OsNIP3;1, a rice boric acid channel, regulates boron distribution and is essential for growth under boron-deficient conditions

Plant Journal

Volumn 78, Issue 5, 2014, Pages 890-902

  Hanaoka, Hideki ^a,d   Uraguchi, Shimpei ^a,b,e   Takano, Junpei ^a,c   Tanaka, Mayuki ^a,b   Fujiwara, Toru ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

^d Scientific Affairs Life Technologies Japan Ltd   (Japan)

^e UNIVERSITY OF BAYREUTH   (Germany)

Author keywords

aquaporin; boron; homeostasis; NIP; nutrient; Oryza sativa L.; transport

Indexed keywords

BORIC ACID; BORIDE COATINGS; CELL MEMBRANES; CYTOLOGY; GENES; HISTOLOGY; NUTRIENTS; PLANTS (BOTANY); TISSUE;

AQUAPORINS; HOMEOSTASIS; NIP; ORYZA SATIVA L; TRANSPORT;

BORON;

BORON; VEGETABLE PROTEIN;

DEFICIENCY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; RICE; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; BORON; GENE EXPRESSION REGULATION, PLANT; MOLECULAR SEQUENCE DATA; ORYZA SATIVA; PLANT PROTEINS;

EID: 84901444716     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12511     Document Type: Article

References (60)

