A roadmap of cell-type specific gene expression during sequential stages of the arbuscular mycorrhiza symbiosis

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Hogekamp, Claudia ^a   Küster, Helge ^a  

^a LEIBNIZ UNIVERSITY HANNOVER   (Germany)

Author keywords

Arbuscular mycorrhizal symbiosis; Cellular expression profiling; Laser microdissection; Medicago GeneChips; Sequential reprogramming; Transcriptional regulators

Indexed keywords

ARBUSCULAR MYCORRHIZA; ARTICLE; BARREL MEDIC; CELL TYPE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EPIDERMIS CELL; FUNGAL COLONIZATION; FUNGUS HYPHAE; GENE ACTIVATION; GENE AMPLIFICATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; GLOMUS INTRARADICES; LASER MICRODISSECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT GROWTH; PLANT ROOT; RNA ISOLATION;

GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GLOMEROMYCOTA; LASER CAPTURE MICRODISSECTION; MEDICAGO TRUNCATULA; MYCORRHIZAE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT ROOTS; RNA, PLANT; SYMBIOSIS;

ARBUSCULAR; EMBRYOPHYTA; FUNGI; GLOMEROMYCOTA; GLOMUS INTRARADICES; MEDICAGO; MEDICAGO TRUNCATULA;

EID: 84877040949     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-306     Document Type: Article

References (61)

