Abstract
BURP domain proteins comprise a broadly distributed, plant-specific family of functionally poorly understood proteins. VfUSP (Vicia faba Unknown Seed Protein) is the founding member of this family. The BURP proteins are characterized by a highly conserved C-terminal protein domain with a characteristic cysteine-histidine pattern. The Arabidopsis genome contains five BURP-domain encoding genes. Three of them are similar to the non-catalytic β-subunit of the polygalacturonase of tomato and form a distinct subgroup. The remaining two genes are AtRD22 and AtUSPL1. The deduced product of AtUSPL1 is similar in size and sequence to VfUSP and that of the Brassica napus BNM2 gene which is expressed during microspore-derived embryogenesis. The protein products of BURP genes have not been found, especially that of VfUSP despite a great deal of interest arising from copious transcription of the gene in seeds. Here, we demonstrate that VfUSP and AtUSPL1 occur in cellular compartments essential for seed protein synthesis and storage, like the Golgi cisternae, dense vesicles, prevaculoar vesicles and the protein storage vacuoles in the parenchyma cells of cotyledons. Ectopic expression of AtUSPL1 leads to a shrunken seed phenotype; these seeds show structural alterations in their protein storage vacuoles and lipid vesicles. Furthermore, there is a reduction in the storage protein content and a perturbation in the seed fatty acid composition. However, loss of AtUSP1 gene function due to T-DNA insertions does not lead to a phenotypic change under laboratory conditions even though the seeds have less storage proteins. Thus, USP is pertinent to seed development but its role is likely shared by other proteins that function well enough under the laboratory growth conditions.
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References
Banzai T, Sumiya K, Hanagata N, Dubinsky Z, Karube I (2002) Molecular cloning and characterization of genes encoding BURP domain-containing protein in the mangrove, Brugniera gymnorrhiza. Trees Structure and Function 16:87–93
Bassüner R, Huth A, Jung R, Wobus U, Rapoport TA, Saalbach G, Müntz K (1988) Abundant embryonic mRNA in field bean (Vicia faba L.) codes for a new class of seed proteins: cDNA cloning and characterization of the primary translation product. Plant Mol Biol 11:321–334
Bäumlein H, Boerjan W, Nagy I, Bassuner R, Van Montagu M, Inzé D, Wobus U (1991) A novel seed protein gene from Vicia faba is developmentally regulated in transgenic tobacco and Arabidopsis plants. Mol Gen Genet 225:459–467
Bäumlein H, Misera S, Luerssen H, Kolle K, Horstmann C, Wobus U, Muller AJ (1994) The FUS3 gene of Arabidopsis thaliana is a regulator of gene expression during late embryogenesis. Plant J 6:379–387
Bechthold N, Elli J, Pelletier G (1993) In planta Agrobacterium-mediated transfer by infiltration of adult Arabidopsis thaliana plants. CR Acad Sci Paris 316:871–883
Boutilier KA, Gines MJ, DeMoor JM, Huang B, Baszczynski CL, Iyer VN, Miki BL (1994) Expression of the BnmNAP subfamily of napin genes coincides with the induction of Brassica microspore embryogenesis. Plant Mol Biol 26:1711–1723
Chen L, Miyazaki C, Kojima A, Sato A, Adachi T (1999) Isolation and characterization of a gene expressed during early embryo sac development in apomictic guinea grass (Panicum maximum). J Plant Physiol 154:55–62
Chesnokov YV, Meister A, Manteuffel R (2002) A chimeric green fluorescent protein gene as an embryogenic marker in transgenic cell culture of Nicotiana plumbaginifolia Viv. Plant Sci 162:59–77
Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci U S A 81:1991–1995
Czihal A, Conrad B, Buchner P, Brevis R, Farouk AA, Manteuffel R, Adler K, Wobus U, Hofemeister J, Bäumlein H (1999) Gene farming in plants: expression of a heatstable Bacillus amylase in transgenic legume seeds. J Plant Physiol 155:183–189
