Transcriptional response of Medicago truncatula sulphate transporters to arbuscular mycorrhizal symbiosis with and without sulphur stress

Planta

Volumn 235, Issue 6, 2012, Pages 1431-1447

  Casieri, Leonardo ^a   Gallardo, Karine ^a   Wipf, Daniel ^a  

^a UNIV BOURGOGNE FRANCHE COMTÉ   (France)

Author keywords

Arbuscular mycorrhiza; Glomus intraradices; Medicago truncatula; Sulphate; Transporters

Indexed keywords

ANION TRANSPORT PROTEIN; MESSENGER RNA; SULFUR;

ANTIBODY SPECIFICITY; ARTICLE; BARREL MEDIC; BIOLOGY; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MYCORRHIZA; PHYLOGENY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SYMBIOSIS;

ANION TRANSPORT PROTEINS; COMPUTATIONAL BIOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; MEDICAGO TRUNCATULA; MYCORRHIZAE; ORGAN SPECIFICITY; PHYLOGENY; RNA, MESSENGER; STRESS, PHYSIOLOGICAL; SULFUR; SYMBIOSIS; TRANSCRIPTION, GENETIC;

ARBUSCULAR; GLOMUS INTRARADICES; MEDICAGO; MEDICAGO TRUNCATULA;

EID: 84861615306     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-012-1645-7     Document Type: Article

References (87)

