, Álvarez A, Montesano M (2012) Physcomitrella patens activates reinforcement of the cell wall, programmed cell death and accumulation of evolutionary conserved defence signals, such as salicylic acid and 12-oxo-phytodienoic acid, but not jasmonic acid, upon Botrytis cinerea infection. Mol Plant Pathol 13:960–974. https://doi.org/10.1111/j.1364-3703.2012.00806.x
Poudel AN, Holtsclaw RE, Kimberlin A, Sen S, Zeng S, Joshi T, Lei ZT, Sumner LW, Singh K, Matsuura H, Koo AJ (2019) 12-Hydroxy-jasmonoyl-l-isoleucine is an active jasmonate that signals through CORONATINE INSENSITIVE 1 and contributes to the wound response in Arabidopsis. Plant Cell Physiol 60:2152–2166. https://doi.org/10.1093/pcp/pcz109
Ribot C, Zimmerli C, Farmer EE, Reymond P, Poirier Y (2008) Induction of the Arabidopsis PHO1;H10 gene by 12-oxo-phytodienoic acid but not jasmonic acid via a CORONATINE INSENSITIVE1-dependent pathway. Plant Physiol 147:696–706. https://doi.org/10.1104/pp.108.119321
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 133:1820–1830. https://doi.org/10.1104/pp.103.027490
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 74:226–238. https://doi.org/10.1111/tpj.12115
Scalschi L, Sanmartin M, Camanes G, Troncho P, Sanchez-Serrano JJ, Garcia-Agustin P, Vicedo B (2015) Silencing of OPR3 in tomato reveals the role of OPDA in callose deposition during the activation of defense responses against Botrytis cinerea. Plant J 81:304–315. https://doi.org/10.1111/tpj.12728
Schaller F, Biesgen C, Mussig C, Altmann T, Weiler EW (2000) 12-Oxophytodienoate reductase 3 (OPR3) is the isoenzyme involved in jasmonate biosynthesis. Planta 210:979–984. https://doi.org/10.1007/s004250050706
Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR, Kobayashi Y, Hsu FF, Sharon M, Browse J, He SY, Rizo J, Howe GA, Zheng N (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468:400–405. https://doi.org/10.1038/nature09430
Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H, Shibuya N (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64:204–214. https://doi.org/10.1111/j.1365-313X.2010.04324.x
Shimizu T, Miyamoto K, Minami E, Nishizawa Y, Iino M, Nojiri H, Yamane H, Okada K (2013) OsJAR1 contributes mainly to biosynthesis of the stress-induced jasmonoyl-isoleucine involved in defense responses in rice. Biosci Biotechnol Biochem 77:1556–1564. https://doi.org/10.1271/bbb.130272
Shinya T, Nakagawa T, Kaku H, Shibuya N (2015) Chitin-mediated plant-fungal interactions: catching, hiding and handshaking. Curr Opin Plant Biol 26:64–71. https://doi.org/10.1016/j.pbi.2015.05.032
Shinya T, Hojo Y, Desaki Y, Christeller JT, Okada K, Shibuya N, Galis I (2016) Modulation of plant defense responses to herbivores by simultaneous recognition of different herbivore-associated elicitors in rice. Sci Rep 6:32537. https://doi.org/10.1038/srep32537
Shinya T, Yasuda S, Hyodo K, Tani R, Hojo Y, Fujiwara Y, Hiruma K, Ishizaki T, Fujita Y, Saijo Y, Galis I (2018) Integration of danger peptide signals with herbivore-associated molecular pattern signaling amplifies anti-herbivore defense responses in rice. Plant J 94:626–637. https://doi.org/10.1111/tpj.13883
Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–2127. https://doi.org/10.1105/tpc.104.023549
Stintzi A, Weber H, Reymond P, Browse J, Farmer EE (2001) Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc Natl Acad Sci USA 98:12837–12842. https://doi.org/10.1073/pnas.211311098
Svyatyna K, Jikumaru Y, Brendel R, Reichelt M, Mithofer A, Takano M, Kamiya Y, Nick P, Riemann M (2014) Light induces jasmonate-isoleucine conjugation via OsJAR1-dependent and -independent pathways in rice. Plant Cell Environ 37:827–839. https://doi.org/10.1111/pce.12201
Taki N, Sasaki-Sekimoto Y, Obayashi T, Kikuta A, Kobayashi K, Ainai T, Yagi K, Sakurai N, Suzuki H, Masuda T, Takamiya K, Shibata D, Kobayashi Y, Ohta H (2005) 12-Oxo-phytodienoic acid triggers expression of a distinct set of genes and plays a role in wound-induced gene expression in Arabidopsis. Plant Physiol 139:1268–1283. https://doi.org/10.1104/pp.105.067058
Tan X, Calderon-Villalobos LI, Sharon M, Zheng C, Robinson CV, Estelle M, Zheng N (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446:640–645. https://doi.org/10.1038/nature05731
Tanabe K, Hojo Y, Shinya T, Galis I (2016) Molecular evidence for biochemical diversification of phenolamide biosynthesis in rice plants. J Integr Plant Biol 58:903–913. https://doi.org/10.1111/jipb.12480
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 SCFCOI1 complex during jasmonate signalling. Nature 448:661–665. https://doi.org/10.1038/nature05960
Uchiyama A, Yaguchi T, Nakagawa H, Sasaki K, Kuwata N, Matsuura H, Takahashi K (2018) Biosynthesis and in vitro enzymatic synthesis of the isoleucine conjugate of 12-oxo-phytodienoic acid from the isoleucine conjugate of α-linolenic acid. Bioorg Med Chem Lett 28:1020–1023. https://doi.org/10.1016/j.bmcl.2018.02.030
