Full establishment of arbuscular mycorrhizal symbiosis in rice occurs independently of enzymatic jasmonate biosynthesis

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Gutjahr, Caroline ^a,b   Siegler, Heike ^a,d   Haga, Ken ^c,e   Iino, Moritoshi ^c   Paszkowski, Uta ^a,f  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b UNIVERSITY OF MUNICH   (Germany)

^c Osaka Prefecture University   (Japan)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

^e NIIGATA UNIVERSITY   (Japan)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

JASMONIC ACID; CYCLOPENTANE DERIVATIVE; HYDROPEROXIDE ISOMERASE; ISOMERASE; OXYLIPIN; PHYTOHORMONE; PLANT PROTEIN;

AMINO ACID SEQUENCE; AOS1 GENE; ARBUSCULAR MYCORRHIZA; ARTICLE; CONTROLLED STUDY; ENZYME SYNTHESIS; FUNGAL COLONIZATION; FUNGAL DEVELOPMENT; FUNGAL GENE; FUNGAL STRUCTURES; FUNGUS; GENE EXPRESSION; GENE INDUCTION; JAPONICA RICE; NONHUMAN; PLANT ROOT; PR4 GENE; RHIZOPHAGUS IRREGULARIS; SIGNAL TRANSDUCTION; SYMBIOSIS; GENETICS; GLOMEROMYCOTA; METABOLISM; MICROBIOLOGY; MUTATION; MYCORRHIZA; ORYZA; PHYSIOLOGY; PLANT GENE;

DICOTYLEDONEAE; EMBRYOPHYTA; FUNGI; GLOMEROMYCOTA; LYCOPERSICON ESCULENTUM; MEDICAGO TRUNCATULA; NICOTIANA ATTENUATA;

CYCLOPENTANES; GENES, PLANT; GLOMEROMYCOTA; INTRAMOLECULAR OXIDOREDUCTASES; MUTATION; MYCORRHIZAE; ORYZA; OXYLIPINS; PLANT GROWTH REGULATORS; PLANT PROTEINS; SYMBIOSIS;

EID: 84929485431     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0123422     Document Type: Article

References (39)

