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

A survey of the natural variation in biomechanical and cell wall properties in inflorescence stems reveals new insights into the utility of Arabidopsis as a wood model

Colleen P. MacMillan A , Philip J. O’Donnell B , Anne-Marie Smit B , Rob Evans C , Zbigniew H. Stachurski D , Kirk Torr B , Mark West B , Jacqueline Baltunis A and Timothy J. Strabala B E
+ Author Affiliations
- Author Affiliations

A CSIRO Plant Industry, Canberra, ACT 2601, Australia.

B Scion, Rotorua 3046, New Zealand.

C CSIRO Materials Science and Engineering, Melbourne, Vic. 3168, Australia.

D College of Engineering, Australian National University, Canberra, ACT 0200, Australia.

E Corresponding author. Email: tim.strabala@scionresearch.com

Functional Plant Biology 40(7) 662-676 https://doi.org/10.1071/FP12386
Submitted: 20 December 2012  Accepted: 24 February 2013   Published: 5 April 2013

Abstract

The natural trait variation in Arabidopsis thaliana (L.) Heynh. accessions is an important resource for understanding many biological processes but it is underexploited for wood-related properties. Twelve A. thaliana accessions from diverse geographical locations were examined for variation in secondary growth, biomechanical properties, cell wall glycan content, cellulose microfibril angle (MFA) and flowering time. The effect of daylength was also examined. Secondary growth in rosette and inflorescence stems was observed in all accessions. Organised cellulose microfibrils in inflorescence stems were found in plants grown under long and short days. A substantial range of phenotypic variation was found in biochemical and wood-related biophysical characteristics, particularly for tensile strength, tensile stiffness, MFA and some cell wall components. The four monosaccharides galactose, arabinose, rhamnose and fucose strongly correlated with each other as well as with tensile strength and MFA, consistent with mutations in arabinogalactan protein and fucosyl- and xyloglucan galactosyl-transferase genes that result in decreases in strength. Conversely, these variables showed negative correlations with lignin content. Our data support the notion that large-scale natural variation studies of wood-related biomechanical and biochemical properties of inflorescence stems will be useful for the identification of novel genes important for wood formation and quality, and therefore biomaterial and renewable biofuel production.

Additional keywords: microfibril angle, neutral carbohydrate content, SilviScan, stiffness, tensile strength.


References

Anastasio AE, Platt A, Horton M, Grotewold E, Scholl R, Borevitz JO, Nordborg M, Bergelson J (2011) Source verification of mis-identified Arabidopsis thaliana accessions. The Plant Journal 67, 554–566.
Source verification of mis-identified Arabidopsis thaliana accessions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVKqt77N&md5=e5b1b2582215d4e711008a8d58f0372dCAS | 21481029PubMed |

Blakeney AB, Harris PJ, Henry RJ, Stone BA (1983) A simple and rapid preparation of alditol acetates for monosaccharide analysis. Carbohydrate Research 113, 291–299.
A simple and rapid preparation of alditol acetates for monosaccharide analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXhsl2kurc%3D&md5=ef1be2c69d27ec350068dd904ee297dfCAS |

Bonin CP, Reiter W-D (2000) A bifunctional epimerase–reductase acts downstream of the MUR1 gene product and completes the de novo synthesis of GDP-L-fucose in Arabidopsis. The Plant Journal 21, 445–454.
A bifunctional epimerase–reductase acts downstream of the MUR1 gene product and completes the de novo synthesis of GDP-L-fucose in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXivVeisLY%3D&md5=1c46691532014be7445f7d7ee1f4108cCAS | 10758496PubMed |

Bonin CP, Potter I, Vanzin GF, Reiter W-D (1997) The MUR1 gene of Arabidopsis thaliana encodes an isoform of GDP-d-mannose-4,6-dehydratase, catalyzing the first step in the de novo synthesis of GDP-L-fucose. Proceedings of the National Academy of Sciences of the United States of America 94, 2085–2090.
The MUR1 gene of Arabidopsis thaliana encodes an isoform of GDP-d-mannose-4,6-dehydratase, catalyzing the first step in the de novo synthesis of GDP-L-fucose.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhslChs70%3D&md5=617d08ce8630fc9165327e930db588e0CAS | 9050909PubMed |

