First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus Glomus intraradices

New Phytologist

Volumn 197, Issue 2, 2013, Pages 617-630

  Li, Tao ^a   Hu, Ya Jun ^a   Hao, Zhi Peng ^a   Li, Hong ^a   Wang, You Shan ^b   Chen, Bao Dong ^a  

^a RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

^b INSTITUTE OF PLANT AND ENVIRONMENT PROTECTION   (China)

Author keywords

Aquaporin; Arbuscular mycorrhizal (AM); Drought tolerance; Glomus intraradices; Heterologous expression; Osmotic stress

Indexed keywords

AQUAPORIN; CALCIUM; FUNGAL PROTEIN; PROTON; WATER;

ARBUSCULAR MYCORRHIZA; CLONE; DROUGHT STRESS; FUNGUS; GENE EXPRESSION; MAIZE; OSMOSIS; POLYMERASE CHAIN REACTION; SYMBIOSIS;

ARTICLE; BACTERIAL COUNT; BIOLOGY; CHEMISTRY; DROUGHT; FUNGAL GENE; GENE EXPRESSION REGULATION; GENETIC TRANSFORMATION; GENETICS; GLOMEROMYCOTA; GROWTH, DEVELOPMENT AND AGING; MAIZE; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; MYCELIUM; MYCORRHIZA; NUCLEOTIDE SEQUENCE; OSMOTIC PRESSURE; PHYLOGENY; PHYSIOLOGICAL STRESS; PICHIA; PLANT ROOT; PROTEIN TRANSPORT; PROTOPLAST;

AQUAPORINS; CALCIUM; CLONING, MOLECULAR; COLONY COUNT, MICROBIAL; COMPUTATIONAL BIOLOGY; DROUGHTS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, PLANT; GENES, FUNGAL; GLOMEROMYCOTA; MOLECULAR SEQUENCE DATA; MYCELIUM; MYCORRHIZAE; OSMOTIC PRESSURE; PHYLOGENY; PICHIA; PLANT ROOTS; PROTEIN TRANSPORT; PROTONS; PROTOPLASTS; STRESS, PHYSIOLOGICAL; TRANSFORMATION, GENETIC; WATER; ZEA MAYS;

ARBUSCULAR; FUNGI; GLOMUS INTRARADICES; ZEA MAYS;

EID: 84871267350     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12011     Document Type: Article

References (72)

