Transport processes of the legume symbiosome membrane

Frontiers in Plant Science

Volumn 5, Issue DEC, 2014, Pages

  Clarke, Victoria C ^a   Loughlin, Patrick C ^a   Day, David A ^b   Smith, Penelope M C ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b FLINDERS UNIVERSITY   (Australia)

Author keywords

Legume; Membrane; Rhizobia; Symbiosis; Transport

Indexed keywords

GLYCINE MAX;

EID: 84918798791     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00699     Document Type: Article

References (92)

1. Andreev, I. M., Dubrovo, P. N., Krylova, V. V., and Izmailov, S. F. (1999). Functional identification of ATP-driven Ca2+ pump in the peribacteroid membrane of broad bean root nodules. FEBS Lett. 447, 49–52. doi: 10.1016/S0014-5793(99)00262-8
2. Bagchi, R., Salehin, M., Adeyemo, O. S., Salazar, C., Shulaev, V., Sherrier, D. J., et al. (2012). Functional assessment of the Medicago truncatula NIP/LATD protein demonstrates that it is a high-affinity nitrate transporter. Plant Physiol. 160, 906–916. doi: 10.1104/pp.112.196444
3. Beatty, P. H., and Good, A. G. (2011). Plant science. Future prospects for cereals that fix nitrogen. Science333, 416–417. doi: 10.1126/science.1209467
4. Beeckman, T., and Friml, J. (2010). Nitrate contra auxin: nutrient sensing by roots. Dev. Cell18, 877–878. doi: 10.1016/j.devcel.2010.05.020
5. Benedito, V. A., Li, H., Dai, X., Wandrey, M., He, J., Kaundal, R., et al. (2010). Genomic inventory and transcriptional analysis of Medicago truncatula transporters. Plant Physiol. 152, 1716–1730. doi: 10.1104/pp.109.148684
6. Benedito, V. A., Torres-Jerez, I., Murray, J. D., Andriankaja, A., Allen, S., Kakar, K., et al. (2008). A gene expression atlas of the model legume Medicago truncatula. Plant J. 55, 504–513. doi: 10.1111/j.1365-313X.2008.03519.x
7. Blumwald, E., Fortin, M. G., Rea, P. A., Verma, D. P. S., and Poole, R. J. (1985). Presence of host plasma membrane type H+-ATPase in the membrane envelope enclosing the bacteroids in soybean root nodules. Plant Physiol. 78, 655–672. doi: 10.1104/pp.78.4.665
8. Bright, L. J., Liang, Y., Mitchell, D. M., and Harris, J. M. (2005). The LATD gene of Medicago truncatula is required for both nodule and root development. Mol. Plant Microbe Interact.18, 521–532. doi: 10.1094/MPMI-18-0521
9. Catalano, C. M., Lane, W. S., and Sherrier, D. J. (2004). Biochemical characteriza-tionof symbiosome membrane proteins from Medicago truncatularoot nodules. Electrophoresis25, 519–531. doi: 10.1002/elps.200305711
10. Colebatch, G., Desbrosses, G., Ott, T., Krusell, L., Montanari, O., Kloska, S., et al. (2004). Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant J. 39, 487–512. doi: 10.1111/j.1365-313X.2004.02150.x
11. Coque, L., Neogi, P., Pislariu, C., Wilson, K. A., Catalano, C., Avadhani, M., et al. (2008). Transcription of ENOD8 in Medicago truncatula nodules directs ENOD8 esterase to developing and mature symbiosomes. Mol. Plant Microbe Interact.21, 404–410. doi: 10.1094/MPMI-21-4-0404
12. Day, D. A., Kaiser, B. N., Thomson, R., Udvardi, M. K., Moreau, S., and Puppo, A. (2001a). Nutrient transport across symbiotic membranes from legume nodules. Aust. J. Plant Physiol.28, 667–674. doi: 10.1071/PP01028
13. Day, D. A., Poole, P. S., Tyerman, S. D., and Rosendahl, L. (2001b). Ammonia and amino acid transport across symbiotic membranes in nitrogen-fixing legume nodules. Cell. Mol. Life Sci.58, 61–71. doi: 10.1007/PL00000778
14. Day, D. A., Whitehead, L. F., Hendriks, J. H. M., and Tyerman, S. D. (1995). “Nitrogen and carbon exchange across symbiotic membranes from soybean nodules,” in Nitrogen Fixation: Fundamentals and Applications, eds I. A. Tikhonovich, N. A. Provorov, V. I. Romanov, and W. E. Newton (Dordrecht: Kluwer Academic Publishers), 557–564.
