DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 51, 2013, Pages

  Floss, Daniela S ^a   Levy, Julien G ^a,b   Lévesque Tremblay, Véronique ^a   Pumplin, Nathan ^a,c   Harrison, Maria J ^a  

^a United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c ETH ZURICH   (Switzerland)

Author keywords

Biotrophic; Cyclops; Endosymbiosis; Lotus japonicus; Phytohormone

Indexed keywords

DELLA1 PROTEIN; DELLA2 PROTEIN; GIBBERELLIC ACID; MUTANT PROTEIN; PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARBUSCULE; ARTICLE; BARREL MEDIC; DMI3 GENE; ENDODERMIS; FUNGUS HYPHAE; GLOMUS (FUNGUS); GLOMUS VERSIFORME; INOCULATION; IPD3 GENE; LOTUS JAPONICUS; MAIZE; MONOCOT; MYCORRHIZA; NSP1 GENE; NSP2 GENE; PHENOTYPE; PLANT GROWTH; PRIORITY JOURNAL; PROMOTER REGION; RICE; ROOT CORTEX; ROOT LENGTH; SIGNAL TRANSDUCTION; SYMBIONT; TIGHT JUNCTION; TRANSCRIPTION REGULATION; VASCULAR TISSUE; WHEAT; WILD TYPE;

EID: 84890818304     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1308973110     Document Type: Article

References (116)