1. Agre P, King LS, Yasui M, Guggino WB, Ottersen OP, Fujiyoshi Y, Engel A, Nielsen S. 2002. Aquaporin water channels-from atomic structure to clinical medicine. The Journal of Physiology 542: 3-16.
2. Allen MF. 2007. Mycorrhizal fungi: highways for water and nutrients in arid soils. Vadose Zone Journal 6: 291-297.
3. Allen MF. 2009. Bidirectional water flows through the soil-fungal-plant mycorrhizal continuum. New Phytologist 182: 290-293.
4. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403-410.
5. Aroca R, Bago A, Sutka M, Antonio PJ, Cano C, Amodeo G, Ruiz-Lozano JM. 2009. Expression analysis of the first arbuscular mycorrhizal fungi aquaporin described reveals concerted gene expression between salt-stressed and nonstressed mycelium. Molecular Plant-Microbe Interactions 22: 1169-1178.
6. Aroca R, Ruiz-Lozano JM. 2009. Induction of plant tolerance to semi-arid environments by beneficial soil microorganisms - a review. Sustainable Agriculture Reviews 2: 121-135.
7. Aroca R, Vernieri P, Ruiz-Lozano JM. 2008. Mycorrhizal and non-mycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous ABA during drought stress and recovery. Journal of Experimental Biology 59: 2029-2041.
8. Augé RM. 2001. Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11: 3-42.
9. Bécard G, Fortin J. 1988. Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytologist 108: 211-218.
10. Beitz E. 2005. Aquaporins from pathogenic protozoan parasites: structure, function and potential for chemotherapy. Biology of the Cell 97: 373-383.
11. Benfenati V, Caprini M, Dovizio M, Mylonakou MN, Ferroni S, Ottersen OP, Amiry-Moghaddam M. 2011. An aquaporin-4/transient receptor potential vanilloid 4 (AQP4/TRPV4) complex is essential for cell-volume control in astrocytes. Proceedings of the National Academy of Sciences, USA 108: 2563-2568.
12. Biermann B, Linderman RG. 1981. Quantifying vercular-arbuscular mycorrhizas: a proposed method towards standardization. New Phytologist 87: 63-67.
13. Bonfante P, Genre A. 2010. Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nature Communications 1: 48.
14. Bray EA. 1997. Plant responses to water deficit. Trends in Plant Science 2: 48-56.
15. Calamita G, Bishai WR, Preston GM, Guggino WB, Agre P. 1995. Molecular cloning and characterization of AqpZ, a water channel from Escherichia coli. Journal of Biological Chemistry 270: 29063-29066.
16. Carvajal M, Cerda A, Martinez V. 2000. Does calcium ameliorate the negative effect of NaCl on melon root water transport by regulating aquaporin activity? New Phytologist 145: 439-447.
17. Compant S, van der Heijden MGA, Sessitsch A. 2010. Climate change effects on beneficial plant-microorganism interactions. FEMS Microbiology Ecology 73: 197-214.
18. Danielson J, Johanson U. 2008. Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biology 8: 45.
19. Dietz S, von Bulow J, Beitz E, Nehls U. 2011. The aquaporin gene family of the ectomycorrhizal fungus Laccaria bicolor: lessons for symbiotic functions. New Phytologist 190: 927-940.
20. Duncan DB. 1955. Multiple range and multiple F-tests. Biometrics 11: 1-42.
21. Egerton-Warburton LM, Querejeta JI, Allen MF. 2007. Common mycorrhizal networks provide a potential pathway for the transfer of hydraulically lifted water between plants. Journal of Experimental Biology 58: 1473-1483.
22. Finlay RD. 2008. Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. Journal of Experimental Biology 59: 1115-1126.
23. Fu D, Libson A, Miercke LJW, Weitzman C, Nollert P, Krucinski J, Stroud RM. 2000. Structure of a glycerol conducting channel and the basis for its selectivity. Science 290: 481-486.
24. Gabor ET, Istvan S. 2001. The HMMTOP transmembrane topology prediction server. Bioinformatics Applications Note 17: 849-850.
25. Gomez SK, Javot H, Deewatthanawong P, Torres-Jerez I, Tang YH, 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 Biology 9: 10.
26. Gónzalez-Guerrero M, Azcón-Aguilar C, Mooney M, Valderas A, MacDiarmid CW, Eide DJ, Ferrol N. 2005. Characterization of a Glomus intraradices gene encoding a putative Zn transporter of the cation diffusion facilitator family. Fungal Genetics and Biology 42: 130-140.
