Two rice plasma membrane intrinsic proteins, OsPIP2;4 and OsPIP2;7, are involved in transport and providing tolerance to boron toxicity

Planta

Volumn 239, Issue 1, 2014, Pages 187-198

  Kumar, Kundan ^a,d   Mosa, Kareem A ^a,b   Chhikara, Sudesh ^a   Musante, Craig ^c   White, Jason C ^c   Dhankher, Om Parkash ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b AL AZHAR UNIVERSITY   (Egypt)

^c Northeast Regional Center for Excellence in Vector Borne Diseases   (United States)

^d BIRLA INSTITUTE OF TECHNOLOGY AND SCIENCE   (India)

Author keywords

Boron tolerance; Boron transport; Plasma membrane intrinsic proteins; Rice; Transgenic Arabidopsis; Yeast HD9 strain

Indexed keywords

ARABIDOPSIS;

ABC TRANSPORTER; ACR3 PROTEIN, S CEREVISIAE; BORON; CARRIER PROTEIN; FPS1 PROTEIN, S CEREVISIAE; MEMBRANE PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; VEGETABLE PROTEIN; YCF1 PROTEIN, S CEREVISIAE;

ARABIDOPSIS; ARTICLE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PLANT LEAF; PLANT ROOT; RICE; SACCHAROMYCES CEREVISIAE; TRANSGENIC PLANT; TRANSPORT AT THE CELLULAR LEVEL;

ARABIDOPSIS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; BORON; GENE EXPRESSION REGULATION, PLANT; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; ORYZA SATIVA; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84891634191     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-013-1969-y     Document Type: Article

References (57)