1. Smith SE, Read DJ (2008) Mycorrhizal Symbiosis (Academic, San Diego).
2. Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: Phylogeny and evolution. Mycol Res 105(12):1414-1421.
3. van der Heijden MGA, et al. (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69-72.
4. Fester T, Sawers R (2011) Progress and Challenges in Agricultural Applications of Arbuscular Mycorrhizal Fungi. Crit Rev Plant Sci 30(5):459-470.
5. Harrison MJ (2012) Cellular programs for arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 15(6):691-698.
6. Parniske M (2008) Arbuscular mycorrhiza: The mother of plant root endosymbioses. Nat Rev Microbiol 6(10):763-775.
7. Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413(6853):297-299.
8. Sanders FE (1974) The effect of foliar-Applied phosphate on the mycorrhizal infections of onion roots. Endomycorrhizas, eds Sanders FE, Mosse B, Tinker PB (Academic, London), pp 261-277.
9. Helber N, et al. (2011) A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp is crucial for the symbiotic relationship with plants. Plant Cell 23(10):3812-3823.
10. Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: New paradigms from cellular to ecosystem scales. Ann Rev Plant Biol 62:227-250.
11. Oldroyd GED (2013) Speak, friend, and enter: Signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11(4):252-263.
12. Lévy J, et al. (2004) A putative Ca2+ and calmodulin-Dependent protein kinase required for bacterial and fungal symbioses. Science 303(5662):1361-1364.
13. Banba M, et al. (2008) Divergence of evolutionary ways among common sym genes: CASTOR and CCaMK show functional conservation between two symbiosis systems and constitute the root of a common signaling pathway. Plant Cell Physiol 49(11): 1659-1671.
14. Gutjahr C, et al. (2008) Arbuscular mycorrhiza-Specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell 20(11):2989-3005.
15. Tirichine L, et al. (2006) Deregulation of a Ca2+/calmodulin-Dependent kinase leads to spontaneous nodule development. Nature 441(7097):1153-1156.
16. Yano K, et al. (2008) CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc Natl Acad Sci USA 105(51):20540-20545.
17. Messinese E, et al. (2007) A novel nuclear protein interacts with the symbiotic DMI3 calcium-And calmodulin-Dependent protein kinase of Medicago truncatula. Mol Plant Microbe Interact 20(8):912-921.
18. Horváth B, et al. (2011) Medicago truncatula IPD3 is a member of the common symbiotic signaling pathway required for rhizobial and mycorrhizal symbioses. Mol Plant Microbe Interact 24(11):1345-1358.
19. Ovchinnikova E, et al. (2011) IPD3 controls the formation of nitrogen-Fixing symbiosomes in pea and Medicago Spp. Mol Plant Microbe Interact 24(11):1333-1344.
20. Pumplin N, et al. (2010) Medicago truncatula Vapyrin is a novel protein required for arbuscular mycorrhizal symbiosis. Plant J 61(3):482-494.
21. Murray JD, et al. (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 J 65(2):244-252.
22. Feddermann N, et al. (2010) The PAM1 gene of petunia, required for intracellular accommodation and morphogenesis of arbuscular mycorrhizal fungi, encodes a homologue of VAPYRIN. Plant J 64(3):470-481.
23. Oldroyd GED, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519-546.
24. Gobbato E, et al. (2012) A GRAS-Type transcription factor with a specific function in mycorrhizal signaling. Curr Biol 22(23):2236-2241.
25. Maillet F, et al. (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469(7328):58-63.
26. Liu J, et al. (2003) Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15(9):2106-2123.
27. Güimil S, et al. (2005) Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc Natl Acad Sci USA 102(22):8066-8070.
28. Hogekamp C, et al. (2011) 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 157(4): 2023-2043.
29. Gaude N, Bortfeld S, Duensing N, Lohse M, Krajinski F (2012) Arbuscule-Containing and non-Colonized cortical cells of mycorrhizal roots undergo extensive and specific reprogramming during arbuscular mycorrhizal development. Plant J 69(3):510-528.
30. Kistner C, et al. (2005) Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 17(8): 2217-2229.
31. Bruce A, Smith SE, Tester M (1994) The development of mycorrhizal infection in cucumber-Effects of P-Supply on root growth, formation of entry points and growth of infection units. New Phytol 127(3):507-514.
32. Pearson JN, Smith SE, Smith FA (1991) Effect of photon irradiance on the development and activity of VA mycorrhizal infection in Allium porrum. Mycol Res 95(6):741-746.
33. Breuillin F, et al. (2010) Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 64(6):1002-1017.
34. Javot H, et al. (2011) Medicago truncatula mtpt4 mutants reveal a role for nitrogen in the regulation of arbuscule degeneration in arbuscular mycorrhizal symbiosis. Plant J 68(6):954-965.
35. Gomez SK, et al. (2009) Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol 9(10):10.
36. Guether M, et al. (2009) Genome-Wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytol 182(1):200-212.
37. Manthey K, et al. (2004) Transcriptome profiling in root nodules and arbuscular mycorrhiza identifies a collection of novel genes induced during Medicago truncatula root endosymbioses. Mol Plant Microbe Interact 17(10):1063-1077.
38. Ortu G, et al. (2012) Plant genes related to gibberellin biosynthesis and signaling are differentially regulated during the early stages of AM fungal interactions. Mol Plant 5(4):951-954.
39. Garrido JMG, Morcillo RJL, Rodríguez JAM, Bote JA (2010) Variations in the mycorrhization characteristics in roots of wild-Type and ABA-Deficient tomato are accompanied by specific transcriptomic alterations. Mol Plant Microbe Interact 23(5): 651-664.