1. Bansal, A., and, Sankararamakrishnan, R., (2007) Homology modeling of major intrinsic proteins in rice, maize and A. thaliana: comparative analysis of transmembrane helix association and aromatic/arginine selectivity filters. BMC Struct. Biol. 7, 27.
2. Bellaloui, N., Yadavc, R.C., Chern, M.S., Hu, H., Gillen, A.M., Greve, C., Dandekar, A.M., Ronald, P.C., and, Brown, P.H., (2003) Transgenically enhanced sorbitol synthesis facilitates phloem-boron mobility in rice. Physiol. Plant. 117, 79-84.
3. Brown, P.H., and, Shelp, B.J., (1997) Boron mobility in plants. Plant Soil, 193, 85-101.
4. Cheng, C., and, Rerkasem, B., (1993) Effects of boron on pollen viability in wheat. Plant Soil, 156, 313-315.
5. Chiu, W., Niwa, Y., Zeng, W., Hirano, T., Kobayashi, H., and, Sheen, J., (1996) Engineered GFP as a vital reporter in plants. Curr. Biol. 6, 325-330.
6. Curtis, M.D., and, Grossniklaus, U., (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462-469.
7. Dannel, F., Pfeffer, H., and, Romheld, V., (2000) Characterization of root boron pools, boron uptake and boron translocation in sunflower using the stable isotopes boron-10 and boron-11. Aust. J. Plant Physiol. 27, 397-405.
8. Fukuda, A., Okada, Y., Suzui, N., Fujiwara, T., Yoneyama, T., and, Hayashi, H., (2004) Cloning and characterization of the gene for a phloem-specific glutathione S-transferase from rice leaves. Physiol. Plant. 120, 595-602.
9. Garg, O., Sharma, A., and, Kona, G., (1979) Effect of boron on the pollen vitality and yield of rice plants (Oryza sativa L. var. Jaya). Plant Soil, 52, 591-594.
10. Gomes, D., Agasse, A., Thiébaud, P., Delrot, S., Gerõs, H., and, Chaumont, F., (2009) Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochim. Biophys. Acta, 1788, 1213-1228.
11. de Groot, B.L., and, Grubmuller, H., (2001) Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Science, 294, 2353-2357.
12. Inoue, H., Higuchi, K., Takahashi, M., Nakanishi, H., Mori, S., and, Nishizawa, N.K., (2003) Three rice nicotianamine synthase genes, OsNAS1, OsNAS2, and OsNAS3 are expressed in cells involved in long-distance transport of iron and differentially regulated by iron. Plant J. 36, 366-381.
13. Kajikawa, M., Fujibe, T., Uraguchi, S., Miwa, K., and, Fujiwara, T., (2011) Expression of the Arabidopsis borate efflux transporter gene, AtBOR4, in rice affects the xylem loading of boron and tolerance to excess boron. Biosci. Biotechnol. Biochem. 75, 2421-2423.
14. Kasai, K., Takano, J., Miwa, K., Toyoda, A., and, Fujiwara, T., (2011) High boron-induced ubiquitination regulates vacuolar sorting of the BOR1 borate transporter in Arabidopsis thaliana. J. Biol. Chem. 286, 6175-6183.
15. Kato, Y., Miwa, K., Takano, J., Wada, M., and, 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.
16. Kouchi, H., and, Kumazawa, K., (1975) Anatomical responses of root tips to boron deficiency. II. Effect of boron deficiency on the cellular growth and development in root tips. Soil Sci. Plant Nutr. 21, 137-150.
17. Li, T., Choi, W.-G., Wallace, I.S., Baudry, J., and, Roberts, D.M., (2011) Arabidopsis thaliana NIP7;1: an anther-specific boric acid transporter of the aquaporin superfamily regulated by an unusual tyrosine in helix 2 of the transport pore. Biochemistry, 50, 6633-6641.
18. Ma, J.F., Tamai, K., Yamaji, N., Mitani, N., Konishi, S., Katsuhara, M., Ishiguro, M., Murata, Y., and, Yano, M., (2006) A silicon transporter in rice. Nature, 440, 688-691.
19. Marschner, H., (1995) Mineral Nutrition of Higher Plants, 2nd edn. San Diego, CA: Academic Press.
20. Matoh, T., and, Ochiai, K., (2005) Distribution and partitioning of newly taken-up boron in sunflower. Plant Soil, 278, 351-360.
21. Matoh, T., Kawaguchi, S., and, Kobayashi, M., (1996) Ubiquity of a borate-rhamnogalacturonan II complex in the cell walls of higher plants. Plant Cell Physiol. 37, 636-640.
22. Maurel, C., (2007) Plant aquaporins: novel functions and regulation properties. FEBS Lett. 581, 2227-2236.
23. Miki, D., and, Shimamoto, K., (2004) Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol. 45, 490-495.
24. Mitani, N., Yamaji, N., and, Ma, J., (2008) Characterization of substrate specificity of a rice silicon transporter, Lsi1. Pflugers Arch. 456, 679-686.
25. Mitani-Ueno, N., Yamaji, N., Zhao, F.-J., and, Ma, J.F., (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.
26. Miwa, K., Takano, J., and, 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.
27. Miwa, K., Takano, J., Omori, H., Seki, M., Shinozaki, K., and, Fujiwara, T., (2007) Plants tolerant of high boron levels. Science, 318, 1417.
28. Miwa, K., Wakuta, S., Takada, S., Ide, K., Takano, J., Naito, S., Omori, H., Matsunaga, T., and, Fujiwara, T., (2013) Roles of BOR2, a boron exporter, in cross linking of rhamnogalacturonan II and root elongation under boron limitation in Arabidopsis. Plant Physiol. 163, 1699-1709.
29. Nable, R.O., Banuelos, G.S., and, Paull, J.G., (1997) Boron toxicity. Plant Soil, 193, 181-198.
30. Nakagawa, Y., Hanaoka, H., Kobayashi, M., Miyoshi, K., Miwa, K., and, 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.
31. O'Neill, M.A., Eberhard, S., Albersheim, P., and, Darvill, A.G., (2001) Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science, 294, 846-849.