Varsani S, Grover S, Zhou S, Koch KG, Huang PC, Kolomiets MV, Williams WP, Heng-Moss T, Sarath G, Luthe DS, Jander G, Louis J (2019) 12-Oxo-phytodienoic acid acts as a regulator of maize defense against corn leaf aphid. Plant Physiol 179:1402–1415. https://doi.org/10.1104/pp.18.01472
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 409:634–639. https://doi.org/10.1016/j.bbrc.2011.05.055
Wang C, Wang G, Zhang C, Zhu P, Dai H, Yu N, He Z, Xu L, Wang E (2017) OsCERK1-mediated chitin perception and immune signaling requires receptor-like cytoplasmic kinase 185 to activate an MAPK cascade in rice. Mol Plant 10:619–633. https://doi.org/10.1016/j.molp.2017.01.006
Wari D, Alamgir KM, Mujiono K, Hojo Y, Shinya T, Tani A, Nakatani H, Galis I (2019) Honeydew-associated microbes elicit defense responses against brown planthopper in rice. J Exp Bot 70:1683–1696. https://doi.org/10.1093/jxb/erz041
Wasternack C, Feussner I (2018) The oxylipin pathways: biochemistry and function. Annu Rev Plant Biol 69:363–386. https://doi.org/10.1146/annurev-arplant-042817-040440
Wasternack C, Strnad M (2018) Jasmonates: news on occurrence, biosynthesis, metabolism and action of an ancient group of signaling compounds. Int J Mol Sci 19:2539. https://doi.org/10.3390/ijms19092539
Xiao Y, Chen Y, Charnikhova T, Mulder PPJ, Heijmans J, Hoogenboom A, Agalou A, Michel C, Morel JB, Dreni L, Kater MM, Bouwmeester H, Wang M, Zhu Z, Ouwerkerk PBF (2014) OsJAR1 is required for JA-regulated floret opening and anther dehiscence in rice. Plant Mol Biol 86:19–33. https://doi.org/10.1007/s11103-014-0212-y
Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091–1094. https://doi.org/10.1126/science.280.5366.1091
Xu J, Wang X, Zu H, Zeng X, Baldwin IT, Lou Y, Li R (2021) Molecular dissection of rice phytohormone signaling involved in resistance to a piercing-sucking herbivore. New Phytol 230:1639–1652. https://doi.org/10.1111/nph.17251
Yamaguchi T, Minami E, Ueki J, Shibuya N (2005) Elicitor-induced activation of phospholipases plays an important role for the induction of defense responses in suspension-cultured rice cells. Plant Cell Physiol 46:579–587. https://doi.org/10.1093/pcp/pci065
Yamaguchi K, Yamada K, Ishikawa K, Yoshimura S, Hayashi N, Uchihashi K, Ishihama N, Kishi-Kaboshi M, Takahashi A, Tsuge S, Ochiai H, Tada Y, Shimamoto K, Yoshioka H, Kawasaki T (2013) A receptor-like cytoplasmic kinase targeted by a plant pathogen effector is directly phosphorylated by the chitin receptor and mediates rice immunity. Cell Host Microbe 13:347–357. https://doi.org/10.1016/j.chom.2013.02.007
Ye W, Munemasa S, Shinya T, Wu W, Ma T, Lu J, Kinoshita T, Kaku H, Shibuya N, Murata Y (2020) Stomatal immunity against fungal invasion comprises not only chitin-induced stomatal closure but also chitosan-induced guard cell death. Proc Natl Acad Sci USA 117:20932–20942. https://doi.org/10.1073/pnas.1922319117
Zimmerman DC, Feng P (1978) Characterization of a prostaglandin-like metabolite of linolenic acid produced by a flaxseed extract. Lipids 13:313–316. https://doi.org/10.1007/BF02533720
Acknowledgements
We thank Drs. Peter Nick and Michael Riemann (Karlsruhe Institute of Technology) for providing hebiba mutant seeds and GST-OsAOC plasmid; Drs. Naoto Shibuya and Hanae Kaku (Meiji University) for providing chitooligosaccharides; Dr. Hideyuki Matsuura (Hokkaido University) for providing deuterated jasmonate standards for LC-MS/MS; Ms. Tomoko Sakazawa for her help with OPDA-AAs purification; Ms. Hiroko Nakatani (Okayama University) for her help with rice callus maintenance. This research was supported by the Ministry of Education, Culture, Sports, Science and Technology (MEXT) as part of the Joint Research Program implemented at the Institute of Plant Science and Resources, Okayama University, Grants-in-Aid for Scientific Research (No. 16K08143 to I.G., No. 18K05558 and 21K05506 to T.S.), and Ohara Foundation for Agriculture Research.
Funding
This research was supported by the Ministry of Education, Culture, Sports, Science and Technology (MEXT) as part of the Joint Research Program implemented at the Institute of Plant Science and Resources, Okayama University, Grants-in-Aid for Scientific Research (No. 16K08143 to I.G., No. 18K05558 and 21K05506 to T.S.), and Ohara Foundation for Agriculture Research.
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TS, KM, KU, HY, IG—designed and conducted experiments, wrote paper; KO—designed experiments, wrote paper; YH, YE—conducted experiments, analyzed data.
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Shinya, T., Miyamoto, K., Uchida, K. et al. Chitooligosaccharide elicitor and oxylipins synergistically elevate phytoalexin production in rice. Plant Mol Biol 109, 595–609 (2022). https://doi.org/10.1007/s11103-021-01217-w
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DOI: https://doi.org/10.1007/s11103-021-01217-w