1. Bansal A, Sankararamakrishnan R (2007) Homology modeling of major intrinsic proteins in rice, maize and Arabidopsis: comparative analysis of transmembrane helix association and aromatic/arginine selectivity filters. BMC Struct Biol 7: 27.
2. Bechtold N, Pelletier G (1993) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. In: Martinez-Zapater J, Salinas J (eds) Arabidopsis protocols. Humana Press, Totowa, pp 259-266.
3. Bienert G, Thorsen M, Schüssler M, Nilsson H, Wagner A, Tamás M, Jahn T (2008) A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3 across membranes. BMC Biol 6: 1-15.
4. Cabello-Hurtado F, Ramos J (2004) Isolation and functional analysis of the glycerol permease activity of two new nodulin-like intrinsic proteins from salt stressed roots of the halophyte Atriplex nummularia. Plant Sci 166: 633-640.
5. Chaumont F, Barrieu F, Jung R, Chrispeels MJ (2000) Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity. Plant Physiol 122: 1025-1034.
6. Chiba Y, Mitani N, Yamaji N, Ma JF (2009) HvLsi1 is a silicon influx transporter in barley. Plant J 57: 810-818.
7. Dannel F, Pfeffer H, Romheld V (2000) Characterization of root boron pools, boron uptake and boron translocation in sunflower using the stable isotopes 10B and 11B. Aust J Plant Physiol 27: 397-405.
8. Dannel F, Pfeffer H, Romheld V (2002) Update on boron in higher plants-uptake, primary translocation and compartmentation. Plant Biol 4: 193-204.
9. Dhankher OP, Li Y, Rosen BP, Shi J, Salt D, Senecoff JF, Sashti NA, Meagher RB (2002) Engineering tolerance and hyperaccumulation of arsenic in plants by combining arsenate reductase and [gamma]-glutamylcysteine synthetase expression. Nat Biotech 20: 1140-1145.
10. Dordas C, Chrispeels MJ, Brown PH (2000) Permeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots. Plant Physiol 124: 1349-1361.
11. Fetter K, van Wilder V, Moshelion M, Chaumont F (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16: 215-228.
12. Fitzpatrick KL, Reid RJ (2009) The involvement of aquaglyceroporins in transport of boron in barley roots. Plant Cell Environ 32: 1357-1365.
13. Garnett TP, Tester MA, Nable RO (1993) The control of boron accumulation by two genotypes of wheat. Plant Soil 155: 305-308.
14. Gerbeau P, Güclü J, Ripoche P, Maurel C (1999) Aquaporin nt-TIPa can account for the high permeability of tobacco cell vacuolar membrane to small neutral solutes. Plant J 18: 577-587.
15. Hanaoka H, Fujiwara T (2007) Channel-mediated boron transport in rice. Plant Cell Physiol 48: S227.
16. Hanba YT, Shibasaka M, Hayashi Y, Hayakawa T, Kasamo K, Terashima I, Katsuhara M (2004) Overexpression of the barley aquaporin HvPIP2;1 increases internal CO2 conductance and CO2 assimilation in the leaves of transgenic rice plants. Plant Cell Physiol 45: 521-529.
17. Hayes JE, Reid R (2004) Boron tolerance in Barley is mediated by efflux of boron from the roots. Plant Physiol 136: 3376-3382.
18. Isayenkov SV, Maathuis FJM (2008) The Arabidopsis thaliana aquaglyceroporin AtNIP7;1 is a pathway for arsenite uptake. FEBS Lett 582: 1625-1628.
19. Kamiya T, Tanaka M, Mitani N, Ma JF, Maeshima M, Fujiwara T (2009) NIP1;1, an aquaporin homolog, determines the arsenite sensitivity of Arabidopsis thaliana. J Biol Chem 284: 2114-2120.
20. Kammerloher W, Fischer U, Piechottka GP, Schäffner AR (1994) Water channels in the plant plasma membrane cloned by immunoselection from a mammalian expression system. Plant J 6: 187-199.
21. Kato Y, Miwa K, Takano J, Wada M, Fujiwara T (2009) Highly boron deficiency-tolerant plants generated by enhanced expression of NIP5;1, a boric acid channel. Plant Cell Physiol 50: 58-66.
22. Li G, Zhang M, Cai W, Sun W, Su W (2008) Characterization of OsPIP2;7, a water channel protein in rice. Plant Cell Physiol 49: 1851-1858.
23. Li R, Ago Y, Liu W, Mitani N, Feldmann J, McGrath SP, Ma JF, Zhao F (2009) The rice aquaporin Lsi1 mediates uptake of methylated arsenic species. Plant Physiol 150: 2071-2080.
24. Liu Z, Shen J, Carbrey JM, Mukhopadhyay R, Agre P, Rosen BP (2002) Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9. Proc Natl Acad Sci 99: 6053-6058.
25. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25: 402-408.
26. Loomis WD, Durst RW (1992) Chemistry and biology of boron. Biofactors 3: 229-239.
27. Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M (2006) A silicon transporter in rice. Nature 440: 688-691.
28. Ma JF, Yamaji N, Mitani N, Xu X, Su Y, McGrath SP, Zhao F (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci 105: 9931-9935.
29. Maciaszczyk-Dziubinska E, Migdal I, Migocka M, Bocer T, Wysocki R (2010) The yeast aquaglyceroporin Fps1p is a bidirectional arsenite channel. FEBS Lett 584: 726-732.
30. Marone M, Mozzetti S, De Ritis D, Pierelli L, Scambia G (2001) Semi-quantitative RT-PCR analysis to assess the expression levels of multiple transcripts from the same sample. Biol Proced 3: 19-25.
31. Matoh T (1997) Boron in plant cell walls. Plant Soil 193: 59-70.