32. Pfahler, P.L., (1967) In vitro germination and pollen tube growth of maize (Zea mays L) pollen: I. Calcium and boron effects. Can. J. Bot. 45, 839-845.
33. Rashid, A., Muhammad, S., and, Rafique, E., (2000) Genotypic variation in rice susceptibility to boron deficiency. Int. Rice Res. Notes, 25, 29-30.
34. Rentsch, D., Laloi, M., Rouhara, I., Schmelzer, E., Delrot, S., and, Frommer, W.B., (1995) NTR1 encodes a high affinity oligopeptide transporter in Arabidopsis. FEBS Lett. 370, 264-268.
35. Rerkasem, B., and, Jamjod, S., (1997) Genotypic variation in plant response to low boron and implications for plant breeding. Plant Soil, 193, 169-180.
36. Römheld, V., (2000) The chlorosis paradox: Fe inactivation as a secondary event in chlorotic leaves of grapevine. J. Plant Nutr. 23, 1629-1643.
37. Sakurai, J., Ishikawa, F., Yamaguchi, T., Uemura, M., and, Maeshima, M., (2005) Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol. 46, 1568-1577.
38. Saleem, M., Khanif, Y.M., Fauziah, C., Samsuri, A.W., and, Hafeez, B., (2010) Effectiveness of borax and colemanite as boron sources for rice grown in flooded acidic soil. In Proceedings of the 19th World Congress of Soil Science; Soil Solutions for a Changing World (, Gilkes, R.J., and, Prakongkep, N., eds). ISBN 978-0-646- 53783-2; Published on DVD, pp. 9-11. http://www.iuss.org.
39. Sasaki, A., Yamaji, N., Yokosho, K., and, Ma, J.F., (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell, 24, 2155-2167.
40. Schnurbusch, T., Hayes, J., Hrmova, M., Baumann, U., Ramesh, S.A., Tyerman, S.D., Langridge, P., and, Sutton, T., (2010) Boron toxicity tolerance in barley through reduced expression of the multifunctional aquaporin HvNIP2;1. Plant Physiol. 153, 1706-1715.
41. Schroeder, J.I., Delhaize, E., Frommer, W.B., et al. (2013) Using membrane transporters to improve crops for sustainable food production. Nature, 497, 60-66.
42. Shelp, B.J., Kitheka, A.M., Vanderpool, R.A., Van Cauwenberghe, O.R., and, Spiers, G.A., (1998) Xylem-to-phloem transfer of boron in broccoli and lupin during early reproductive growth. Physiol. Plant. 104, 533-540.
43. Shorrocks, V.M., (1997) The occurrence and correction of boron deficiency. Plant Soil, 193, 121-148.
44. Takano, J., Yamagami, M., Noguchi, K., Hayashi, H., and, Fujiwara, T., (2001) Preferential translocation of boron to young leaves in Arabidopsis thaliana regulated by the BOR1 gene. Soil Sci. Plant Nutr. 47, 345-357.
45. Takano, J., Noguchi, K., Yasumori, M., Kobayashi, M., Gajdos, Z., Miwa, K., Hayashi, H., Yoneyama, T., and, Fujiwara, T., (2002) Arabidopsis boron transporter for xylem loading. Nature, 420, 337-340.
46. Takano, J., Miwa, K., Yuan, L., von Wiren, N., and, Fujiwara, T., (2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc. Natl Acad. Sci. USA, 102, 12276-12281.
47. Takano, J., Wada, M., Ludewig, U., Schaaf, G., von Wiren, N., and, 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.
48. Takano, J., Miwa, K., and, Fujiwara, T., (2008) Boron transport mechanisms: collaboration of channels and transporters. Trends Plant Sci. 13, 451-457.
49. Takano, J., Tanaka, M., Toyoda, A., Miwa, K., Kasai, K., Fuji, K., Onouchi, H., Naito, S., and, Fujiwara, T., (2010) Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proc. Natl Acad. Sci. USA, 107, 5220-5225.
50. Tanaka, M., Wallace, I.S., Takano, J., Roberts, D.M., and, 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.
51. Tanaka, M., Takano, J., Chiba, Y., Lombardo, F., Ogasawara, Y., Onouchi, H., Naito, S., and, Fujiwara, T., (2011) Boron-dependent degradation of NIP5;1 mRNA for acclimation to excess boron conditions in Arabidopsis. Plant Cell, 23, 3547-3559.
52. Tanaka, N., Uraguchi, S., Saito, A., Kajikawa, M., Kasai, K., Sato, Y., Nagamura, Y., and, Fujiwara, T., (2013) Roles of pollen-specific boron efflux transporter, OsBOR4, in the rice fertilization process. Plant Cell Physiol. 54, 2011-2019.
53. Tanaka, N., Uraguchi, S., and, Fujiwara, T., (2014) Exogenous boron supplementation partially rescues fertilization defect of osbor4 mutant. Plant Signal. Behav. 9, e28356.
54. Toki, S., (1997) Rapid and efficient Agrobacterium-mediated transformation in rice. Plant Mol. Biol. Rep. 15, 16-21.
55. Uraguchi, S., and, Fujiwara, T., (2011) Significant contribution of boron stored in seeds to initial growth of rice seedlings. Plant Soil, 340, 435-442.
56. Wallace, I.S., and, Roberts, D.M., (2004) Homology modeling of representative subfamilies of Arabidopsis major intrinsic proteins. Classification based on the aromatic/arginine selectivity filter. Plant Physiol. 135, 1059-1068.
57. Wallace, I.S., and, Roberts, D.M., (2005) Distinct transport selectivity of two structural subclasses of the nodulin-like intrinsic protein family of plant aquaglyceroporin channels. Biochemistry, 44, 16826-16834.
58. Wallace, I.S., Choi, W.G., and, Roberts, D.M., (2006) The structure, function and regulation of the nodulin 26-like intrinsic protein family of plant aquaglyceroporins. Biochim. Biophys. Acta, 1758, 1165-1175.
59. Warington, K., (1923) The effect of boric acid and borax on the broad bean and certain other plants. Ann. Bot. 32, 629-672.
60. Wongmo, J., Jamjod, S., and, Rerkasem, B., (2004) Contrasting responses to boron deficiency in barley and wheat. Plant Soil, 259, 103-110.