Beneficial Plant-Microbe Interaction Research
National Key Laboratory of Plant Molecular Genetics
Jeremy Murray
Personal Profile
2017-present CEPAMS, Institute of Plant Physiology & Ecology, CAS, Principle Invistigator, Shanghai, China
2010-2017 John Innes Centre, Group leader, Norwich, UK
2006-2009 The Noble Institute, Oklahoma, USA,Postdoc
2003-2006 SCPFRC, London, Canada, Postdoc
1998-2003 PhD University of Guelph, Guelph, Canada
1993-1997 MSc University of Western Ontario, London, Canada
1989-1993 BSc Dalhousie University, Halifax, Canada
Research Work
Our research seeks to uncover the molecular mechanisms underlying symbiotic infection of plants by beneficial microbes. To do this we are studying the processes underlying infection of plant roots by rhizobia and arbuscular mycorrhiza. Rhizobia are N-fixing bacteria that colonize the roots of plants to form an endosymbiosis with legumes in which fixed N is provided to the host plant in specialized organs called nodules. This symbiosis, called nodulation, has evolved from a more ancient interaction that arbuscular mycorrhizal fungi form with most land plants. In order to understand how these microbes are accommodated by the host plant we will identify host components required for the colonization of plant roots and the formation of intracellular infection structures.
Main Achievements
Recent research accomplishments include the identification of NLP2 as a key transcription factor for expression of leghemoglobins in nodules (Jiang et al., 2021, Science) and the role of NPF6.5 transporter in chloride uptake and plant preference for nitrate over chloride (Xiao et al., 2021, EMBO). We have also shown that components of a mitotic module are involved in rhizobial infection (Gao et al., 2022, PNAS; Breakspear et al., 2014, Plant Cell). In earlier studies we identified VAPYRIN as the first ‘common symbiotic’ protein, required for infection of both rhizobia and arbuscular mycorrhizal fungi (Murray et al., 2011, Plant Journal) and showed it belongs to a complex which is found at the growing tip of rhizobial infection threads which we named the ‘infectosome’ (Liu et al., 2019, Nature Communications).
Publications
1. Gao J.P.#, Liang W.J.#, Jiang S.Y., Yan Z.Y., Zhou C.E., Wang E.T., Murray J.D.* (2023) NODULE INCEPTION activates gibberellin biosynthesis genes during rhizobial infection, New Phytol, doi: 10.1111/nph.18759.
2. Gao J.P., Jiang S.Y., Su Y.Y., Xu P., Wang J.J., Liang W.J., Liu C.W., Murray J.D.* (2022) Intracellular infection by symbiotic bacteria requires the mitotic kinase AURORA1, PNAS, 119(43):e2202606119. doi: 10.1073/pnas.2202606119.
3. Kumar A., Lin H., Li Q.J., Ruan Y.T., Cousins D., Li F.Y., Gao S., Jackson K., Wen J.Q., Murray J.D.*, Xu P.* (2022) Anthocyanin pigmentation as a quantitative visual marker for arbuscular mycorrhizal fungal colonization of Medicago truncatula roots, New Phytol, 236:1988-1998. doi: 10.1111/nph.18504.
4. Gu B.G., Chen Y., Xie F., Murray J.D., Millar A.J.* (2022) Inorganic Nitrogen Transport and Assimilation in Pea ( Pisum sativum), Genes (Basel), 13(1):158, doi: 10.3390/genes13010158.
5. Wang D.P., Dong W.T., Murray J.D.*, Wang E.T.* (2022) Innovation and Appropriation in Mycorrhizal and Rhizobial Symbioses, Plant Cell, koac039, doi: 10.1093/plcell/koac039.
6. Jiang S.Y., Jardinaud M-F, Gao J.P., Pecrix Y., Wen J.Q., Mysore K., Xu P., Sanchez-Canizares C., Ruan Y.T., Li Q.J., Zhu M.J., Li F.Y., Wang E.T., Poole P.S., Gamas P., and Murray J.D.* (2021) NIN-Like Protein Transcription factors regulate leghemoglobin genes in legume nodules, Science, 374, 6567, doi: 10.1126/science.abg5945.
