Functional analysis of the novel mycorrhiza-specific phosphate transporter AsPT1 and PHT1 family from Astragalus sinicus during the arbuscular mycorrhizal symbiosis

New Phytologist

Volumn 198, Issue 3, 2013, Pages 836-852

  Xie, Xianan ^a   Huang, Wu ^a   Liu, Fengchuan ^a   Tang, Nianwu ^a   Liu, Yi ^a   Lin, Hui ^a   Zhao, Bin ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

Arbuscular mycorrhizas; AsPT1; AsPT4; Astragalus sinicus; Overexpression; Pht1 family; RNA interference

Indexed keywords

PHOSPHATE TRANSPORTER; VEGETABLE PROTEIN;

FUNCTIONAL ROLE; GENE; GENE EXPRESSION; LEGUME; PHENOTYPE; PHOSPHATE; PLANT COMMUNITY; RNA; SYMBIOSIS; YEAST;

AMINO ACID SEQUENCE; ARTICLE; ASTRAGALUS PLANT; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MYCORRHIZA; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; PLANT ROOT; PROMOTER REGION; RNA INTERFERENCE; SYMBIOSIS; TRANSGENIC PLANT; YEAST;

AMINO ACID SEQUENCE; ASTRAGALUS PLANT; CONSERVED SEQUENCE; GENE EXPRESSION REGULATION, PLANT; GENETIC COMPLEMENTATION TEST; MOLECULAR SEQUENCE DATA; MYCORRHIZAE; PHOSPHATE TRANSPORT PROTEINS; PHYLOGENY; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; RNA INTERFERENCE; SYMBIOSIS; YEASTS;

ARBUSCULAR; ASTRAGALUS SINICUS;

EID: 84876418117     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12188     Document Type: Article

References (58)

