Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Metabolism of polysaccharides in dynamic middle lamellae during cotton fibre development

  • 349 Accesses

  • 2 Citations

Abstract

Main conclusion

Evidence is presented that cotton fibre adhesion and middle lamella formation are preceded by cutin dilution and accompanied by rhamnogalacturonan-I metabolism.

Cotton fibres are single cell structures that early in development adhere to one another via the cotton fibre middle lamella (CFML) to form a tissue-like structure. The CFML is disassembled around the time of initial secondary wall deposition, leading to fibre detachment. Observations of CFML in the light microscope have suggested that the development of the middle lamella is accompanied by substantial cell-wall metabolism, but it has remained an open question as to which processes mediate adherence and which lead to detachment. The mechanism of adherence and detachment were investigated here using glyco-microarrays probed with monoclonal antibodies, transcript profiling, and observations of fibre auto-digestion. The results suggest that adherence is brought about by cutin dilution, while the presence of relevant enzyme activities and the dynamics of rhamnogalacturonan-I side-chain accumulation and disappearance suggest that both attachment and detachment are accompanied by rhamnogalacturonan-I metabolism.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Abbreviations

CDTA:

1,2-Cyclohexanediamine-tetraacetic acid

CFML:

Cotton fibre middle lamella

CoMPP:

Comprehensive microarray polymer profiling

DPA:

Days post-anthesis

GT:

Glycosyltransferase

KOR:

Korrigan

RG-I:

Rhamnogalacturonan-I

References

  1. Ademe MS, He S, Pan Z, Sun J, Wang Q, Qin H, Liu J, Liu H, Yang J, Xu D, Yang J, Ma Z, Zhang J, Li Z, Cai Z, Zhang X, Zhang X, Huang A, Yi X, Zhou G, Li L, Zhu H, Pang B, Wang L, Jia Y, Du X (2017) Association mapping analysis of fiber yield and quality traits in upland cotton (Gossypium hirsutum L.). Mol Genet Genom 292:1267–1280. https://doi.org/10.1007/s00438-017-1346-9

  2. Arsovski AA, Popma TM, Haughn GW, Carpita NC, McCann MC, Western TL (2009) AtBXL1 encodes a bifunctional β-D-xylosidase/α-L-arabinofuranosidase required for pectic arabinan modification in Arabidopsis mucilage secretory cells. Plant Physiol 150:1219–1234

  3. Avci U, Pattathil S, Singh B, Brown VL, Hahn MG, Haigler CH (2013) Cotton fiber cell walls of Gossypium hirsutum and Gossypium barbadense have differences related to loosely-bound xyloglucan. Plos One 8:e56315

  4. Buffetto F, Cornuault V, Rydahl MG, Ropartz D, Alvarado C, Echasserieau V, Le Gall S, Bouchet B, Tranquet O, Verhertbruggen Y, Willats WGT, Knox JP, Ralet MC, Guillon F (2015) The deconstruction of pectic rhamnogalacturonan I unmasks the occurrence of a novel arabinogalactan oligosaccharide epitope. Plant Cell Physiol 56:2181–2196

  5. Byg I, Diaz J, Øgendal LH, Harholt J, Jørgensen B, Rolin C, Svava R, Ulvskov P (2012) Large-scale extraction of rhamnogalacturonan I from industrial potato waste. Food Chem 131:07–1216

  6. Fich EA, Segerson NA, Rose JCK (2016) The plant polyester cutin: biosynthesis, structure, and biological roles. Annu Rev Plant Biol 67:207–233

  7. Haigler CH, Betancur L, Stiff MR, Tuttle JR (2012) Cotton fiber: a powerful single-cell model for cell wall and cellulose research. Front Plant Sci 3:104. https://doi.org/10.3389/fpls.2012.00104

  8. Hande AS, Katageri IS, Jadhav MP, Adiger S, Gamanagatti S, Padmalatha KV, Dhandapani G, Kanakachari M, Kumar PA, Reddy VS (2017) Transcript profiling of genes expressed during fibre development in diploid cotton (Gossypium arboreum L.). BMC Genom 18:675. https://doi.org/10.1186/s12864-017-4066-y

  9. Harholt J, Jensen JK, Verhertbruggen Y, Sogaard C, Bernard S, Nafisi M, Poulsen CP, Geshi N, Sakuragi Driouich A, Knox JP, Scheller HV (2012) ARAD proteins associated with pectic arabinan biosynthesis form complexes when transiently overexpressed in planta. Planta 236:115–128