32. Maurel C, Verdoucq L, Luu D, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59: 595-624.
33. Mitani N, Chiba Y, Yamaji N, Ma JF (2009) Identification and characterization of maize and barley Lsi2-like silicon efflux transporters reveals a distinct silicon uptake system from that in rice. Plant Cell 21: 2133-2142.
34. Mitani-Ueno N, Yamaji N, Zhao F, Ma JF (2011) The aromatic/arginine selectivity filter of NIP aquaporins plays a critical role in substrate selectivity for silicon, boron, and arsenic. J Exp Bot 62: 4391-4398.
35. Miwa K, Takano J, Fujiwara T (2006) Improvement of seed yields under boron-limiting conditions through overexpression of BOR1, a boron transporter for xylem loading, in Arabidopsis thaliana. Plant J 46: 1084-1091.
36. Miwa K, Takano J, Omori H, Seki M, Shinozaki K, Fujiwara T (2007) Plants tolerant of high boron levels. Science 318: 1417.
37. Mosa KA, Kumar K, Chhikara S, Joseph M, Liu Z, Musante C, White JC, Dhankher OP (2012) Members of rice plasma membrane intrinsic protein subfamily are involved in arsenite permeability and tolerance in plants. Transgenic Res 21: 1265-1277.
38. Moshelion M, Becker D, Biela A, Uehlein N, Hedrich R, Otto B, Levi H, Moran N, Kaldenhoff R (2002) Plasma membrane aquaporins in the motor cells of Samanea saman: diurnal and circadian regulation. Plant Cell 14: 727-739.
39. Nable RO, Bañuelos GS, Paull JG (1997) Boron toxicity. Plant Soil 193: 181-198.
40. Nakagawa Y, Hanaoka H, Kobayashi M, Miyoshi K, Miwa K, Fujiwara T (2007) Cell-type specificity of the expression of OsBOR1, a rice efflux boron transporter gene, is regulated in response to boron availability for efficient boron uptake and xylem loading. Plant Cell 19: 2624-2635.
41. Oertli JJ, Kohl HC (1961) Some considerations about the tolerance of various plant species to excessive supplies of boron. Soil Sci 92: 243-247.
42. Pang Y, Li L, Ren F, Lu P, Wei P, Cai J, Xin L, Zhang J, Chen J, Wang X (2010) Overexpression of the tonoplast aquaporin AtTIP5;1 conferred tolerance to boron toxicity in Arabidopsis. J Genet Genomics 37: 389-397.
43. Ralston NV, Hunt CD (2001) Diadenosine phosphates and S-adenosylmethionine: novel boron binding biomolecules detected by capillary electrophoresis. Biochim Biophys Acta 1527: 20-30.
44. Reid R (2007) Identification of boron transporter genes likely to be responsible for tolerance to boron toxicity in wheat and barley. Plant Cell Physiol 48: 1673-1678.
45. Reid R, Fitzpatrick K (2009) Influence of leaf tolerance mechanisms and rain on boron toxicity in barley and wheat. Plant Physiol 151: 413-420.
46. Sakurai J, Ishikawa F, Yamaguchi T, Uemura M, Maeshima M (2005) Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol 46: 1568-1577.
47. Schnurbusch T, Hayes J, Hrmova M, Baumann U, Ramesh SA, Tyerman SD, Langridge P, Sutton T (2010) Boron toxicity tolerance in barley through reduced expression of the multifunctional aquaporin HvNIP2;1. Plant Physiol 153: 1706-1715.
48. Siefritz F, Otto B, Bienert GP, van Der Krol A, Kaldenhoff R (2004) The plasma membrane aquaporin NtAQP1 is a key component of the leaf unfolding mechanism in tobacco. Plant J 37: 147-155.
49. Sutton T, Baumann U, Hayes J, Collins NC, Shi B, Schnurbusch T, Hay A, Mayo G, Pallotta M, Tester M, Langridge P (2007) Boron-toxicity tolerance in barley arising from efflux transporter amplification. Science 318: 1446-1449.
50. Takano J, Noguchi K, Yasumori M, Kobayashi M, Gajdos Z, Miwa K, Hayashi H, Yoneyama T, Fujiwara T (2002) Arabidopsis boron transporter for xylem loading. Nature 420: 337-340.
51. Takano J, Wada M, Ludewig U, Schaaf G, Wirén NV, Fujiwara T (2006) The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 18: 1498-1509.
52. Tanaka M, Wallace IS, Takano J, Roberts DM, Fujiwara T (2008) NIP6;1 is a boric acid channel for preferential transport of boron to growing shoot tissues in Arabidopsis. Plant Cell 20: 2860-2875.
53. Wallace IS, Roberts DM (2004) Homology modeling of representative subfamilies of arabidopsis major intrinsic proteins classification based on the aromatic/arginine selectivity filter. Plant Physiol 135: 1059-1068.
54. Weig A, Deswarte C, Chrispeels MJ (1997) The major intrinsic protein family of Arabidopsis has 23 members that form three distinct groups with functional aquaporins in each group. Plant Physiol 114: 1347-1357.
55. Wimmer MA, Mühling KH, Läuchli A, Brown PH, Gold-bach HE (2002) Boron toxicity: the importance of soluble boron. In: Gold- bach HE, Rerkasem B, Wimmer MA, Brown PH, Bell RW (eds) Boron in plant and animal nutrition. Kluwer, New York, pp 241-253.
56. Yamada S, Katsuhara M, Kelly WB, Michalowski CB, Bohnert HJ (1995) A family of transcripts encoding water channel proteins: tissue-specific expression in the common ice plant. Plant Cell 7: 1129-1142.
57. Zhao F, Ago Y, Mitani N, Li R, Su Y, Yamaji N, McGrath SP, Ma JF (2010) The role of the rice aquaporin Lsi1 in arsenite efflux from roots. New Phytol 186: 392-399.