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Mechanism of transport of vegetative storage proteins to the vacuole of the paraveinal mesophyll of soybean leaf

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Summary

Microscopy techniques were used to identify the pathway of transport of soybean leaf vegetative storage proteins (VSPα/β and VSP94) to the vacuoles of a specialized cell type, the paraveinal mesophyll (PVM), where they accumulate. PVM cells are enriched in endoplasmic reticulum and Golgi bodies relative to surrounding mesophyll cells. The margins of medial and trans Golgi cisternae had attached or closely associated noncoated vesicles with densely staining membranes and lumenal contents of the same appearance as material that accumulated in the vacuole. These vesicles appeared to be transported preferentially to the tonoplast, where fusion with the membrane released the granular contents into the vacuole. Cytochemical staining with phosphotungstic acid and silver methenamine supported this interpretation as both the Golgi vesicles and the tonoplast stained intensely with these reagents, unlike the tonoplast of mesophyll cells which do not accumulate VSP. Immunocytochemical localization for VSPα/β labeled the Golgi bodies and associated vesicles, and vacuolar material in PVM cells, but not in mesophyll. Similar labeling was seen in PVM of another legume species previously found to accumulate antigenically similar VSPs. Immunolocalization for VSP94, a lipoxygenase, labeled the PVM cytosol and material in the PVM vacuole, but not the Golgi or vesicles. The results of this study demonstrate that the Golgi pathway is utilized for transport of VSPα/β in the PVM, which follows the mechanism of deposition demonstrated for certain seed storage proteins. VSP94 appeared to follow a separate path for accumulation in PVM vacuoles.

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Abbreviations

LOX:

lipoxygenase

PVM:

paraveinal mesophyll

RER:

rough endoplasmic reticulum

TEM:

transmission electron

References

  • Bednarek SY, Raikhel NV (1992) Intracellular trafficking of secretory proteins. Plant Mol Biol 20: 133–150

    Google Scholar 

  • Brubaker CL, Lersten NR (1995) Paraveinal mesophyll: review and survey of the subtribe Erythrininae (Phaseoleae, Papilionoideae, Leguminosae). Plant Syst Evol 196: 31–62

    Google Scholar 

  • Chrispeels MJ (1984) Biosynthesis, processing and transport of storage proteins and lectins in cotyledons of developing legume seeds. Philos Trans R Soc Lond Biol Sci 304: 309–322

    Google Scholar 

  • — (1985) The role of the Golgi apparatus in the transport and post-translational modification of vacuolar (protein body) proteins. In: Miflin BJ (ed) Oxford surveys of plant molecular and cell biology, vol 2. Oxford University Press, Oxford, pp 43–68

    Google Scholar 

  • — (1991) Sorting of proteins in the secretory system. Annu Rev Plant Physiol Plant Mol Biol 42: 21–53

    Google Scholar 

  • Craig S (1988) Structural aspects of protein accumulation in developing legume seeds. Biochem Physiol Pflanzen 183: 159–171

    Google Scholar 

  • —, Goodchild DJ (1984) Periodate-acid treatment of sections permits on-grid immunogold localization of pea seed vicilin in ER and Golgi. Protoplasma 122: 35–44

    Google Scholar 

  • DeWald DB, Mason HS, Mullet JE (1992) The soybean vegetative storage proteins VSPα and VSPβ are acid phosphatases active on polyphosphates. J Biol Chem 267: 15958–15964

    Google Scholar 

  • Driouich A, Faye L, Staehelin LA (1993) The plant Golgi apparatus: a factory for complex polysaccharides and glycoproteins. Trends Biochem Sci 18: 210–214

    Google Scholar 

  • —, Levy S, Staehelin LA, Faye L (1994) Structural and functional organization of the Golgi apparatus in plant cells. Plant Physiol Biochem 32: 731–749

    Google Scholar 

  • Fisher DB (1967) An unusual layer of cells in the mesophyll of soybean leaf. Bot Gaz 138: 215–218

    Google Scholar 

  • — (1970) Kinetics of C-14 translocation in soybean: I. kinetics in the stem. Plant Physiol 45: 107–113

    Google Scholar 

  • Franceschi VR, Giaquinta RT (1983a) The paraveinal mesophyll of soybean leaves in relation to assimilate transfer and compartmentation: I. ultrastructure and histochemistry during vegetative development. Planta 157: 411–421

    Google Scholar 

  • — — (1983b) The paraveinal mesophyll of soybean leaves in relation to assimilate transfer and compartmentation. II. structural, metabolic, and compartmental changes during reproductive growth. Planta 157: 422–431

    Google Scholar 

  • — — (1983c) Specialized cellular arrangements in legume leaves in relation to assimilate transport and compartmentation: comparison of the paraveinal mesophyll. Planta 159: 415–422

    Google Scholar 

  • —, Lucas WJ (1981) The glycosome ofChara: ultrastructure, development, and composition. J Ultrastruct Res 75: 218–228

    Google Scholar 

  • —, Wittenbach VA, Giaquinta RT (1983) Paraveinal mesophyll of soybean leaves in relation to assimilate transport and compartmentation: III Immunohistochemical localization of specific glycopeptides in the vacuole after depodding. Plant Physiol 72: 586–589

    Google Scholar 

  • —, Ku MSB, Wittenbach VA (1984) Isolation of mesophyll and paraveinal mesophyll protoplasts from soybean leaves. Plant Sci Lett 36: 181–186

    Google Scholar 

  • Grayburn WS, Schneider GR, Hamilton-Kemp TR, Bookjans G, Ali K, Hildebrand DF (1991) Soybean leaves contain multiple lipoxygenases. Plant Physiol 95: 1214–1218

    Google Scholar 

  • Greenwood JS, Chrispeels MJ (1985) Immunocytochemical localization of phaseolin and phytohemagglutinin in the endoplasmic reticulum and Golgi complex of developing bean cotyledons. Planta 164: 295–302

    Google Scholar 

  • Grimes HD, Koetje DS, Franceschi VR (1992) Expression, activity and cellular accumulation of methyl jasmonate-induced lipoxygenase in soybean seedlings. Plant Physiol 100: 433–443

    Google Scholar 

  • Hawes C, Satiat-Jeunemaitre B (1996) Stacks of questions: how does the plant Golgi work? Trends Plant Sci 1: 395–401

    Google Scholar 

  • Hayat MA (1975) Positive staining for electron microscopy. Van Nostrand Reinhold, New York

    Google Scholar 

  • Hohl I, Robinson DG, Chrispeels MJ, Hinz G (1996) Transport of storage proteins to the vacuole is mediated by vesicles without a clathrin coat. J Cell Sci 109: 2539–2550

    Google Scholar 

  • Kato T, Ohta H, Tanaka K, Shibata D (1992) Appearance of new lipoxygenases in soybean cotyledons after germination and evidence for expression of a major new lipoxygenase gene. Plant Physiol 98: 324–330

    Google Scholar 

  • —, Shirano Y, Iwamoto H, Shibata D (1993) Soybean lipoxygenase L-4, a component of the 94-kilodalton storage protein in vegetative tissues: expression and accumulation in leaves induced by pod removal and by methyl jasmonate. Plant Cell Physiol 34: 1063–1072

    Google Scholar 

  • Kevekordes KG, McCully ME, Canny MJ (1988) The occurrence of an extended bundle sheath system (paraveinal mesophyll) in the legumes. Can J Bot 66: 94–100

    Google Scholar 

  • Khoo B, Wolf MJ (1970) Origin and development of protein granules in maize endosperm. Am J Bot 57: 1042–1050

    Google Scholar 

  • Kim WT, Franceschi VR, Krishnan HT, Okita TK (1988) Formation of wheat protein bodies: involvement of the Golgi apparatus in gliadin transport. Planta 176: 173–182

    Google Scholar 

  • Klauer SF, Franceschi VR, Ku MSB (1991) Protein compositions of mesophyll and paraveinal mesophyll of soybean leaves at various developmental stages. Plant Physiol 97: 1306–1316

    Google Scholar 

  • — — —, Zhang D (1996) Identification and localization of vegetative storage proteins in legume leaves. Am J Bot 83: 1–10

    Google Scholar 

  • Klionoski DJ, Cueva R, Yaver DS (1992) Aminopeptidase I ofSaccharomyces cerevisiae is localized to the vacuole independent of the secretory pathway. J Cell Biol 119: 287–299

    Google Scholar 

  • Krishnan HB, Franceschi VR, Okita TW (1986) Immunochemical studies on the role of the Golgi complex in protein body formation in rice seeds. Planta 169: 471–480

    Google Scholar 

  • Lackey JA (1978) Leaflet anatomy of Phaseoleae (Leguminosae: Papilionoideae) and its relation to taxonomy. Bot Gaz 139: 436–446

    Google Scholar 

  • Larkins BA, Hurkman WJ (1978) Synthesis and deposition of protein bodies of maize endosperm. Plant Physiol 62: 256–263

    Google Scholar 

  • Lersten NR, Brubaker CL (1989) Paraveinal mesophyll, and its relationship to vein endings, inSolidago canadensis (Asteraceae). Can J Bot 67: 1429–1433

    Google Scholar 

  • —, Curtis JD (1993) Paraveinal mesophyll inCalliandra tweedii andC. emarginata (Leguminosae; Mimosoideae). Am J Bot 80: 561–568

    Google Scholar 

  • Mason HS, Mullet JE (1990) Expression of two vegetative storage protein genes during development and in response to water deficit, wounding and jasmonic acid. Plant Cell 2: 569–579