40. Shaul-Keinan O, et al. (2002) Hormone concentrations in tobacco roots change during arbuscular mycorrhizal colonization with Glomu intraradices. New Phytol 154(2):501-507.
41. El Ghachtouli N, Martin-Tanguy J, Paynot M, Gianinazzi S (1996) First report of the inhibition of arbuscular mycorrhizal infection of Pisum sativum by specific and irreversible inhibition of polyamine biosynthesis or by gibberellic acid treatment. FEBS Lett 385(3):189-192.
42. Brian PW (1959) EFFECTS OF GIBBERELLINS ON PLANT GROWTH AND DEVELOPMENT. Biol Rev Camb Philos Soc 34(1):37-84.
43. Harberd NP, et al. (1998) Gibberellin: Inhibitor of an inhibitor of. Bioessays 20(12): 1001-1008.
44. Achard P, et al. (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311(5757):91-94.
45. Achard P, et al. (2007) Dellas contribute to plant photomorphogenesis. Plant Physiol 143(3):1163-1172.
46. Achard P, Renou JP, Berthomé R, Harberd NP, Genschik P (2008) Plant Dellas restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr Biol 18(9):656-660.
47. Navarro L, et al. (2008) Dellas control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr Biol 18(9):650-655.
48. Hedden P, Thomas SG (2012) Gibberellin biosynthesis and its regulation. Biochem J 444(1):11-25.
49. Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225-251.
50. Alvey L, Harberd NP (2005) Della proteins: Integrators of multiple plant growth regulatory inputs Physiol Plant 123(2):153-160.
51. Sun TP (2010) Gibberellin-GID1-DELLA: A pivotal regulatory module for plant growth and development. Plant Physiol 154(2):567-570.
52. Davière JM, Achard P (2013) Gibberellin signaling in plants. Development 140(6): 1147-1151.
53. Harberd NP (2003) Botany. Relieving Della restraint. Science 299(5614):1853-1854.
54. Sasaki A, et al. (2003) Accumulation of phosphorylated repressor for gibberellin signaling in an F-Box mutant. Science 299(5614):1896-1898.
55. Peng JR, et al. (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev 11(23):3194-3205.
56. Lee SC, et al. (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-Like gene whose expression is up-Regulated following imbibition. Genes Dev 16(5):646-658.
57. Dill A, Sun TP (2001) Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159(2):777-785.
58. Silverstone AL, Ciampaglio CN, Sun TP (1998) The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10(2):155-169.
59. Wen CK, Chang C (2002) Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14(1):87-100.
60. Weston DE, et al. (2008) The Pea Della proteins LA and CRY are important regulators of gibberellin synthesis and root growth. Plant Physiol 147(1):199-205.
61. Ikeda A, et al. (2001) slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-Regulating gene GAI/RGA/RHT/D8. Plant Cell 13(5):999-1010.
62. Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218(5):683-692.
63. Harberd NP, Belfield E, Yasumura Y (2009) The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism: How an inhibitor of an inhibitor enables flexible response to fluctuating environments. Plant Cell 21(5):1328-1339.
64. de Lucas M, et al. (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451(7177):480-484.
65. Feng SH, et al. (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451(7177):475-479.
66. Gallego-Bartolomé J, et al. (2012) Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proc Natl Acad Sci USA 109(33):13446-13451.
67. Hirano K, et al. (2012) The suppressive function of the rice Della protein SLR1 is dependent on its transcriptional activation activity. Plant J 71(3):443-453.
68. Hong GJ, Xue XY, Mao YB, Wang LJ, Chen XY (2012) Arabidopsis MYC2 interacts with Della proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24(6):2635-2648.
69. Hou XL, Lee LYC, Xia KF, Yan Y, Yu H (2010) Dellas modulate jasmonate signaling via competitive binding to JAZs. Dev Cell 19(6):884-894.
70. Park J, Nguyen KT, Park E, Jeon J-S, Choi G (2013) Della proteins and their interacting RING Finger proteins repress gibberellin responses by binding to the promoters of a subset of gibberellin-Responsive genes in Arabidopsis. Plant Cell 25(3): 927-943.
71. Jiang CF, Gao XH, Liao L, Harberd NP, Fu XD (2007) Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiol 145(4):1460-1470.
72. Foo E, Ross JJ, Jones WT, Reid JB (2013) Plant hormones in arbuscular mycorrhizal symbioses: An emerging role for gibberellins. Ann Bot (Lond) 111(5):769-779.
73. Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14(10):2413-2429.
74. Frenzel A, et al. (2005) Combined transcriptome profiling reveals a novel family of arbuscular mycorrhizal-Specific Medicago truncatula lectin genes. Mol Plant Microbe Interact 18(8):771-782.
75. Isayenkov S, Fester T, Hause B (2004) Rapid determination of fungal colonization and arbuscule formation in roots of Medicago truncatula using real-Time (RT) PCR. J Plant Physiol 161(12):1379-1383.
76. Zentella R, et al. (2007) Global analysis of Della direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19(10):3037-3057.
77. Silverstone AL, et al. (2001) Repressing a repressor: Gibberellin-Induced rapid reduction of the RGA protein in Arabidopsis. Plant Cell 13(7):1555-1566.
78. McGinnis KM, et al. (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-Box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15(5):1120-1130.
79. Ubeda-Tomás S, et al. (2008) Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nat Cell Biol 10(5):625-628.
80. Takeda N, Maekawa T, Hayashi M (2012) Nuclear-Localized and deregulated calciumand calmodulin-Dependent protein kinase activates rhizobial and mycorrhizal responses in Lotus japonicus. Plant Cell 24(2):810-822.
81. Maekawa T, et al. (2009) Gibberellin controls the nodulation signaling pathway in Lotus japonicus. Plant J 58(2):183-194.