15. Dean, R.M., Rivers, R.L., Zeidel, M. L., and Roberts, D.M.(1999). Purification and functional reconstitution of soybean nodulin 26. An aquaporin with water and glycerol transport properties. Biochemistry38, 347–353. doi: 10.1021/bi982110c
16. Delgado, M. J., Tresierra-Ayala, A., Talbi, C., and Bedmar, E. J. (2006). Functional characterization of the Bradyrhizobium japonicum modA and modB genes involved in molybdenum transport. Microbiology152, 199–207. doi: 10.1099/mic.0.28347-0
17. Esseling, J. J., Lhuissier, F. G. P., and Emons, A. M. C. (2003). Nod factor-induced root hair curling: continuous polar growth towards the point of nod factor application. Plant Physiol. 132, 1982–1988. doi: 10.1104/pp.103.021634
18. Fedorova, E., Thomson, R., Whitehead, L. F., Maudoux, O., Udvardi, M. K., and Day, D. A. (1999). Localization of H+-ATPases in soybean root nodules. Planta209, 25–32. doi: 10.1007/s004250050603
19. Fortin, M. G., Morrison, N. A., and Verma, D. P. S. (1987). Nodulin-26, a peribacteroid membrane nodulin is expressed independently of the development of the peribacteroid compartment. Nucleic Acids Res. 15, 813–824. doi: 10.1093/nar/15.2.813
20. Frary, A., Nesbitt, T. C., Grandillo, S., Knaap, E., Cong, B., Liu, J., et al. (2000). fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289, 85–88. doi: 10.1126/science.289.5476.85
21. Hakoyama, T., Niimi, K., Watanabe, H., Tabata, R., Matsubara, J., Sato, S., et al. (2009). Host plant genome overcomes the lack of a bacterial gene for symbiotic nitrogen fixation. Nature462, 514–517. doi: 10.1038/nature08594
22. Hakoyama, T., Niimi, K., Yamamoto, T., Isobe, S., Sato, S., Nakamura, Y., et al. (2012). The integral membrane protein SEN1 is required for symbiotic nitrogen fixation in Lotus japonicus nodules. Plant Cell Physiol. 53, 225–236. doi: 10.1093/pcp/pcr167
23. Halbleib, C. M., and Ludden, P. W. (2000). Regulation of biological nitrogen fixation. J. Nutr.130, 1081–1084.
24. Harris, J. M., and Dickstein, R. (2010). Control of root architecture and nodu-lation by the LATD/NIP transporter. Plant Signal. Behav.5, 1365–1369. doi: 10.4161/psb.5.11.13165
25. Herridge, D. F., Peoples, M. B., and Boddy, R. M. (2008). Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil311, 1–18. doi: 10.1007/s11104-008-9668-3
26. Hirsch, A. M. (1992). Developmental biology of legume nodulation. New Phytol. 122, 211–237. doi: 10.1111/j.1469-8137.1992.tb04227.x
27. Hohnjec, N., Lenz, F., Fehlberg, V., Vieweg, M. F., Baler, M. C., Hause, B., et al. (2009). The signal peptide of the Medicago truncatula modular nodulin MtNOD25 operates as an address label for the specific targeting of proteins to nitrogen-fixing symbiosomes. Mol. Plant Microbe Interact.22, 63–72. doi: 10.1094/MPMI-22-1-0063
28. Hoover, T. R., Imperial, J., Ludden, P. W., and Shah, V. K. (1989). Homocitrate is a component of the iron-molybdenum cofactor of nitrogenase. Biochemistry28, 2768–2771. doi: 10.1021/bi00433a004