1. Allen JW, Shachar-Hill Y (2009) Sulfur transfer through an arbuscular mycorrhiza. Plant Physiol 149: 549-560.
2. Allen WM, Patterson DS, Slater TF (1974) A biochemical study of experimental Johne's disease. Protein metabolism in sheep and mice. J Comp Pathol 84: 391-398.
3. Baier MC, Keck M, Gödde V, Niehaus K, Küster H, Hohnjec N (2010) Knockdown of the symbiotic sucrose synthase MtSucS1 affects arbuscule maturation and maintenance in mycorrhizal roots of Medicago truncatula. Plant Physiol 152: 1000-1014.
4. Banerjee R, Evande R, Kabil O, Ojha S, Taoka S (2003) Reaction mechanism and regulation of cystathionine beta-synthase. Biochim Biophys Acta 1647: 30-35.
5. Benedito VA, Li H, Dai X, Wandrey M, He J, Kaundal R, Torres-Jerez I, Gomez SK, Harrison MJ, Tang Y, Zhao PX, Udvardi MK (2010) Genomic inventory and transcriptional analysis of Medicago truncatula transporters. Plant Physiol 152: 1716-1730.
6. Benning C, Ohta H (2005) Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants. J Biol Chem 280: 2397-2400.
7. Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U, Hause B, Bucher M, Kretzschmar T, Bossolini E, Kuhlemeier C, Martinoia E, Franken P, Scholz U, Reinhardt D (2010) Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 64: 1002-1017.
8. 2S and pedospheric sulfate nutrition. Plant Physiol 136: 3396-3408.
9. Chen A, Hu J, Sun S, Xu G (2007) Conservation and divergence of both phosphate- and mycorrhiza-regulated physiological responses and expression patterns of phosphate transporters in solanaceous species. New Phytol 173: 817-831.
10. Cherest H, Davidien J-C, Thomas D, Benes V, Ansorge W, Surdin-Kerjan Y (1997) Molecular characterization of two high affinity sulfate transporters in Saccharomyces cerevisiae. Genetics 145: 627-635.
11. Chiou TJ, Liu H, Harrison MJ (2001) The spatial expression patterns of a phosphate transporter (MtPT1) from Medicago truncatula indicate a role in phosphate transport at the root/soil interface. Plant J 25: 281-293.
12. Cooper KM, Tinker PB (1978) Translocation and transfer of nutrients in vesicular-arbuscular mycorrhizas. 2. Uptake and translocation of phosphorus, zinc and sulfur. New Phytol 81: 43-52.
13. Davidian J-C, Hatzfeld Y, Cathala N, Tagmount A, Vidmar JJ (2000) Sulfate uptake and transport in plants. In: Brunold C, Rennenberg H, De Kok LJ, Stulen I, Davidian J-C (eds) Sulfur nutrition and sulfur assimilation in higher plants: molecular, biochemical and physiological aspects. Paul Haupt, Bern, pp 19-40.
14. Eriksen J, Askegaard M (2000) Sulphate leaching in an organic crop rotation on sandy soil in Denmark. Agric Ecosyst Environ 78: 107-114.
15. Ferrol N, Pérez-Tienda J (2009) Coordinated nutrient exchange in arbuscular mycorrhiza. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas-functional processes and ecological impact. Springer, Berlin, pp 73-87.
16. Foley JA, DeFries R, Asner JP, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe MT, Daily GC, Gibbs HK, Helkowski JH, Holloway T, Howard EA, Kucharik CJ, Monfreda C, Patz JA, Prentice IC, Ramankutty N, Snyder PK (2005) Global consequences of land use. Science 209: 570-574.
17. Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Sign 11: 861-905.
18. 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: 510-528.
19. Gerdemann JW (1968) Vescicular-arbuscular mycorrhiza and plant growth. Annu Rev Phytopathol 6: 397-441.
20. Gomez SK, Javot H, Deewatthanawong P, Torres-Jerez I, Tang Y, Blancaflor EB, Udvardi MK, Harrison MJ (2009) Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol 9: 10.
21. Gordon-Weeks R, Tong Y, Davies TG, Leggewie G (2003) Restricted spatial expression of a high-affinity phosphate transporter in potato roots. J Cell Sci 116: 3135-3144.
22. Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW, Bucking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435: 819-823.
23. Gray LE, Gerdemann JW (1973) Uptake of sulphur-35 by vesicular arbuscular mycorrhizae. Plant Soil 39: 687-689.
24. Guether M, Balestrini R, Hannah MA, Udvardi MK, Bonfante P (2009a) Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytol 182: 200-212.
25. Guether M, Neuhäuser B, Balestrini R, Dynowski M, Ludewig U, Bonfante P (2009b) A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol 150: 73-83.
26. Güimil S, Chang HS, Zhu T, Sesma A, Osbourn A, Roux C, Ionnidis V, Oakeley EJ, Docquier M, Descombes P, Briggs SP, Paszkowski U (2005) Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc Natl Acad Sci USA 102: 8066-8070.
27. Guo T, Zhang JL, Christie P, Li XL (2007) Pungency of spring onion as affected by inoculation with arbuscular mycorrhizal fungi and sulfur supply. J Plant Nutr 30: 1023-1034.
28. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41: 95-98.
29. Harrison MJ, Dewbre GR, Liu JY (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14: 2413-2429.
30. Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition, 2nd edn. Commonwealth Agricultural Bureaux, Farnham Royal.
