In vitro cell wall extensibility controls age-related changes in the growth rate of etiolated Arabidopsis hypocotyls
Dmitry Suslov A B , Alexander Ivakov C , Agnieszka K. Boron A and Kris Vissenberg A DA Biology Department, Plant Growth and Development, University of Antwerp, Groenenborgerlaan 171, 2020 Antwerpen, Belgium.
B Saint Petersburg State University, Faculty of Biology, Department of Plant Physiology and Biochemistry, Universitetskaya emb. 7/9, 199034 Saint Petersburg, Russia.
C Centre of Excellence in Plant Cell Walls, School of BioSciences, The University of Melbourne, Parkville, Vic. 3010, Australia.
D Corresponding author. Email: kris.vissenberg@uantwerp.be
Functional Plant Biology 42(11) 1068-1079 https://doi.org/10.1071/FP15190
Submitted: 24 January 2015 Accepted: 5 September 2015 Published: 12 October 2015
Abstract
Plant cell growth is controlled by cell wall extensibility, which is currently estimated indirectly by various microtensile and nano/microindentation techniques. Their outputs differ in the accuracy of growth rate and in vivo extensibility prediction. Using the creep method we critically tested several metrics (creep rate, creep rate × stress–1, in vitro cell wall extensibility (ϕ) and in vitro cell wall yield threshold (y)) for their ability to predict growth rates of etiolated Arabidopsis thaliana (L. Heynh.) hypocotyls. We developed novel approaches for ϕ and y determination and statistical analysis based on creep measurements under single loads coupled with wall stress calculation. The best indicator of growth rate was ϕ because the 3-fold developmental decrease in the growth rate of 4- vs 3-day-old hypocotyls was accompanied by a 3-fold decrease in ϕ determined at pH 5. Although the acid-induced expansin-mediated creep of cell walls resulted exclusively from increasing ϕ values, the decrease in ϕ between 3- and 4-day-old hypocotyls was not mediated by a decrease in expansin abundance. We give practical recommendations on the most efficient use of creep rate, creep rate × stress–1, ϕ and y in different experimental situations and provide scripts for their automated calculations and statistical comparisons.
Additional keywords: biomechanics, cell wall stress, creep test, expansion growth, yieldins.
References
Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics International 11, 36–41.Baskin TI (2005) Anisotropic expansion of the plant cell wall. Annual Review of Cell and Developmental Biology 21, 203–222.
| Anisotropic expansion of the plant cell wall.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlektbrO&md5=1261b41db62b57a10c75b46cfd150407CAS | 16212493PubMed |
Baskin TI, Jensen OE (2013) On the role of stress anisotropy in the growth of stems. Journal of Experimental Botany 64, 4697–4707.
| On the role of stress anisotropy in the growth of stems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslCrsbjF&md5=18aefa2fd8c9281db7e1c46b09a65c29CAS | 23913952PubMed |
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B. Methodological 57, 289–300.
Boron AK, Van Loock B, Suslov D, Markakis MN, Verbelen JP, Vissenberg K (2015) Over-expression of AtEXLA2 alters etiolated Arabidopsis hypocotyl growth. Annals of Botany 115, 67–80.
| Over-expression of AtEXLA2 alters etiolated Arabidopsis hypocotyl growth.Crossref | GoogleScholarGoogle Scholar | 25492062PubMed |
Boyer JS, Cavalieri AJ, Schulze ED (1985) Control of the rate of cell enlargement: excision, wall relaxation, and growth-induced water potentials. Planta 163, 527–543.
| Control of the rate of cell enlargement: excision, wall relaxation, and growth-induced water potentials.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2c7osVahtA%3D%3D&md5=02e8f7854aeaabf7f8de4263c9102a04CAS | 24249452PubMed |
Burgert I, Keplinger T (2013) Plant micro- and nanomechanics: experimental techniques for plant cell-wall analysis. Journal of Experimental Botany 64, 4635–4649.
| Plant micro- and nanomechanics: experimental techniques for plant cell-wall analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslCrsbjE&md5=d86d354526c8bb5005104e75aee6d65aCAS | 24064925PubMed |
Cleland R (1967) Extensibility of isolated cell walls: measurement and changes during cell elongation. Planta 74, 197–209.
| Extensibility of isolated cell walls: measurement and changes during cell elongation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2sXhtFCrsrw%3D&md5=7ece38061fe1ec17fdbd156428406e41CAS | 24549947PubMed |
Cosgrove DJ (1985) Cell wall yield properties of growing tissue: evaluation by in vivo stress relaxation. Plant Physiology 78, 347–356.
| Cell wall yield properties of growing tissue: evaluation by in vivo stress relaxation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhs1Cisw%3D%3D&md5=370d0c97a8e0589c03499637b0f16f22CAS | 16664243PubMed |
Cosgrove D (1986) Biophysical control of plant cell growth. Annual Review of Plant Physiology 37, 377–405.
| Biophysical control of plant cell growth.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MnlvValtQ%3D%3D&md5=ad9534835e24feadc9e79e5532dc237aCAS | 11539701PubMed |
Cosgrove DJ (1987) Wall relaxation in growing stems: comparison of four species and assessment of measurement techniques. Planta 171, 266–278.
| Wall relaxation in growing stems: comparison of four species and assessment of measurement techniques.Crossref | GoogleScholarGoogle Scholar | 24227336PubMed |
Cosgrove DJ (1993) Wall extensibility: its nature, measurement and relationship to plant cell growth. New Phytologist 124, 1–23.
| Wall extensibility: its nature, measurement and relationship to plant cell growth.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mnls1amug%3D%3D&md5=841bbb7d704a509144b804b8ba022b19CAS | 11537718PubMed |
Cosgrove DJ (2011) Measuring in vitro extensibility of growing plant cell walls. Methods in Molecular Biology 715, 291–303.
| Measuring in vitro extensibility of growing plant cell walls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXntlakurk%3D&md5=c97e31212dde091a623d796acaf2a85eCAS | 21222092PubMed |
De Cnodder T, Vissenberg K, Van Der Straeten D, Verbelen J-P (2005) Regulation of cell length in the Arabidopsis thaliana root by the ethylene precursor 1-aminocyclopropane-1-carboxylic acid: a matter of apoplastic reactions. New Phytologist 168, 541–550.
| Regulation of cell length in the Arabidopsis thaliana root by the ethylene precursor 1-aminocyclopropane-1-carboxylic acid: a matter of apoplastic reactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlWgs7%2FM&md5=79abca2ed8c5c0abe5c60b88e1418a46CAS | 16313637PubMed |
Derbyshire P, McCann MC, Roberts K (2007) Restricted cell elongation in Arabidopsis hypocotyls is associated with a reduced average pectin esterification level. BMC Plant Biology 7, 31
| Restricted cell elongation in Arabidopsis hypocotyls is associated with a reduced average pectin esterification level.Crossref | GoogleScholarGoogle Scholar | 17572910PubMed |
Estelle MA, Somerville C (1987) Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology. Molecular & General Genetics 206, 200–206.
| Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhsFeht7c%3D&md5=ca51491d71efad333f92b8b793bfbb3dCAS |
Ezaki N, Kido N, Takahashi K, Katou K (2005) The role of wall Ca2+ in the regulation of wall extensibility during the acid-induced extension of soybean hypocotyl cell walls. Plant & Cell Physiology 46, 1831–1838.
| The role of wall Ca2+ in the regulation of wall extensibility during the acid-induced extension of soybean hypocotyl cell walls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Ons7bF&md5=d869dc5c8dbb6e2e17c9ead9352bbd11CAS |
Felle HH (2001) pH: signal and messenger in plant cells. Plant Biology 3, 577–591.
| pH: signal and messenger in plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsVyktA%3D%3D&md5=e956bdbcc41cd25cdae77f9cd683fd70CAS |
Frensch J, Hsiao TC (1995) Rapid response of the yield threshold and turgor regulation during adjustment of root growth to water stress in Zea mays. Plant Physiology 108, 303–312.
Gendreau E, Traas J, Desnos T, Grandjean O, Caboche M, Höfte H (1997) Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiology 114, 295–305.
| Cellular basis of hypocotyl growth in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtleitbc%3D&md5=56baa3637b76e18e00d43c9716376668CAS | 9159952PubMed |
Gibson LJ (2012) The hierarchical structure and mechanics of plant materials. Journal of the Royal Society, Interface 9, 2749–2766.
| The hierarchical structure and mechanics of plant materials.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslWrsr7K&md5=6d9f0d8943e81d8d4f12ee6ea8f0c892CAS | 22874093PubMed |
Gjetting KS, Ytting CK, Schulz A, Fuglsang AT (2012) Live imaging of intra- and extracellular pH in plants using pHusion, a novel genetically encoded biosensor. Journal of Experimental Botany 63, 3207–3218.
| Live imaging of intra- and extracellular pH in plants using pHusion, a novel genetically encoded biosensor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnt1elsrc%3D&md5=b836544e5876285a37c0478fa0c601caCAS | 22407646PubMed |
Goh HH, Sloan J, Malinowski R, Fleming A (2014) Variable expansin expression in Arabidopsis leads to different growth responses. Journal of Plant Physiology 171, 329–339.
| Variable expansin expression in Arabidopsis leads to different growth responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs12ktrbE&md5=5fc81f86b0e0a5d0dd270a7dcaaa9befCAS | 24144490PubMed |
Hansen SL, Ray PM, Karlsson AO, Jorgensen B, Borkhardt B, Petersen BL, Ulvskov P (2011) Mechanical properties of plant cell walls probed by relaxation spectra. Plant Physiology 155, 246–258.
| Mechanical properties of plant cell walls probed by relaxation spectra.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFagtrw%3D&md5=34d4fac9f6b568bf4df2aeb7c4b0adaaCAS | 21075961PubMed |
Hunt R (1990) ‘Basic growth analysis: plant growth analysis for beginners.’ (Unwin Hyman: London)
Jamet E, Roujol D, San-Clemente H, Irshad M, Soubigou-Taconnat L, Renou JP, Pont-Lezica R (2009) Cell wall biogenesis of Arabidopsis thaliana elongating cells: transcriptomics complements proteomics. BMC Genomics 10, 505
| Cell wall biogenesis of Arabidopsis thaliana elongating cells: transcriptomics complements proteomics.Crossref | GoogleScholarGoogle Scholar | 19878582PubMed |
Jarvis MC (1984) Structure and properties of pectin gels in plant cell walls. Plant, Cell & Environment 7, 153–164.
Lockhart JA (1965) An analysis of irreversible plant cell elongation. Journal of Theoretical Biology 8, 264–275.
| An analysis of irreversible plant cell elongation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF2s7jvFyhsg%3D%3D&md5=050a585d21854b1868a1d4021817c8f3CAS | 5876240PubMed |
Maris A, Suslov D, Fry SC, Verbelen JP, Vissenberg K (2009) Enzymic characterization of two recombinant xyloglucan endotransglucosylase/hydrolase (XTH) proteins of Arabidopsis and their effect on root growth and cell wall extension. Journal of Experimental Botany 60, 3959–3972.
| Enzymic characterization of two recombinant xyloglucan endotransglucosylase/hydrolase (XTH) proteins of Arabidopsis and their effect on root growth and cell wall extension.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtV2ks7zO&md5=d09685352bc3013b14108fecb3d5b061CAS | 19635745PubMed |
Maris A, Kaewthai N, Eklöf JM, Miller JG, Brumer H, Fry SC, Verbelen J-P, Vissenberg K (2011) Differences in enzymic properties of five recombinant xyloglucan endotransglucosylase/hydrolase (XTH) proteins of Arabidopsis thaliana. Journal of Experimental Botany 62, 261–271.
| Differences in enzymic properties of five recombinant xyloglucan endotransglucosylase/hydrolase (XTH) proteins of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFamurfI&md5=997f82eb051b1a57683b9838d58ceeaaCAS | 20732879PubMed |
McQueen-Mason S, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall extension in plants. The Plant Cell 4, 1425–1433.
| Two endogenous proteins that induce cell wall extension in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXls1ekug%3D%3D&md5=0a1261e9a867b84cd007f0d6f17fa86bCAS | 11538167PubMed |
Miedes E, Zarra I, Hoson T, Herbers K, Sonnewald U, Lorences EP (2011) Xyloglucan endotransglucosylase and cell wall extensibility. Journal of Plant Physiology 168, 196–203.
| Xyloglucan endotransglucosylase and cell wall extensibility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1ajtbjL&md5=299f81a2728a31b86e28101988378da2CAS | 20828871PubMed |
Miedes E, Suslov D, Vandenbussche F, Kenobi K, Ivakov A, Van Der Straeten D, Lorences EP, Mellerowicz EJ, Verbelen J-P, Vissenberg K (2013) Xyloglucan endotransglucosylase/hydrolase (XTH) overexpression affects growth and cell wall mechanics in etiolated Arabidopsis hypocotyls. Journal of Experimental Botany 64, 2481–2497.
| Xyloglucan endotransglucosylase/hydrolase (XTH) overexpression affects growth and cell wall mechanics in etiolated Arabidopsis hypocotyls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnvV2ntb8%3D&md5=e05c3bd93cc306040ab18d04ed9f19e4CAS | 23585673PubMed |
Milani P, Braybrook SA, Boudaoud A (2013) Shrinking the hammer: micromechanical approaches to morphogenesis. Journal of Experimental Botany 64, 4651–4662.
| Shrinking the hammer: micromechanical approaches to morphogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslCrsbnL&md5=d6b52d08a0be455313a125cf2cd8e64bCAS | 23873995PubMed |
Okamoto H, Okamoto A (1994) The pH-dependent yield threshold of the cell wall in a glycerinated hollow cylinder (in vitro system) of cowpea hypocotyl. Plant, Cell & Environment 17, 979–983.
| The pH-dependent yield threshold of the cell wall in a glycerinated hollow cylinder (in vitro system) of cowpea hypocotyl.Crossref | GoogleScholarGoogle Scholar |
Okamoto-Nakazato A (2002) A brief note on the study of yieldin, a wall-bound protein that regulates the yield threshold of the cell wall. Journal of Plant Research 115, 309–313.
| A brief note on the study of yieldin, a wall-bound protein that regulates the yield threshold of the cell wall.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xoslyhtr8%3D&md5=84664f784ba47f14005c1a6066e2c0d0CAS | 12582736PubMed |
Okamoto-Nakazato A, Nakamura T, Okamoto A (2000) The isolation of wall-bound proteins regulating yield threshold in glycerinated hollow cylinders of cowpea hypocotyls. Plant, Cell & Environment 23, 145–154.
| The isolation of wall-bound proteins regulating yield threshold in glycerinated hollow cylinders of cowpea hypocotyls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisFWmsL8%3D&md5=f74da0d5ca2c132f48ed6a36145f27bfCAS |
Park YB, Cosgrove DJ (2012) Changes in cell wall biomechanical properties in the xyloglucan-deficient xxt1/xxt2 mutant of Arabidopsis. Plant Physiology 158, 465–475.
| Changes in cell wall biomechanical properties in the xyloglucan-deficient xxt1/xxt2 mutant of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltFSnt70%3D&md5=8b8ea12c21981b484381004120346105CAS | 22108526PubMed |
Peaucelle A, Braybrook SA, Le Guillou L, Bron E, Kuhlemeier C, Höfte H (2011) Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. Current Biology 21, 1720–1726.
| Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtl2hsLjF&md5=29fb50c35378fa588a2d3ddaec507232CAS | 21982593PubMed |
Radotić K, Roduit C, Simonović J, Hornitschek P, Fankhauser C, Mutavdžić D, Steinbach G, Dietler G, Kasas S (2012) Atomic force microscopy stiffness tomography on living Arabidopsis thaliana cells reveals the mechanical properties of surface and deep cell-wall layers during growth. Biophysical Journal 103, 386–394.
| Atomic force microscopy stiffness tomography on living Arabidopsis thaliana cells reveals the mechanical properties of surface and deep cell-wall layers during growth.Crossref | GoogleScholarGoogle Scholar | 22947854PubMed |
Refrégier G, Pelletier S, Jaillard D, Höfte H (2004) Interaction between wall deposition and cell elongation in dark-grown hypocotyl cells in Arabidopsis. Plant Physiology 135, 959–968.
| Interaction between wall deposition and cell elongation in dark-grown hypocotyl cells in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 15181211PubMed |
Richmond PA, Métraux JP, Taiz L (1980) Cell expansion patterns and directionality of wall mechanical properties in Nitella. Plant Physiology 65, 211–217.
| Cell expansion patterns and directionality of wall mechanical properties in Nitella.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhsVemsbw%3D&md5=1582a540325e037a214cb22b915ac200CAS | 16661162PubMed |
Ripley BD, Thompson M (1987) Regression techniques for the detection of analytical bias. Analyst 112, 377–383.
| Regression techniques for the detection of analytical bias.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhs1Ortbs%3D&md5=aa6d991995c5f15969d37b741730da86CAS |
Routier-Kierzkowska AL, Smith RS (2013) Measuring the mechanics of morphogenesis. Current Opinion in Plant Biology 16, 25–32.
| Measuring the mechanics of morphogenesis.Crossref | GoogleScholarGoogle Scholar | 23218971PubMed |
Routier-Kierzkowska AL, Weber A, Kochova P, Felekis D, Nelson BJ, Kuhlemeier C, Smith RS (2012) Cellular force microscopy for in vivo measurements of plant tissue mechanics. Plant Physiology 158, 1514–1522.
| Cellular force microscopy for in vivo measurements of plant tissue mechanics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xns1eiu70%3D&md5=aac27996c51c4576ab5ec2ee421cf213CAS | 22353572PubMed |
Ryden P, Sugimoto-Shirasu K, Smith AC, Findlay K, Reiter W-D, McCann MC (2003) Tensile properties of Arabidopsis cell walls depend on both a xyloglucan cross-linked microfibrillar network and rhamnogalacturonan II-borate complexes. Plant Physiology 132, 1033–1040.
| Tensile properties of Arabidopsis cell walls depend on both a xyloglucan cross-linked microfibrillar network and rhamnogalacturonan II-borate complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkslertbk%3D&md5=0332d5ca41117d3658fcb8427ccaeeeaCAS | 12805631PubMed |
Scheres B, Wolkenfelt H, Willemsen V, Terlouw M, Lawson E, Dean C, Weisbeek P (1994) Embryonic origin of the Arabidopsis primary root and root meristem initials. Development 120, 2475–2487.
Suslov D, Verbelen J-P (2006) Cellulose orientation determines mechanical anisotropy in onion epidermis cell walls. Journal of Experimental Botany 57, 2183–2192.
| Cellulose orientation determines mechanical anisotropy in onion epidermis cell walls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnvF2murg%3D&md5=ee1ac5acc114997a4e11d7995f31e66bCAS | 16720609PubMed |
Suslov D, Verbelen J-P, Vissenberg K (2009) Onion epidermis as a new model to study the control of growth anisotropy in higher plants. Journal of Experimental Botany 60, 4175–4187.
| Onion epidermis as a new model to study the control of growth anisotropy in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1WqtLjL&md5=dd9267e36a78b6f4e81899ce91ec36a9CAS | 19684107PubMed |
Suslov D, Verbelen J-P, Vissenberg K (2010) Is acid-induced extension in seed plants only protein-mediated? Plant Signaling & Behavior 5, 757–759.
| Is acid-induced extension in seed plants only protein-mediated?Crossref | GoogleScholarGoogle Scholar |
Taguchi T, Uraguchi A, Katsumi M (1999) Auxin- and acid-induced changes in the mechanical properties of the cell wall. Plant & Cell Physiology 40, 743–749.
| Auxin- and acid-induced changes in the mechanical properties of the cell wall.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkvVejs74%3D&md5=72716f56e67a206e6f3e05682103f96aCAS |
Takahashi K, Hirata S, Kido N, Katou K (2006) Wall-yielding properties of cell walls from elongating cucumber hypocotyls in relation to the action of expansin. Plant & Cell Physiology 47, 1520–1529.
| Wall-yielding properties of cell walls from elongating cucumber hypocotyls in relation to the action of expansin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlWqsr%2FL&md5=0cc43e12fc9f7841f8696803536d6463CAS |
Thompson DS (2001) Extensiometric determination of the rheological properties of the epidermis of growing tomato fruit. Journal of Experimental Botany 52, 1291–1301.
| Extensiometric determination of the rheological properties of the epidermis of growing tomato fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsVCms7Y%3D&md5=d21deab0a23940efff7661c980b1d119CAS | 11432948PubMed |
Thompson DS (2008) Space and time in the plant cell wall: relationships between cell type, cell wall rheology and cell function. Annals of Botany 101, 203–211.
| Space and time in the plant cell wall: relationships between cell type, cell wall rheology and cell function.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c%2Fgs1Kksg%3D%3D&md5=4ac7fcb1a107975f4fd6f6319e505847CAS | 17660182PubMed |
Van Sandt V, Suslov D, Verbelen J-P, Vissenberg K (2007) Xyloglucan endotransglucosylase activity loosens a plant cell wall. Annals of Botany 100, 1467–1473.
| Xyloglucan endotransglucosylase activity loosens a plant cell wall.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFKis7k%3D&md5=d87a6f96200516011ad254b474bc81d8CAS | 17916584PubMed |
Vandenbussche F, Suslov D, De Grauwe L, Leroux O, Vissenberg K, Van Der Straeten D (2011) The role of brassinosteroids in shoot gravitropism. Plant Physiology 156, 1331–1336.
| The role of brassinosteroids in shoot gravitropism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptFWks7w%3D&md5=c48aacb75209e741e62c49a3b5ba6aafCAS | 21571670PubMed |