Brennan M, McLean J, Altaner C, Ralph J, Harris P (2012) Cellulose microfibril angles and cell-wall polymers in different wood types of Pinus radiata. Cellulose (London, England) 19, 1385–1404.
Cellulose microfibril angles and cell-wall polymers in different wood types of Pinus radiata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XosFemt7c%3D&md5=fe4d237d126060b73e7f85e3ab1d457cCAS |

Cave ID, Walker JCF (1994) Stiffness of wood in fast-grown plantation softwoods – the influence of microfibril angle. Forest Products Journal 44, 43–48.

Chaffey N, Cholewa E, Regan S, Sundberg B (2002) Secondary xylem development in Arabidopsis: a model for wood formation. Physiologia Plantarum 114, 594–600.
Secondary xylem development in Arabidopsis: a model for wood formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjvFCnt7k%3D&md5=74f2614d90ef7faf253c7774aed38169CAS | 11975734PubMed |

Chang XF, Chandra R, Berleth T, Beatson RP (2008) Rapid, microscale, acetyl bromide-based method for high-throughput determination of lignin content in Arabidopsis thaliana. Journal of Agricultural and Food Chemistry 56, 6825–6834.
Rapid, microscale, acetyl bromide-based method for high-throughput determination of lignin content in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXptFCrsbg%3D&md5=90bbe5f9967872985b405b3060c84defCAS | 18666780PubMed |

Etchells JP, Turner SR (2010) The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division. Development 137, 767–774.
The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksVChu7g%3D&md5=f7b965b460eab64ed5450678a952b577CAS | 20147378PubMed |

Fournier-Level A, Korte A, Cooper MD, Nordborg M, Schmitt J, Wilczek AM (2011) A map of local adaptation in Arabidopsis thaliana. Science 334, 86–89.
A map of local adaptation in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Gms7%2FJ&md5=d75dcf7e859339d7bfc426044bd11a41CAS | 21980109PubMed |

Gan X, Stegle O, Behr J, Steffen JG, Drewe P, Hildebrand KL, Lyngsoe R, Schultheiss SJ, Osborne EJ, Sreedharan VT, Kahles A, Bohnert R, Jean G, Derwent P, Kersey P, Belfield EJ, Harberd NP, Kemen E, Toomajian C, Kover PX, Clark RM, Ratsch G, Mott R (2011) Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477, 419–423.
Multiple reference genomes and transcriptomes for Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFers7%2FL&md5=b3f2a73d52d443bc44253a38bf2f1ca8CAS | 21874022PubMed |

Girault R, Bert F, Rihouey C, Jauneau A, Morvan C, Jarvis M (1997) Galactans and cellulose in flax fibres: putative contributions to the tensile strength. International Journal of Biological Macromolecules 21, 179–188.
Galactans and cellulose in flax fibres: putative contributions to the tensile strength.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXltl2muro%3D&md5=ed9c1af1cf6dc453806b8d621b913026CAS | 9283034PubMed |

Hancock AM, Brachi B, Faure N, Horton MW, Jarymowycz LB, Sperone FG, Toomajian C, Roux F, Bergelson J (2011) Adaptation to climate across the Arabidopsis thaliana genome. Science 334, 83–86.
Adaptation to climate across the Arabidopsis thaliana genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Gms7%2FI&md5=6f193fae212779927cd6b1acddd1b1c0CAS | 21980108PubMed |

Hatfield RD, Grabber J, Ralph J, Brei K (1999) Using the acetyl bromide assay to determine lignin concentrations in herbaceous plants: some cautionary notes. Journal of Agricultural and Food Chemistry 47, 628–632.
Using the acetyl bromide assay to determine lignin concentrations in herbaceous plants: some cautionary notes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitlyksA%3D%3D&md5=79ecf0526dbf44a6dc5197639db5a42fCAS | 10563943PubMed |

Hepworth DG, Vincent JFV (1998) Modelling the mechanical properties of xylem tissue from tobacco plants (Nicotiana tabacum ‘Samsun’) by considering the importance of molecular and micromechanisms. Annals of Botany 81, 761–770.
Modelling the mechanical properties of xylem tissue from tobacco plants (Nicotiana tabacum ‘Samsun’) by considering the importance of molecular and micromechanisms.Crossref | GoogleScholarGoogle Scholar |

Herakovich CT (1998) ‘Mechanics of fibrous composites.’ (John Wiley & Sons: New York)

Horton MW, Hancock AM, Huang YS, Toomajian C, Atwell S, Auton A, Muliyati NW, Platt A, Sperone FG, Vilhjalmsson BJ, Nordborg M, Borevitz JO, Bergelson J (2012) Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel. Nature Genetics 44, 212–216.
Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlsF2jsw%3D%3D&md5=83f10196596a048f69a4fc0f724ce5d3CAS | 22231484PubMed |

Ito Y, Nakanomyo I, Motose H, Iwamoto K, Sawa S, Dohmae N, Fukuda H (2006) Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313, 842–845.
Dodeca-CLE peptides as suppressors of plant stem cell differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnvVynt7o%3D&md5=81fa521a4205f23d307baa3bb809f1e7CAS | 16902140PubMed |

Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290, 344–347.
Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsVGiurw%3D&md5=00b2dfe0876a2ab099b40c396a81875bCAS | 11030654PubMed |

Karlsson BH, Sills GR, Nienhuis J (1993) Effects of photoperiod and vernalization on the number of leaves at flowering in 32 Arabidopsis thaliana (Brassicaceae) ecotypes. American Journal of Botany 80, 646–648.
Effects of photoperiod and vernalization on the number of leaves at flowering in 32 Arabidopsis thaliana (Brassicaceae) ecotypes.Crossref | GoogleScholarGoogle Scholar |

Keckes J, Burgert I, Fruhmann K, Muller M, Kolln K, Hamilton M, Burghammer M, Roth SV, Stanzl-Tschegg S, Fratzl P (2003) Cell-wall recovery after irreversible deformation of wood. Nature Materials 2, 810–813.
Cell-wall recovery after irreversible deformation of wood.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptlemt70%3D&md5=eaa540a2894a4d25f64f6f1a7e6576e4CAS | 14625541PubMed |

Koornneef M, Blankestijndevries H, Hanhart C, Soppe W, Peeters T (1994) The phenotype of some late-flowering mutants is enhanced by a locus on chromosome 5 that is not effective in the Landsberg erecta wild-type. The Plant Journal 6, 911–919.
The phenotype of some late-flowering mutants is enhanced by a locus on chromosome 5 that is not effective in the Landsberg erecta wild-type.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjsFyqu7w%3D&md5=54911e710a2d7b7d0f6bb21103c937a4CAS |

Kover PX, Valdar W, Trakalo J, Scarcelli N, Ehrenreich IM, Purugganan MD, Durrant C, Mott R (2009) A multiparent advanced generation inter-cross to fine-map quantitative traits in Arabidopsis thaliana. PLOS Genetics 5, e1000551
A multiparent advanced generation inter-cross to fine-map quantitative traits in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 19593375PubMed |

Kutscha, NP, Gray, JR (1972) ‘The suitability of certain stains for studying lignification in balsam fir, Abies balsamea (L.) Mill.’ (University of Maine: Orono)

Lens F, Smets E, Melzer S (2012) Stem anatomy supports Arabidopsis thaliana as a model for insular woodiness. New Phytologist 193, 12–17.
Stem anatomy supports Arabidopsis thaliana as a model for insular woodiness.Crossref | GoogleScholarGoogle Scholar | 21906070PubMed |

Levy S, York WS, Stuikeprill R, Meyer B, Staehelin LA (1991) Simulations of the static and dynamic molecular conformations of xyloglucan – the role of the fucosylated side-chain in surface-specific side-chain folding. The Plant Journal 1, 195–215.
Simulations of the static and dynamic molecular conformations of xyloglucan – the role of the fucosylated side-chain in surface-specific side-chain folding.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s3ltFSqtA%3D%3D&md5=45a0a37b44020904c49fa221b522b8e7CAS | 1844884PubMed |