1. Ai P, Sun S, Zhao J, Fan X, Xin W, Guo Q, Yu L, Shen Q, Wu P, Miller AJ. 2009. Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation. Plant Journal 57: 798-809.
2. Andriankaja A, Boisson-Dernier A, Frances L, Sauviac L, Jauneau A, Barker DG, Carvalho-Niebel F. 2007. AP2-ERF transcription factors mediate Nod factor-dependent MtENOD11 activation in root hairs via a novel cis-regulatory motif. Plant Cell 19: 2866-2885.
3. Boisson-Dernier A, Chabaud M, Garcia F, Bécard G, Rosenberg C, Barker DG. 2001. Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Molecular Plant-Microbe Interactions 14: 695-700.
4. Bucher M. 2007. Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytologist 173: 11-26.
5. Bucher M, Rausch C, Daram P. 2001. Molecular and biochemical mechanisms of phosphorus uptake into plants. Journal of Plant Nutrition and Soil Science 164: 209-217.
6. Chen A, Gu M, Sun S, Zhu L, Hong S, Xu G. 2011. Identification of two conserved cis-acting elements, MYCS and P1BS, involved in the regulation of mycorrhiza-activated phosphate transporters in eudicot species. New Phytologist 189: 1157-1169.
7. 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 Phytologist 173: 817-831.
8. Chu Z, Yuan M, Yao J, Ge X, Yuan B, Xu C, Li X, Fu B, Li Z, Bennetzen JL. 2006. Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes & Development 20: 1250-1255.
9. Daram P, Brunner S, Rausch C, Steiner C, Amrhein N, Bucher M. 1999. Pht2;1 encodes a low-affinity phosphate transporter from Arabidopsis. Plant Cell 11: 2153-2166.
10. Denison RF, Kiers ET. 2011. Life histories of symbiotic rhizobia and mycorrhizal fungi. Current Biology 21: R775-R785.
11. Dermatsev V, Weingarten-Baror C, Resnick N, Gadkar V, Wininger S, Kolotilin I, Mayzlish-Gati E, Zilberstein A, Koltai H, Kapulnik Y. 2010. Microarray analysis and functional tests suggest the involvement of expansins in the early stages of symbiosis of the arbuscular mycorrhizal fungus Glomus intraradices on tomato (Solanum lycopersicum). Molecular Plant Pathology 11: 121-135.
12. Drissner D, Kunze G, Callewaert N, Gehrig P, Tamasloukht MB, Boller T, Felix G, Amrhein N, Bucher M. 2007. Lyso-phosphatidylcholine is a signal in the arbuscular mycorrhizal symbiosis. Science 318: 265-268.
13. Ezawa T, Cavagnaro TR, Smith SE, Smith FA, Ohtomo R. 2004. Rapid accumulation of polyphosphate in extraradical hyphae of an arbuscular mycorrhizal fungus as revealed by histochemistry and a polyphosphate kinase/luciferase system. New Phytologist 161: 387-392.
14. Fehlberg V, Vieweg MF, Dohmann EMN, Hohnjec N, Pühler A, Perlick AM, Küster H. 2005. The promoter of the leghaemoglobin gene VfLb29: functional analysis and identification of modules necessary for its activation in the infected cells of root nodules and in the arbuscule-containing cells of mycorrhizal roots. Journal of Experimental Botany 56: 799-806.
15. Floss DS, Hause B, Lange PR, Küster H, Strack D, Walter MH. 2008. 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 Journal 56: 86-100.
16. Frenzel A, Tiller N, Hause B, Krajinski F. 2006. The conserved arbuscular mycorrhiza-specific transcription of the secretory lectin MtLec5 is mediated by a short upstream sequence containing specific protein binding sites. Planta 224: 792-800.
17. Gomez-Ariza J, Balestrini R, Novero M, Bonfante P. 2009. Cell-specific gene expression of phosphate transporters in mycorrhizal tomato roots. Biology and Fertility of Soils 45: 845-853.
18. 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: 2413-2429.
19. Hong J, Park YS, Bravo A, Bhattarai KK, Daniels DA, Harrison MJ. 2012. Diversity of morphology and function in arbuscular mycorrhizal symbioses in Brachypodium distachyon. Planta 236: 851-865.
20. Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ. 2007a. A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences, USA 104: 1720-1725.
21. Javot H, Pumplin N, Harrison MJ. 2007b. Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant, Cell & Environment 30: 310-322.
22. Jia H, Ren H, Gu M, Zhao J, Sun S, Zhang X, Chen J, Wu P, Xu G. 2011. The phosphate transporter gene OsPht1;8 is involved in phosphate homeostasis in rice. Plant Physiology 156: 1164-1175.
23. Karandashov V, Bucher M. 2005. Symbiotic phosphate transport in arbuscular mycorrhizas. Trends in Plant Science 10: 22-29.
24. Karandashov V, Nagy R, Wegmüller S, Amrhein N, Bucher M. 2004. Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences, USA 101: 6285-6290.
25. Kouchi H, Hata S. 1993. Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Molecular & General Genetics 238: 106-119.
26. Li Y, Zhou L, Chen D, Tan X, Lei L, Zhou J. 2008. A nodule-specific plant cysteine proteinase, AsNODF32, is involved in nodule senescence and nitrogen fixation activity of the green manure legume Astragalus sinicus. New Phytologist 180: 185-192.
27. Liu C, Muchhal US, Uthappa M, Kononowicz AK, Raghothama KG. 1998a. Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus. Plant Physiology 116: 91-99.
28. Liu F, Wang Z, Ren H, Shen C, Li Y, Ling HQ, Wu C, Lian X, Wu P. 2010. OsSPX1 suppresses the function of OsPHR2 in the regulation of expression of OsPT2 and phosphate homeostasis in shoots of rice. Plant Journal 62: 508-517.