1. Schüßler A, Schwarzott D, Walker C. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 2001, 105:1413-1421.
2. Redecker D, Kodner R, Graham LE. Glomalean fungi from the Ordovician. Science 2000, 289(5486):1920-1. 10.1126/science.289.5486.1920, 10988069.
3. Parniske M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 2008, 6(10):763-75. 10.1038/nrmicro1987, 18794914.
4. Douds DD, Pfeffer PE, Shachar-Hill Y. Carbon partioning, cost and metabolism of Arbuscular Mycorrhizae. Arbuscular Mycorrhizas Physiology and Function 2000, 107-130. Dordrecht, The Netherlands: Kluwer Academic Publishers, Douds DD, Kalpunik Y.
5. Davies FT, Potter JR, Linderman RG. Drought Resistance of Mycorrhizal Pepper Plants Independent of Leaf P-Concentration - Response in Gas-Exchange and Water Relations. Physiol Plant 1993, 87(1):45-53.
6. George E, Marschner H, Jakobsen I, George E, Marschner H, Jakobsen I. Role of Arbuscular Mycorrhizal Fungi in Uptake of Phosphorus and Nitrogen from Soil. Crit Rev Biotechnol 1995, 15(3-4):257-270.
7. Kosuta S, Chabaud M, Lougnon G, Gough C, Denarie J, Barker DG, Becard G. A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol 2003, 131(3):952-62. 10.1104/pp.011882, 166861, 12644648.
8. Akiyama K, Matsuzaki K, Hayashi H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 2005, 435(7043):824-7. 10.1038/nature03608, 15944706.
9. Maillet F, Poinsot V, Andre O, Puech-Pages V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Becard G, Denarie J. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 2011, 469(7328):58-63. 10.1038/nature09622, 21209659.
10. Czaja LF, Hogekamp C, Lamm P, Maillet F, Martinez EA, Samain E, Denarie J, Kuster H, Hohnjec N. Transcriptional responses toward diffusible signals from symbiotic microbes reveal MtNFP- and MtDMI3-dependent reprogramming of host gene expression by arbuscular mycorrhizal fungal lipochitooligosaccharides. Plant Physiol 2012, 159(4):1671-85. 10.1104/pp.112.195990, 22652128.
11. Harrison MJ. Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 2005, 59:19-42. 10.1146/annurev.micro.58.030603.123749, 16153162.
12. Liu J, Blaylock L, Endre G, Cho J, Town C, VandenBosch K, Harrison MJ. Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 2003, 15:2106-2123. 10.1105/tpc.014183, 181334, 12953114.
13. Wulf A, Manthey K, Doll J, Perlick AM, Linke B, Bekel T, Meyer F, Franken P, Küster H, Krajinski F. Transcriptional changes in response to arbuscular mycorrhiza development in the model plant Medicago truncatula. Mol Plant Microbe Interact 2003, 16(4):306-14. 10.1094/MPMI.2003.16.4.306, 12744459.
14. Frenzel A, Manthey K, Perlick AM, Meyer F, Puhler A, Kuster H, Krajinski F. Combined transcriptome profiling reveals a novel family of arbuscular mycorrhizal-specific Medicago truncatula lectin genes. Mol Plant Microbe Interact 2005, 18(8):771-82. 10.1094/MPMI-18-0771, 16134889.
15. Hohnjec N, Vieweg MF, Puhler A, Becker A, Küster H. Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol 2005, 137(4):1283-301. 10.1104/pp.104.056572, 1088321, 15778460.
16. Hohnjec N, Henckel K, Bekel T, Gouzy J, Dondrup M, Goesmann A, Küster H. Transcriptional snapshots provide insights into the molecular basis of arbuscular mycorrhiza in the model legume Medicago truncatula. Funct Plant Biol 2006, 33:737-748.
17. Küster H, Vieweg MF, Manthey K, Baier MC, Hohnjec N, Perlick AM. Identification and expression regulation of symbiotically activated legume genes. Phytochemistry 2007, 68(1):8-18. 10.1016/j.phytochem.2006.09.029, 17081575.
18. Brechenmacher L, Weidmann S, van Tuinen D, Chatagnier O, Gianinazzi S, Franken P, Gianinazzi-Pearson V. Expression profiling of up-regulated plant and fungal genes in early and late stages of Medicago truncatula-Glomus mosseae interactions. Mycorrhiza 2004, 14(4):253-62. 10.1007/s00572-003-0263-4, 13680319.
19. Weidmann S, Sanchez L, Descombin J, Chatagnier O, Gianinazzi S, Gianinazzi-Pearson V. Fungal elicitation of signal transduction-related plant genes precedes mycorrhiza establishment and requires the dmi3 gene in Medicago truncatula. Mol Plant Microbe Interact 2004, 17(12):1385-93. 10.1094/MPMI.2004.17.12.1385, 15597744.
20. Sanchez L, Weidmann S, Arnould C, Bernard AR, Gianinazzi S, Gianinazzi-Pearson V. Pseudomonas fluorescens and Glomus mosseae trigger DMI3-dependent activation of genes related to a signal transduction pathway in roots of Medicago truncatula. Plant Physiol 2005, 139:1065-77. 10.1104/pp.105.067603, 1256018, 16183836.
21. Amiour N, Recorbet G, Robert F, Gianinazzi S, Dumas-Gaudot E. Mutations in DMI3 and SUNN modify the appressorium-responsive root proteome in arbuscular mycorrhiza. Mol Plant Microbe Interact 2006, 19(9):988-97. 10.1094/MPMI-19-0988, 16941903.