Lewandowska-Sabat AM, Winge P, Fjellheim S, Dørum G, Bones AM, Rognli OA (2012) Genome wide transcriptional profiling of acclimation to photoperiod in high-latitude accessions of Arabidopsis thaliana. Plant Science 185–186, 143–155.
Genome wide transcriptional profiling of acclimation to photoperiod in high-latitude accessions of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 22325875PubMed |

Li Y, Huang Y, Bergelson J, Nordborg M, Borevitz JO (2010) Association mapping of local climate-sensitive quantitative trait loci in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 107, 21199–21204.
Association mapping of local climate-sensitive quantitative trait loci in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFyls7fJ&md5=390058e1945930c5d0398a1bdea851ffCAS | 21078970PubMed |

MacKay JJ, O’Malley DM, Presnell T, Booker FL, Campbell MM, Whetten TW, Sederoff RR (1997) Inheritance, gene expression, and lignin characterization in a mutant pine deficient in cinnamyl alcohol dehydrogenase. Proceedings of the National Academy of Sciences of the United States of America 94, 8255–8260.
Inheritance, gene expression, and lignin characterization in a mutant pine deficient in cinnamyl alcohol dehydrogenase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkvVShtr4%3D&md5=235f560f21cf0ec514925bac3a9cff70CAS | 9223348PubMed |

MacMillan CP, Mansfield SD, Stachurski ZH, Evans R, Southerton SG (2010) Fasciclin-like arabinogalactan proteins: specialization for stem biomechanics and cell wall architecture in Arabidopsis and Eucalyptus. The Plant Journal 62, 689–703.
Fasciclin-like arabinogalactan proteins: specialization for stem biomechanics and cell wall architecture in Arabidopsis and Eucalyptus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnt1Ghsbg%3D&md5=0cecf727374f28c00f89d5a9fb3d40daCAS | 20202165PubMed |

Mellerowicz EJ, Gorshkova TA (2012) Tensional stress generation in gelatinous fibres: a review and possible mechanism based on cell-wall structure and composition. Journal of Experimental Botany 63, 551–565.
Tensional stress generation in gelatinous fibres: a review and possible mechanism based on cell-wall structure and composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos1Cqtw%3D%3D&md5=3d86d7839fa536e90a8d2e0c1001b2edCAS | 22090441PubMed |

Melzer S, Lens F, Gennen J, Vanneste S, Rohde A, Beeckman T (2008) Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana. Nature Genetics 40, 1489–1492.
Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVWhu7fK&md5=7f1b8c80b0a6aacbbda480789dc3e250CAS | 18997783PubMed |

Motose H, Sugiyama M, Fukuda H (2004) A proteoglycan mediates inductive interaction during plant vascular development. Nature 429, 873–878.
A proteoglycan mediates inductive interaction during plant vascular development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltVKlt7Y%3D&md5=a9c4a7411de9b9140a72d8f7ebcd235dCAS | 15215864PubMed |

Mouille G, Witucka-Wall H, Bruyant M-P, Loudet O, Pelletier S, Rihouey C, Lerouxel O, Lerouge P, Höfte H, Pauly M (2006) Quantitative trait loci analysis of primary cell wall composition in Arabidopsis. Plant Physiology 141, 1035–1044.
Quantitative trait loci analysis of primary cell wall composition in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xnt1Ogtrs%3D&md5=e44382caa975fcd8ad35d2bc196a399dCAS | 16714406PubMed |

Nordborg M, Bergelson J (1999) The effect of seed and rosette cold treatment on germination and flowering time in some Arabidopsis thaliana (Brassicaceae) ecotypes. American Journal of Botany 86, 470–475.
The effect of seed and rosette cold treatment on germination and flowering time in some Arabidopsis thaliana (Brassicaceae) ecotypes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MnhtVKjsA%3D%3D&md5=f51a059aa74f6b3a99b1bf6772a5f437CAS | 10205066PubMed |

Oda Y, Fukuda H (2012) Secondary cell wall patterning during xylem differentiation. Current Opinion in Plant Biology 15, 38–44.
Secondary cell wall patterning during xylem differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFCrs7Y%3D&md5=252b7183c38ded72b93dce3b4bff9ea2CAS | 22078063PubMed |

