Plant Physiol. Journal of Pharmacology and Experimental Therapeutics
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First published online April 15, 2009; 10.1104/pp.109.135459

Plant Physiology 150:684-699 (2009)
© 2009 American Society of Plant Biologists

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CELL BIOLOGY AND SIGNAL TRANSDUCTION

A Specialized Outer Layer of the Primary Cell Wall Joins Elongating Cotton Fibers into Tissue-Like Bundles1,[W],[OA]

Bir Singh, Utku Avci2, Sarah E. Eichler Inwood3, Mark J. Grimson, Jeff Landgraf, Debra Mohnen, Iben Sørensen, Curtis G. Wilkerson, William G.T. Willats and Candace H. Haigler*

North Carolina State University, Department of Crop Science, Raleigh, North Carolina 27695–7620 (B.S., U.A., C.H.H.); University of Georgia, Complex Carbohydrate Research Center, Athens, Georgia 30602–4712 (S.E.E.I.); Texas Tech University, Department of Biological Sciences/Imaging Center, Lubbock, Texas 79409–3131 (M.J.G.); Michigan State University, Research Technology Support Facility/Genomics, East Lansing, Michigan 48824–1319 (J.L.); University of Georgia, Department of Biochemistry and Molecular Biology, Athens, Georgia 30602–4712 (D.M.); University of Copenhagen, Department of Biology, 2200 Copenhagen N, Denmark (I.S., W.G.T.W.); Michigan State University, Research Technology Support Facility/Bioinformatics, East Lansing, Michigan 48824–1319 (C.G.W.); and North Carolina State University, Department of Plant Biology, Raleigh, North Carolina 27695–7620 (C.H.H.)

Cotton (Gossypium hirsutum) provides the world's dominant renewable textile fiber, and cotton fiber is valued as a research model because of its extensive elongation and secondary wall thickening. Previously, it was assumed that fibers elongated as individual cells. In contrast, observation by cryo-field emission-scanning electron microscopy of cotton fibers developing in situ within the boll demonstrated that fibers elongate within tissue-like bundles. These bundles were entrained by twisting fiber tips and consolidated by adhesion of a cotton fiber middle lamella (CFML). The fiber bundles consolidated via the CFML ultimately formed a packet of fiber around each seed, which helps explain how thousands of cotton fibers achieve their great length within a confined space. The cell wall nature of the CFML was characterized using transmission electron microscopy, including polymer epitope labeling. Toward the end of elongation, up-regulation occurred in gene expression and enzyme activities related to cell wall hydrolysis, and targeted breakdown of the CFML restored fiber individuality. At the same time, losses occurred in certain cell wall polymer epitopes (as revealed by comprehensive microarray polymer profiling) and sugars within noncellulosic matrix components (as revealed by gas chromatography-mass spectrometry analysis of derivatized neutral and acidic glycosyl residues). Broadly, these data show that adhesion modulated by an outer layer of the primary wall can coordinate the extensive growth of a large group of cells and illustrate dynamic changes in primary wall structure and composition occurring during the differentiation of one cell type that spends only part of its life as a tissue.

1 This work was supported by Cotton, Inc., of Cary, North Carolina, by the National Science Foundation (Plant Genome grant nos. DBI–0211797, R98RA1829, and DBI–0110173), and by the National Research Initiative, Cooperative State Research, Education, and Extension Service, U.S. Department of Agriculture (grant no. 2006–35318–17301). Development and distribution of some antibodies (from the CarboSource Services at the Complex Carbohydrate Research Center, University of Georgia) were supported by the National Science Foundation (grant nos. RCN0090281 and DBI0421683).

2 Present address: 2048 Complex Carbohydrate Research Center, University of Georgia, 315 Riverbend Road, Athens, GA 30602.

3 Present address: BioResources, LLC, P.O. Box 1464, Auburn, AL 36831.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Candace H. Haigler (candace_haigler{at}ncsu.edu).

[W] The online version of this article contains Web-only data.

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www.plantphysiol.org/cgi/doi/10.1104/pp.109.135459

* Corresponding author; e-mail candace_haigler{at}ncsu.edu.

Received January 8, 2009; accepted April 7, 2009; published April 15, 2009.


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