27. Gupta AB, Sankararamakrishnan R. 2009. Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: characterization of XIP subfamily of aquaporins from evolutionary perspective. BMC Plant Biology 9: 134.
28. Helber N, Requena N. 2008. Expression of the fluorescence markers DsRed and GFP fused to a nuclear localization signal in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytologist 177: 537-548.
29. Heller KB, Lin EC, Wilson TH. 1980. Substrate specificity and transport properties of the glycerol facilitator of Escherichia coli. Journal of Bacteriology 144: 274-278.
30. Herrera-Medina MJ, Steinkellner S, Vierheilig H, Ocampo Bote JA, García Garrido JM. 2007. Abscisic acid determines arbuscule development and functionality in tomato arbuscular mycorrhiza. New Phytologist 175: 554-564.
31. Ian SW, Daniel MR. 2004. Homology modeling of representative subfamilies of Arabidopsis major intrinsic proteins. Classification based on the aromatic/arginine selectivity filter. Plant Physiology 135: 1059-1068.
32. Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. 2006. Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant and Cell Physiology 47: 141-153.
33. Jahromi F, Aroca R, Porcel R, Ruiz-Lozano JM. 2008. Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular responses of mycorrhizal lettuce plants. Microbial Ecology 55: 45-53.
34. Jakobsen I, Abbott LK, Robson AD. 1992. External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum. 1: spread of hyphae and phosphorus inflow into roots. New Phytologist 120: 371-380.
35. Johansson I, Karlsson M, Shukla VK, Chrispeels MJ, Larsson C, Kjellbom P. 1998. Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 10: 451-459.
36. 2+ regulation of aquaporin water permeability. Journal of General Physiology 123: 573-580.
37. King LS, Kozono D, Agre P. 2004. From structure to disease: the evolving tale of aquaporin biology. Nature Reviews Molecular Cell Biology 5: 687-698.
38. Krüger M, Krüger C, Walker C, Stockinger H, Schüssler A. 2011. Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytologist 193: 970-984.
39. Laizé V, Tacnet F, Ripoche P, Hohmann S. 2000. Polymorphism of Saccharomyces cerevisiae aquaporins. Yeast 16: 897-903.
40. Martinez-Ballesta MDC, Martinez V, Carvajal M. 2000. Regulation of water channel activity in whole roots and in protoplasts from roots of melon plants grown under saline conditions. Australian Journal of Plant Physiology 27: 685-691.
41. Maurel C, Verdoucq L, Luu DT, Santoni V. 2008. Plant aquaporins: membrane channels with multiple integrated functions. Annual Review of Plant Biology 59: 595-624.
42. Nemeth-Cahalan KL, Hall JE. 2000. pH and calcium regulate the water permeability of aquaporin 0. Journal of Biological Chemistry 275: 6777-6782.
43. Nyblom M, Frick A, Wang Y, Ekvall M, Hallgren K, Hedfalk K, Neutze R, Tajkhorshid E, Törnroth-Horsefield S. 2009. Structural and functional analysis of SoPIP2;1 mutants adds insight into plant aquaporin gating. Journal of Molecular Biology 387: 653-668.
44. Oliveira R, Lages F, Silva GM, Lucas C. 2003. Fps1p channel is the mediator of the major part of glycerol passive diffusion in Saccharomyces cerevisiae: artefacts and re-definitions. Biochimica et Biophysica Acta 1613: 57-71.
45. Peng Y, Lin W, Cai W, Arora R. 2007. Overexpression of a Panax ginseng tonoplast aquaporin alters salt tolerance, drought tolerance and cold acclimation ability in transgenic Arabidopsis plants. Planta 226: 729-740.
46. Pettersson N, Filipsson C, Becit E, Brive L, Hohmann S. 2005. Aquaporins in yeasts and filamentous fungi. Biology of the Cell 97: 487-500.
47. Pettersson N, Hagstrom J, Bill RM, Hohmann S. 2006. Expression of heterologous aquaporins for functional analysis in Saccharomyces cerevisiae. Current Genetics 50: 247-255.
48. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29: 45.
49. Phillips JM, Hayman DS. 1970. Improved procedure of clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55: 159-161.
