The rice LysM receptor-like kinase OsCERK1 is required for the perception of short-chain chitin oligomers in arbuscular mycorrhizal signaling

New Phytologist

Volumn 214, Issue 4, 2017, Pages 1440-1446

  Carotenuto, Gennaro ^a   Chabaud, Mireille ^b   Miyata, Kana ^c   Capozzi, Martina ^a   Takeda, Naoya ^d   Kaku, Hanae ^c   Shibuya, Naoto ^c   Nakagawa, Tomomi ^d,e   Barker, David G ^b   Genre, Andrea ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c MEIJI UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^e NAGOYA UNIVERSITY   (Japan)

Author keywords

arbuscular mycorrhiza (AM); chitin oligomer signaling; LysM receptor like kinase (RLK); nuclear calcium spiking; Oryza sativa; plant microbe interactions; root symbiosis

Indexed keywords

ARBUSCULAR MYCORRHIZA; CHITIN; FUNGUS; GENE EXPRESSION; GENETIC ANALYSIS; MUTATION; PATHOGENICITY; POLYMER; PROTEIN; RICE; ROOT; SYMBIOSIS;

FUNGI; ORYZA SATIVA;

CALCIUM; CHITIN; PLANT PROTEIN; PROTEIN SERINE THREONINE KINASE;

GENE KNOCKOUT; GENETICS; METABOLISM; MICROBIOLOGY; MUTATION; MYCORRHIZA; ORYZA; PHYSIOLOGY; PLANT ROOT; SIGNAL TRANSDUCTION;

CALCIUM; CHITIN; GENE KNOCKOUT TECHNIQUES; MUTATION; MYCORRHIZAE; ORYZA; PLANT PROTEINS; PLANT ROOTS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

EID: 85016733111     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.14539     Document Type: Article

References (35)