31. Higashi Y, Hirai MY, Fujiwara T, Naito S, Noji M, Saito K (2006) Proteomic and transcriptomic analysis of Arabidopsis seed: molecular evidence for successive processing of seed proteins and its implication in the stress response to sulphur nutrition. Plant J 48: 557-571.
32. Hildebrandt U, Schmelzer E, Bothe H (2002) Expression of nitrate transporter genes in tomato colonized by an arbuscular mycorrhizal fungus. Physiol Plant 115: 125-136.
33. Hohnjec N, Vieweg ME, Pühler A, Becker A, Küster H (2005) 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 137: 1283-1301.
34. Javot H, Pumplin N, Harrison MJ (2007) Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ 30: 310-322.
35. Javot H, Penmetsa VR, Breuillin F, Bhattarai KK, Noar RD, Gomez SK, Zhang Q, Cook DR, Harrison MJ (2011) Medicago truncatula mtpt4 mutants reveal a role for nitrogen in the regulation of arbuscule degeneration in arbuscular mycorrhizal symbiosis. Plant J 68: 954-965.
36. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8: 275-282.
37. Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci 10: 22-29.
38. Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller KE (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem 41: 1233-1244.
39. Kataoka T, Hayashi N, Yamaya T, Takahashi H (2004a) Root-to-shoot transport of sulfate in Arabidopsis: evidence for the role of SULTR3; 5 as a component of low-affinity sulfate transport system in the root vasculature. Plant Physiol 136: 4198-4204.
40. Kataoka T, Watanabe-Takahashi A, Hayashi N, Ohnishi M, Mimura T, Bucher M, Hawkesford MJ, Yamaya T, Takahashi H (2004b) Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell 16: 2693-2704.
41. Kobae Y, Tamura Y, Takai S, Banba M, Hata S (2010) Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in soybean. Plant Cell Physiol 51: 1411-1415.
42. Kopriva S, Rennenberg H (2004) Control of sulphate assimilation and glutathione synthesis: interaction with N and C metabolism. J Exp Bot 55: 1831-1842.
43. Krusell L, Krause K, Ott T, Desbrosses G, Kramer U, Sato S, Nakamura Y, Tabata S, James EK, Sandal N, Stougaard J, Kawaguchi M, Miyamoto A, Suganuma N, Udvardi MK (2005) The sulfate transporter SST1 is crucial for symbiotic nitrogen fixation in Lotus japonicus root nodules. Plant Cell 17: 1625-1636.
44. Leustek T (1996) Molecular genetics of sulfate assimilation in plants. Physiol Plant 97: 411-419.
45. Lewandowska M, Sirko A (2008) Recent advances in understanding plant response to sulfur-deficiency stress. Acta Biochim Pol 55: 457-471.
46. Maeda D, Ashida K, Iguchi K, Chechetka SA, Hijikata A, Okusako Y, Deguchi Y, Izui K, Hata S (2006) Knockdown of an arbuscular mycorrhiza-inducible phosphate transporter gene of Lotus japonicus suppresses mutualistic symbiosis. Plant Cell Physiol 47: 807-817.
47. Maruyama-Nakashita A, Inoue E, Watanabe-Takahashi A, Yarnaya T, Takahashi H (2003) Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. Plant Physiol 132: 597-605.
48. McGrath SP, Zhao FJ, Withers PJA (1996) Development of sulphur deficiency in crops and its treatment. In: Proceedings of the Fertilizer Society 379, St. Petersburg.
49. Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N, Doumas P, Nacry P, Herrerra-Estrella L, Nussaume L, Thibaud MC (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 102: 11934-11939.
50. Mudge SR, Rae AL, Diatloff E, Smith FW (2002) Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. Plant J 31: 341-353.
51. Nagy R, Karandashov V, Chague V, Kalinkevich K, Tamasloukht B, Xu G, Jakobsen I, Levy AA, Amrhein N, Bucher M (2005) The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant J 42: 236-250.
52. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York.
53. Nikiforova VJ, Kopka J, Tolstikov V, Fiehn O, Hopkins L, Hawkesford MJ et al (2005) Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants. Plant Physiol 138: 304-318.
54. Ohkama-Ohtsu N, Wasaki J (2010) Recent progress in plant nutrition research: cross-talk between nutrients, plant physiology and soil microorganisms. Plant Cell Physiol 51: 1255-1264.
55. Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucl Acids Res 35(Database issue): D846-D851.
56. Paradi I, van Tuinen D, Morandi D, Ochatt S, Robert F, Jacas L, Dumas-Gaudot E (2010) Transcription of two blue copper-binding protein isogenes is highly correlated with arbuscular mycorrhizal development in Medicago truncatula. MPMI 23: 1175-1183.
57. Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Nat Acad Sci USA 99: 13324-13329.
58. Popper Z, Michel G, Herve C, Domozych D, Willats WGT, Tuohy MG, Kloareg B, Stengel DB (2011) Evolution and diversity of plant cell walls: from algae to flowering plants. Annu Rev Plant Biol 62: 567-590.
59. Rhodes LH, Gerdemann JW (1978) Hyphal translocation and uptake of sulfur by vesicular-arbuscular mycorrhizae of onion. Soil Biol Biochem 10: 355-360.