7. Xiao Q.Y.#, Chen Y.#, Liu C.W.#, Robson F., Roy S., Cheng X.F., Wen J.Q., Mysore K., Miller A.J.*, Murray J.D.* (2021) MtNPF6.5 mediates chloride uptake and nitrate preference in Medicago roots. EMBO J. doi: 10.15252/embj.2020106847.
8. Banasiak J., Jamruszka T., Murray J.D., Jasiński M. (2021) A roadmap of plant membrane transporters in arbuscular mycorrhizal and legume-rhizobium symbioses, Plant Physiology, kiab280, doi: 10.1093/plphys/kiab280.
9. Gao J.P., Xu P., Wang M.X., Zhang X.W., Yang J., Zhou Y., Murray J.D., Song C.P., Wang E.T.* (2021) Nod factor receptor complex phosphorylates GmGEF2 to stimulate ROP signaling during nodulation. Curr Biol. 31:3538-3550. doi: 10.1016/j.cub.2021.06.011.
10. Jacott C., Ridout C., Murray J.D.* (2021) Unmasking mildew resistance Locus O, Trends in Plant Science, doi: 10.1016/j.tplants.2021.05.009
11. Karas, B.J., Ross L., Novero M., Amyot L., Shrestha A., Inada, Sa., Nakano, M., Sakai T., Bonetta D., Sato Sushei, Murray J.D., Bonfante P., Szczyglowski K.* (2021) Intragenic complementation at the Lotus japonicus CELLULOSE SYNTHASE-LIKE D1 locus rescues root hair defects. Plant Physiology, 186: 2037–2050.
12. Ruan Y., Chen K., Su Y., Jiang S., Xu P.*, and Murray J.D.* (2021) A root tip-specific expressing anthocyanin marker for direct identification of transgenic tissues by the naked eye in symbiotic studies. Plants (Basel).10(3):605. doi: 10.3390/plants10030605.
13. Roy S., Breakspear A., Cousins D., Torres-Jerez I., Jackson, K., Kumar, A., Su Y., Liu, C-W, Krom, N., Udvardi M., Xu P., Murray J.D.* (2021) Three common symbiotic ABC-B transporters in Medicago truncatula are regulated by a NIN-independent branch of the symbiosis signalling pathway, Mol Plant Microbe Interact. doi: 10.1094/MPMI-02-21-0036-R.
14. Liu M.X., Jia N., Li X.L., Liu R.J., Xie Q., Murray J.D., Downie J.A., Xie F.* (2021) CERBERUS is critical for stabilization of VAPYRIN during rhizobial infection in Lotus japonicus. New Phytol. 229(3):1684-1700. doi: 10.1111/nph.16973.
15. Jacott C., Charpentier M., Murray J.D.*, Ridout C.* (2020) Mildew Locus O facilitates colonization by arbuscular mycorrhizal fungi in angiosperms. New Phytol. 227(2):343-351. doi: 10.1111/nph.16465.
16. Kumar A.#, Cousins D.R.#, Liu C.W., Xu P.*, Murray J.D.* (2020) Nodule inception is not required for arbuscular mycorrhizal colonization of Medicago truncatula. Plants (Basel). 9(1):71. doi: 10.3390/plants9010071.
17. Li H.X., Liu Y.*, Qin H.H., Lin X.L., Tang D., Wu Z.J., Luo W., Shen Y., Dong F.Q., Wang Y.L., Feng T.T., Wang L.L., Li L.Y., Chen D.D., Zhang Y., Murray J.D., Chao D.Y., Chong K., Cheng Z.K.*, Meng Z* (2020) A rice chloroplast-localized ABC transporter ARG1 modulates cobalt and nickel homeostasis and contributes to photosynthetic capacity. New Phytol. 228(1):163-178. doi: 10.1111/nph.16708.