22. Kosuta S, Hazledine S, Sun J, Miwa H, Morris RJ, Downie JA, Oldroyd GE. Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc Natl Acad Sci USA 2008, 105(28):9823-8. 10.1073/pnas.0803499105, 2474534, 18606999.
23. Levy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ane JM, Lauber E, Bisseling T, Denarie J, Rosenberg C, Debelle F. A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 2004, 303(5662):1361-4. 10.1126/science.1093038, 14963335.
24. Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG. Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 2005, 17(12):3489-99. 10.1105/tpc.105.035410, 1315383, 16284314.
25. Genre A, Chabaud M, Faccio A, Barker DG, Bonfante P. Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota. Plant Cell 2008, 20(5):1407-20. 10.1105/tpc.108.059014, 2438458, 18515499.
26. Siciliano V, Genre A, Balestrini R, Cappellazzo G, DeWit PJ, Bonfante P. Transcriptome analysis of arbuscular mycorrhizal roots during development of the prepenetration apparatus. Plant Physiol 2007, 144(3):1455-66. 10.1104/pp.107.097980, 1914140, 17468219.
27. Ortu G, Balestrini R, Pereira PA, Becker JD, Kuster H, Bonfante P. Plant genes related to gibberellin biosynthesis and signaling are differentially regulated during the early stages of AM fungal interactions. Mol Plant 2012, 5(4):951-4. 10.1093/mp/sss027, 22451647.
28. Balestrini R, Gomez-Ariza J, Lanfranco L, Bonfante P. Laser-microdissection reveals that transcripts for five plant and one fungal phosphate transporter genes are contemporaneously present in arbusculated cells. Mol Plant Microbe Interact 2007, 20(9):1055-62. 10.1094/MPMI-20-9-1055, 17849708.
29. Fiorilli V, Catoni M, Miozzi L, Novero M, Accotto GP, Lanfranco L. Global and cell-type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. New Phytol 2009, 184(4):975-87. 10.1111/j.1469-8137.2009.03031.x, 19765230.
30. Guether M, Balestrini R, Hannah M, He J, Udvardi MK, Bonfante P. Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytol 2009, 182(1):200-12. 10.1111/j.1469-8137.2008.02725.x, 19192192.
31. Gomez SK, Javot H, Deewatthanawong P, Torres-Jerez I, Tang Y, Blancaflor EB, Udvardi MK, Harrison MJ. Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol 2009, 9:10. 10.1186/1471-2229-9-10, 2649119, 19161626.
32. Hogekamp C, Arndt D, Pereira PA, Becker JD, Hohnjec N, Kuster H. Laser-microdissection unravels cell-type-specific transcription in arbuscular mycorrhizal roots, including CAAT-box transcription factor gene expression correlating with fungal contact and spread. Plant Physiol 2011, 157(4):2023-43. 10.1104/pp.111.186635, 3327204, 22034628.
33. Gaude N, Bortfeld S, Duensing N, Lohse M, Krajinski F. Arbuscule-containing and non-colonized cortical cells of mycorrhizal roots undergo extensive and specific reprogramming during arbuscular mycorrhizal development. Plant J 2012, 69(3):510-28. 10.1111/j.1365-313X.2011.04810.x, 21978245.
34. Stockinger H, Walker C, Schüssler A. 'Glomus intraradices DAOM197198', a model fungus in arbuscular mycorrhiza research, is not Glomus intraradices. New Phytol 2009, 183:1176-1187. 10.1111/j.1469-8137.2009.02874.x, 19496945.
35. Benedito VA, Torres-Jerez I, Murray JD, Andriankaja A, Allen S, Kakar K, Wandrey M, Verdier J, Zuber H, Ott T, Moreau S, Niebel A, Frickey T, Weiller G, He J, Dai X, Zhao PX, Tang Y, Udvardi MK. A gene expression atlas of the model legume Medicago truncatula. Plant J 2008, 55(3):504-13. 10.1111/j.1365-313X.2008.03519.x, 18410479.
36. Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ. A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 2007, 104(5):1720-5. 10.1073/pnas.0608136104, 1785290, 17242358.
37. Grunwald U, Nyamsuren O, Tamasloukht M, Lapopin L, Becker A, Mann P, Gianinazzi-Pearson V, Krajinski F, Franken P. Identification of mycorrhiza-regulated genes with arbuscule development-related expression profile. Plant Mol Biol 2004, 55(4):553-66. 10.1007/s11103-004-1303-y, 15604700.
38. Manthey K, Krajinski F, Hohnjec N, Firnhaber C, Puhler A, Perlick AM, Küster H. Transcriptome profiling in root nodules and arbuscular mycorrhiza identifies a collection of novel genes induced during Medicago truncatula root endosymbioses. Mol Plant Microbe Interact 2004, 17(10):1063-77. 10.1094/MPMI.2004.17.10.1063, 15497399.
39. Doll J, Hause B, Demchenko K, Pawlowski K, Krajinski F. A member of the germin-like protein family is a highly conserved mycorrhiza-specific induced gene. Plant Cell Physiol 2003, 44(11):1208-14. 10.1093/pcp/pcg153, 14634158.
