The Medicago truncatula GRAS protein RAD1 supports arbuscular mycorrhiza symbiosis and Phytophthora palmivora susceptibility

Journal of Experimental Botany

Volumn 68, Issue 21-22, 2017, Pages 5871-5881

  Rey, Thomas ^a   Bonhomme, Maxime ^b   Chatterjee, Abhishek ^a   Gavrin, Aleksandr ^a   Toulotte, Justine ^a   Yang, Weibing ^a   André, Olivier ^b   Jacquet, Christophe ^b   Schornack, Sebastian ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITÉ PAUL SABATIER   (France)

Author keywords

Arbuscular mycorrhiza; genome wide association mapping; host susceptibility; Medicago truncatula; MtSymSCL3; oomycete; Phytophthora palmivora; RAD1; root colonization; symbiosis

Indexed keywords

DEOXYRIBONUCLEASE; PLANT PROTEIN;

BARREL MEDIC; DISEASE PREDISPOSITION; GENE EXPRESSION REGULATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; PHYTOPHTHORA; PLANT DISEASE; SYMBIOSIS;

DISEASE SUSCEPTIBILITY; ENDODEOXYRIBONUCLEASES; GENE EXPRESSION REGULATION, PLANT; GENOME-WIDE ASSOCIATION STUDY; HOST-PATHOGEN INTERACTIONS; MEDICAGO TRUNCATULA; MYCORRHIZAE; PHYTOPHTHORA; PLANT DISEASES; PLANT PROTEINS; SYMBIOSIS;

EID: 85042720058     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erx398     Document Type: Article

References (56)