50. Porcel R, Aroca R, Azcon R, Ruiz-Lozano JM. 2006. PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance. Plant Molecular Biology 60: 389-404.
51. 1-pyrroline-5-carboxylate synthetase (P5CS) during drought stress in arbuscular mycorrhizal Glycine max and Lactuca sativa plants. Physiological and Molecular Plant Pathology 65: 211-221.
52. Prudent S, Marty F, Charbonnier M. 2005. The yeast osmosensitive mutant fps1Δ transformed by the cauliflower BobTIP1;1 aquaporin withstand a hypo-osmotic shock. FEBS Letters 579: 3872-3880.
53. Querejeta JI, Egerton-Warburton LM, Allen MF. 2009. Topographic position modulates the mycorrhizal response of oak trees to interannual rainfall variability. Ecology 90: 649-662.
54. Ruiz-Lozano JM. 2003. Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13: 309-317.
55. Ruiz-Lozano JM, Azcon R. 1997. Effect of calcium application on the tolerance of mycorrhizal lettuce plants to polyethylene glycol-induced water stress. Symbiosis 23: 9-22.
56. Ruiz-Lozano JM, Del Mar Alguacil M, Barzana G, Vernieri P, Aroca R. 2009. Exogenous ABA accentuates the differences in root hydraulic properties between mycorrhizal and non mycorrhizal maize plants through regulation of PIP aquaporins. Plant Molecular Biology 70: 565-579.
57. Ruiz-Lozano JM, Porcel R, Aroca R. 2006. Does the enhanced tolerance of arbuscular mycorrhizal plants to water deficit involve modulation of drought-induced plant genes? New Phytologist 171: 693-698.
58. Ruíz-Sánchez M, Armada E, Muñoz Y, de Salamone IEG, Aroca R, Ruíz-Lozano JM, Azcón R. 2011. Azospirillum and arbuscular mycorrhizal colonization enhance rice growth and physiological traits under well-watered and drought conditions. Journal of Plant Physiology 168: 1031-1037.
59. Sade N, Vinocur BJ, Diber A, Shatil A, Ronen G, Nissan H, Wallach R, Karchi H, Moshelion M. 2009. Improving plant stress tolerance and yield production: is the tonoplast aquaporin SlTIP2;2 a key to isohydric to anisohydric conversion? New Phytologist 181: 651-661.
60. Sanders IR, Croll D. 2010. Arbuscular mycorrhiza: the challenge to understand the genetics of the fungal partner. Annual Review of Genetics 44: 271-292.
61. Shabala L, Ross T, McMeekin T, Shabala S. 2006. Non-invasive microelectrode ion flux measurements to study adaptive responses of microorganisms to the environment. FEMS Microbiology Review 30: 472-486.
62. + in Escherichia coli using ion-selective microelectrodes. Journal of Microbiological Methods 46: 119-129.
63. Sui H, Han BG, Lee JK, Walian P, Jap BK. 2001. Structural basis of water specific transport through the AQP1 water channel. Nature 414: 872-878.
64. Tamas MJ, Luyten K, Sutherland FC, Hernandez A, Albertyn J, Valadi H, Li H, Prior BA, Kilian SG, Ramos J. 1999. Fps1p controls the accumulation and release of the compatible solute glycerol in yeast osmoregulation. Molecular Microbiology 31: 1087-1104.
65. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596-1599.
66. Tanghe A, Van Dijck P, Thevelein JM. 2006. Why do microorganisms have aquaporins? Trends in Microbiology 14: 78-85.
67. Tisserant E, Kohler A, Dozolme-Seddas P, Balestrini R, Benabdellah K, Colard A, Croll D, Da Silva C, Gomez SK, Koul R et al. 2012. The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytologist 193: 755-769.
68. Verdoucq L, Grondin A, Maurel C. 2008. Structure-function analysis of plant aquaporin at PIP2;1 gating by divalent cations and protons. Biochemical Journal 415: 409-416.
69. Waterham HR, Digan ME, Koutz PJ, Lair SV, Cregg JM. 1997. Isolation of the Pichia pastoris glyceraldehyde-3-phosphate dehydrogenase gene and regulation and use of its promoter. Gene 186: 37-44.
70. Xiong LM, Schumaker KS, Zhu JK. 2002. Cell signaling during cold, drought, and salt stress. Plant Cell 14: 165-183.
71. Yu Q, Hu Y, Li J, Wu Q, Lin Z. 2005. Sense and antisense expression of plasma membrane aquaporin BnPIP1 from Brassica napus in tobacco and its effects on plant drought resistance. Plant Science 169: 647-656.
72. Zimmerberg J, Parsegian VA. 1986. Polymer inaccessible volume changes during opening and closing of a voltage-dependent ionic channel. Nature 323: 36-39.