    Google Scholar 

  • —, Guerrero FD, Boyer JS, Mullet JE (1988) Proteins homologous to leaf glycoproteins are abundant in stems of dark-grown soybean seedlings: analysis of proteins and cDNAs. Plant Mol Biol 11: 845–856

    Google Scholar 

  • Monroe JD, Salminen MD, Preiss J (1991) Nucleotide sequence of a cDNA clone encoding a β-amylase fromArabidopsis thaliana. Plant Physiol 97: 1599–1601

    Google Scholar 

  • Muntz K (1989) Intracellular protein sorting and the formation of protein reserves in storage tissue cells of plant seeds. Biochem Physiol Pflanzen 183: 313–335

    Google Scholar 

  • Nakamura K, Matsuoka K (1993) Protein targeting to the vacuole in plant cells. Plant Physiol 101: 1–5

    Google Scholar 

  • Okita TW, Rogers JC (1996) Compartmentation of proteins in the endomembrane system of plant cells. Annu Rev Plant Physiol Plant Mol Biol 47: 327–350

    Google Scholar 

  • Oparka A, Harris N (1982) Rice protein body formation: all types are initiated by dilation of the endoplasmic reticulum. Planta 154: 184–188

    Google Scholar 

  • Park TK, Polacco JC (1989) Distinct lipoxygenase species appear in the hypocotyl/radicle of germinating soybean. Plant Physiol 90: 285–290

    Google Scholar 

  • Parker ML (1982) Protein accumulation in developing endosperm of a high-protein line ofTriticum dicoccoides. Plant Cell Environ 5: 37–43

    Google Scholar 

  • Robinson DG (1996) Clathrin-mediated trafficking. Trends Plant Sci 1: 349–355

    Google Scholar 

  • —, Hoh B, Hinz G, Jeong BK (1995) One vacuole or two vacuoles: Do protein storage vacuoles arise de novo during pea cotyledon development? J Plant Physiol 145: 654–664

    Google Scholar 

  • Russin WA, Evert RF (1984) Studies on the leaf ofPopulus deltoides (Salicaceae): morphology and anatomy. Am J Bot 71: 1398–1415

    Google Scholar 

  • Saravitz DM, Siedow JN (1995) The lipoxygenase isozymes in soybean (Glycinemax (L.) Merr.) leaves: changes during leaf development, after wounding, and following reproductive sink removal. Plant Physiol 107: 535–543

    Google Scholar 

  • Siedow JN (1991) Plant lipoxygenase: structure and function. Annu Rev Plant Physiol Plant Mol Biol 42: 145–188

    Google Scholar 

  • Staehelin LA, Moore I (1995) The plant Golgi apparatus: stucture, functional organization and trafficking mechanisms. Annu Rev Plant Physiol Plant Mol Biol 46: 261–288

    Google Scholar 

  • Staswick PE (1988) Soybean vegetative protein structure and gene expression. Plant Physiol 87: 250–254

    Google Scholar 

  • — (1990) Novel regulation of vegetative storage protein genes. Plant Cell 2: 1–6

    Google Scholar 

  • — (1994) Storage proteins of vegetative plant tissues. Annu Rev Plant Physiol Plant Mol Bio 45: 303–322

    Google Scholar 

  • Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76: 4350–4354

    Google Scholar 

  • Tranbarger TJ, Franceschi VR, Hildebrand DF, Grimes HD (1991) The soybean 94-kilodalton vegetative storage protein is a lipoxygenase that is localized in paraveinal mesophyll cell vacuoles. Plant Cell 3: 973–987

    Google Scholar 

  • Wittenbach VA (1982) Effect of pod removal on leaf senescence in soybeans. Plant Physiol 70: 1544–1548

    Google Scholar 

  • — (1983a) Effect of pod removal on leaf photosynthesis and soluble protein composition of field-grown soybeans. Plant Physiol 73: 121–124

    Google Scholar 

  • — (1983b) Purification and characterization of a soybean leaf storage glycoprotein. Plant Physiol 73: 125–129

    Google Scholar 

  • Yoshihasa T, Anraku Y (1990) A novel pathway of import of α-mannosidase, a marker enzyme of vacuolar membrane, inSaccharomyces cerevisiae. J Biol Chem 265: 22418–22425

    Google Scholar 

  • Zur Nieden U, Manteuffel R, Weber E, Neumann D (1984) Dictyosomes participate in the intracellular pathway of storage proteins in developingVicia faba cotyledons. Eur J Cell Biol 34: 9–17

    Google Scholar 

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Correspondence to Vincent R. Franceschi.

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Klauer, S.F., Franceschi, V.R. Mechanism of transport of vegetative storage proteins to the vacuole of the paraveinal mesophyll of soybean leaf. Protoplasma 200, 174–185 (1997). https://doi.org/10.1007/BF01283293

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