18. Menéndez E.#, Robledo M.#, Jiménez-Zurdo J.I., Velázquez E., Rivas R., Murray J.D., Mateos P.F.* (2019) Legumes display common and host-specific responses to the rhizobial cellulase CelC2 during primary symbiotic infection. Sci Rep. 9(1):13907. doi: 10.1038/s41598-019-50337-3.
19. Liu C.W. , Breakspear A., Stacey N., Findlay K., Nakashima J., Ramakrishnan K., Endre G., de Carvalho-Niebel F., Oldroyd G.E.D., Udvardi M.K., Fournier J.*, Murray J.D.* (2019) A protein complex required for polar growth of rhizobial infection threads. Nature Comm. 10(1):2848. doi: 10.1038/s41467-019-10029-y.
20. Liu C.W.#, Breakspear A.#, Guan D., Cerri M.R., Abbs K., Jiang S.Y., Robson FC, Radhakrishnan G., Roy S., Bone C., Stacey N., Rogers C., Trick M., Niebel A., Oldroyd G.E., de Carvalho-Niebel F., Murray J.D.*(2019) NIN acts as a Network Hub Controlling a Growth Module Required for Rhizobial Infection. Plant Physiol. 179(4):1704-1722. doi: 10.1104/pp.18.01572.
21. Murray J.D.*, Liu C.W., Chen Y., Miller A.J.* (2017) Nitrogen sensing in legumes. J Exp Bot. 68(8):1919-1926. doi: 10.1093/jxb/erw405. (review)
22. Roy S., Robson F., Lilley J., Liu C.W., Cheng X.F., Wen J.Q., Walker S., Sun J., Cousins D., Bone C., Bennett M.J., Downie J.A, Swarup R., Oldroyd G., Murray J.D.* (2017) MtLAX2, an orthologue of the Arabidopsis auxin influx transporter AUX1, is required for nodule organogenesis. Plant Physiol. 174(1):326-338. doi: 10.1104/pp.16.01473.
23. Liu C.W., Murray J.D.* (2016) The role of flavonoid and related compounds in nodulation host-range specificity: an update. Plants (MDPI). 5(3):33. doi: 10.3390/plants5030033.
24. Hossain M.S., Shrestha A., Zhong S., Miri M., Austin R.S., Sato S., Ross L., Huebert T., Tromas A., Torres-Jerez I., Tang Y., Udvardi M., Murray J.D., Szczyglowski K.* (2016) Lotus japonicus NF-YA1 Plays an essential role During Nodule Differentiation and Targets Members of the SHI/STY Gene Family. Mol Plant Microbe Interact. 29(12):950-964. doi: 10.1094/MPMI-10-16-0206-R.
25. Kryvoruchko I.S.#, Sinharoy S.#, Torres-Jerez I., Sosso D., Pislariu C.I., Guan D., Murray J.D., Benedito V.A., Frommer W.B., Udvardi M.K.* (2016) MtSWEET11, a nodule-specific sucrose transporter of Medicago truncatula. Plant Physiol. 171(1):554-65. doi: 10.1104/pp.15.01910.
26. Sinharoy S., Liu C., Breakspear A., Guan D., Shailes S., Nakashima J., Zhang S. Wen J., Torres-Jerez I., Oldroyd G., Murray J.D., Udvardi MK.* (2016) A Medicago truncatula cystathionine-β-synthase-like domain-containing protein is required for rhizobial infection and symbiotic nitrogen fixation. Plant Physiol. 170(4):2204-17. doi: 10.1104/pp.15.01853.
27. Chen D.S., Liu C.W., Roy S., Cousins D., Stacey N., Murray J.D.* (2015) Identification of a core set of rhizobial infection genes using data from single cell-types. Front Plant Sci. 6:575. doi: 10.3389/fpls.2015.00575.
