Deposition patterns of cellulose microfibrils in flange wall ingrowths of transfer cells indicate clear parallels with those of secondary wall thickenings
Mark J. Talbot A B , Geoffrey Wasteneys C D , David W. McCurdy A E and Christina E. Offler AA School of Environmental and Life Sciences, The University of Newcastle, Newcastle, NSW 2308, Australia.
B Current address: Microscopy Unit, CSIRO Plant Industry, Canberra, ACT 2000, Australia.
C Plant Cell Biology Group, Research School of Biological Sciences, The Australian National University, Canberra, ACT 2601, Australia.
D Current address: Department of Botany, University of British Columbia, 3529-6270 University Boulevard, Vancouver, British Columbia V6T 1Z4, Canada.
E Corresponding author. Email: david.mccurdy@newcastle.edu.au
F This paper originates from an International Symposium in Memory of Vincent R. Franceschi, Washington State University, Pullman, Washington, USA, June 2006.
Functional Plant Biology 34(4) 307-313 https://doi.org/10.1071/FP06273
Submitted: 27 October 2006 Accepted: 13 March 2007 Published: 19 April 2007
Abstract
The arrangement of cellulose microfibrils and cortical microtubules in transfer cells depositing flange wall ingrowths have been determined with field emission scanning electron microscopy and immunofluorescence confocal microscopy. In xylem transfer cells of wheat (Triticum aestivum) stem nodes and transfer cells of corn (Zea mays) endosperm tissue, cellulose microfibrils were aligned in parallel bundles to form the linear wall ingrowths characteristic of flange ingrowth morphology. In both cell types, linear bundles of cellulose microfibrils were deposited over an underlying wall composed of randomly arranged microfibrils. Acid extraction of wheat xylem transfer cells established that flange ingrowths were composed of crystalline cellulose. Immunofluorescence labelling of microtubules in wheat xylem transfer cells showed that bundles of microtubules were positioned directly below and parallel with developing flange ingrowths, whereas more mature ingrowths were flanked by bundles of microtubules. These results show that the parallel organisation of cellulose microfibrils in flange wall ingrowths is similar to those in secondary wall thickenings in xylem elements, and that deposition of these structures in transfer cells is also likely to involve bundling of parallel arrays of microtubules. Our observations are discussed in terms of the possible role of microtubules in building flange-type wall ingrowths and the consequences in terms of predicted mechanisms required to build the fundamentally different reticulate-type wall ingrowths.
Additional keywords: cellulose microfibril, field emission scanning electron microscopy, microtubules, transfer cell, wall ingrowth.
Acknowledgements
The FESEM imaging of cellulose microfibrils was carried out as part of a collaborative Research Scholarship awarded to M. J. T., in partnership with the Research School of Biological Sciences (RSBS), Australian National University. We thank the staff at the Electron Microscope Unit at RSBS for their kind assistance with FESEM imaging. This contribution is dedicated to Vincent Franceschi, a very special colleague and friend who shared with us and many others his love of plant structure and his unique microscopy skills. Thank you Vince for who you were and what you gave to the international community of plant scientists.
Baskin TI
(2001) On the alignment of cellulose microfibrils by cortical microtubules: a review and a model. Protoplasma 215, 150–171.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Baskin TI,
Beemster GTS,
Judy-March JE, Marga F
(2004) Disorganization of cortical microtubules stimulates tangential expansion and reduces the uniformity of cellulose microfibril alignment among cells in the root of Arabidopsis. Plant Physiology 135, 2279–2290.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Davis RW,
Smith JD, Cobb BG
(1990) A light and electron microscope investigation of the transfer cell region of maize caryopses. Canadian Journal of Botany 68, 471–479.
Emons AMC
(1994) Winding threads around plant cells: a geometrical model for microfibril deposition. Plant, Cell & Environment 17, 3–14.
| Crossref | GoogleScholarGoogle Scholar |
Emons AMC, Mulder BM
(2000) How the deposition of cellulose microfibrils builds cell wall architecture. Trends in Plant Science 5, 35–40.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Falconer MM, Seagull RW
(1985) Immunofluorescent and calcofluor white staining of developing tracheary elements in Zinnia elegans L. suspension cultures. Protoplasma 125, 190–198.
| Crossref | GoogleScholarGoogle Scholar |
Funada R,
Miura H,
Shibagaki M,
Furusawa O,
Miura T,
Fukatsu E, Kitin P
(2001) Involvement of localized cortical microtubules in the formation of a modified structure of wood. Journal of Plant Research 114, 491–497.
| Crossref | GoogleScholarGoogle Scholar |
Gardiner JC,
Taylor NG, Turner SR
(2003) Control of cellulose synthase complex localization in developing xylem. The Plant Cell 15, 1740–1748.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hepler PK, Fosket DE
(1971) The role of microtubules in vessel member differentiation in Coleus. Protoplasma 72, 213–236.
