Abstract
Plant cell wall extensibility is mediated, in part, by xyloglucan endotransglycosylases/hydrolases (XTH) that are able to cleave and reattach xyloglucan polymers that make up the hemicelluloses matrix of type I cell walls. In Arabidopsis and other plants, XTHs are encoded by relatively large gene families that are regulated in specific spatial and temporal patterns. In silico screening of a cotton expressed sequence tag (EST) database identified 23 sequences with close sequence similarity to Arabidopsis XTH coding sequences. Analysis of full-length cotton cDNAs derived from these ESTs allow for the identification of three distinct GhXTH cDNAs (denoted GhXTH1, GhXTH2 and GhXTH3) based primarily on their 3′ untranslated sequences. The three GhXTH genes were expressed differently with GhXTH1 predominantly expressed in elongating cotton fibers. The function of GhXTH1 in mediating cotton fiber elongation was analyzed in transgenic cotton plants that express a transgene consisting of the GhXTH1 coding sequence under transcriptional control of the CaMV 35S promoter. Plants that over-expressed GhXTH1 had increased XTH activity and produced mature cotton fibers that were between 15 and 20% longer than wild-type cotton plants under both greenhouse and field growth conditions. Segregation analysis showed that the 35S::GhXTH1 transgene acts as a dominant fiber length allele in transgenic cotton. These results confirm that GhXTH1 is the predominant XTH in elongating fibers and its expression limits cotton fiber elongation.
Similar content being viewed by others
Abbreviations
- ABA:
-
Abscisic acid
- AFIS:
-
Advanced fiber information system
- BAC:
-
Bacterial artificial chromosome
- BL:
-
Brassinolide
- BLAST:
-
Basic local alignment search tool
- DPA:
-
Days post-anthesis
- EST:
-
Expressed sequence tag
- HVI:
-
High volume instrument
- NAA:
-
Naphthalene acetic acid
- SFC:
-
Short fiber content
- XEH:
-
Xyloglucan hydrolase
- XET:
-
Xyloglucan endotransglycosylase
- XTH:
-
Xyloglucan endotransglycosylase/hydrolase
References
Akamatsu T, Hanzawa Y, Ohtake Y, Takahashi T, Nishitani K, Komeda Y (1999) Expression of endoxyloglucan transferase genes in acaulis mutants of Arabidopsis. Plant Physiol 121:715–722
Antosiewicz DM, Purugganan MM, Polisensky DH, Braam J (1997) Cellular localization of Arabidopsis xyloglucan endotransglycosylase-related proteins during development and after wind stimulation. Plant Physiol 115:1319–1328
Baumann MJ, Eklof JM, Michel G, Kallas AM, Teeri TT, Czjzek M, Brumer H (2007) Structural evidence for the evolution of xyloglucanase activity from xyloglucan endo-transglycosylases: biological implications for cell wall metabolism. Plant Cell 19:1947–1963
Berlin JD (1986) The outer epidermis of the cotton seed. In: Mauney JR Stewart JMcD (eds) Cotton physiology. The Cotton Foundation, Memphis, pp 375–414
Bourquin V, Nishikubo N, Abe H, Brumer H, Denman S, Eklund M, Christiernin M, Teeri TT, Sundberg B, Mellerowicz EJ (2002) Xyloglucan endotransglycosylases have a function during the formation of secondary cell walls of vascular tissues. Plant Cell 14:3073–3088
Campbell P, Braam J (1999) Xyloglucan endotransglycosylases: diversity of genes, enzymes and potential wall-modifying functions. Trends Plant Sci 4:361–366
Carpita NC (1996) Structure and biogenesis of the cell walls of grasses. Annu Rev Plant Physiol Plant Mol Biol 47:445–476
Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30
Catalá C, Rose JKC, York WS, Albersheim P, Darvill AG, Bennett AB (2001) Characterization of a tomato xyloglucan endotransglycosylase gene that is down-regulated by auxin in etiolated hypocotyls. Plant Physiol 127:1180–1192
Cho HT, Cosgrove DJ (2000) Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:9783–9788
Choi D, Lee Y, Cho HT, Kende H (2003) Regulation of expansin gene expression affects growth and development in transgenic rice plants. Plant Cell 15:1386–1398
Cosgrove DJ (2001) Wall structure and wall loosening, a look backwards and forward. Plant Physiol 125:131–134
Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861
Cutillas-Iturralde A, Lorences EP (1997a) