Role of vacuolar membrane proton pumps in the acidification of protein storage vacuoles following germination

Plant Physiology and Biochemistry

Volumn 104, Issue , 2016, Pages 242-249

  Wilson, Karl A ^a   Chavda, Burzin J ^a,b   Pierre Louis, Gandhy ^a   Quinn, Adam ^a   Tan Wilson, Anna ^a  

^a BINGHAMTON UNIVERSITY   (United States)

^b Geisinger Health Geisinger Commonwealth School of Medicine   (United States)

Author keywords

Acidification; Protein storage vacuole; Proteolysis; Seedling growth; Soybean; Storage proteins

Indexed keywords

ACID; BETA-CONGLYCININ PROTEIN, GLYCINE MAX; ENZYME INHIBITOR; GLOBULIN; PHOSPHATE; PLANT ANTIGEN; PLANT PROTEIN; PROTON PUMP; PROTON PUMP INHIBITOR; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; SEED STORAGE PROTEIN; SOYBEAN PROTEIN;

CELL VACUOLE; COTYLEDON; DRUG EFFECTS; GERMINATION; INTRACELLULAR MEMBRANE; METABOLISM; PROTEIN DEGRADATION; SEEDLING; SOYBEAN;

ACIDS; ANTIGENS, PLANT; COTYLEDON; ENZYME INHIBITORS; GERMINATION; GLOBULINS; INTRACELLULAR MEMBRANES; PHOSPHATES; PLANT PROTEINS; PROTEOLYSIS; PROTON PUMP INHIBITORS; PROTON PUMPS; PROTON-TRANSLOCATING ATPASES; SEED STORAGE PROTEINS; SEEDLINGS; SOYBEAN PROTEINS; SOYBEANS; VACUOLES;

EID: 84962250981     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2016.03.031     Document Type: Article

References (40)