29. Liu H, Trieu AT, Blaylock LA, Harrison MJ. 1998b. Cloning and characterization of two phosphate transporters from Medicago truncatula roots: regulation in response to phosphate and to colonization by arbuscular mycorrhizal (AM) fungi. Molecular Plant-Microbe Interactions 11: 14-22.
30. Liu Y-G, Chen Y. 2007. High-efficiency thermal asymmetric interlaced PCR for amplification of unknown flanking sequences. BioTechniques 43: 649-656.
31. Loth-Pereda V, Orsini E, Courty PE, Lota F, Kohler A, Diss L, Blaudez D, Chalot M, Nehls U, Bucher M et al. 2011. Structure and expression profile of the phosphate Pht1 transporter gene family in mycorrhizal Populus trichocarpa. Plant Physiology 156: 2141-2154.
32. 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 and Cell Physiology 47: 807-817.
33. Nagarajan VK, Jain A, Poling MD, Lewis AJ, Raghothama KG, Smith AP. 2011. Arabidopsis Pht1;5 mobilizes phosphate between source and sink organs and influences the interaction between phosphate homeostasis and ethylene signaling. Plant Physiology 156: 1149-1163.
34. Nagy R, Karandashov V, Chague V, Kalinkevich K, Tamasloukht MB, 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 Journal 42: 236-250.
35. Pao SS, Paulsen IT, Saier MH Jr. 1998. Major facilitator superfamily. Microbiology and Molecular Biology Reviews 62: 1-34.
36. Paszkowski U, Kroken S, Roux C, Briggs SP. 2002. Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences, USA 99: 13 324-13 329.
37. Rae AL, Cybinski DH, Jarmey JM, Smith FW. 2003. Characterization of two phosphate transporters from barley; evidence for diverse function and kinetic properties among members of the Pht1 family. Plant Molecular Biology 53: 27-36.
38. Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M. 2001. A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414: 462-470.
39. Reinders A, Schulze W, Kühn C, Barker L, Schulz A, Ward JM, Frommer WB. 2002. Protein-protein interactions between sucrose transporters of different affinities colocalized in the same enucleate sieve element. The Plant Cell 14: 1567-1577.
40. Remy E, Cabrito TR, Batista RA, Teixeira MC, Sa′-Correia I, Duque P. 2012. The Pht1;9 and Pht1;8 transporters mediate inorganic phosphate acquisition by the Arabidopsis thaliana root during phosphorus starvation. New Phytologist 195: 356-371.
41. Remy W, Taylor TN, Hass H, Kerp H. 1994. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proceedings of the National Academy of Sciences, USA 91: 11 841-11 843.
42. Schaffer G, Peterson L. 1993. Modifications to clearing methods used in combination with vital staining of roots colonized with vesiculararbuscular mycorrhizal fungi. Mycorrhiza 4: 29-35.
43. Scotto-Lavino E, Du GW, Frohman MA. 2006a. 5′ end cDNA amplification using classic RACE. Nature Protocols 1: 2555-2562.
44. Scotto-Lavino E, Du G, Frohman MA. 2006b. 3′ end cDNA amplification using classic RACE. Nature Protocols 1: 2742-2745.
45. Shin H, Shin HS, Chen R, Harrison MJ. 2006. Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation. Plant Journal 45: 712-726.
46. Shin H, Shin HS, Dewbre GR, Harrison MJ. 2004. Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high- phosphate environments. Plant Journal 39: 629-642.
47. Smith SE, Jakobsen I, Groenlund 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 Physiology 156: 1050-1057.
48. Smith SE, Read DJ. 2008. Mycorrhizal symbiosis. San Diego, CA, USA: Academic Press.
49. Smith SE, Smith FA, Jakobsen I. 2003. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiology 133: 16-20.
50. Sun S, Gu M, Cao Y, Huang X, Zhang X, Ai P, Zhao J, Fan X, Xu G. 2012. A constitutive expressed phosphate transporter, OsPht1;1, modulates phosphate uptake and translocation in phosphate-replete rice. Plant Physiology 159: 1571-1581.
51. Tamura Y, Kobae Y, Mizuno T, Hata S. 2012. Identification and expression analysis of arbuscular mycorrhiza-inducible phosphate transporter genes of soybean. Bioscience, Biotechnology, and Biochemistry 76: 309-313.
52. Tatsuhiro E, Sally ES. 2001. Differentiation of polyphosphate metabolism between the extra- and intraradical hyphae of arbuscular mycorrhizal fungi. New Phytologist 149: 555-563.
53. Thevelein JM, Voordeckers K. 2009. Functioning and evolutionary significance of nutrient transceptors. Molecular Biology and Evolution 26: 2407-2414.
54. Trouvelot A. 1986. Mesure du taux de mycorhization VA d'un systeme radiculaire. Recherche de methodes d'estimation ayant une significantion fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S, eds. Physiological and genetical aspects of Mycorrhizae. Paris, France: INRA, 217-221.
55. Wu Z, Zhao J, Gao R, Hu G, Gai J, Xu GH, Xing H. 2011. Molecular cloning, characterization and expression analysis of two members of the Pht1 family of phosphate transporters in Glycine max. PLoS ONE 6: e19752.
56. Xu G, 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. Journal of Experimental Botany 58: 2491-2501.
57. Yang S, Grønlund M, Jakobsen I, Grotemeyer MS, Rentsch D, Miyao A, Hirochik H, Kumar CS, Sundaresan V, Salamin N et al. 2012. Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the PHOSPHATE TRANSPORTER1 gene family. Plant Cell 24: 4236-4251.
58. Zhang Q, Blaylock LA, Harrison MJ. 2010. Two Medicago truncatula half-ABC transporters are essential for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Cell 22: 1483-1497.