40. Floss DS, Hause B, Lange PR, Kuster H, Strack D, Walter MH. Knock-down of the MEP pathway isogene 1-deoxy-D-xylulose 5-phosphate synthase 2 inhibits formation of arbuscular mycorrhiza-induced apocarotenoids, and abolishes normal expression of mycorrhiza-specific plant marker genes. Plant J 2008, 56(1):86-100. 10.1111/j.1365-313X.2008.03575.x, 18557838.
41. Krajinski F, Hause B, Gianinazzi-Pearson V, Franken P. Mtha1, a plasma membrane H+-ATPase gene from Medicago truncatula, shows arbuscule-specific induced expression in mycorrhizal tissue. Plant Biol. 2002, 4:754-761.
42. Pumplin N, Mondo SJ, Topp S, Starker CG, Gantt JS, Harrison MJ. Medicago truncatula Vapyrin is a novel protein required for arbuscular mycorrhizal symbiosis. Plant J 2010, 61(3):482-94. 10.1111/j.1365-313X.2009.04072.x, 19912567.
43. Haney CH, Long SR. Plant flotillins are required for infection by nitrogen-fixing bacteria. Proc Natl Acad Sci USA 2010, 107(1):478-83. 10.1073/pnas.0910081107, 2806772, 20018678.
44. Glomus intraradices DB http://mycor.nancy.inra.fr.
45. Medicago truncatula DB http://www.medicago.org.
46. Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW, Bucking H, Lammers PJ, Shachar-Hill Y. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 2005, 435(7043):819-23. 10.1038/nature03610, 15944705.
47. Walter MH, Hans J, Strack D. Two distantly related genes encoding 1-deoxy-d-xylulose 5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots. Plant J 2002, 31(3):243-54. 10.1046/j.1365-313X.2002.01352.x, 12164805.
48. Navazio L, Moscatiello R, Genre A, Novero M, Baldan B, Bonfante P, Mariani P. A diffusible signal from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells. Plant Physiol 2007, 144(2):673-81. 10.1104/pp.106.086959, 1914206, 17142489.
49. Hayashi S, Reid DE, Lorenc MT, Stiller J, Edwards D, Gresshoff PM, Ferguson BJ. Transient Nod factor-dependent gene expression in the Nodulation-competent zone of soybean (Glycine max[L.] Merr.) roots. Plant Biotech J 2012, 10:995-1010.
50. Pumplin N, Harrison MJ. Live-cell imaging reveals periarbuscular membrane domains and organelle location in Medicago truncatula roots during arbuscular mycorrhizal symbiosis. Plant Physiol 2009, 151(2):809-19. 10.1104/pp.109.141879, 2754618, 19692536.
51. Zhang Q, Blaylock LA, Harrison MJ. Two Medicago truncatula half-ABC transporters are essential for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Cell 2010, 22(5):1483-97. 10.1105/tpc.110.074955, 2899874, 20453115.
52. Uehlein N, Fileschi K, Eckert M, Bienert GP, Bertl A, Kaldenhoff R. Arbuscular mycorrhizal symbiosis and plant aquaporin expression. Phytochemistry 2007, 68(1):122-9. 10.1016/j.phytochem.2006.09.033, 17109903.
53. Murray JD. Invasion by invitation: rhizobial infection in legumes. Mol Plant Microbe Interact 2011, 24(6):631-9. 10.1094/MPMI-08-10-0181, 21542766.
54. Hohnjec N, Perlick AM, Puhler A, Küster H. The Medicago truncatula sucrose synthase gene MtSucS1 is activated both in the infected region of root nodules and in the cortex of roots colonized by arbuscular mycorrhizal fungi. Mol Plant Microbe Interact 2003, 16(10):903-15. 10.1094/MPMI.2003.16.10.903, 14558692.
55. Baier MC, Keck M, Godde V, Niehaus K, Küster H, Hohnjec N. Knockdown of the symbiotic sucrose synthase MtSucS1 affects arbuscule maturation and maintenance in mycorrhizal roots of Medicago truncatula. Plant Physiol 2010, 152(2):1000-14. 10.1104/pp.109.149898, 2815868, 20007443.
56. Genre A, Ivanov S, Fendrych M, Faccio A, Zarsky V, Bisseling T, Bonfante P. Multiple exocytotic markers accumulate at the sites of perifungal membrane biogenesis in arbuscular mycorrhizas. Plant Cell Physiol 2011, 53(1):244-55.
57. Ivanov S, Fedorova EE, Limpens E, De Mita S, Genre A, Bonfante P, Bisseling T. Rhizobium-legume symbiosis shares an exocytotic pathway required for arbuscule formation. Proc Natl Acad Sci USA 2012, 109(21):8316-21. 10.1073/pnas.1200407109, 3361388, 22566631.
58. Vierheilig H, Coughlan AP, Wyss U, Piche Y. Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 1998, 64(12):5004-7. 90956, 9835596.
59. Robin Software http://mapman.gabipd.org/web/guest/robin.
60. Bekel T, Henckel K, Küster H, Meyer F, Mittard Runte V, Neuweger H, Paarmann D, Rupp O, Zakrzewski M, Pühler A, Stoye J, Goesmann A. The Sequence Analysis and Management System -SAMS-2.0: data management and sequence analysis adapted to changing requirements from traditional sanger sequencing to ultrafast sequencing technologies. J Biotechnol 2009, 140(1-2):3-12. 10.1016/j.jbiotec.2009.01.006, 19297685.
61. Oliveros JC. VENNY. An interactive tool for comparing lists with Venn Diagrams 2007, http://bioinfogp.cnb.csic.es/tools/venny/index.html.