1. Acevedo-Garcia J, Kusch S, Panstruga R. 2014. Magical mystery tour: MLO proteins in plant immunity and beyond. New Phytologist 204, 273-281.
2. Atwell S, Huang YS, Vilhjálmsson BJ, et al. 2010. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465, 627-631.
3. Balzergue C, Puech-Pagès V, Bécard G, Rochange SF. 2011. The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events. Journal of Experimental Botany 62, 1049-1060.
4. Benedito VA, Torres-Jerez I, Murray JD, et al. 2008. A gene expression atlas of the model legume Medicago truncatula. The Plant Journal 55, 504-513.
5. Boisson-Dernier A, Chabaud M, Garcia F, Bécard G, Rosenberg C, Barker DG. 2001. Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fxing and endomycorrhizal symbiotic associations. Molecular Plant-Microbe Interactions 14, 695-700.
6. Bonhomme M, André O, Badis Y, et al. 2014. High-density genome-wide association mapping implicates an F-box encoding gene in Medicago truncatula resistance to Aphanomyces euteiches. New Phytologist 201, 1328-1342.
7. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES. 2007. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23, 2633-2635.
8. Branca A, Paape TD, Zhou P, Briskine R, Farmer AD, Mudge J, Bharti AK, Woodward JE, May GD, Gentzbittel L. 2011. Whole-genome nucleotide diversity, recombination, and linkage disequilibrium in the model legume Medicago truncatula. Proceedings of the National Academy of Sciences, USA 108, E864-E870.
9. Bravo A, Brands M, Wewer V, Dörmann P, Harrison MJ. 2017. Arbuscular mycorrhiza-specifc enzymes FatM and RAM2 fne-tune lipid biosynthesis to promote development of arbuscular mycorrhiza. New Phytologist 214, 1631-1645.
10. Bravo A, York T, Pumplin N, Mueller LA, Harrison MJ. 2016. Genes conserved for arbuscular mycorrhizal symbiosis identifed through phylogenomics. Nature Plants 2, 15208.
11. Chaparro-Garcia A, Wilkinson RC, Gimenez-Ibanez S, Findlay K, Coffey MD, Zipfel C, Rathjen JP, Kamoun S, Schornack S. 2011. The receptor-like kinase SERK3/BAK1 is required for basal resistance against the late blight pathogen Phytophthora infestans in Nicotiana benthamiana. PLoS One 6, e16608.
12. Curtin SJ, Tiffn P, Guhlin J, et al. 2017. Validating genome-wide association candidates controlling quantitative variation in nodulation. Plant Physiology 173, 921-931.
13. Dangl JL, Horvath DM, Staskawicz BJ. 2013. Pivoting the plant immune system from dissection to deployment. Science 341, 746-751.
14. Dreher D, Yadav H, Zander S, Hause B. 2017. Is there genetic variation in mycorrhization of Medicago truncatula? PeerJ 5, e3713.
15. Evangelisti E, Gogleva A, Hainaux T, Doumane M, Tulin F, Quan C, Yunusov T, Floch K, Schornack S. 2017. Time-resolved dual transcriptomics reveal early induced Nicotiana benthamiana root genes and conserved infection-promoting Phytophthora palmivora effectors. BMC Biology 15, 39.
16. Evangelisti E, Rey T, Schornack S. 2014. Cross-interference of plant development and plant-microbe interactions. Current Opinion in Plant Biology 20, 118-126.
17. Floss DS, Lévesque-Tremblay V, Park HJ, Harrison MJ. 2016. DELLA proteins regulate expression of a subset of AM symbiosis-induced genes in Medicago truncatula. Plant Signaling and Behavior 11, e1162369.
18. Floss DS, Levy JG, Lévesque-Tremblay V, Pumplin N, Harrison MJ. 2013. DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences, USA 110, E5025-E5034.
19. Gobbato E, Wang E, Higgins G, Bano SA, Henry C, Schultze M, Oldroyd GE. 2013. RAM1 and RAM2 function and expression during arbuscular mycorrhizal symbiosis and Aphanomyces euteiches colonization. Plant Signaling and Behavior 8, e26049.
20. Gutjahr C, Parniske M. 2013. Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annual Review of Cell and Developmental Biology 29, 593-617.
21. Haas BJ, Kamoun S, Zody MC, et al. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461, 393-398.
22. Hirsch S, Kim J, Muñoz A, Heckmann AB, Downie JA, Oldroyd GE. 2009. GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. The Plant Cell 21, 545-557.
23. Huisman R, Bouwmeester K, Brattinga M, Govers F, Bisseling T, Limpens E. 2015. Haustorium formation in Medicago truncatula roots infected by Phytophthora palmivora does not involve the common endosymbiotic program shared by arbuscular mycorrhizal fungi and rhizobia. Molecular Plant-Microbe Interactions 28, 1271-1280.
24. Jones JD, Dangl JL. 2006. The plant immune system. Nature 444, 323-329.
25. Kang HM, Sul JH, Service SK, Zaitlen NA, Kong SY, Freimer NB, Sabatti C, Eskin E. 2010. Variance component model to account for sample structure in genome-wide association studies. Nature Genetics 42, 348-354.
26. Kang Y, Sakiroglu M, Krom N, Stanton-Geddes J, Wang M, Lee YC, Young ND, Udvardi M. 2015. Genome-wide association of drought-related and biomass traits with HapMap SNPs in Medicago truncatula. Plant, Cell and Environment 38, 1997-2011.
27. Kim G-B, Nam Y-W. 2013. A novel GRAS protein gene MtSymSCL1 plays a role in regulating nodule number in Medicago truncatula. Plant Growth Regulation 71, 77-92.
28. Laffont C, Rey T, André O, Novero M, Kazmierczak T, Debellé F, Bonfante P, Jacquet C, Frugier F. 2015. The CRE1 cytokinin pathway is differentially recruited depending on Medicago truncatula root environments and negatively regulates resistance to a pathogen. PLoS One 10, e0116819.