29. Howitt, S. M., Udvardi, M. K., Day, D. A., and Gresshoff, P. M. (1986). Ammonia transport in free-living and symbiotic Rhizobium sp. ANU289. J. Gen. Microbiol.132, 257–261. doi: 10.1099/00221287-132-2-257
30. Hwang, J. H., Ellingson, S. R., and Roberts, D. M. (2010). Ammonia permeability of the soybean nodulin 26 channel. FEBS Lett. 584, 4339–4343. doi: 10.1016/j.febslet.2010.09.033
31. Imaizumi-Anraku, H., Kawaguchi, M., Koiwa, H., Akao, S., and Syono, K. (1997). Two ineffective-nodulating mutants of Lotus japonicus—different phenotypes caused by the blockage of endocytotic bacterial release and nodule maturation. Plant Cell Physiol. 38, 871–881. doi: 10.1093/oxfordjournals.pcp.a029246
32. Ivanov, S., Fedorova, E. E., Limpens, E., De Mita, S., Genre, A., Bonfante, P., et al. (2012). Rhizobium–legume symbiosis shares an exocytotic pathway required for arbuscule formation. Proc. Natl. Acad. Sci. U.S.A. 109, 8316–8321. doi: 10.1073/pnas.1200407109
33. Jeong, J., Suh, S., Guan, C., Tsay, Y. F., Moran, N., Oh, C. J., et al. (2004). A nodule-specific dicarboxylate transporter from alder is a member of the peptide transporter family. Plant Physiol. 134, 969–978. doi: 10.1104/pp.103.032102
34. Kaiser, B. N., Moreau, S., Castelli, J., Thomson, R., Lambert, A., Bogliolo, S., et al. (2003). The soybean NRAMP homologue, GmDMT1, is a symbiotic divalent metal transporter capable of ferrous iron transport. Plant J. 35, 295–304. doi: 10.1046/j.1365-313X.2003.01802.x
35. Kim, S. A., Punshon, T., Lanzirotti, A., Li, L., Alonso, J. M., Ecker, J. R., et al. (2006). Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science314, 1295–1298. doi: 10.1126/science.1132563
36. Krouk, G., Lacombe, B., Bielach, A., Perrine-Walker, F., Malinska, K., Mounier, E., et al. (2010). Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell18, 927–937. doi: 10.1016/j.devcel.2010.05.008
37. Krusell, L., Krause, K., Ott, T., Desbrosses, G., Krämer, U., Sato, S., et al. (2005). The sulfate transporter SST1 is crucial for symbiotic nitrogen fixation in Lotusjaponicus root nodules. Plant Cell17, 1625–1636. doi: 10.1105/tpc.104.030106
38. Krylova, V., Andreev, I. M., Zartdinova, R., and Izmailov, S. F. (2012). Biochemical characteristics of the Ca2+ pumping ATPase in the peribacteroid membrane from broad bean root nodules. Protoplasma250, 531–538. doi: 10.1007/s00709-012-0436-0
39. Lanquar, V., Lelievre, F., Bolte, S., Hames, C., Alcon, C., Neumann, D., et al. (2005). Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J. 24, 4041–4051. doi: 10.1038/sj.emboj.7600864
40. Léran, S., Varala, K., Boyer, J. C., Chiurazzi, M., Crawford, N., Daniel-Vedele, F., et al. (2014). A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants. Trends Plant Sci. 19, 5–9. doi: 10.1016/j.tplants.2013.08.008
41. LeVier, K., Day, D. A., and Guerinot, M. L. (1996). Iron uptake by symbiosomes from soybean root nodules. Plant Physiol. 111, 893–900.
