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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Soybean vegetative lipoxygenases are not vacuolar storage proteins

Glenn W. Turner A , Howard D. Grimes B and B. Markus Lange A C
+ Author Affiliations
- Author Affiliations

A Institute of Biological Chemistry, Washington State University, Pullman, WA 99164-6340, USA.

B School of Molecular Biosciences, Washington State University, Pullman, WA 99164-7520, USA.

C Corresponding author. Email: lange-m@wsu.edu

Functional Plant Biology 38(10) 778-787 https://doi.org/10.1071/FP11047
Submitted: 15 February 2011  Accepted: 23 July 2011   Published: 16 September 2011

Abstract

The paraveinal mesophyll (PVM) of soybean is a distinctive uniseriate layer of branched cells situated between the spongy and palisade chlorenchyma of leaves that contains an abundance of putative vegetative storage proteins, Vspα and Vspβ, in its vacuoles. Soybean vegetative lipoxygenases (five isozymes designated as Vlx(A–E)) have been reported to co-localise with Vsp in PVM vacuoles; however, conflicting results regarding the tissue-level and subcellular localisations of specific Vlx isozymes have been reported. We employed immuno-cytochemistry with affinity-purified, isozyme-specific antibodies to reinvestigate the subcellular locations of soybean Vlx isozymes during a sink limitation experiment. VlxB and VlxC were localised to the cytoplasm and nucleoplasm of PVM cells, whereas VlxD was present in the cytoplasm and nucleoplasm of mesophyll chlorenchyma (MC) cells. Label was not associated with storage vacuoles or any evident protein bodies, so our results cast doubt on the hypothesis that Vlx isozymes function as vegetative storage proteins.

Additional keywords: localisation, paraveinal mesophyll, vegetative lipoxygenase.


References

Berger S, Bell E, Sadka V, Mullet JE (1995) Arabidopsis thaliana Atvsp is homologous to soybean VspA and VspB, genes encoding vegetative storage protein acid phosphatases and is regulated similarly by methyl jasmonate, wounding, sugar light and phosphate. Plant Molecular Biology 27, 933–942.
Arabidopsis thaliana Atvsp is homologous to soybean VspA and VspB, genes encoding vegetative storage protein acid phosphatases and is regulated similarly by methyl jasmonate, wounding, sugar light and phosphate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmtFSgsL8%3D&md5=3b204b68b5f4a32e1c5de7e7a5256570CAS |

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=606a1898fb14c5ab3908d2f4fe5a0f08CAS |

Brock TG, McNish RW, Bailie MB, Peters-Golden M (1997) Rapid Import of cytosolic 5-lipoxygenase into the nucleus of neutrophils after in vivo recruitment and in vitro adherence. Journal of Biological Chemistry 272, 8276–8280.
Rapid Import of cytosolic 5-lipoxygenase into the nucleus of neutrophils after in vivo recruitment and in vitro adherence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXitF2lsbg%3D&md5=36feb51f3013bd26da04cbc89bd1e4d3CAS |

Brock TG, Anderson JA, Fries FP, Peters-Golden M, Sporn PHS (1999) Decreased leukotriene C4 synthesis accompanies adherence-dependent nuclear import of 5-lipoxygenase in human blood eosinophils. Journal of Immunology 162, 1669–1676.

Brubaker CL, Lersten NR (1995) Paraveinal mesophyll: review and survey of the subtribe Erythrinae (Phaseolae, Papilionoideae, Leguminosae). Plant Systematics and Evolution 196, 31–62.
Paraveinal mesophyll: review and survey of the subtribe Erythrinae (Phaseolae, Papilionoideae, Leguminosae).Crossref | GoogleScholarGoogle Scholar |

Bunker TW, Koetje DS, Stephenson LC, Creelman RA, Mullet JE, Grimes HD (1995) Sink limitation induces the expression of multiple soybean vegetative lipoxygenase mRNAs while the endogenous jasmonic acid level remains low. The Plant Cell 7, 1319–1331.

DeWald DB, Mason HS, Mullet JE (1992) The soybean vegetative storage proteins VSPα and VSPβ are acid phosphatases active on phosphates. Journal of Biological Chemistry 267, 15958–15964.

Dubbs WE, Grimes HD (2000) The mid-pericarp cell layer in soybean pod walls is a multicellular compartment enriched in specific lipoxygenase isoforms. Plant Physiology 123, 1281–1288.
The mid-pericarp cell layer in soybean pod walls is a multicellular compartment enriched in specific lipoxygenase isoforms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtVehurw%3D&md5=6d429c464e591779956f1ea7f7edc541CAS |

Felton GW (2005) Indigestion in a plant’s best defense. Proceedings of the National Academy of Sciences of the United States of America 102, 18771–18772.
Indigestion in a plant’s best defense.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XivVyktA%3D%3D&md5=ccd4d711e4fc9c79baec7dc7f2bb6751CAS |

Felton GW, Bi JL, Summers CB, Mueller AJ, Duffy SS (1994) Potential role of lipoxygenases in defense against insect herbivory. Journal of Chemical Ecology 20, 651–666.
Potential role of lipoxygenases in defense against insect herbivory.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXis1Kjsb0%3D&md5=b7a1d1e3085e6ef901970460189ba870CAS |

Fischer AM, Dubbs WE, Baker RA, Fuller MA, Stephenson LC, Grimes HD (1999) Protein dynamics, activity and cellular localisation of soybean lipoxygenases indicate distinct functional roles for individual isoforms. The Plant Journal 19, 543–554.
Protein dynamics, activity and cellular localisation of soybean lipoxygenases indicate distinct functional roles for individual isoforms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvV2hurs%3D&md5=7638f37f4f33b9e6755cb5d4a3a23d73CAS |

Fisher DB (1967) An unusual layer of cells in the mesophyll of the soybean leaf. Botanical Gazette (Chicago, Ill.) 128, 215–218.
An unusual layer of cells in the mesophyll of the soybean leaf.Crossref | GoogleScholarGoogle Scholar |

Franceschi VR, Giaquinta RT (1983a) Specialised cellular arrangements in legume leaves in relation to assimilate transport and compartmentation. Comparison of the paraveinal mesophyll. Planta 159, 415–422.
Specialised cellular arrangements in legume leaves in relation to assimilate transport and compartmentation. Comparison of the paraveinal mesophyll.Crossref | GoogleScholarGoogle Scholar |

Franceschi VR, Giaquinta RT (1983b) The paraveinal mesophyll of soybean leaves in relation to assimilate transfer and compartmentation. Ultrastructure and histochemistry during vegetative development. Planta 157, 422–431.
The paraveinal mesophyll of soybean leaves in relation to assimilate transfer and compartmentation. Ultrastructure and histochemistry during vegetative development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXhvFGjur0%3D&md5=6f8f613a19cfe6ef0cb81909be46c2fcCAS |

Franceschi VR, Grimes HD (1991) Induction of soybean vegetative storage proteins and anthocyanins by low-level atmospheric methyl jasmonate. Proceedings of the National Academy of Sciences of the United States of America 88, 6745–6749.
Induction of soybean vegetative storage proteins and anthocyanins by low-level atmospheric methyl jasmonate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXltlaitrg%3D&md5=f4ded972588602903a849db73281852aCAS |

Franceschi VR, Wittenbach VA, Giaquinta RT (1983) Paraveinal mesophyll of soybean leaves in relation to assimilate transfer and compartmentation. Plant Physiology 72, 586–589.
Paraveinal mesophyll of soybean leaves in relation to assimilate transfer and compartmentation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXks1OmsL8%3D&md5=8416fa871c4ef157abbad6e029646aa7CAS |

Franceschi VR, Ding B, Lucas WJ (1994) Mechanism of plasmodesmata formation in characean algae in relation to evolution of intercellular commnunication in higher plants. Planta 192, 347–358.
Mechanism of plasmodesmata formation in characean algae in relation to evolution of intercellular commnunication in higher plants.Crossref | GoogleScholarGoogle Scholar |

Fuller MA, Weichert H, Fischer AM, Feussner I, Grimes HD (2001) Activity of soybean lipoxygenase isoforms against esterified fatty acids indicates functional specificity. Archives of Biochemistry and Biophysics 388, 146–154.
Activity of soybean lipoxygenase isoforms against esterified fatty acids indicates functional specificity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhvFGqu7g%3D&md5=c8b7e68197ddd27104069f790cbd4a27CAS |

Grayburn SW, Schneider GR, Hamilton-Kemp TR, Bookjans G, Ali K, Hildebrand DF (1991) Soybean leaves contain multiple lipoxygenases. Plant Physiology 95, 1214–1218.
Soybean leaves contain multiple lipoxygenases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXit1GktL8%3D&md5=5854a07d9bc6341db4bc5d614900eadaCAS |

Hanaka H, Shimizu T, Izumi T (2002) Nuclear-localisation-signal-dependent and nuclear-export-signal-dependent mechanisms determine the localisation of 5-lipoxygenase. Biochemical Journal 361, 505–514.
Nuclear-localisation-signal-dependent and nuclear-export-signal-dependent mechanisms determine the localisation of 5-lipoxygenase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhslOqsbc%3D&md5=1032afe182d484293c6e0b67c8a0d5c6CAS |

Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annual Review of Plant Biology 59, 41–66.
Plant immunity to insect herbivores.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqs7c%3D&md5=e0107a81b5aec0813d7de207495c78a7CAS |

Kato T, 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 Physiology 34, 1063–1072.