  10. Hernandez-Gomez MC, Runavot JL, Guo XY, Bourot S, Benians TAS, Willats WGT, Meulewaeter F, Knox JP (2015a) Heteromannan and heteroxylan cell wall polysaccharides display different dynamics during the elongation and secondary cell wall deposition phases of cotton fiber cell development. Plant Cell Physiol 56:1786–1797

  11. Hernandez-Gomez MC, Rydahl MG, Rogowski A, Morland C, Cartmell A, Crouch L, Labourel A, Fontes CMGA, Willats WGT, Gilbert HJ, Knox JP (2015b) Recognition of xyloglucan by the crystalline cellulose-binding site of a family 3a carbohydrate-binding module. FEBS Lett 589:2297–2303

  12. Hernandez-Gomez MC, Runavot JL, Meulewaeter F, Knox JP (2017) Developmental features of cotton fibre middle lamellae in relation to cell adhesion and cell detachment in cultivars with distinct fibre qualities. BMC Plant Biol 17:69. https://doi.org/10.1186/s12870-017-1017-3

  13. Ichinose H, Nishikubo N, Demura T, Kaneko S (2010) Characterization of α-L-arabinofuranosidase related to the secondary cell walls formation in Arabidopsis thaliana. Plant Biotechnol 27:259–266

  14. Jarvis MC, Briggs SPH, Knox JP (2003) Intercellular adhesion and cell separation in plants. Plant Cell Environ 26:977–989

  15. Jones L, Seymour GB, Knox JP (1997) Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1 → 4)-β-D-galactan. Plant Physiol 113:1405–1412

  16. Kim HJ, Triplett BA (2001) Cotton fiber growth in planta and in vitro. Models for plant cell elongation and cell wall biogenesis. Plant Physiol 127:1361–1366

  17. Kljun A, El-Dessouky HM, Benians TAS, Goubet F, Meulewaeter F, Knox JP, Blackburn JS (2014) Analysis of the physical properties of developing cotton fibres. Eur Polym J 51:57–68

  18. Larsen FH, Byg I, Diaz J, Engelsen SB, Ulvskov P (2011) Residue specific hydration of primary cell wall potato pectin identified by solid-state 13C single-pulse MAS and CP/MAS NMR spectroscopy. Biomacromolecules 12:1844–1850

  19. Lee KJD, Cornuault V, Manfield I, Ralet M-C, Knox JP (2013) Multiscale spatial heterogeneity of pectic rhamnogalacturonan-I (RG-I) in tobacco seed endosperm cell walls. Plant J 75:1018–1027

  20. Li Z, Fernie AR, Persson S (2016) Transition of primary to secondary cell wall synthesis. Sci Bull 61:838–846

  21. Liwanag AJM, Ebert B, Verhertbruggen Y, Rennie EA, Rautengarten C, Oikawa A, Andersen MCF, Clausen MH, Scheller HV (2012) Pectin biosynthesis: GALS1 in Arabidopsis thaliana is a β-1,4-galactan β-1,4-galactosyltransferase. Plant Cell 24:5024–5036

  22. MacMillan CP, Birke H, Chuah A, Brill E, Tsuji Y, Ralph J, Dennis ES, Llewellyn D, Pettolino FA (2017) Tissue and cell-specific transcriptomes in cotton reveal the subtleties of gene regulation underlying the diversity of plant secondary walls. BMC Genom 18:539

  23. Maltby D, Carpita NC, Montezinos D, Kulow C, Delmer DP (1979) β-1,3-glucan in developing cotton fibers—structure, localization, and relationship of synthesis to that of secondary wall cellulose. Plant Physiol 63:1158–1164

  24. Marcus SE, Verhertbruggen Y, Hervé C, Ordaz-Ortiz JJ, Farkas V, Pedersen HL, Willats WG, Knox JP (2008) Pectic homogalacturonan masks abundant sets of xyloglucan epitopes in plant cell walls. BMC Plant Biol 8:60. https://doi.org/10.1186/1471-2229-8-60