1. Ayele B.T., Ozga J.A., Kurepin L.V., Reinecke D.M. Developmental and embryo axis regulation of gibberellin biosynthesis during germination and young seedling growth of pea. Plant Physiol. 2006, 142:1267-1281. 10.1104/pp.106.086199.
2. Bolte S., Lanquar V., Soler M.-N., Beebo A., Satiat-Jeunemaître B., Bouhidel K., Thomine S. Distinct lytic vacuolar compartments are embedded inside the protein storage vacuole of dry and germinating Arabidopsis thaliana seeds. Plant Cell Physiology 2011, 52:1142-1152. 10.1093/pcp/pcro65.
3. Bowman E.J., Siebers A., Altendorf K. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:7972-7976.
4. Davies H.V., Slack P.T. The control of food mobilization in seeds of dicotylenous plants. New Phytol. 1981, 88:41-51. 10.1111/j.1469-8137.1981.tb04566.x.
5. Dell'orto M., Nisi P.D., Vigani G., Zocchi G. Fe deficiency differentially affects the vacuolar proton pumps in cucumber and soybean roots. Front. Plant Sci. 2013, 4:1-15. 10.3389/fpls.2013.00326.
6. Diaz P., Wilson K.A., Tan-Wilson A.L. Immunocytochemical analysis of proteolysis in germinating soybean. Phytochemistry 1993, 33:961-968. 10.1016/0031-9422(93)85005-C.
7. Drose S., Altendorf K. Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases. J. Exp. Biol. 1997, 200:1-8.
8. +-PPase is central for proper resumption of early plant development. Plant Signal. Behav. 2012, 7:38-42. 10.4161/psb.7.1.18573.
9. Gonzalez D.O., Vodkin L.O. Specific elements of the glyoxylate pathway play a significant role in the functional transition of the soybean cotyledon during seedling development. BMC Genomics 2007, 8:468. 10.1186/1471-2164-8-468.
10. He F., Huang F., Wilson K.A., Tan-Wilson A. Protein storage vacuole acidification as a control of storage protein mobilization in soybeans. J. Exp. Bot. 2007, 58:1059-1070. 10.1093/jxb/erl267.
11. Johannes E., Felle H. Proton gradient across the tonoplast of Riccia fluitans as a result of the joint action of two electroenzymes. Plant Physiol. 1990, 93:412-417. 10.1104/pp.93.2.412.
12. Krebs M., Beyhl D., Gorlich E., Al-Rasheid K.A., Marten I., Stierhof Y.D., Hedrich R., Schumacher K. Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:3251-3256. 10.1073/pnas.0913035107.
13. +-translocating pyrophosphatase. Nature 2012, 484:399-403. 10.1038/nature10963.
14. Liu X., Zhang Z., Barnaby N., Wilson K.A., Tan-Wilson A. Soybean subtilisin-like protease involved in initiating storage protein degradation. Seed Sci. Res. 2001, 11:55-68. 10.1079/SSR200060.
15. Maeshima M. Vacuolar H(+)-pyrophosphatase. Biochim. Biophys. Acta 2000, 1465:37-51. 10.1016/S0005-2736(00)00130-9.
16. Maeshima M., Hara-Nishimura I., Takeuchi Y., Nishimura M. Accumulation of vacuolar H(+)-pyrophosphatase and H(+)-ATPase during reformation of the central vacuole in germinating pumpkin seeds. Plant Physiol. 1994, 106:61-69. 10.2307/4276024.
17. Maruyama N., Okuda E., Nakagawa S., Utsumi S., Barba de la Rosa A.P., Katsube T., Wada Y., Oh M.H. The roles of the N-linked glycans and extension regions of soybean beta-conglycinin in folding, assembly and structural features. Eur. J. Biochem. 1998, 258:854-862. 10.1046/j.1432-1327.1998.2580854.x.
18. Maruyama Y., Maruyama N., Mikami B., Utsumi S. Structure of the core region of the soybean beta-conglycinin alpha' subunit. Acta Crystallogr. D. Biol. Crystallogr. 2004, 60:289-297. 10.1107/s0907444903027367.
19. +-ATPase in a nonvacuolar organelle is required for the sorting of soluble vacuolar protein precursors in tobacco cells. Plant Cell 1997, 9:533-546. 10.1105/tpc.9.4.533.
20. Millot C., Millot J.M., Morjani H., Desplaces A., Manfait M. Characterization of acidic vesicles in multidrug-resistant and sensitive cancer cells by acridine orange staining and confocal microspectrofluorometry. J. Histochem. Cytochem 1997, 45:1255-1264. 10.1177/002215549704500909.
21. Müntz K. Protein dynamics and proteolysis in plant vacuoles. J. Exp. Bot. 2007, 58:2391-2407. 10.1093/jxb/erm089.
22. Nakanishi Y., Maeshima M. Molecular cloning of vacuolar H(+)-pyrophosphatase and its developmental expression in growing hypocotyl of mung bean. Plant Physiol. 1998, 116:589-597. 10.1104/pp.116.2.589.
23. Nielsen N.C. The chemistry of legume storage proteins. Phil. Trans. R. Soc. Lond. B Biol. Sci. 1984, 304:287-296. 10.1098/rstb.1984.0024.
24. Perez-Castineira J.R., Hernandez A., Drake R., Serrano A. A plant proton-pumping inorganic pyrophosphatase functionally complements the vacuolar ATPase transport activity and confers bafilomycin resistance in yeast. Biochem. J. 2011, 437:269-278. 10.1042/bj20110447.
25. Ponte L.F., Silva A.L., Carvalho F.E., Maia J.M., Voigt E.L., Silveira J.A. Salt-induced delay in cotyledonary globulin mobilization is abolished by induction of proteases and leaf growth sink strength at late seedling establishment in cashew. J. Plant Physiol. 2014, 171:1362-1371. 10.1016/j.jplph.2014.06.01.
26. Qi X., Chen R., Wilson K.A., Tan-Wilson A.L. Characterization of a soybean beta-conglycinin-degrading protease cleavage site. Plant Physiol. 1994, 104:127-133. 10.1104/pp.104.1.127.
27. Qi X., Wilson K.A., Tan-Wilson A.L. Characterization of the major protease involved in the soybean beta-conglycinin storage protein mobilization. Plant Physiol. 1992, 99:725-733. 10.1104/pp.99.2.725.
28. Rocha Facanha A., de Meis L. Reversibility of H+-ATPase and H+-pyrophosphatase in tonoplast vesicles from maize coleoptiles and seeds. Plant Physiol. 1998, 116:1487-1495. 10.1104/pp.106.4.1487.
29. Seo S., Tan-Wilson A., Wilson K.A. Protease C2, a cysteine endopeptidase involved in the continuing mobilization of soybean beta-conglycinin seed proteins. Biochim. Biophys. Acta 2001, 1545:192-206. 10.1016/s0167-4838(00)00277-6.
30. Shutov A.D., Baumlein H., Blattner F.R., Muntz K. Storage and mobilization as antagonistic functional constraints on seed storage globulin evolution. J. Exp. Bot. 2003, 54:1645-1654. 10.1093/jxb/erg165.
31. Szabo C.M., Oldfield E. An investigation of bisphosphonate inhibition of a vacuolar proton-pumping pyrophosphatase. Biochem. Biophys. Res. Commun. 2001, 287:468-473. 10.1006/bbrc.2001.5617.
32. Tan-Wilson A.L., Liu X., Chen R., Qi X., Wilson K.A. An acidic amino acid-specific protease from germinating soybeans. Phytochemistry 1996, 42:313-319. 10.1016/0031-9422(95)00896-9.
33. Tan-Wilson A.L., Wilson K.A. Mobilization of seed protein reserves. Physiol. Plant 2012, 145:140-153. 10.1111/j.1399-3054.2011.01535.x.
34. Taneyama M., Okamoto T., Yamane H., Minamikawa T. Involvement of gibberellins in expression of a cysteine proteinase (SH-EP) in cotyledons of Vigna mungo seedlings. Plant Cell Physiol. 2001, 42:1290-1293. 10.1093/pcp/pce153.
35. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U. S. A. 1979, 76:4350-4354.
36. Verma G., Mishra S., Sangwan N., Sharma S. Reactive oxygen species mediate axis-cotyledon signaling to induce reserve mobilization during germination and seedling establishment in Vigna radiata. J. Plant Physiol. 2015, 184:79-88. 10.1016/j.jplph.2015.07.01.
37. Wilson K.A., Papastoitsis G., Hartl P., Tan-Wilson A.L. Survey of the proteolytic activities degrading the Kunitz trypsin inhibitor and glycinin in germinating soybeans (Glycine max). Plant Physiol. 1988, 88:355-360. 10.1104/pp.88.2.355.
38. Wilson K.A., Rightmire B.R., Chen J.C., Tan-Wilson A.L. Differential proteolysis of glycinin and beta-conglycinin pduring soybean germination and seedling growth. Plant Physiol. 1986, 82:71-76. 10.1104/pp.82.1.71.
39. Wilson K.A., Tan-Wilson A. Proteolysis of the peanut allergen Ara h 1 by an endogenous aspartic protease. Plant Physiol. Biochem. 2015, 96:301-310. 10.1016/j.plaphy.2015.08.008.
40. Yaklich R.W. Beta-conglycinin and glycinin in high-protein soybean seeds. J. Agric. Food Chem. 2001, 49:729-735. 10.1021/jf001110S.