Klauer SF, Franceschi VR (1997) Mechanism of transport of vegetative storage proteins to the vacuole of the paraveinal mesophyll. Protoplasma 200, 174–185.
Mechanism of transport of vegetative storage proteins to the vacuole of the paraveinal mesophyll.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhvV2nsbo%3D&md5=dfe7032f24f71658b9d76d495b737e8cCAS |

Leelapon O, Sarath G, Staswick PE (2004) A single amino acid substitution in soybean VSPα increases its acid phosphatase activity nearly 20 fold. Planta 219, 1071–1079.
A single amino acid substitution in soybean VSPα increases its acid phosphatase activity nearly 20 fold.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotlKgtLc%3D&md5=435fb97f13160da3b15db6f90a98bd82CAS |

Murphy KA, Kuhle RA, Fischer AM, Anterola AM, Grimes HD (2005) The functional status of paraveinal mesophyll vacuoles changes in response to altered metabolic conditions in soybean leaves. Functional Plant Biology 32, 335–344.
The functional status of paraveinal mesophyll vacuoles changes in response to altered metabolic conditions in soybean leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjsFyksbY%3D&md5=3619144d62c27a2750b899242bc5ca87CAS |

Nakai K, Horton P (1999) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localisation. Trends in Biochemical Sciences 24, 34–35.
PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localisation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXks12qtLk%3D&md5=1d02b10c67f094cbbca3295746470addCAS |

Porta H, Rocha-Sosa M (2002) Plant lipoxygenases. Physiological and molecular features. Plant Physiology 130, 15–21.
Plant lipoxygenases. Physiological and molecular features.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntFOrsL0%3D&md5=4f4db0423231a3311c6264fa5b30af62CAS |

Sellhorn GE, Youn B, Webb BN, Gloss LM, Kang C, Grimes H (2011) Biochemical characterisation, kinetic analysis and molecular modeling of recombinant vegetative lipoxygenases from soybean. International Journal of Biology 3, 44–62.

Staswick PE (1988) Soybean vegetative storage protein structure and gene expression. Plant Physiology 87, 250–254.
Soybean vegetative storage protein structure and gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhvFWrtw%3D%3D&md5=499c8ec7038072c6e14e739367cb119aCAS |

Staswick PE (1989) Developmental regulation and the influence of plant sinks on vegetative storage protein gene expression in soybean leaves. Plant Physiology 89, 309–315.
Developmental regulation and the influence of plant sinks on vegetative storage protein gene expression in soybean leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhtlahurs%3D&md5=e2e68731541f82f12b0a3cd2d418285dCAS |

Staswick PE (1994) Storage proteins of vegetative plant tissues. Annual Review of Plant Physiology and Plant Molecular Biology 45, 303–322.
Storage proteins of vegetative plant tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlt12rs7c%3D&md5=8cde0254247c18afe2f2f1275f57f175CAS |

Stephenson LC, Bunker TW, Dubbs WE, Grimes HD (1998) Specific soybean lipoxygenases localise to discrete subcellular compartments and their mRNAs are differentially regulated by source-sink status. Plant Physiology 116, 923–933.
Specific soybean lipoxygenases localise to discrete subcellular compartments and their mRNAs are differentially regulated by source-sink status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitVKqu78%3D&md5=8615808304ea0b223aeb703328e9d9ddCAS |

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

Wittenbach VA (1982) Effect of pod removal on leaf senescence in soybeans. Plant Physiology 70, 1544–1548.
Effect of pod removal on leaf senescence in soybeans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXltVGmtQ%3D%3D&md5=24ca2c9988f558827e8939a19c1849e4CAS |

Wittenbach VA (1983a) Effect of pod removal on leaf photosynthesis and soluble protein composition of field-grown soybeans. Plant Physiology 73, 121–124.
Effect of pod removal on leaf photosynthesis and soluble protein composition of field-grown soybeans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlvFWqsrg%3D&md5=be2be38dd3d879157bd8bff3c0ad75f3CAS |

Wittenbach VA (1983b) Purification and characterisation of a soybean leaf storage glycoprotein. Plant Physiology 73, 125–129.
Purification and characterisation of a soybean leaf storage glycoprotein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlsFGhtLg%3D&md5=9508198c984bb78a5ff467426a3d41bfCAS |

Youn B, Sellhorn GE, Mirchel RJ, Gaffney BJ, Grimes HD, Kang C (2006) Crystal structures of vegetative soybean lipoxygenase VLX-B and VLX-D and comparisons with seed isoforms LOX-1 and LOX-3. Proteins 65, 1008–1020.
Crystal structures of vegetative soybean lipoxygenase VLX-B and VLX-D and comparisons with seed isoforms LOX-1 and LOX-3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1eisLjL&md5=b3cb149ec7ee86b6229a57cb46fd3683CAS |

Zhu-Salzman K, Luthe DS, Felton GW (2008) Arthropod-inducible proteins: broad spectrum defenses against multiple herbivores. Plant Physiology 146, 852–858.
Arthropod-inducible proteins: broad spectrum defenses against multiple herbivores.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsVKgsLk%3D&md5=5c6efa0c030a0c96dc0e3cb0229d3170CAS |