1. Antolín-Llovera M, Petutsching EK, Ried MK, Lipka V, Nürnberg T, Robatzek S, Parniske M. 2014. Knowing your friends and foes – plant receptor-like kinases as initiators of symbiosis or defence. New Phytologist 204: 791–802.
2. Arrighi JF, Barre A, Ben Amor B, Bersoult A, Soriano LC, Mirabella R, de Carvalho-Niebel F, Journet EP, Ghérardi M, Huguet T et al. 2006. The Medicago truncatula lysine motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiology 142: 265–279.
3. 2+ signalling in arbuscular mycorrhizal and actinorhizal endosymbioses: on the trail of novel underground signals. New Phytologist 214: 533–538.
4. Berruti A, Lumini E, Balestrini R, Bianciotto V. 2016. Arbuscular mycorrhizal fungi as natural biofertilizers: let's benefit from past successes. Frontiers in Microbiology 6: 1559.
5. Buendia L, Wang T, Girardin A, Lefebvre B. 2015. The LysM receptor-like kinase SlLYK10 regulates the arbuscular mycorrhizal symbiosis in tomato. New Phytologist 210: 184–195.
6. Campos-Soriano L, Gómez-Ariza J, Bonfante P, San Segundo B. 2011. A rice calcium-dependent protein kinase is expressed in cortical root cells during the presymbiotic phase of the arbuscular mycorrhizal symbiosis. BMC Plant Biology 11: 90.
7. 2+ spiking in the legume and nonlegume root epidermis. New Phytologist 189: 347–355.
8. Delaux P-M, Radhakrishnan GV, Jayaraman D, Cheem J, Malbreil M, Volkening JD, Sekimoto H, Nishiyama T, Melkonian M, Pokorny L et al. 2015. Algal ancestors of land plants were preadapted for symbiosis. Proceedings of the National Academy of Sciences, USA 112: 13390–13395.
9. Fitter AH, Helgason T, Hodge A. 2011. Nutritional exchanges in the arbuscular mycorrhizal symbiosis: implications for sustainable agriculture. Fungal Biology Reviews 25: 68–72.
10. 2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytologist 198: 179–189.
11. Harrison MJ. 2012. Cellular programs for arbuscular mycorrhizal symbiosis. Current Opinion in Plant Biology 15: 691–698.
12. Hayafune M, Berisio R, Marchetti R, Silipo A, Kayama M, Desaki Y, Arima S, Squeglia F, Ruggiero A, Tokuyasu K et al. 2014. Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proceedings of the National Academy of Sciences, USA 111: E404–E413.
13. 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. Proceedings of the National Academy of Sciences, USA 103: 11086–11091.
14. Kistner C, Winzer T, Pitzschke A, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Webb KJ et al. 2005. Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 17: 2217–2229.
15. Kouzai Y, Nakajima K, Hayafune M, Ozawa K, Kaku H, Shibuya N, Minami E, Nishizawa Y. 2014. CEBiP is the major chitin oligomer-binding protein in rice and plays a main role in the perception of chitin oligomers. Plant Molecular Biology 84: 519–528.
16. Liu S, Wang J, Han Z, Gong X, Zhang H, Chai J. 2016. Molecular mechanism for fungal cell wall recognition by rice chitin receptor Os CEBiP. Structure 24: 1192–1200.
17. Liu T, Liu Z, Song C, Hu Y, Han Z, She J, Fan F, Wang J, Jin C, Chang J et al. 2012. Chitin-induced dimerization activates a plant immune receptor. Science 336: 1160–1164.
18. Maekawa T, Kusakabe M, Shimoda Y, Sato S, Tabata S, Murooka Y, Hayashi M. 2008. Polyubiquitin promoter-based binary vectors for overexpression and gene silencing in Lotus japonicus. Molecular Plant-Microbe Interactions 21: 375–382.
19. Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M, Dénarié J. 2011. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469: 58–63.
20. Miwa H, Sun J, Oldroyd GED, Downie JA. 2006. Analysis of calcium spiking using a cameleon calcium sensor reveals that nodulation gene expression is regulated by calcium spike number and the developmental status of the cell. Plant Journal 48: 883–894.
21. Miyata K, Hayafune M, Kobae Y, Kaku H, Nishizawa Y, Masuda Y, Shibuya N, Nakagawa T. 2016. Evaluation of the role of the LysM Receptor-Like Kinase, OsNFR5/OsRLK2 for AM symbiosis in rice. Plant and Cell Physiology 57: 2283–2290.
22. Miyata K, Kozaki T, Kouzai Y, Ozawa K, Ishii K, Asamizu E, Okabe Y, Umehara Y, Miyamoto A, Kobae Y et al. 2014. The bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice. Plant and Cell Physiology 55: 1864–1872.
23. 2+ by circularly permuted yellow fluorescent proteins. Proceedings of the National Academy of Sciences, USA 101: 10554–10559.
24. Oldroyd GED, Downie JA. 2006. Nuclear calcium changes at the core of symbiosis signalling. Current Opinion in Plant Biology 9: 351–357.
25. Op den Camp R, Streng A, De Mita S, Cao Q, Polone E, Liu W, Ammiraju JSS, Kudrna D, Wing R, Untergasser A et al. 2011. LysM-type mycorrhizal receptor recruited for Rhizobium symbiosis in nonlegume Parasponia. Science 331: 909–912.
26. Ozawa K, Takaiwa F. 2010. Highly efficient Agrobacterium-mediated transformation of suspension-cultured cell clusters of rice (Oryza sativa L.). Plant Science 179: 333–337.
27. Russo G, Spinella S, Sciacca E, Bonfante P, Genre A. 2013. Automated analysis of calcium spiking profiles with CaSA software: two case studies from root-microbe symbioses. BMC Plant Biology 13: 224.
28. Schmitz AM, Harrison MJ. 2014. Signaling events during initiation of arbuscular mycorrhizal symbiosis. Journal of Integrative Plant Biology 56: 250–261.
29. Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H et al. 2010. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant Journal 64: 204–214.
30. Shinya T, Motoyama N, Ikeda A, Wada M, Kamiya K, Hayafune M, Kaku H, Shibuya N. 2012. Functional characterization of CEBiP and CERK1 homologs in Arabidopsis and rice reveals the presence of different chitin receptor systems in plants. Plant and Cell Physiology 53: 1696–1706.
31. Shinya T, Nakagawa T, Kaku H, Shibuya N. 2015. Chitin-mediated plant–fungal interactions: catching, hiding and handshaking. Current Opinion in Plant Biology 26: 64–71.
32. Sun J, Miller JB, Granqvist E, Wiley-Kalil A, Gobbato E, Maillet F, Cottaz S, Samain E, Venkateshwaran M, Fort S et al. 2015. Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice. Plant Cell 27: 823–838.
33. Suzaki T, Kim CS, Takeda N, Szczyglowski K, Kawaguchi M. 2013. TRICOT encodes an AMP1-related carboxypeptidase that regulates root nodule development and shoot apical meristem maintenance in Lotus japonicus. Development 140: 353–361.
34. Willis A, Rodrigues BF, Harris PJC. 2013. The ecology of arbuscular mycorrhizal fungi. Critical Reviews in Plant Sciences 32: 1–20.
35. Zhang X, Dong W, Sun J, Feng F, Deng Y, He Z, Oldroyd GED, Wang E. 2015. The receptor kinase CERK1 has dual functions in symbiosis and immunity signalling. Plant Journal 81: 258–267.