A SDD1-like subtilase is exuded by tobacco roots
Tim Wendlandt A , Martin Moche B , Dörte Becher B and Christine Stöhr A C
+ Author Affiliations
- Author Affiliations
A Institute of Botany and Landscape Ecology, Ernst-Moritz-Arndt-University, Greifswald, Soldmannstrasse 15, D-17487 Greifswald, Germany.
B Institute of Microbiology, Ernst-Moritz-Arndt-University Greifswald, F.-L.-Jahn-Str. 15, D-17487 Greifswald, Germany.
C Corresponding author. Email: stoehr@uni-greifswald.de
Functional Plant Biology 43(2) 141-150 https://doi.org/10.1071/FP15211
Submitted: 27 July 2015 Accepted: 3 November 2015 Published: 17 December 2015
Abstract
Hydroponically grown tobacco (Nicotiana tabacum L. cv. Samsun) roots exude proteases under non-stressed conditions. Ten different proteases could be distinguished by 2D-zymography of root exudate. The majority of the gelatinolytic activity was susceptible to serine protease inhibitors. One of the proteases could be assigned to an EST (SGN-P361478) by mass spectrometry of immune-purified root exudate. The sequence was completed by RACE-PCR and shows typical serine protease features of subtilase family S8A. Thermostability and SDS-insensitivity indicate a kinetically stable enzyme. Phylogenetic classification of this highly gelatinolytic subtilase showed SDD1 to be the closest relative in Arabidopsis thaliana (L. Heynh.). Even closer related protein sequences could be found in other distant plant genera indicating a high conservation of the subtilase. A 5-methyltetrahydropteroyltriglutamate-homocysteine methyltransferase-like protein and suberisation-associated anionic peroxidase-like protein were co-immune-purified and identified by mass spectrometry and may constitute potential interaction partners.
Additional keywords: exudate, protease, root.
References
Adamczyk B, Godlewski M, Smolander A, Kitunen V (2009) Degradation of proteins by enzymes exuded by Allium porrum roots – a potentially important strategy for acquiring organic nitrogen by plants. Plant Physiology and Biochemistry 47, 919–925.| Degradation of proteins by enzymes exuded by Allium porrum roots – a potentially important strategy for acquiring organic nitrogen by plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXps1WlsLs%3D&md5=9ba7f35bce80d5e2225d51c6d86364b2CAS | 19540770PubMed |
Adamczyk B, Smolander A, Kitunen V, Godlewski M (2010) Proteins as nitrogen source for plants: a short story about exudation of proteases by plant roots. Plant Signaling & Behavior 5, 817–819.
| Proteins as nitrogen source for plants: a short story about exudation of proteases by plant roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVyqurc%3D&md5=16386a109f16848e0dffccc06069425cCAS |
Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant, Cell & Environment 32, 666–681.
| Regulation and function of root exudates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmslemsLw%3D&md5=8bc000bed560f6e09a387b727dedfa05CAS |
Barkla BJ, Vera-Estrella R, Miranda-Vergara MC, Pantoja O (2014) Quantitative proteomics of heavy metal exposure in Arabidopsis thaliana reveals alterations in one-carbon metabolism enzymes upon exposure to zinc. Journal of Proteomics 111, 128–138.
| Quantitative proteomics of heavy metal exposure in Arabidopsis thaliana reveals alterations in one-carbon metabolism enzymes upon exposure to zinc.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXlsF2lsrY%3D&md5=3bb70a2b44b8db59da040e31a856b004CAS | 24642212PubMed |
Barrett AJ, Rawlings ND, Salvesen G, Fred Woessner J (2013) Introduction. ‘Handbook of proteolytic enzymes (3rd edn) (Eds ND Rawlings, G Salvesen) pp. li–liv. (Academic Press: New York)
Basu U, Francis JL, Whittal RM, Stephens JL, Wang Y, Zaiane OR, Goebel R, Muench DG, Good AG, Taylor GJ (2006) Extracellular proteomes of Arabidopsis thaliana and Brassica napus roots: analysis and comparison by MudPIT and LC-MS/MS. Plant and Soil 286, 357–376.
| Extracellular proteomes of Arabidopsis thaliana and Brassica napus roots: analysis and comparison by MudPIT and LC-MS/MS.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xps1Wisrg%3D&md5=52816a3312d0ac99a05ba0a08be34691CAS |
Cedzich A, Huttenlocher F, Kuhn BM, Pfannstiel J, Gabler L, Stintzi A, Schaller A (2009) The protease-associated domain and C-terminal extension are required for zymogen processing, sorting within the secretory pathway, and activity of tomato subtilase 3 (SlSBT3). Journal of Biological Chemistry 284, 14 068–14 078.
| The protease-associated domain and C-terminal extension are required for zymogen processing, sorting within the secretory pathway, and activity of tomato subtilase 3 (SlSBT3).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvV2jtLs%3D&md5=9879342713546960ff5088ba3a5a5091CAS |
Chen Q, Guo W, Feng L, Ye X, Xie W, Huang X, Liu J (2015) Transcriptome and proteome analysis of Eucalyptus infected with Calonectria pseudoreteaudii. Journal of Proteomics 115, 117–131.
| Transcriptome and proteome analysis of Eucalyptus infected with Calonectria pseudoreteaudii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXmt12msw%3D%3D&md5=62d579ba840b74561cbfc3a70c4da52cCAS | 25540935PubMed |
Cheng F, Blackburn K, Lin Y, Goshe MB, Williamson JD (2009) Absolute protein quantification by LC/MSE for global analysis of salicylic acid-induced plant protein secretion responses. Journal of Proteome Research 8, 82–93.
| Absolute protein quantification by LC/MSE for global analysis of salicylic acid-induced plant protein secretion responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlGrsrfL&md5=bfe288050002c23389127170e8edb838CAS | 18998720PubMed |
Chichkova NV, Shaw J, Galiullina RA, Drury GE, Tuzhikov AI, Kim SH, Kalkum M, Hong TB, Gorshkova EN, Torrance L, Vartapetian AB, Taliansky M (2010) Phytaspase, a relocalisable cell death promoting plant protease with caspase specificity. EMBO Journal 29, 1149–1161.
| Phytaspase, a relocalisable cell death promoting plant protease with caspase specificity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovVGhtA%3D%3D&md5=9c7e56d60275d615c65bd2d6432892caCAS | 20111004PubMed |
Ding Y, Wang J, Wang J, Stierhof Y-D, Robinson DG, Jiang L (2012) Unconventional protein secretion. Trends in Plant Science 17, 606–615.
| Unconventional protein secretion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVSgt7vE&md5=2e01d73be2e70c056d3ce8defb8eea62CAS | 22784825PubMed |
Eick M, Stöhr C (2009) Proteolysis at the plasma membrane of tobacco roots: biochemical evidence and possible roles. Plant Physiology and Biochemistry 47, 1003–1008.
| Proteolysis at the plasma membrane of tobacco roots: biochemical evidence and possible roles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVajsrnF&md5=89aa478ba389282e5dbfea0be89bd223CAS | 19651520PubMed |
Ejima D, Yumioka R, Tsumoto K, Arakawa T (2005) Effective elution of antibodies by arginine and arginine derivatives in affinity column chromatography. Analytical Biochemistry 345, 250–257.
| Effective elution of antibodies by arginine and arginine derivatives in affinity column chromatography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVGrs7bI&md5=4451b86ac16767f57d5d6ed229a9257aCAS | 16125126PubMed |
Falvo S, Di Carli M, Desiderio A, Benvenuto E, Moglia A, America T, Lanteri S, Acquadro A (2012) 2-D DIGE analysis of UV-C radiation-responsive proteins in globe artichoke leaves. Proteomics 12, 448–460.
| 2-D DIGE analysis of UV-C radiation-responsive proteins in globe artichoke leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtlKmtQ%3D%3D&md5=fe5484062fc78d449b0e9a5b61b850e7CAS | 22162389PubMed |
Gicquel M, Esnault M-A, Jorrín-Novo JV, Cabello-Hurtado F (2011) Application of proteomics to the assessment of the response to ionising radiation in Arabidopsis thaliana. Journal of Proteomics 74, 1364–1377.
| Application of proteomics to the assessment of the response to ionising radiation in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvFGitbs%3D&md5=9b9d02817445edbc118f34d8a6c65c21CAS | 21447410PubMed |
Godlewski M, Adamczyk B (2007) The ability of plants to secrete proteases by roots. Plant physiology and biochemistry: PPB/Société française de physiologie végétale 45, 657–664.
| The ability of plants to secrete proteases by roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVOgur3J&md5=a2e798a50d786b1bee5cf2a71ed5fd86CAS |
Hara K, Kajita R, Torii KU, Bergmann DC, Kakimoto T (2007) The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. Genes & Development 21, 1720–1725.
| The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXoslSisLg%3D&md5=913b2a61989489f98a20dc1bab6e5457CAS |
Haruta M, Sabat G, Stecker K, Minkoff BB, Sussman MR (2014) A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343, 408–411.
| A peptide hormone and its receptor protein kinase regulate plant cell expansion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtV2gu7s%3D&md5=0571de814bfe9ab734c4c319175cc803CAS | 24458638PubMed |
Hempel K, Herbst F-A, Moche M, Hecker M, Becher D (2011) Quantitative proteomic view on secreted, cell surface-associated, and cytoplasmic proteins of the methicillin-resistant human pathogen Staphylococcus aureus under iron-limited conditions. Journal of Proteome Research 10, 1657–1666.
| Quantitative proteomic view on secreted, cell surface-associated, and cytoplasmic proteins of the methicillin-resistant human pathogen Staphylococcus aureus under iron-limited conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjt1SgtL0%3D&md5=cfd1a0625826978ca401ec0e472a23a6CAS | 21323324PubMed |
Hiltner L (1904) Über neuere Erfahrungen und Probleme auf dem Gebiete der Bodenbakteriologie unter besonderer Berücksichtigung der Gründüngung und Brache. Arbeiten der Deutschen Landwirtschafts-Gesellschaft 98, 59–78.
Jiang H, Zhang S, Feng L, Korpelainen H, Li C (2015) Transcriptional profiling in dioecious plant Populus cathayana reveals potential and sex-related molecular adaptations to solar UV-B radiation. Physiologia Plantarum 153, 105–118.
| Transcriptional profiling in dioecious plant Populus cathayana reveals potential and sex-related molecular adaptations to solar UV-B radiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVOhtrrP&md5=4c69b7c3ff2aa8ea04b86879e28209e6CAS | 24813713PubMed |
Kelley LA, Sternberg MJE (2009) Protein structure prediction on the web: a case study using the Phyre server. Nature Protocols 4, 363–371.
| Protein structure prediction on the web: a case study using the Phyre server.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivF2itbs%3D&md5=1042edb9f1fca50cbe858ccbc150f5f2CAS | 19247286PubMed |
Kim Y-C, Morrison SL (2009) A rapid and economic in-house DNA purification method using glass syringe filters. PLoS One 4, e7750
| A rapid and economic in-house DNA purification method using glass syringe filters.Crossref | GoogleScholarGoogle Scholar | 19924285PubMed |
Kohli A, Narciso JO, Miro B, Raorane M (2012) Root proteases: reinforced links between nitrogen uptake and mobilization and drought tolerance. Physiologia Plantarum 145, 165–179.
| Root proteases: reinforced links between nitrogen uptake and mobilization and drought tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XntV2gur0%3D&md5=daaf5a99f8f7baba8cfe5346b62a81c7CAS | 22242864PubMed |
Kukavica BM, Veljovicć-Jovanovicć SD, Menckhoff L, Lüthje S (2012) Cell wall-bound cationic and anionic class III isoperoxidases of pea root: biochemical characterization and function in root growth. Journal of Experimental Botany 63, 4631–4645.
| Cell wall-bound cationic and anionic class III isoperoxidases of pea root: biochemical characterization and function in root growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1egtbnE&md5=16d23f4c43d2db70796949392e338bd8CAS | 22760472PubMed |
Liu J-X, Srivastava R, Che P, Howell SH (2007) Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. The Plant Journal 51, 897–909.
| Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVKmurfK&md5=aebf8ab0bdfabd7cf23f694c90328f17CAS | 17662035PubMed |
Manning M, Colón W (2004) Structural basis of protein kinetic stability: resistance to sodium dodecyl sulfate suggests a central role for rigidity and a bias toward β-sheet structure. Biochemistry 43, 11248–11254.
| Structural basis of protein kinetic stability: resistance to sodium dodecyl sulfate suggests a central role for rigidity and a bias toward β-sheet structure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmsFSgtrw%3D&md5=012388b461e29d0cf30c99aab998f35bCAS | 15366934PubMed |
Matos JL, Fiori CS, Silva-Filho MC, Moura DS (2008) A conserved dibasic site is essential for correct processing of the peptide hormone AtRALF1 in Arabidopsis thaliana. FEBS Letters 582, 3343–3347.
| A conserved dibasic site is essential for correct processing of the peptide hormone AtRALF1 in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Snur3F&md5=f4f7789d05bc3c64bf2db42dbfd9f0ddCAS | 18775699PubMed |
Matsubayashi Y, Ogawa M, Morita A, Sakagami Y (2002) An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 296, 1470–1472.
| An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFanurY%3D&md5=e144b7bd5831156a89dbdc73bfe00506CAS | 12029134PubMed |
Murayama K, Kato-Murayama M, Hosaka T, Sotokawauchi A, Yokoyama S, Arima K, Shirouzu M (2012) Crystal structure of cucumisin, a subtilisin-like endoprotease from Cucumis melo L. Journal of Molecular Biology 423, 386–396.
| Crystal structure of cucumisin, a subtilisin-like endoprotease from Cucumis melo L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtF2gurjI&md5=77aa1a9fd81cc747269d5d366b26070aCAS | 22841692PubMed |
Nour-Eldin HH, Geu-Flores F, Halkier BA (2010) USER cloning and USER fusion: the ideal cloning techniques for small and big laboratories. ‘Plant secondary metabolism engineering’. pp. 185–200. (Humana Press, c/o Springer Science & Business Media, LLC: New York)
Ottmann C, Rose R, Huttenlocher F, Cedzich A, Hauske P, Kaiser M, Huber R, Schaller A (2009) Structural basis for Ca2+-independence and activation by homodimerization of tomato subtilase 3. Proceedings of the National Academy of Sciences of the United States of America 106, 17 223–17 228.
| Structural basis for Ca2+-independence and activation by homodimerization of tomato subtilase 3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlamtrvI&md5=4e28f975e0e221b6c2faa8872b558682CAS |
Pinto FL, Lindblad P (2010) A guide for in-house design of template-switch-based 5ʹ rapid amplification of cDNA ends systems. Analytical Biochemistry 397, 227–232.
| A guide for in-house design of template-switch-based 5ʹ rapid amplification of cDNA ends systems.Crossref | GoogleScholarGoogle Scholar | 19837043PubMed |
Pinto FL, Svensson H, Lindblad P (2006) Generation of non-genomic oligonucleotide tag sequences for RNA template-specific PCR. BMC Biotechnology 6, 31
| Generation of non-genomic oligonucleotide tag sequences for RNA template-specific PCR.Crossref | GoogleScholarGoogle Scholar | 16820068PubMed |
Pribyl T, Moche M, Dreisbach A, Bijlsma JJE, Saleh M, Abdullah MR, Hecker M, van Dijl JM, Becher D, Hammerschmidt S (2014) Influence of impaired lipoprotein biogenesis on surface and exoproteome of Streptococcus pneumoniae. Journal of Proteome Research 13, 650–667.
| Influence of impaired lipoprotein biogenesis on surface and exoproteome of Streptococcus pneumoniae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitFKgug%3D%3D&md5=811931f6db47767bdc77499b97ee5adfCAS | 24387739PubMed |
Ramírez V, López A, Mauch-Mani B, Gil MJ, Vera P (2013) An extracellular subtilase switch for immune priming in Arabidopsis. PLoS Pathogens 9, e1003445
| An extracellular subtilase switch for immune priming in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 23818851PubMed |
Rautengarten C, Steinhauser D, Büssis D, Stintzi A, Schaller A, Kopka J, Altmann T (2005) Inferring hypotheses on functional relationships of genes: analysis of the Arabidopsis thaliana subtilase gene family. PLoS Computational Biology 1, e40
| Inferring hypotheses on functional relationships of genes: analysis of the Arabidopsis thaliana subtilase gene family.Crossref | GoogleScholarGoogle Scholar | 16193095PubMed |
Rose R, Schaller A, Ottmann C (2010) Structural features of plant subtilases. Plant Signaling & Behavior 5, 180–183.
| Structural features of plant subtilases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptF2mtLs%3D&md5=c7f54211116d4091087d414bea04102eCAS |
Rosenberg IM (2006) ‘Protein analysis and purification: benchtop techniques.’ (Springer Science & Business Media Birkhäuser Science: Basel, Switzerland)
Sénéchal F, Graff L, Surcouf O, Marcelo P, Rayon C, Bouton S, Mareck A, Mouille G, Stintzi A, Höfte H, Lerouge P, Schaller A, Pelloux J (2014) Arabidopsis pectin methylesterase17 is co-expressed with and processed by SBT3.5, a subtilisin-like serine protease. Annals of Botany 114, 1161–1175.
| Arabidopsis pectin methylesterase17 is co-expressed with and processed by SBT3.5, a subtilisin-like serine protease.Crossref | GoogleScholarGoogle Scholar | 24665109PubMed |
Shpak ED, McAbee JM, Pillitteri LJ, Torii KU (2005) Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309, 290–293.
| Stomatal patterning and differentiation by synergistic interactions of receptor kinases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsl2jt7k%3D&md5=8bb7340ca25083b5e719cdc99a693c17CAS | 16002616PubMed |
Srivastava R, Liu J-X, Howell SH (2008) Proteolytic processing of a precursor protein for a growth-promoting peptide by a subtilisin serine protease in Arabidopsis. The Plant Journal 56, 219–227.
| Proteolytic processing of a precursor protein for a growth-promoting peptide by a subtilisin serine protease in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlChu7rM&md5=e5bf66977f028c21b5d11cbfa5a1ebf5CAS | 18643977PubMed |
Srivastava R, Liu J-X, Guo H, Yin Y, Howell SH (2009) Regulation and processing of a plant peptide hormone, AtRALF23, in Arabidopsis. The Plant Journal 59, 930–939.
| Regulation and processing of a plant peptide hormone, AtRALF23, in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1yrsrjI&md5=322a5058867072733e5d6a91887870f5CAS | 19473327PubMed |
Tanaka H, Watanabe M, Sasabe M, Hiroe T, Tanaka T, Tsukaya H, Ikezaki M, Machida C, Machida Y (2007) Novel receptor-like kinase ALE2 controls shoot development by specifying epidermis in Arabidopsis. Development 134, 1643–1652.
| Novel receptor-like kinase ALE2 controls shoot development by specifying epidermis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmt1aitbc%3D&md5=3e491713874c5ba55ec96818cc5e69e8CAS | 17376810PubMed |
The Angiosperm Phylogeny Group (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society 161, 105–121.
| An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III.Crossref | GoogleScholarGoogle Scholar |
Valentinuzzi F, Cesco S, Tomasi N, Mimmo T (2015) Influence of different trap solutions on the determination of root exudates in Lupinus albus L. Biology and Fertility of Soils 51, 757–765.
| Influence of different trap solutions on the determination of root exudates in Lupinus albus L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXntFSlsrw%3D&md5=773ea8ae964a49a346b0aae1d927e7bcCAS |
van der Hoorn RAL (2008) Plant proteases: from phenotypes to molecular mechanisms. Annual Review of Plant Biology 59, 191–223.
| Plant proteases: from phenotypes to molecular mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqsLs%3D&md5=54edeb9761c71fcd35e3b5d30b7d144bCAS |
Volpicella M, Leoni C, Costanza A, De Leo F, Gallerani R, Ceci LR (2011) Cystatins, serpins and other families of protease inhibitors in plants. Current Protein & Peptide Science 12, 386–398.
| Cystatins, serpins and other families of protease inhibitors in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVSms7bE&md5=fa0e26956a14bbb3998dd6783b2c1fffCAS |
von Groll U, Berger D, Altmann T (2002) The subtilisin-like serine protease SDD1 mediates cell-to-cell signaling during Arabidopsis stomatal development. The Plant Cell 14, 1527–1539.
| The subtilisin-like serine protease SDD1 mediates cell-to-cell signaling during Arabidopsis stomatal development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlvV2rsbw%3D&md5=e395893c2c13c6abb482fb7410aadf8cCAS | 12119372PubMed |
Wang H-M, Yin W-C, Wang C-K, To K-Y (2009) Isolation of functional RNA from different tissues of tomato suitable for developmental profiling by microarray analysis. Botanical Studies 50, 115–125.
Wen F, VanEtten HD, Tsaprailis G, Hawes MC (2007) Extracellular proteins in pea root tip and border cell exudates. Plant Physiology 143, 773–783.
| Extracellular proteins in pea root tip and border cell exudates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhvFWnsbY%3D&md5=2b929c7d75e515f96171d99449431d12CAS | 17142479PubMed |
Xia K, Manning M, Hesham H, Lin Q, Bystroff C, Colon W (2007) Identifying the subproteome of kinetically stable proteins via diagonal 2D SDS/PAGE. Proceedings of the National Academy of Sciences of the United States of America 104, 17329–17334.
| Identifying the subproteome of kinetically stable proteins via diagonal 2D SDS/PAGE.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1ymtrjN&md5=c066cbf17ea488ef8248e83c654dc779CAS | 17956990PubMed |
Xu X, Song Y, Li Y, Chang J, Zhang H, An L (2010) The tandem affinity purification method: An efficient system for protein complex purification and protein interaction identification. Protein Expression and Purification 72, 149–156.
| The tandem affinity purification method: An efficient system for protein complex purification and protein interaction identification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtFChtL8%3D&md5=be313010d9daa0b973e82a67577bde5dCAS | 20399864PubMed |