Horváth B., Domonkos á., Kereszt A., Sz?cs A., ábrahám E., Ayaydin F., Bóka K., Chen Y., Chen R., Murray J.D., Udvardi MK., Kondorosi é, Kaló P.* (2015) Loss of the nodule-specific cysteine rich peptide, NCR169, abolishes symbiotic nitrogen fixation in the Medicago truncatula dnf7 mutant. PNAS 112(49):15232-7. doi: 10.1073/pnas.1500777112.
28. Liu C.W., Breakspear A., Roy S., Murray J.D.* (2015) Cytokinin responses counterpoint auxin signaling during rhizobial infection. Plant Signal Behav. 10(6):e1019982. doi: 10.1080/15592324.2015.1019982.
29. Breakspear A., Liu C., Roy S., Stacey N., Rogers C., Trick M., Morieri G., Mysore K.S., Wen J., Oldroyd G.E.D., Downie J.A., Murray J.D.* (2014) The root hair ‘Infectome’ of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for auxin signalling in rhizobial infection. Plant Cell. 26(12):4680-701. doi: 10.1105/tpc.114.133496.
30. Wang E., Yu N., Asma Bano S., Liu C., Miller A.J., Cousins D., Zhang X., Ratet P., Tadege M., Mysore K.S., Downie J.A., Murray J.D., Oldroyd G.E.D., Schultze M.* (2014) A H+-ATPase that energizes nutrient uptake during mycorrhizal symbioses in rice and Medicago truncatula. Plant Cell. 26(4):1818-1830. doi: 10.1105/tpc.113.120527.
Murray J.D.*, Cousins D.R., Jackson K.J., Liu C. (2013) Signaling at the root surface: the role of cutin monomers in mycorrhization. Mol. Plant. 6(5):1381-3. doi: 10.1093/mp/sst090.
31. Wang M., Verdier J., Benedito V.A., Tang Y., Murray J.D., Ge Y., Becker J.D., Carvalho H., Rogers C., Udvardi M., He J. (2013) LegumeGRN: a gene regulatory network prediction server for functional and comparative studies. Plos One. 8(7):e67434. doi: 10.1371/journal.pone.0067434.
32. Guan D., Stacey N., Liu C., Wen J., Mysore K.S., Torres-Jerez I., Vernie T., Tadege M., Zhou C., Wang Z.Y., Udvardi M.K., Oldroyd G.E., and Murray J.D.* (2013) Rhizobial infection is associated with the development of peripheral vasculature in nodules of Medicago truncatula. Plant Physiol. 162(1):107-15. doi: 10.1104/pp.113.215111.
33. Verdier J., Torres-Jerez I., Wang M., Andriankaja A., Allen S.N., He J., Tang Y., Murray J.D., Udvardi M.K.* (2013) Establishment of the Lotus japonicus Gene Expression Atlas (LjGEA) and its use to explore legume seed maturation. Plant Journal. 74(2):351-62. doi: 10.1111/tpj.12119.
34. Pislariu C.I.#, Murray J.D.#, Wen J., Cosson V., Muni R.R., Wang M., Benedito V.A., Andriankaja A., Cheng X., Jerez I.T., Mondy S., Zhang S., Taylor M.E., Tadege M., Ratet P., Mysore K.S., Chen R., Udvardi M.K.* (2012) A Medicago truncatula tobacco retrotransposon insertion mutant collection with defects in nodule development and symbiotic nitrogen fixation. Plant Physiol. 159(4):1686-99. doi: 10.1104/pp.112.197061.
35. Xie F., Murray J.D., Kim J., Heckmann A.B., Edwards A., Oldroyd G.E., Downie J.A.* (2012) Legume pectate lyase required for root infection by rhizobia. PNAS. 109(2):633-8. doi: 10.1073/pnas.1113992109.