1. 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: 1021-1058. doi: 10.1093/aob/mct067 PMID: 23558912
2. Balbi V, Devoto. A Jasmonate signalling network in Arabidopsis thaliana: crucial regulatory nodes and new physiological scenarios. New Phytol 2008; 177: 301-318. PMID: 18042205
3. Browse J. Jasmonate passes muster: A receptor and targets for the defense hormone. Ann Rev Plant Biol 2009; 60: 183-205. doi: 10.1146/annurev.arplant.043008.092007 PMID: 19025383
4. Thaler JS, Humphrey PT, Whiteman NK. Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 2012; 17: 260-270. doi: 10.1016/j.tplants.2012.02.010 PMID: 22498450
5. Beckers G, Spoel S. Fine-tuning plant defence signaling: salicylate versus jasmonate. Plant Biol 2006; 8: 1-10. PMID: 16435264
6. Gutjahr C, Paszkowski U. Weights in the balance: Jasmonic acid and salicylic acid signaling in root-biotroph interactions. Mol Plant-Microbe Interact 2009; 22: 763-772. doi: 10.1094/MPMI-22-7-0763 PMID: 19522558
7. Schüßler A, Schwarzott D, Walker C. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 2001; 105: 1413-1421.
8. Gutjahr C. Phytohormone signaling in arbuscular mycorhiza development. Curr Op Plant Biol 2014; 20: 26-34.
9. Hause B, Mrosk C, Isayenkov S, Strack D. Jasmonate in arbuscular mycorrhizal interactions. Phytochemistry 2007; 68: 101-110. PMID: 17097695
10. Foo E, Ross JJ, Jones WT, Reid JB Plant hormones in arbuscular mycorrhizal symbioses: an emerging role for gibberellins. Ann Bot 2013; 111: 769-779. doi: 10.1093/aob/mct041 PMID: 23508650
11. Nadal M, Paszkowski U. Polyphony in the rhizosphere: presymbiotic communication in arbuscular mycorrhizal symbiosis. Curr Op Plant Biol 2013; 16: 473-479. doi: 10.1016/j.pbi.2013.06.005 PMID: 23834765
12. Gutjahr C, Parniske M Cell and developmental biology of the arbuscular mycorrhiza symbiosis. Ann Rev Cell Dev Biol 2013; 29: 593-617. doi: 10.1146/annurev-cellbio-101512-122413 PMID: 24099088
13. Smith S, Read D. Mycorrhizal Symbiosis: Academic Press London; 2008.
14. Sawers RJH, Gutjahr C, Paszkowski U. Cereal mycorrhiza: an ancient symbiosis in modern agriculture. Trends Plant Sci 2008; 13: 93-97. doi: 10.1016/j.tplants.2007.11.006 PMID: 18262822
15. Hause B, Meier W, Miersch O, Kramell R, Strack D. Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 2002; 130: 1213-1220. PMID: 12427988
16. Tejeda-Sartorius M, Martinez de la Vega O, Délano-Frier J. Jasmonic acid influences mycorrhizal colonization in tomato plants by modifying the expression of genes involved in carbohydrate partitioning. Physiol Plant 2008; 133: 339-353. doi: 10.1111/j.1399-3054.2008.01081.x PMID: 18331402
17. Isayenkov S, Mrosk C, Stenzel I, Strack D, Hause B. Suppression of Allene Oxide Cyclase in hairy roots of Medicago truncatula reduces jasmonate levels and the degree of mycorrhization with Glomus intraradices. Plant Physiol 2005; 139: 1401-1410. PMID: 16244141
18. 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: 1344-1357. doi: 10.1111/j.1365-3040.2012.02495.x PMID: 22329418
19. Isayenkov S, Fester T, Hause B. Rapid determination of fungal colonization and arbuscule formation in roots of Medicago truncatula using real-time (RT) PCR. J Plant Physiol 2004; 161: 1379-1383. PMID: 15658808
20. Javot H, Pumplin N, Harrison M. Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant, Cell Environ 2007; 30: 310-322. PMID: 17263776
21. Herrera Medina M, Tamayo M, Vierheilig H, Ocampo J, García Garrido J. The jasmonic acid signalling pathway restricts the development of the arbuscular mycorrhizal association in tomato. J Plant Growth Regul 2008; 27: 221-230.
22. Hause B, Schaarschmidt S. The role of jasmonates in mutualistic symbioses between plants and soilborn microorganisms. Phytochemistry 2009; 70: 1589-1599. doi: 10.1016/j.phytochem.2009.07.003 PMID: 19700177
23. Yang S-Y, Grønlund M, Jakobsen I, Grotemeyer MS, Rentsch D, Miyao A, et al. Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the PHOSPHATE TRANSPORTER1 gene family. Plant Cell 2012; 24: 4236-4251. doi: 10.1105/tpc.112.104901 PMID: 23073651
24. 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 Physiol2011; 157: 305-316. doi: 10.1104/pp.111.177576 PMID: 21715672
25. Zhou G, Qi J, Ren N, Cheng J, Erb M, Mao B, et al. Silencing OsHI-LOX makes rice more susceptible to chewing herbivores, but enhances resistance to a phloem feeder. Plant J 2009; 60: 638-648. doi: 10.1111/j.1365-313X.2009.03988.x PMID: 19656341
26. Riemann M, Haga K, Shimizu T, Okada K, Ando S, Mochizuki S, et al. Identification of rice Allene Oxide Cyclase mutants and the function of jasmonate for defence against Magnaporthe oryzae. Plant J 2013; 74: 226-238. doi: 10.1111/tpj.12115 PMID: 23347338
27. Nordstrom KJV, Albani MC, James GV, Gutjahr C, Hartwig B, Turck F, et al. Mutation identification by direct comparison of whole-genome sequencing data from mutant and wild-type individuals using kmers. Nature Biotech 2013; 31: 325-330.
28. Riedel T, Groten K, Baldwin IT. Symbiosis between Nicotiana attenuata and Glomus intraradices: ethylene plays a role, jasmonic acid does not. Plant, Cell Environ 2008; 31: 1203-1213. doi: 10.1111/j.1365-3040.2008.01827.x PMID: 18507809
29. Carbonnel S, Gutjahr C. Control of arbuscular mycorhiza development by nutrient signals. 2014;Front Plant Sci 5.
30. Gutjahr C, Banba M, Croset V, An K, Miyao A, Gynheung A, et al. Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell 2008; 20: 2989-3005. doi: 10.1105/tpc.108.062414 PMID: 19033527
31. Riemann M, Muller A, Korte A, Furuya M, Weiler EW, Nick P. Impaired induction of the jasmonate pathway in the rice mutant hebiba. Plant Physiol 2003; 133: 1820-1830. PMID: 14605232
32. Moreno JE, Tao Y, Chory J, Ballaré CL Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity. Proc Natl Acad Sci, USA 2009; 106: 4935-4940. doi: 10.1073/pnas.0900701106 PMID: 19251652
33. Robson F, Okamoto H, Patrick E, Harris S-R, Wasternack C, Brearley C, et al. Jasmonate and phytochrome A signaling in arabidopsis wound and shade responses are integrated through JAZ1 stability. Plant Cell 2010; 22: 1143-1160. doi: 10.1105/tpc.109.067728 PMID: 20435902
34. Suzuki A, Suriyagoda L, Shigeyama T, Tominaga A, Sasaki M, Hirazuka Y, et al. Lotus japonicus nodulation is photomorphogenetically controlled by sensing the red/far red (R/FR) ratio through jasmonic acid (JA) signaling. Proc Natl Acad Sci, USA 2011; 108: 16837-16842. doi: 10.1073/pnas.1105892108 PMID: 21930895
35. Haga K, Iino M Phytochrome-Mediated Transcriptional Up-regulation of ALLENE OXIDE SYNTHASE in Rice Seedlings. Plant Cell Physiol 2004; 45: 119-128. PMID: 14988482
36. Oldroyd G Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 2013; 11: 252-263. doi: 10.1038/nrmicro2990 PMID: 23493145
37. Sun J, Cardoza V, Mitchell D, Bright L, Oldroyd G, Harris JM. Crosstalk between jasmonate, ethylene and Nod-factor signaling allows integration of diverse inputs for regulation of nodulation. Plant J 2006; 46: 961-970. PMID: 16805730
38. Güimil S, Chang H, Zhu T, Sesma A, Osbourn A, Roux C, et al. Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc Natl Acad Sci, USA 2005; 102: 8066-8070. PMID: 15905328
39. Fernández I, Merlos M, López-Ráez JA, Martínez-Medina A, Ferrol N, Azcón C, et al. Defense related phytohormones regulation in arbuscular mycorrhizal symbioses depends on the partner genotypes. J Chem Ecol 2014; 40: 791-803. doi: 10.1007/s10886-014-0473-6 PMID: 24997625