42. Libault, M., Farmer, A., Brechenmacher, L., Drnevich, J., Langley, R. J., Bilgin, D. D., et al. (2010). Complete transcriptome of the soybean root hair cell, a single-cell model, and its alteration in response to Bradyrhizobium japonicum infection. Plant Physiol. 152, 541–552. doi: 10.1104/pp.109.148379
43. Libault, M., and Stacey, G. (2010). Evolution of FW2.2-like (FWL) and PLAC8 genes in eukaryotes. Plant Signal. Behav.5, 1226–1228. doi: 10.4161/psb.5.10.12808
44. Limpens, E., Lvanov, S., Van Esse, W., Voets, G., Fedorova, E., and Bisseling, T. (2009). Medicago N2-Fixing symbiosomes acquire the endocytic identity marker Rab7 but delay the acquisition of vacuolar identity. Plant Cell21, 2811–2828. doi: 10.1105/tpc.108.064410
45. Liu, J., Miller, S. S., Graham, M., Bucciarelli, B., Catalano, C. M., Sherrier, D. J., et al. (2006). Recruitment of novel calcium-binding proteins for root nodule symbiosis in Medicago truncatula. Plant Physiol. 141, 167–177. doi: 10.1104/pp.106.076711
46. Lodwig, E., and Poole, P. S. (2003). Metabolism of Rhizobium bacteroids. Crit. Rev. Plant Sci.22, 37–78. doi: 10.1080/713610850
47. Masalkar, P., Wallace, I. S., Hwang, J. H., and Roberts, D. M. (2010). Interaction of cytosolic glutamine synthetase of soybean root nodules with the C-terminal domain of the symbiosome membrane nodulin 26 aquaglyceroporin. J. Biol. Chem.285, 23880–23888. doi: 10.1074/jbc.M110.135657
48. Meckfessel, M. H., Blancaflor, E. B., Plunkett, M., Dong, Q., and Dickstein, R. (2012). Multiple domains in MtENOD8 protein including the signal peptide target it to the symbiosome. Plant Physiol. 159, 299–310. doi: 10.1104/pp.111.191403
49. Moreau, S., Day, D. A., and Puppo, A. (1998). Ferrous iron is transported across the peribacteroid membrane of soybean nodules. Planta207, 83–87. doi: 10.1007/s004250050458
50. Moreau, S., Meyer, J. M., and Puppo, A.(1995). Uptakeof iron by symbiosomes and bacteroids from soybean nodules. FEBS Lett.361, 225–228. doi: 10.1016/0014-5793(95)00155-3
51. Moreau, S., Thompson, R. M., Kaiser, B. N., Trevaskis, B., Guerinot, M. L., Udvardi, M. K., et al. (2002). GmZIP1 encodes a symbiosome-specific zinc transporter in soybean. J. Biol. Chem.277, 4738–4746. doi: 10.1074/jbc.M106754200
52. Morere-Le Paven, M. C., Viau, L., Hamon, A., Vandecasteele, C., Pellizzaro, A., Bourdin, C., et al. (2011). Characterization of a dual-affinity nitrate transporter MtNRT1.3 in the model legume Medicago truncatula. J. Exp. Biol. 62, 5595–5605. doi: 10.1093/jxb/err243
53. Niemietz, C. M., and Tyerman, S. D. (2000). Channel-mediated permeation of ammonia gas through the peribacteroid membrane of soybean nodules. FEBS Lett. 465, 110–114. doi: 10.1016/S0014-5793(99)01729-9
54. Nour-Eldin, H. H., Andersen, T. G., Burow, M., Madsen, S. R., Jorgensen, M. E., Olsen, C. E., et al. (2012). NRT/PTR transporters are essential for transloca-tion of glucosinolate defence compounds to seeds. Nature488, 531–534. doi: 10.1038/nature11285
55. Oldroyd, G. E., and Downie, J. A. (2004). Calcium, kinases and nodulation signalling in legumes. Nat. Rev. Mol. Cell Biol.5, 566–576. doi: 10.1038/nrm1424
56. Oldroyd, G. E. D., Murray, J. D., Poole, P. S., and Downie, J. A. (2011). The rules of engagement in the legume–rhizobial symbiosis. Annu. Rev. Genet.45, 119–44. doi: 10.1146/annurev-genet-110410-132549
57. Ouyang, L. J., Whelan, J., Weaver, C. D., Roberts, D. M., and Day, D. A. (1991). Protein phosphorylation stimulates the rate of malate uptake across the peribacteroid membrane of soybean nodules. FEBS Lett. 293, 188–190. doi: 10.1016/0014-5793(91)81183-9
58. Prell, J., White, J. P., Bourdes, A., Bunnewell, S., Bongaerts, R. J., and Poole, P. S. (2009). Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids. Proc. Natl. Acad. Sci. U.S.A.106, 12477–12482. doi: 10.1073/pnas.0903653106
59. Rivers, R. L., Dean, R. M., Chandy, G., Hall, J. E., Roberts, D. M., and Zeidel, M. L. (1997). Functional analysis of nodulin 26, an aquaporin in soybean root nodule symbiosomes. J. Biol. Chem. 272, 16256–16261. doi: 10.1074/jbc.272.26.16256
60. Rosendahl, L., and Jochimsen, B. U. (1995). In vitro indole-3-acetic acid uptake in symbiosomes from soybean (Glycine max L.) root nodules. Symbiosis19, 99–110.