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=e753b6d3c697dc9bdd1f91adbf82aac9CAS | 12805631PubMed |

Strabala TJ, O’Donnell PJ, Smit A-M, Ampomah-Dwamena C, Martin EJ, Netzler N, Nieuwenhuizen N, Quinn B, Foote HCC, Hudson KR (2006) Gain-of-function phenotypes of many CLAVATA3/ESR genes, including four new family members, correlate with tandem variations in the conserved CLAVATA3/ESR domain. Plant Physiology 140, 1331–1344.
Gain-of-function phenotypes of many CLAVATA3/ESR genes, including four new family members, correlate with tandem variations in the conserved CLAVATA3/ESR domain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjslyqu7k%3D&md5=c2670b634235303b41ede67ad2461e46CAS | 16489133PubMed |

Theander O (1991) Chemical analysis of lignocellulose materials. Animal Feed Science and Technology 32, 35–44.
Chemical analysis of lignocellulose materials.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlsFOht7g%3D&md5=9afbdbcae570d399b5305a28053a6f98CAS |

Turner SR, Somerville CR (1997) Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. The Plant Cell 9, 689–701.

Updegraff DM (1969) Semimicro determination of cellulose in biological materials. Analytical Biochemistry 32, 420–424.
Semimicro determination of cellulose in biological materials.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3cXivVOltQ%3D%3D&md5=f5c5b85cc1b7dfa74f8b6a5f99f5d0d4CAS | 5361396PubMed |

Vanzin GF, Madson M, Carpita NC, Raikhel NV, Keegstra K, Reiter W-D (2002) The mur2 mutant of Arabidopsis thaliana lacks fucosylated xyloglucan because of a lesion in fucosyltransferase AtFUT1. Proceedings of the National Academy of Sciences of the United States of America 99, 3340–3345.
The mur2 mutant of Arabidopsis thaliana lacks fucosylated xyloglucan because of a lesion in fucosyltransferase AtFUT1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1Cqt74%3D&md5=6262f114324c7469726b3cc768ce2709CAS | 11854459PubMed |

Wagner A, Ralph J, Akiyama T, Flint H, Phillips L, Torr K, Nanayakkara B, Te Kiri L (2007) Exploring lignification in conifers by silencing hydroxycinnamoyl-CoA : shikimate hydroxycinnamoyltransferase in Pinus radiata. Proceedings of the National Academy of Sciences of the United States of America 104, 11 856–11 861.
Exploring lignification in conifers by silencing hydroxycinnamoyl-CoA : shikimate hydroxycinnamoyltransferase in Pinus radiata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotVWhur0%3D&md5=cbffc4360ca127c7e7c6e7ad6baba019CAS |

Wyatt SE, Sederoff R, Flaishman MA, Lev-Yadun S (2010) Arabidopsis thaliana as a model for gelatinous fiber formation. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 57, 363–367.
Arabidopsis thaliana as a model for gelatinous fiber formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlslCksL4%3D&md5=307bb2fd2ca2304d04234cc56df018dfCAS |

Xu P, Liu H, Donaldson LA, Zhang Y (2011) Mechanical performance and cellulose microfibrils in wood with high S2 microfibril angles. Journal of Materials Science 46, 534–540.
Mechanical performance and cellulose microfibrils in wood with high S2 microfibril angles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlCgt7jF&md5=71d107f972cdb9af71e3ba640ba2fb17CAS |

Zhang J, Elo A, Helariutta Y (2011) Arabidopsis as a model for wood formation. Current Opinion in Biotechnology 22, 293–299.
Arabidopsis as a model for wood formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkvFWrsLY%3D&md5=23fc15b96c1ee59bb3d3de79330bc51cCAS | 21144727PubMed |

Zhong R, Burk DH, Morrison WH, Ye Z-H (2002) A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. The Plant Cell 14, 3101–3117.
A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtFClsg%3D%3D&md5=8cc882bc59d611fea97726ae3271c130CAS | 12468730PubMed |