  25. McCann M, Roberts K (1994) Changes in cell wall architecture during cell elongation. J Exp Bot 45:1683–1691

  26. Meikle PJ, Bonig I, Hoogenraad NJ, Clarke AE, Stone BA (1991) The location of (1 → 3)-β-glucans in the walls of pollen tubes of Nicotiana alata using a (1 → 3)-β-glucan- specific monoclonal antibody. Planta 185:1–8

  27. Michailidis G, Argiriou A, Darzentas N, Tsaftaris A (2009) Analysis of xyloglucan endotransglycosylase/hydrolase (XTH) genes from allotetraploid (Gossypium hirsutum) cotton and its diploid progenitors expressed during fiber elongation. J Plant Physiol 166:403–416

  28. Minic Z, Do CT, Rihouey C, Morin H, Lerouge P, Jouanin L (2006) Purification, functional characterization, cloning, and identification of mutants of a seed-specific arabinan hydrolase in Arabidopsis. J Exp Bot 57:2339–2351

  29. Minic Z, Jamet E, Negroni L, der Garabedian PA, Zivy M, Jouanin L (2007) A sub-proteome of Arabidopsis thaliana mature stems trapped on concanavalin A is enriched in cell wall glycoside hydrolases. J Exp Bot 58:2503–2512

  30. Mishra DK, Agrawa N, Choudhary A, Yadav VK, Yadav VK (2018) An overview on advances in cotton genome and regulation of fiber development. ISJR 7:294–300

  31. Molhoj M, Johansen B, Ulvskov P, Borkhardt B (2001) Expression of a membrane-anchored endo-1,4-β-glucanase from Brassica napus, orthologous to KOR from Arabidopsis thaliana, is inversely correlated to elongation in light-grown plants. Plant Mol Biol 45:93–105

  32. Moller I, Marcus SE, Haeger A, Verhertbruggen Y, Verhoef R, Schols H, Ulvskov P, Mikkelsen JD, Knox JP, Willats W (2008) High-throughput screening of monoclonal antibodies against plant cell wall glycans by hierarchical clustering of their carbohydrate microarray binding profiles. Glycoconj J 25:37–48

  33. Montes RAC, Ranocha P, Martinez Y, Minic Z, Jouanin L, Marquis M, Saulnier L, Fulton LM, Cobbett CS, Bitton F, Renou JP, Jauneau A, Goffner D (2008) Cell wall modifications in Arabidopsis plants with altered α-L-arabinofuranosidase activity. Plant Physiol 147:63–77

  34. Nicol F, His I, Jauneau A, Vernhettes S, Canut H, Höfte H (1998) A plasma membrane-bound putative endo-1,4-β-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J 17:5563–5576

  35. Øbro J, Harholt J, Scheller HV, Orfila C (2004) Rhamnogalacturonan I in Solanum tuberosum tubers contains complex arabinogalactan structures. Phytochemistry 65:1429–1438

  36. Orford SJ, Timmis JN (1998) Specific expression of an expansin gene during elongation of cotton fibres. BBA-Gene Struct Expr 1398:342–346

  37. Pedersen HL, Fangel JU, McCleary B, Ruzanski C, Rydahl MG, Ralet MC, Farkas V, von Schantz L, Marcus SE, Andersen MC, Field R, Ohlin M, Knox JP, Clausen MH, Willats WG (2012) Versatile high resolution oligosaccharide microarrays for plant glycobiology and cell wall research. J Biol Chem 287:39429–39438. https://doi.org/10.1074/jbc.M112.396598

  38. Ralet M-C, Tranquet O, Poulain D, Moise A, Guillon F (2010) Monoclonal antibodies to rhamnogalacturonan I backbone. Planta 231:1373–1383

  39. Ruprecht C, Mutwil M, Saxe F, Eder M, Nikoloski Z, Persson S (2011) Large-scale co-expression approach to dissect secondary cell wall formation across plant species. Front Plant Sci 2:23. https://doi.org/10.3389/fpls.2011.00023

  40. Scheller HV, Ulvskov P (2010) Hemicelluloses. Ann Rev Plant Biol 61:263–28

  41. Shao MY, Wang XD, Ni M, Bibi N, Yuan SN, Malik W, Zhang HP, Liu YX, Hua SJ (2011) Regulation of cotton fiber elongation by xyloglucan endotransglycosylase/hydrolase genes. Genet Mol Res 10:3771–3782

  42. Shimizu Y, Aotsuka S, Hasegawa O, Kawada T, Sakuno T, Sakai F, Hayashi T (1997) Changes in levels of mRNAs for cell wall-related enzymes in growing cotton fiber cells. Plant Cell Physiol 38:375–378