Datta N, LaFayette PR, Kroner PA, Nagao RT, Key JL (1993) Isolation and characterization of three families of auxin down-regulated cDNA clones. Plant Mol Biol 21:859–869
Fiedler U, Filistein R, Wobus U, Bäumlein H (1993) A complex ensemble of cis-regulatory elements controls the expression of a Vicia faba non-storage seed protein gene. Plant Mol Biol 22:669–679
Giersberg M, Saalbach I, Bäumlein H (2004) Gene farming in pea under field conditions. In: Fischer RSS (ed) Molecular farming. Wiley-VCH, Weinheim, pp 183–190
Granger C, Coryell V, Khanna A, Keim P, Vodkin L, Shoemaker RC (2002) Identification, structure, and differential expression of members of a BURP domain containing protein family in soybean. Genome 45:693–701
Hara-Nishimura I, Shimada T, Hatano K, Takeuchi Y, Nishimura M (1998) Transport of storage proteins to protein storage vacuoles is mediated by large precursor-accumulating vesicles. Plant Cell 10:825–836
Hattori J, Boutilier KA, Van Lookeren Campagne MM, Miki BL (1998) A conserved BURP domain defines a novel group of plant proteins with unusual primary structures. Mol Gen Genet 259:424–428
Held BM, John I, Wang H, Moragoda L, Tirimanne TS, Wurtele ES, Colbert JT (1997) ZRP2: a novel maize gene whose mRNA accumulates in the root cortex and mature stems. Plant Mol Biol 35:367–375
Hillmer S, Movafeghi A, Robinson DG, Hinz G (2001) Vacuolar storage proteins are sorted in the cis-cisternae of the pea cotyledon Golgi apparatus. J Cell Biol 152:41–50
Hinz G, Hoh B, Hohl I, Robinson DG (1995) Stratification of storage proteins in the protein storage vacuole of developing cotyledons in Pisum sativum L. J Plant Physiol 145:437–442
Hinz G, Colanesi S, Hillmer S, Rogers JC, Robinson DG (2007) Localization of vacuolar transport receptors and cargo proteins in the Golgi apparatus of developing Arabidopsis embryos. Traffic 8:1452–1464
Joosen R, Cordewener J, Supena EDJ, Vorst O, Lammers M, Maliepaard C, Zeilmaker T, Miki B, America T, Custers J, Boutilier K (2007) Combined transcriptome and proteome analysis identifies pathways and markers associated with the establishment of rapeseed microspore-derived embryo development. Plant Physiol 144:155–172
Mönke G, Altschmied L, Tewes A, Reidt W, Mock HP, Bäumlein H, Conrad U (2004) Seed-specific transcription factors ABI3 and FUS3: molecular interaction with DNA. Planta 219:158–166
Nair RB, Joy RWIV, Kurylo E, Shi X, Schnaider J, Datla RSS, Keller WA, Selvaraj G (2000) Identification of a CYP84 family of cytochrome P450-dependent mono-oxygenase genes in Brassica napus and perturbation of their expression for engineering sinapine reduction in the seeds. Plant Physiol 123:1623–1634. doi:10.1104/pp.123.4.1623
Otegui MS, Herder R, Schulze J, Jung R, Staehelin LA (2006) The proteolytic processing of seed storage proteins in Arabidopsis embryo cells starts in the multivesicular bodies. Plant Cell 18:2567–2581
Phillips J, Artsaenko O, Fiedler U, Horstmann C, Mock HP, Müntz K, Conrad U (1997) Seed-specific immunomodulation of abscisic acid activity induces a developmental switch. EMBO J 16:4489–4496
Ragland M, Soliman K (1997) Sali5–4a and sali3–2: two genes induced by aluminum in soybean roots. Plant Physiol 114:395
Reidt W, Wohlfarth T, Ellerström M, Czihal A, Tewes A, Ezcurra I, Rask L, Bäumlein H (2000) Gene regulation during late embryogenesis: the RY motif of maturation-specific gene promoters is a direct target of the FUS3 gene product. Plant J 21:401–408
Robinson DG, Hoh B, Hinz G, Joeng BK (1995) One vacuole or two vacuoles: do protein storage vacuoles arise de novo during pea cotyledon development? J Plant Physiol 145:654–664
Robinson DG, Bäumer M, Hinz G, Hohl I (1998) Vesicle transfer of storage proteins to the vacuole: the role of the Golgi apparatus and multivesicular bodies. J Plant Physiol 152:659–667
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Cold Spring Harbor, NY
Scheller J, Leps M, Conrad U (2006) Forcing single-chain variable fragment production in tobacco seeds by fusion to elastin-like polypeptides. Plant Biotechnol J 4:243–249
Steffens P, Van Nong H, Milliner S, Saalbach I, Müntz K (1997) Subcellular localization of the 2S globulin narbonin in seeds of Vicia narbonensis. Planta 203:44–50
Tiedemann J, Rutten T, Mönke G, Vorwieger A, Rolletschek H, Meissner D, Milkowski C, Petereck S, Mock HP, Zank T, Bäumlein H (2008) Dissection of a complex seed phenotype: novel insights of FUSCA3 regulated developmental processes. Dev Biol 317:1–12
Treacy BK, Hattori J, Prud’homme I, Barbour E, Boutilier K, Baszczynski CL, Huang B, Johnson DA, Miki BL (1997) Bnm1, a Brassica pollen-specific gene. Plant Mol Biol 34:603–611
Tse YC, Mo BX, Hillmer S, Zhao M, Lo SW, Robinson DG, Jiang LW (2004) Identification of multivesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. Plant Cell 16:672–693
Wang WK, Kruus K, Wu JHD (1994) Cloning and expression of the Clostridium thermocellum celS gene in Escherichia coli. Appl Microbiol Biotechnol 42:346–352
Wang A, Xia Q, Xie W, Datla R, Selvaraj G (2003) The classical Ubisch bodies carry a sporophytically produced structural protein (RAFTIN) that is essential for pollen development. Proc Natl Acad Sci U S A 100:14487–14492
Wang JQ, Li YB, Lo SW, Hillmer S, Sun SSM, Robinson DG, Jiang LW (2007) Protein mobilization in germinating mung bean seeds involves vacuolar sorting receptors and multivesicular bodies. Plant Physiol 143:1628–1639
Wang JQ, Suen PK, Xu ZF, Jiang LW (2009) A 64 kDa sucrose binding protein is membrane-associated and tonoplast-localized in developing mung bean seeds. J Exp Bot 60:629–639
Watson CF, Zheng L, DellaPenna D (1994) Reduction of tomato polygalacturonase b-subunit expression affects pectin solubilization and degradation during fruit ripening. Plant Cell 6:1623–1634
Wenzel D, Schauermann G, von Lüpke A, Hinz G (2005) The cargo in vacuolar storage protein transport vesicles is stratified. Traffic 6:45–55
Wohlfarth T, Braun H, Kirik V, Kolle K, Czihal A, Tewes A, Luerssen H, Misera S, Shutov A, Baumlein H (1998) Regulation and evolution of seed globulin genes. J Plant Physiol 152:600–606
Yamaguchi-Shinozaki K, Shinozaki K (1993) The plant hormone abscisic acid mediates the drought-induced expression but not the seed-specific expression of rd22, a gene responsive to dehydration stress in Arabidopsis thaliana. Mol Gen Genet 238:17–25
Yang Z, El Aidi J, Ait-Ali T, Augur C, Teller G, Schoentgen F, Durand R, Durand B (1998) Sex-specific marker and trans-zeatin ribosidase in female annual mercury. Plant Sci 139:93–103
Yu S, Zhang L, Zuo K, Li Z, Tang K (2004) Isolation and characterization of a BURP domain-containing gene BnBDC1 from Brassica napus involved in abiotic and biotic stress. Physiol Plant 122:210–218
Zheng L, Heupel RC, DellaPenna D (1992) The b subunit of tomato fruit polygalacturonase isoenzyme 1: isolation, characterization, and identification of unique structural features. Plant Cell 4:1147–1156
Acknowledgments
We would like to thank Andreas Czihal, Elke Liemann and Monika Gottowik for excellent technical assistance. The work was supported by the Ministry of Education, Hanoi, Vietnam and the IPK Gatersleben. We would like to thank Lars Rask, Uppsala, Sweden, for kindly providing cruciferin antibodies.
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Van Son, L., Tiedemann, J., Rutten, T. et al. The BURP domain protein AtUSPL1 of Arabidopsis thaliana is destined to the protein storage vacuoles and overexpression of the cognate gene distorts seed development. Plant Mol Biol 71, 319 (2009). https://doi.org/10.1007/s11103-009-9526-6
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DOI: https://doi.org/10.1007/s11103-009-9526-6