Protoplasma

, Volume 248, Issue 3, pp 579–590 | Cite as

Polysaccharide and glycoprotein distribution in the epidermis of cotton ovules during early fiber initiation and growth

  • Andrew J. Bowling
  • Kevin Christopher Vaughn
  • Rickie B. Turley
Original Article

Abstract

The cotton fiber is a model system to study cell wall biosynthesis because the fiber cell elongates (∼3 cm in ∼20 days) without mitosis. In this study, developing cotton ovules, examined from 1 day before anthesis (DBA) to 2 days post-anthesis (DPA), that would be difficult to investigate via classical carbohydrate biochemistry were probed using a battery of antibodies that recognize a large number of different wall components. In addition, ovules from these same stages were investigated in three fiberless lines. Most antibodies reacted with at least some component of the ovule, and several of the antibodies reacted specifically with the epidermal layer of cells that may give clues as to the nature of the development of the fibers and the neighboring, nonfiber atrichoblasts. Arabinogalactan proteins (AGPs) labeled the epidermal layers more strongly than other ovular tissue, even at 1 DBA. One of the AGP antibodies, CCRC-M7, which recognizes a 1➔6 galactan epitope of AGPs, is lost from the fiber cells by 2 DPA, although labeling in the atrichoblasts remained strong. In contrast, LM5 that recognizes a 1➔4 galactan RGI side chain is unreactive with sections until the fibers are produced and only the fibers are reactive. Dramatic changes also occur in the homogalacturonans (HGs). JIM5, which recognizes highly de-esterified HGs, only weakly labels epidermal cells of 1 DBA and 0 DPA ovules, but labeling increases in fibers cells, where a pectinaceous sheath is produced around the fiber cell and stronger reaction in the internal and external walls of the atrichoblast. In contrast, JIM7-reactive, highly esterifed HGs are present at high levels in the epidermal cells throughout development. Fiberless lines displayed similar patterns of labeling to the fibered lines, except that all of the cells had the labeling pattern of atrichoblasts. That is, CCRC-M7 labeled all cells of the fiberless lines, and LM5 labeled no cells at 2 DPA. These data indicate that a number of polysaccharides are unique in quantity or presence in the epidermal cell layers, and some of these might be critical participants in the early stages of initiation and elongation of cotton fibers.

Keywords

Cotton Fiber initiation Pectins Arabinogalactan proteins Esterification 

Abbreviations

AGP

Arabinogalactan protein

BSA

Bovine serum albumin

DBA

Days before anthesis

DPA

Days post-anthesis

HG

Homogalacturonan

IGS

Immunogold–silver

PBS

Phosphate-buffered saline

RGI

Rhamnogalacturonan I

Notes

Acknowledgments

The authors would like to thank Grant Cochran for excellent technical assistance. AJB was supported in part by a headquarters-funded research associate position to KCV. Production of the monoclonal antibodies of the CCRC series was provided by NSF grants DBI-0421683 and RCN-0090281 to the Complex Carbohydrate Center, University of Georgia. Mention of a trademark, proprietary product, or vendor does not constitute an endorsement by the US Department of Agriculture.