| Crossref | GoogleScholarGoogle Scholar |
Jung G, Wernicke W
(1990) Cell shaping and microtubules in developing mesophyll of wheat. Protoplasma 153, 141–148.
| Crossref | GoogleScholarGoogle Scholar |
Kremer C, Drinnan A
(2004) Secondary walls in hyaline cells of Sphagnum. Australian Journal of Botany 52, 243–256.
| Crossref | GoogleScholarGoogle Scholar |
Oda Y,
Mimura T, Hasezawa S
(2005) Regulation of secondary wall development by cortical microtubules during tracheary element differentiation in Arabidopsis cell suspensions. Plant Physiology 137, 1027–1036.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Offler CE,
McCurdy DW,
Patrick JW, Talbot MJ
(2003) Transfer cells: cells specialized for a special purpose. Annual Review of Plant Biology 54, 431–454.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Panteris E,
Apostolakos P, Galatis B
(1993a) Microtubules and morphogenesis in ordinary epidermal cells of Vigna siensis leaves. Protoplasma 174, 91–100.
| Crossref | GoogleScholarGoogle Scholar |
Panteris E,
Apostolakos P, Galatis B
(1993b) Microtubule organization and cell morphogenesis in two semi-lobed cell types of Adiantum capillus-veneris L. leaflets. New Phytologist 125, 509–520.
| Crossref | GoogleScholarGoogle Scholar |
Roberts AW,
Frost AO,
Roberts EM, Haigler CH
(2004) Roles of microtubules and cellulose microfibril assembly in the localization of secondary-cell-wall deposition in developing tracheary elements. Protoplasma 224, 217–229.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Satiat-Jeunemaitre B
(1987) Inhibition of the helicoidal assembly of the cellulose–hemicellulose complex by 2,6-dichlorobenzonitrile (DCB). Biology of the Cell 59, 89–96.
Seagull RW
(1990) The effects of microtubule and microfilament disrupting agents on cytoskeletal arrays and wall deposition in developing cotton fibers. Protoplasma 159, 44–59.
| Crossref | GoogleScholarGoogle Scholar |
Seagull RW
(1993) Cytoskeletal involvement in cotton fiber growth and development. Micron 24, 643–660.
| Crossref |
Sugimoto K,
Williamson RE, Wasteneys GO
(2000) New techniques enable comparative analysis of microtubule orientation, wall texture, and growth rate in intact roots of Arabidopsis. Plant Physiology 124, 1493–1506.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sugimoto K,
Williamson RE, Wasteneys GO
(2001) Wall architecture in the cellulose-deficient rsw1 mutant of Arabidopsis thaliana: microfibrils but not microtubules lose their transverse alignment before microfibrils become unrecognizable in the mitotic and elongation zones of roots. Protoplasma 215, 172–183.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sugimoto K,
Himmelspach R,
Williamson RE, Wasteneys GO
(2003) Mutation or drug-dependent microtubule disruption causes radial swelling without altering parallel cellulose microfibril deposition in Arabidopsis root cells. The Plant Cell 15, 1414–1429.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Takeda K, Shibaoka H
(1981) Effects of gibberellin and colchicine on microfibril arrangement in epidermal cell walls of Vigna angularis Ohwi et Ohashi epicotyls. Planta 151, 393–398.
| Crossref | GoogleScholarGoogle Scholar |
Talbot MJ,
Franceschi VR,
McCurdy DW, Offler CE
(2001) Wall ingrowth architecture in epidermal cells of Vicia faba cotyledons. Protoplasma 215, 191–203.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Talbot MJ,
Offler CE, McCurdy DW
(2002) Transfer cell wall architecture: a contribution towards understanding localized wall deposition. Protoplasma 219, 197–209.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Talbot MJ,
Wasteneys GO,
Offler CE, McCurdy DW
(2007) Cellulose synthesis is required for deposition of reticulate wall ingrowths in transfer cells. Plant & Cell Physiology 48, 147–158.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Taylor JG, Haigler CH
(1993) Patterned secondary cell-wall assembly occurs in a self-perpetuating cascade. Acta Botanica Neerlandica 42, 153–163.
Updegraff DM
(1969) Semimicro determination of cellulose in biological materials. Analytical Biochemistry 32, 420–424.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wasteneys GO
(2004) Progress in understanding the role of microtubules in plant cells. Current Opinion in Plant Biology 7, 651–660.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wernicke W,
Gunther P, Jung G
(1993) Microtubules and cell shaping in the mesophyll of Nigella damascena L. Protoplasma 173, 8–12.
| Crossref | GoogleScholarGoogle Scholar |