60. Rouached H, Berthomieu P, El Kassis E, Cathala N, Catherinot V, Labesse G, Davidien J-C, Fourcroy P (2005) Structural and functional analysis of the C-terminal STAS (sulfate transporter and anti-sigma antagonist) domain of the Arabidopsis thaliana sulfate transporter SULTR1. 2. J Biol Chem 280: 15976-15983.
61. Saito K (2004) Sulfur assimilatory metabolism. The long and smelling road. Plant Physiol 136: 2443-2450.
62. Sawers RJH, Yang S-Y, Gutjahr C, Paszkowsky U (2008) The molecular components of nutrient exchange in arbuscular mycorrhizal interactions. In: Siddiqui ZA, Akhtar MS, Futai K (eds) Mycorrhizae: sustainable agriculture and forestry. Springer, Heidelberg, pp 37-59.
63. Scherer HW (2001) Sulphur in crop production. Eur J Agron 14: 81-111.
64. Sheng M, Tang M, Chen H, Yang B, Zhang F, Huang Y (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18: 287-296.
65. Shibagaki N, Grossman AR (2004) Probing the function of STAS domains of the Arabidopsis sulfate transporters. J Biol Chem 279: 30791-30799.
66. Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62: 1-16. 24.
67. Smith SE, Smith FA (2012) Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia 104: 1-13.
68. Smith FW, Ealing PM, Hawkesford MJ, Clarkson DT (1995) Plant members of a family of sulfate transporters reveal functional subtypes. Proc Natl Acad Sci USA 92: 9373-9377.
69. Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156: 1050-1057.
70. Tabe LM, Droux M (2001) Sulfur assimilation in developing lupin cotyledons could contribute significantly to the accumulation of organic sulfur reserves in the seed. Plant Physiol 126: 176-187.
71. Tabe LM, Venables I, Grootemaat A, Lewis D (2003) Sulfur transport and assimilation in developing embryos of chickpea (Cicer arietinum). In: Davidien J-C, Grill D, De Kok LJ, Stulen I, Hawkesford MJ, Schnug E, Rennenberg H (eds) Sulfur transport and assimilation in plants. Backhuys Publishers, Leiden, pp 335-337.
72. Takahashi H (2010) Sulfate transport and assimilation in plants. Int Rev Cell Mol Biol 281: 129-159.
73. Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, Engler JA, Engler G, van Montagu M, Saito K (1997) Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate starved roots plays a central role in Arabidopsis thaliana. Proc Natl Acad Sci USA 94: 11102-11107.
74. Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ, Saito K (2000) The role of three functional sulfate transporters involved in uptake and translocation of sulfate in Arabidopsis thaliana. Plant J 23: 171-182.
75. Takahashi H, Kopriva S, Giordano M, Saito K, Hell R (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62: 157-184.
76. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. doi: 10. 1093/molbev/msr121.
77. Tietjen GL, Moore RH (1972) Some Grubbs-type statistics for the detection of outliers. Technometrics 14: 583-597.
78. Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Physiological and genetical aspects of mycorrhizae. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Recherche de méthodes d'estimation ayant une signification fonctionnelle. INRA, France, pp 217-221.
79. Valot B, Negroni L, Zivy M, Gianinazzi S, Dumas-Gaudot E (2006) A mass spectrometric approach to identify arbuscular mycorrhiza-related proteins in root plasma membrane fractions. Proteomics 6: S145-S155.
80. Vauclare P, Kopriva S, Fell D, Suter M, Sticher L, von Ballmoos P, Krähenbühl U, Op den Camp R, Brunold C (2002) Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 59-phosphosulphate reductase is more susceptible to negative control by thiols than ATP sulphurylase. Plant J 31: 729-740.
81. Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microb 64: 5004-5007.
82. Wright DP, Scholes JD, Read DJ (1998) Effects of VA mycorrhizal colonization on photosynthesis and biomass production of Trifolium repens L. Plant Cell Environ 21: 209-216.
83. Xu GH, Chague V, Melamed-Bessudo C, Kapulnik Y, Jain A, Raghothama KG, Levy AA, Silber A (2007) Functional characterization of LePT4: a phosphate transporter in tomato with mycorrhiza- enhanced expression. J Exp Bot 58: 2491-2501.
84. Yoshimoto N, Inoue E, Saito K, Yamaya T, Takahashi H (2003) Phloem-localizing sulfate transporter, Sultr1; 3, mediates re-distribution of sulfur from source to sink organs in Arabidopsis. Plant Physiol 131: 1511-1517.
85. Yoshimoto N, Inoue E, Watanabe-Takahashi A, Saito K, Takahashi H (2007) Posttranscriptional regulation of high-affinity sulfate transporters in Arabidopsis by sulfur nutrition. Plant Physiol 145: 378-388.
86. Young ND, Debellé F, Oldroyd GED et al (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480: 520-524.
87. Zuber H, Davidien JC, Aubert G, Aimé D, Belghazi M, Lugan R, Heintz D, Wirtz M, Hell R, Thompson R, Gallardo K (2010) The seed composition of Arabidopsis mutants for the group 3 sulfate transporters indicates a role in sulfate translocation within developing seed. Plant Physiol 154: 913-926.