61. Roth, E., Jeon, K., and Stacey, G. (1988). “Homology in endosymbiotic systems: the term ‘symbiosome’,” in Molecular Genetics of Plant Microbe Interactions, eds R. Palacios and D. P. S. Verma (St Paul, MN: American Phytopathological Society Press), 220–225.
62. Roth, L. E., and Stacey, G. (1989). Cytoplasmic membrane systems involved in bacterium release into soybean nodule cells as studied with two Bradyrhizobium japonicum mutant strains. Eur. J. Cell Biol.49, 24–32.
63. Saalbach, G., Erik, P., and Wienkoop, S. (2002). Characterisation by proteomics of peribacteroid space and peribacteroid membrane preparations from pea (Pisum sativum) symbiosomes. Proteomics 2, 325–337. doi: 10.1002/1615-9861(200203)2:3<325::AID-PROT325>3.0.CO;2-W
64. Schmutz, J., Cannon, S. B., Schlueter, J., Ma, J., Mitros, T., Nelson, W., et al. (2010). Genome sequence of the palaeopolyploid soybean. Nature463, 178–183. doi: 10.1038/nature08670
65. Severin, A. J., Woody, J. L., Bolon, Y. T., Joseph, B., Diers, B. W., Farmer, A. D., et al. (2010). RNA-seq atlas of glycine max: a guide to the soybean transcriptome. BMC Plant Biol. 10:160. doi: 10.1186/1471-2229-10-160
66. Song, W. Y., Choi, K. S., Kim Do, Y., Geisler, M., Park, J., Vincenzetti, V., et al. (2010). Arabidopsis PCR2 is a zinc exporter involved in both zinc extrusion and long-distance zinc transport. Plant Cell 22, 2237–2252. doi: 10.1105/tpc.109.070185
67. Song, W. Y., Hortensteiner, S., Tomioka, R., Lee, Y., and Martinoia, E. (2011). Common functions or only phylogenetically related? The large family of PLAC8 motif-containing/PCR genes. Mol. Cells31, 1–7. doi: 10.1007/s10059-011-0024-8
68. Song, W. Y., Martinoia, E., Lee, J., Kim, D., Kim, D. Y., Vogt, E., et al. (2004). A novel family of cys-rich membrane proteins mediates cadmium resistance in Arabidopsis. Plant Physiol. 135, 1027–1039. doi: 10.1104/pp.103.037739
69. Stacey, G., Koh, S., Granger, C., and Becker, J. M. (2002). Peptide transport in plants. Trends Plant Sci. 7, 257–263. doi: 10.1016/S1360-1385(02)02249-5
70. Streeter, J., and Wong, P. P. (1988). Inhibition of legume nodule formation and N2 fixation by nitrate. Crit. Re v. Plant Sci.7, 1–23. doi: 10.1080/07352688809382257
71. Timmers, A. C., Auriac, M. C., and Truchet, G. (1999). Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development126, 3617–3628.