  43. Singh B, Avci U, Inwood SEE, Grimson MJ, Landgraf J, Mohnen D, Sorensen I, Wilkerson CG, Willats WGT, Haigler CH (2009) A specialized outer layer of the primary cell wall joins elongating cotton fibers into tissue-like bundles. Plant Physiol 150:684–699

  44. Sørensen SO, Pauly M, Bush M, Skjøt M, McCann MC, Borkhardt B, Ulvskov P (2000) Pectin engineering: modification of potato pectin by in vivo expression of an endo-1,4-β-D-galactanase. Proc Natl Acad Sci USA 97:7639–7644

  45. Stalberg K, Stahl U, Stymne S, Ohlrogge J (2009) Characterization of two Arabidopsis thaliana acyltransferases with preference for lysophosphatidylethanolamine. BMC Plant Biol 9:60. https://doi.org/10.1186/1471-2229-9-60

  46. Tang F, Zhu J, Wang T, Shao D (2017) Water deficit effects on carbon metabolism in cotton fibers during fiber elongation phase. Acta Physiol Plant 39:69

  47. Tuttle JR, Nah G, Duke MV, Alexander DC, Guan X, Song Q, Chen ZJ, Scheffler BE, Haigler CH (2015) Metabolic and transcriptomic insights into how cotton fiber transitions to secondary wall synthesis, represses lignification, and prolongs elongation. BMC Genom 16:477

  48. Ulvskov P, Wium H, Bruce D, Jørgensen B, Bruun Qvist K, Skjøt M, Hepworth DM, Borkhardt B, Sørensen S (2005) Biophysical consequences of remodeling the neutral side chains of rhamnogalacturonan I in tubers of transgenic potatoes. Planta 220:609–620

  49. van der Schoot C, Dietrich MA, Storms M, Verbeke JA, Lucas WJ (1995) Establishment of a cell-to-cell communication pathway between separate carpels during gynoecium development. Planta 195:450–455

  50. Verbeke JA (1992) Fusion events during floral morphogenesis. Annu Rev Plant Physiol 43:583–598

  51. Willats WGT, Marcus SE, Knox JP (1998) Generation of a monoclonal antibody specific to (1 → 5)-α-l-arabinan. Carbohydr Res 308:149–152

  52. Yang YW, Bian SM, Yao Y, Liu JY (2008) Comparative proteomic analysis provides new insights into the fiber elongating process in cotton. Proteome Res 7:4623–4637

  53. Yuan D, Tang Z, Wang M, Gao W, Tu L, Jin X, Chen L, He Y, Zhang L, Zhu L, Li Y, Liang Q, Lin Z, Yang X, Liu N, Jin S, Lei Y, Ding Y, Li G, Ruan X, Ruan Y, Zhang X (2015) The genome sequence of Sea-Island cotton (Gossypium barbadense) provides insights into the allopolyploidization and development of superior spinnable fibres. Nat Sci Rep 5:17662. https://doi.org/10.1038/srep17662

  54. Zhong J, Preston JC (2015) Bridging the gaps: evolution and development of perianth fusion. New Phytol 208:330–335

  55. Zhong RQ, Burk DH, Ye ZH (2001) Fibers. A model for studying cell differentiation, cell elongation, and cell wall biosynthesis. Plant Physiol 126:477–479

  56. Zykwinska AW, Ralet MCJ, Garnier CD, Thibault JFJ (2005) Evidence for in vitro binding of pectin side chains to cellulose. Plant Physiol 139:397–407

Download references

Funding

This work was supported by Villum Foundation project PLANET (Grant No. 00009283) and the European Union Seventh Framework Programme under the WallTraC project (Grant agreement No. 263916). This paper reflects the authors’ views only. The European Community is not liable for any use that may be made of the information contained herein. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Correspondence to Peter Ulvskov.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Guo, X., Runavot, J., Bourot, S. et al. Metabolism of polysaccharides in dynamic middle lamellae during cotton fibre development. Planta 249, 1565–1581 (2019). https://doi.org/10.1007/s00425-019-03107-4

Download citation

Keywords

  • Arabinofuranosidase
  • Cuticle
  • Post-genital fusion
  • Rhamnogalacturonan-I
  • Xyloglucan