Conflicts of Interest

None

References

  1. Andeme-Onzighi C, Sivaguru M, Judy-March J, Baskin TI, Driouich A (2002) The reb1-1 mutation of Arabidopsis alters the morphology of trichoblasts, the expression of arabinogalactan-proteins and the organization of cortical microtubules. Planta 215:949–958PubMedCrossRefGoogle Scholar
  2. Basra AS, Malik CP (1984) Development of the cotton fiber. Int Rev Cytol 87:65–113CrossRefGoogle Scholar
  3. Bowling AJ, Vaughn KC (2008a) A simple technique to minimize heat damage to specimens during thermal polymerization of LR White plastic in gelatin capsules. J Microsc 231:186–189PubMedCrossRefGoogle Scholar
  4. Bowling AJ, Vaughn KC (2008b) Immunocytochemical characterization of tension wood: gelatinous fibers contain more than just cellulose. Am J Bot 95:655–663PubMedCrossRefGoogle Scholar
  5. Bowling AJ, Maxwell HB, Vaughn KC (2008) Unusual trichome structure and composition in mericarps of catchweeed bedstraw (Galium aparine). Protoplasma 232:153–163PubMedCrossRefGoogle Scholar
  6. Freshour G, Clay RP, Fuller MS, Albersheim P, Darvill AG, Hahn MG (1996) Developmental and tissue-specific structural alterations of the cell wall polysaccharides of Arabidopsis thaliana roots. Plant Physiol 110:1413–1429PubMedGoogle Scholar
  7. Lee JJ, Woodward AW, Chen ZJ (2007) Gene expression changes and early events in cotton fibre development. Ann Bot 100:1391–1401PubMedCrossRefGoogle Scholar
  8. Meinert MC, Delmer DP (1977) Changes in biochemical composition of the cell wall of the cotton fiber during development. Plant Physiol 59:1088–1097PubMedCrossRefGoogle Scholar
  9. Nguema-Ona E, Andeme-Onzighi C, Aboughe-Angone S, Bardor M, Ishii T, Lerouge P, Driouich A (2006) The reb1-1 mutation of Atabidopsis. Effect on the structure and localization of galactose-containing cell wall polysaccharides. Plant Physiol 140:1406–1417PubMedCrossRefGoogle Scholar
  10. Percival AE (1987) The national collection of Gossypium germplasm. Southern Coop Ser Bull 321Google Scholar
  11. Ruan YL (2005) Recent advances in understanding cotton fibre and seed development. Seed Sci Res 15:269–280CrossRefGoogle Scholar
  12. Ruan YL (2007) Rapid cell expansion and cellulose synthase regulated by plasmodesmata and sugar: insights from the single-celled cotton fibre. Funct Plant Biol 34:1–10CrossRefGoogle Scholar
  13. Ruan YL, Chourey PS (1998) A fiberless seed mutation in cotton is associated with lack of fiber cell initiation in ovule epidermis and alterations in sucrose synthase expression and carbon partitioning in developing seeds. Plant Physiol 118:399–406PubMedCrossRefGoogle Scholar
  14. Ryser U (1999) Cotton fiber initiation and histodifferentiation. In: Basra SA (ed) Cotton fibers. Hawthorne, Binghamton, pp 1–46Google Scholar
  15. Stafstrom JP, Staehelin LA (1988) Antibody localization of extensin in cell walls of carrot storage roots. Planta 174:321-332Google Scholar
  16. Salnikov VV, Grimson MJ, Seagull RW, Haigler CH (2003) Localization of sucrose synthase and callose in freeze-substituted secondary-wall-stage cotton fibers. Protoplasma 221:175–184PubMedGoogle Scholar
  17. Steffan W, Kovac P, Albersheim P, Darvill AG, Albersheim P (1998) Characterization of a monoclonal antibody that recognizes an arabinosylated (1➔6) β-d-galactan epitope in plant complex carbohydrates. Carbohydr Res 275:295–307CrossRefGoogle Scholar
  18. Stewart JM (1975) Fiber initiation on the cotton ovule (Gossypium hirsutum). Am J Bot 62:261–288Google Scholar
  19. Taliercio EW, Boykin D (2007) Analysis of gene expression in cotton fiber initials. BMC Plant Biol 7:22PubMedCrossRefGoogle Scholar
  20. Tokumoto H, Wakabayashi K, Kamisaka S, Hoson T (2002) Changes in the sugar composition and molecular mass distribution of matrix polysaccharides during cotton fiber development. Plant Cell Physiol 43:411–418PubMedCrossRefGoogle Scholar
  21. Turley RB (2002) Registration of MD171 fiberless upland cotton as a genetic stock. Crop Sci 42:994–995CrossRefGoogle Scholar
  22. Turley RB, Ferguson DL (1996) Changes in ovule proteins during early fiber development in a normal and a fiberless line of cotton (Gossypium hirsutum L.). J Plant Physiol 149:695–702Google Scholar
  23. Turley RB, Kloth RH (2002) Identification of a third fuzzless seed locus in upland cotton (Gossypium hirsutum L.). J Hered 93:359–364PubMedCrossRefGoogle Scholar
  24. Turley RB, Kloth RH (2008) The inheritance model for the fiberless trait in upland cotton (Gossypium hirsutum L.) line SL 1-7-1: variation on a theme. Euphytica 164:123–132CrossRefGoogle Scholar
  25. Van’t Hof J, Saha S (1997) Cotton fibers can undergo cell division. Am J Bot 84:1231–1235CrossRefGoogle Scholar
  26. Vaughn KC (2006) Conversion of the searching hyphae of dodder into xylic and phloic hyphae: A cytochemical and immunocytochemical investigation. Intern J Plant Sci 167:1099-1114Google Scholar
  27. Vaughn KC, Turley RB (1999) The primary walls of cotton fibers contain an ensheathing pectin layer. Protoplasma 209:226–237CrossRefGoogle Scholar
  28. Vaughn KC, Turley RB (2001) Ultrastructural effects of cellulose biosynthesis inhibitor herbicides on developing cotton fibers. Protoplasma 216:80–93PubMedCrossRefGoogle Scholar
  29. Weis KG, Jacobsen KR, Jernstedt JA (1999) Cytochemistry of developing cotton fibers: a hypothesized relationship between motes and non-dyeing fibers. Field Crops Res 62:107–117CrossRefGoogle Scholar
  30. Zhang TZ, Pan JJ (1991) Genetic analysis of a fuzzless-lintless mutant in Gossypium hirsutum L. Jiangsu J Agric Sci 7:13–16Google Scholar

Copyright information

© Springer-Verlag (outside the USA) 2010

Authors and Affiliations

  • Andrew J. Bowling
    • 1
    • 3
  • Kevin Christopher Vaughn
    • 1
  • Rickie B. Turley
    • 2
  1. 1.Crop Production Systems Research Unit, US Department of AgricultureThe Agricultural Research Service (USDA-ARS)StonevilleUSA
  2. 2.Crop Genetics Research UnitUSDA-ARSStonevilleUSA
  3. 3.Dow AgrosciencesIndianapolisUSA

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