36. Young N.D.#, Debellé F. #, Oldroyd G.E.#, Geurts R., Cannon S.B., Udvardi M.K., Benedito V.A., Mayer K.F., Gouzy J., Schoof H., Van de Peer Y., Proost S., Cook D.R., Meyers B.C., Spannagl M., Cheung F., De Mita S., Krishnakumar V., Gundlach H., Zhou S., Mudge J., Bharti A.K., Murray J.D., Naoumkina M.A., Rosen B., Silverstein K.A., Tang H., Rombauts S., Zhao P.X., Zhou P., Barbe V., Bardou P., Bechner M., Bellec A., Berger A., Bergès H., Bidwell S., Bisseling T., Choisne N., Couloux A., Denny R., Deshpande S., Dai X., Doyle J.J., Dudez A.M., Farmer A.D., Fouteau S., Rogers J., Town C.D., Roe B.A.* (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature. 480(7378):520-4. doi: 10.1038/nature10625.
37. Murray J.D.* (2011) Invasion by invitation: rhizobial infection in legumes. Molecular Plant Microbe Interactions 24:631-9. (Review)
38. Oldroyd G.E., Murray J.D., Poole P.S., Downie J.A.* (2011) The rules of engagement in the legume-rhizobial symbiosis. Annual Review of Genetics 45:119-144. (Review)
39. Murray J.D., Muni R.R.D., Torres-Jerez I., Tang Y., Allen S., Andriankaja M., Li G., Laxmi A., Cheng X., Wen J., Vaughan D., Schultze M., Sun J., Charpentier M., Oldroyd G., Tadege M., Ratet P., Mysore K.S., Chen R., Udvardi M.K.* (2011) Vapyrin, a gene essential for intracellular progression of arbuscular mycorrhizal symbiosis, is also essential for infection by rhizobia in the nodule symbiosis of Medicago truncatula. Plant Journal. 65(2):244-52. doi: 10.1111/j.1365-313X.2010.04415.x.
40. Lefebvre B., Timmers T., Mbengue M., Moreau S., Hervé C., Tóth K., Bittencourt-Silvestre J., Klaus D., Deslandes L., Godiard L., Murray J.D., Udvardi M.K., Raffaele S., Mongrand S., Cullimore J., Gamas P., Niebel A., Ott T.* (2010) A remorin protein interacts with symbiotic receptors and regulates bacterial infection. PNAS. 107(5):2343-8. doi: 10.1073/pnas.0913320107.
41. Frugier F., Kosuta S., Murray J., Crespi M.*, Szczyglowski K.* (2008) Cytokinin: secret agent of symbiosis. Trends in Plant Science. 13(3):115-20. doi: 10.1016/j.tplants.2008.01.003.
42. He J.#*, Benedito V.A.#, Wang M., Murray J.D., Zhao P.X., Tang Y., Udvardi M.K.* (2009) The Medicago truncatula gene expression atlas web server. BMC Bioinformatics. 10:441. doi: 10.1186/1471-2105-10-441.
43. Benedito V.A., Torres-Jerez, I., Murray J.D., Andriankaja A., Allen S., Kakar K., Wandrey M., Gallardo K., Thompson R., Ott T., Moreau S., Niebel A., He J., Dai X., Zhao P.X., Tang Y., Udvardi M.K.* (2008) A gene expression atlas of the model legume, Medicago truncatula. Plant Journal .55(3):504-13. doi: 10.1111/j.1365-313X.2008.03519.x.
44. Udvardi M.K.*, Kakar K., Wandrey M., Ombretta M., Murray J.D., Andriankaja A., Zhang, J.Y., Benedito, V., Hofer J.M.I., Chueng F., Town C.D. (2007) Legume transcription factors: global regulators of plant development and response to the environment. Plant Physiol. 144(2):538-49. doi: 10.1104/pp.107.098061.
45. Murray J., Karas B.J., Sato S., Tabata S., Amyot L., Szczyglowski K.* (2007) A cytokinin perception mutant colonized by rhizobium in the absence of nodule organogenesis. Science. 315(5808):101-4. doi: 10.1126/science.1132514.