29. Lauressergues D, Delaux PM, Formey D, Lelandais-Brière C, Fort S, Cottaz S, Bécard G, Niebel A, Roux C, Combier JP. 2012. The microRNA miR171h modulates arbuscular mycorrhizal colonization of Medicago truncatula by targeting NSP2. The Plant Journal 72, 512-522.
30. Le Signor C, Aimé D, Bordat A, et al. 2017. Genome-wide association studies with proteomics data reveal genes important for synthesis, transport and packaging of globulins in legume seeds. New Phytologist 214, 1597-1613.
31. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408.
32. Moreau S, Fromentin J, Vailleau F, Vernié T, Huguet S, Balzergue S, Frugier F, Gamas P, Jardinaud M F. 2014. The symbiotic transcription factor MtEFD and cytokinins are positively acting in the Medicago truncatula and Ralstonia solanacearum pathogenic interaction. New Phytologist 201, 1343-1357.
33. Mukhtar MS, Carvunis AR, Dreze M, et al. 2011. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333, 596-601.
34. Murakami Y, Yokoyama H, Fukui R, Kawaguchi M. 2013. Down-regulation of NSP2 expression in developmentally young regions of Lotus japonicus roots in response to rhizobial inoculation. Plant and Cell Physiology 54, 518-527.
35. Nars A, Rey T, Laftte C, et al. 2013. An experimental system to study responses of Medicago truncatula roots to chitin oligomers of high degree of polymerization and other microbial elicitors. Plant Cell Reports 32, 489-502.
36. Oldroyd GE. 2013. Speak, friend, and enter: signalling systems that promote benefcial symbiotic associations in plants. Nature Reviews. Microbiology 11, 252-263.
37. Oldroyd GE, Murray JD, Poole PS, Downie JA. 2011. The rules of engagement in the legume-rhizobial symbiosis. Annual Review of Genetics 45, 119-144.
38. Park HJ, Floss DS, Levesque-Tremblay V, Bravo A, Harrison MJ. 2015. Hyphal branching during arbuscule development requires reduced arbuscular mycorrhiza1. Plant Physiology 169, 2774-2788.
39. Pimprikar P, Carbonnel S, Paries M, et al. 2016. A CCaMK-CYCLOPS-DELLA complex activates transcription of RAM1 to regulate arbuscule branching. Current Biology 26, 987-998.
40. Pislariu CI, Murray JD, Wen J, et al. 2012. A Medicago truncatula tobacco retrotransposon insertion mutant collection with defects in nodule development and symbiotic nitrogen fxation. Plant Physiology 159, 1686-1699.
41. Popp C, Ott T. 2011. Regulation of signal transduction and bacterial infection during root nodule symbiosis. Current Opinion in Plant Biology 14, 458-467.
42. Rey T, Chatterjee A, Buttay M, Toulotte J, Schornack S. 2015. Medicago truncatula symbiosis mutants affected in the interaction with a biotrophic root pathogen. New Phytologist 206, 497-500.
43. Rey T, Laporte P, Bonhomme M, Jardinaud MF, Huguet S, Balzergue S, Dumas B, Niebel A, Jacquet C. 2016. MtNF-YA1, a central transcriptional regulator of symbiotic nodule development, is also a determinant of Medicago truncatula susceptibility toward a root pathogen. Frontiers in Plant Science 7, 1837.
44. Rey T, Nars A, Bonhomme M, et al. 2013. NFP, a LysM protein controlling Nod factor perception, also intervenes in Medicago truncatula resistance to pathogens. New Phytologist 198, 875-886.
45. Rey T, Schornack S. 2013. Interactions of benefcial and detrimental root-colonizing flamentous microbes with plant hosts. Genome Biology 14, 121.
46. Saville RJ, Gosman N, Burt CJ, Makepeace J, Steed A, Corbitt M, Chandler E, Brown JK, Boulton MI, Nicholson P. 2012. The 'Green Revolution' dwarfng genes play a role in disease resistance in Triticum aestivum and Hordeum vulgare. Journal of Experimental Botany 63, 1271-1283.
47. Stanton-Geddes J, Paape T, Epstein B, et al. 2013. Candidate genes and genetic architecture of symbiotic and agronomic traits revealed by whole-genome, sequence-based association genetics in Medicago truncatula. PLoS One 8, e65688.
48. Urbanski DF, Małolepszy A, Stougaard J, Andersen SU. 2012. Genome-wide LORE1 retrotransposon mutagenesis and high-throughput insertion detection in Lotus japonicus. The Plant Journal 69, 731-741.
49. van Schie CC, Takken FL. 2014. Susceptibility genes 101: how to be a good host. Annual Review of Phytopathology 52, 551-581.
50. Verdier J, Torres-Jerez I, Wang M, Andriankaja A, Allen SN, He J, Tang Y, Murray JD, Udvardi MK. 2013. Establishment of the Lotus japonicus gene expression atlas (LjGEA) and its use to explore legume seed maturation. The Plant Journal 74, 351-362.
51. Wang E, Schornack S, Marsh JF, Gobbato E, Schwessinger B, Eastmond P, Schultze M, Kamoun S, Oldroyd GE. 2012. A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Current Biology 22, 2242-2246.
52. Xue L, Cui H, Buer B, Vijayakumar V, Delaux PM, Junkermann S, Bucher M. 2015. Network of GRAS transcription factors involved in the control of arbuscule development in Lotus japonicus. Plant Physiology 167, 854-871.
53. Yan HZ, Liou R F. 2006. Selection of internal control genes for real-time quantitative RT-PCR assays in the oomycete plant pathogen Phytophthora parasitica. Fungal Genetics and Biology 43, 430-438.
54. Young ND, Debellé F, Oldroyd GE, et al. 2011. The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480, 520-524.
55. Yu J, Pressoir G, Briggs WH, et al. 2006. A unifed mixed-model method for association mapping that accounts for multiple levels of relatedness. Nature Genetics 38, 203-208.
56. Zhang Z, Ersoz E, Lai CQ, et al. 2010. Mixed linear model approach adapted for genome-wide association studies. Nature Genetics 42, 355-360.