72. Tomatsu, H., Takano, J., Takahashi, H., Watanabe-Takahashi, A., Shibagaki, N., and Fujiwara, T. (2007). An Arabidopsis thaliana high-affinity molybdate transporter required for efficient uptake of molybdate from soil. Proc. Natl. Acad. Sci. U.S.A.104, 18807–18812. doi: 10.1073/pnas.0706373104
73. Tsay, Y. F., Chiu, C. C., Tsai, C. B., Ho, C. H., and Hsu, P. K. (2007). Nitrate transporters and peptide transporters. FEBS Lett. 581, 2290–2300. doi: 10.1016/j.febslet.2007.04.047
74. Tyerman, S. D., Whitehead, L. F., and Day, D. A. (1995). A channel-like transporter for NH4+ on the symbiotic interface of N2-fixing plants. Nature378, 629–632. doi: 10.1038/378629a0
75. Udvardi, M., and Poole, P. S. (2013). Transport and metabolism in legume-rhizobia symbioses. Annu. Rev. Plant Biol.64, 781–805. doi: 10.1146/annurev-arplant-050312-120235
76. Udvardi, M. K., and Day, D. A. (1989). Electrogenic ATPase activity on the perib-acteroid membrane of soybean (Glycine max L.) root nodules. Plant Physiol. 90, 982–987. doi: 10.1104/pp.90.3.982
77. Udvardi, M. K., and Day, D. A. (1997). Metabolite transport across symbiotic membranes of legume nodules. Annu. Rev. Plant Physiol. Plant Mol. Biol.48, 493–523. doi: 10.1146/annurev.arplant.48.1.493
78. Udvardi, M. K., Lister, D. L., and Day, D. A. (1991). ATPase activity and anion transport across the peribacteroid membrane of isolated soybean symbiosomes. Arch. Microbiol.156, 362–366. doi: 10.1007/BF00248711
79. Udvardi, M. K., Price, G. D., Gresshoff, P. M., and Day, D. A. (1988). A dicarboxylate transporter on the peribacteroid membrane of soybean nodules. FEBS Lett. 231, 36–40. doi: 10.1016/0014-5793(88)80697-5
80. Vance, C. P. (2001). Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiol. 127, 390–397. doi: 10.1104/pp.010331
81. Verdier, J., Torres-Jerez, I., Wang, M., Andriankaja, A., Allen, S. N., He, J., et al. (2013). Establishment of the Lotus japonicus Gene Expression Atlas (LjGEA) and its use to explore legume seed maturation. Plant J. 74, 351–362. doi: 10.1111/tpj.12119
82. Vincill, E. D., Szczyglowski, K., and Roberts, D. M. (2005). GmN70 and LjN70. Anion transporters of the symbiosome membrane of nodules with a transport preference for nitrate. Plant Physiol. 137, 1435–1444. doi: 10.1104/pp.104.051953
83. Weaver, C. D., Crombie, B., Stacey, G., and Roberts, D. M. (1991). Calcium-dependent phosphorylation of symbiosome membrane proteins from nitrogen-fixing soybean nodules: evidence for phosphorylation of nodulin-26. Plant Physiol. 95, 222–227. doi: 10.1104/pp.95.1.222
84. Weaver, C. D., Shomer, N. H., Louis, C. F., and Roberts, D. M. (1994). Nodulin 26, a nodule-specific symbiosome membrane protein from soybean, is an ion channel. J. Biol. Chem.269, 17858–17862.
85. Whitehead, L. F., and Day, D. A. (1997). The peribacteroid membrane. Physiol. Plant.100, 30–44. doi: 10.1111/j.1399-3054.1997.tb03452.x
86. Whitehead, L. F., Young, S., and Day, D. A. (1998). Aspartate and alanine movement across symbiotic membranes of soybean nodules. Soil Biol. Biochem. 30, 1583–1589. doi: 10.1016/S0038-0717(97)00229-0
87. Wienkoop, S., and Saalbach, G.(2003). Proteome analysis. Novel proteins identified at the peribacteroid membrane from Lotus japonicus root nodules. Plant Physiol. 131, 1080–1090. doi: 10.1104/pp.102.015362
88. Williams, L. E., and Millar, A. J. (2001). Transporters responsible for the uptake and partitioning of nitrogenous solutes. Annu. Rev. Plant Physiol. Plant Mol. Biol.52, 659–688. doi: 10.1146/annurev.arplant.52.1.659
89. Wong, F. H., Chen, J. S., Reddy, V., Day, J. L., Shlykov, M. A., Wakabayashi, S. T., et al. (2012). The amino acid-polyamine-organocation superfamily. J. Mol. Microbiol. Biotechnol.22, 105–113. doi: 10.1159/000338542
90. Wudick, M. M., Luu, D. T., and Maurel, C. (2009). A look inside: localization patterns and functions of intracellular plant aquaporins. New Phytol. 184, 289–302. doi: 10.1111/j.1469-8137.2009.02985.x
91. Yendrek, C. R., Lee, Y. C., Morris, V., Liang, Y., Pislariu, C. I., Burkart, G., et al. (2010). A putative transporter is essential for integrating nutrient and hormone signaling with lateral root growth and nodule development in Medicago trun-catula. Plant J. 62, 100–112. doi: 10.1111/j.1365-313X.2010.04134.x
92. Zheng, L., White, R. H., and Dean, D. R. (1997). Purification of the Azotobacter vinelandii nifV-encoded homocitrate synthase. J. Bacteriol.179, 5963–5966.