46. Murray J., Karas B., Ross L., Brachmann A., Wagg C., Geil R., Perry J., Nowakowski K., MacGillivary M., Held M., Stougaard J., Peterson L., Parniske M., Szczyglowski K* (2006) Genetic suppressors of the Lotus japonicus har1-1 hypernodulation phenotype. Mol Plant Microbe Interact. 19(10):1082-91. doi: 10.1094/MPMI-19-1082.
47. Murray J., Geil R., Wagg C., Karas B., Szczyglowski K., Peterson R.L.* (2006) Genetic supressors of Lotus japonicus har1-1 hypernodulation show altered interactions with Glomus intraradices. Funct Plant Biol. 33(8):749-755. doi: 10.1071/FP06083.
48. Sandal N.*, Petersen T.R., Murray J., Umehara Y., Karas B., Yano K., Kumagai H., Yoshikawa M., Saito K., Hayashi M., Murakami Y., Wang X., Hakoyama T., Imaizumi-Anraku H., Sato S., Kato T., Chen W., Hossain Md.S., Shibata S., Wang T., Yokota K., Larsen K., Kanamori N., Madsen E., Radutoiu S., Madsen L.H., Radu T.G., Krusell L., Ooki Y., Banba M., Betti M., Rispail N., Sk?t L., Tuck E., Perry J., Yoshida S., Vickers K., Pike J., Mulder L., Charpentier M., Ohtomo .R, Kojima T., Ando S., Marquez A.J., Gresshoff P.M., Harada K., Webb J., Hata S., Suganuma N., Kouchi H., Kawasaki S., Tabata S., Hayashi M., Parniske M., Szczyglowski K., Kawaguchi M., Stougaard J. (2006). Genetics of symbiosis in Lotus japonicus: Recombinant inbred lines, comparative genetic maps and map position of 35 symbiotic loci. Mol Plant Microbe Interact. 19(1):80-91. doi: 10.1094/MPMI-19-0080.
49. Karas B.J.#, Murray J.D.#, Gorzelak M., Smith A., Sato S., Tabata S., Szczyglowski K.* (2005). Invasion of Lotus japonicus root hairless 1 by Mesorhizobium loti Involves the Nodulation Factor-Dependent Induction of Root Hairs. Plant Physiol. 137(4):1331-44. doi: 10.1104/pp.104.057513.
50. Murray J.D., Michaels T.E., Cardona C., Schaafsma A.W., Pauls K.P.* (2004) Quantitative trait loci for leafhopper (Empoasca fabae and Empoasca kraemeri) resistance and seed weight in the common bean. Plant Breeding. 123(5):474-479. doi: 10.1111/j.1439-0523.2004.01020.x.
51. Murray J.D., Michaels T.E., Pauls K.P., Cardona C., Schaafsma A.W.* (2004) Yield and insect injury in leafhopper (Empoasca fabae Harris and Empoasca kraemeri Ross & Moore) infested dry beans in Ontario and Colombia. Can. J of Plant Sci. 84(3):891-900. doi: 10.4141/p02-161.
52. Murray J.D., Larsen J., Michaels T.E., Schaafsma A., Vallejos C.E., Pauls K.P.* (2002) Identification of putative genes in bean (Phaseolus vulgaris) genomic (Bng) RFLP clones and their conversion to STSs. Genome. 45(6):1013-24. doi: 10.1139/g02-069.
53. Murray J.D., Michaels T.E., Pauls K.P., Schaafsma A.W.* (2001) Determination of traits associated with leafhopper (Empoasca fabae and Empoasca kraemeri) resistance and dissection of leafhopper damage symptoms in the common bean (Phaseolus vulgaris). Annals of Applied Biology. 139: 319-32. doi: 10.1111/j.1744-7348.2001.tb00145.x.