82. Lauressergues D, et al. (2012) The microRNA miR171h modulates arbuscular mycorrhizal colonization of Medicago truncatula by targeting NSP2. Plant J 72(3): 512-522.
83. Delaux PM, Bécard G, Combier JP (2013) NSP1 is a component of the Myc signaling pathway. New Phytol 199(1):59-65.
84. Liu W, et al. (2011) Strigolactone biosynthesis in Medicago truncatula and rice requires the symbiotic GRAS-Type transcription factors NSP1 and NSP2. Plant Cell 23(10):3853-3865.
85. Peng JR, et al. (1999) 'Green revolution' genes encode mutant gibberellin response modulators. Nature 400(6741):256-261.
86. Evans L (1998) Feeding the Ten Billion: Plants and Population Growth (Cambridge Univ Press, Cambridge, UK).
87. Allan RE (1980) Influence of Semidwarfism and Genetic Background on Stand Establishment of Wheat. Crop Sci 20(5):634-638.
88. Allan RE (1983) Harvest indexes of backcross-Derived wheat lines differening in culm height. Crop Sci 23(6):1029-1032.
89. Allan RE (1989) Registration of 16 lines of soft white spring wheat germplasm. Crop Sci 29(4):1098-1099.
90. Sisaphaithong T, Kondo D, Matsunaga H, Kobae Y, Hata S (2012) Expression of plant genes for arbuscular mycorrhiza-Inducible phosphate transporters and fungal vesicle formation in sorghum, barley, and wheat roots. Biosci Biotechnol Biochem 76(12): 2364-2367.
91. Winkler RG, Helentjaris T (1993) Dominant dwarfs. Maize Genet. Coop. Newsl. 67: 110-111.
92. Hans J, Hause B, Strack D, Walter MH (2004) Cloning, characterization, and immunolocalization of a mycorrhiza-Inducible 1-Deoxy-D-Xylulose 5-Phosphate reductoisomerase in arbuscule-Containing cells of maize. Plant Physiol 134(2):614-624.
93. Wild M, et al. (2012) The Arabidopsis Della RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signaling responses. Plant Cell 24(8):3307-3319.
94. Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 104(5):1720-1725.
95. Kiers ET, et al. (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333(6044):880-882.
96. Hammer EC, Pallon J, Wallander H, Olsson PA (2011) Tit for tat A mycorrhizal fungus accumulates phosphorus under low plant carbon availability. FEMS Microbiol Ecol 76(2):236-244.
97. Ritchie S, Gilroy S (1998) Tansley Review No. 100-Gibberellins: Regulating genes and germination. New Phytol 140(3):363-383.
98. Chen PW, Chiang CM, Tseng TH, Yu SM (2006) Interaction between rice MYBGA and the gibberellin response element controls tissue-Specific sugar sensitivity of alphaamylase genes. Plant Cell 18(9):2326-2340.
99. Gutjahr C, et al. (2009) Presymbiotic factors released by the arbuscular mycorrhizal fungus Gigaspora margarita induce starch accumulation in Lotus japonicus roots. New Phytol 183(1):53-61.
100. Koide RT, Schreiner RP (1992) Regulation of the vesicular-Arbuscular mycorrhizal symbiosis. Annu Rev Plant Physiol Plant Mol Biol 43:557-581.
101. Amijee F, Stribley DP, Tinker PB (1993) The development of endomycorrhizal root systems. VIII. Effects of soil phosphorus and fungal colonization on the concentration of soluble carbohydrates in roots. New Phytol 123(2):297-306.
102. Amijee F, Tinker PB, Stribley DP (1989) The development of endomycorrhizal root systems. New Phytol 111(3):435-446.
103. Tester M, Smith SE, Smith FA, Walker NA (1986) Effects of photon irradiance on the growth of shoots and roots, on the rate of initiation of mycorrhizal infection and on the growth of infection units in Trifolium subterraneum L. New Phytol 103(2): 375-390.
104. Shani E, et al. (2013) Gibberellins accumulate in the elongating endodermal cells of Arabidopsis root. Proc Natl Acad Sci USA 110(12):4834-4839.
105. Liu J, Blaylock L, Harrison MJ (2004) cDNA arrays as tools to identify mycorrhizaregulated genes: Identification of mycorrhiza-Induced genes that encode or generate signaling molecules implicated in the control of root growth. Can J Bot 82 (8):1177-1185.
106. Lopez-MeyerM, Harrison MJ (2006) An experimental system to synchronize the early events of development of the arbuscular mycorrhizal symbiosis. Biology of Molecular Plant-Microbe Interactions, eds Sánchez F, Quinto C, López-Lara IM, Geiger O (International Society for Molecular Plant-Microbe Interactions, St. Paul), Vol 5, pp 546-551.
107. Hong JJ, et al. (2012) Diversity of morphology and function in arbuscular mycorrhizal symbioses in Brachypodium distachyon. Planta 236(3):851-865.
108. McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method that gives an objective measure of colonization of roots by vesicular-Arbuscular mycorrhizal fungi. New Phytol 115(3):495-501.
109. Liu JY, et al. (2008) Closely related members of the Medicago truncatula PHT1 phosphate transporter gene family encode phosphate transporters with distinct biochemical activities. J Biol Chem 283(36):24673-24681.
110. Dill A, Jung H-S, Sun TP (2001) The Della motif is essential for gibberellin-Induced degradation of RGA. Proc Natl Acad Sci USA 98(24):14162-14167.
111. Chiu W, et al. (1996) Engineered GFP as a vital reporter in plants. Curr Biol 6(3): 325-330.
112. Boisson-Dernier A, et al. (2001) Agrobacterium rhizogenes-Transformed roots of Medicago truncatula for the study of nitrogen-Fixing and endomycorrhizal symbiotic associations. Mol Plant Microbe Interact 14(6):695-700.
113. Limpens E, et al. (2004) RNA interference in Agrobacterium rhizogenes-Transformed roots of Arabidopsis and Medicago truncatula. J Exp Bot 55(399):983-992.
114. Charpentier M, et al. (2008) Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 20(12):3467-3479.
115. Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol 8:115-118.
116. Hartweck LM (2008) Gibberellin signaling. Planta 229(1):1-13.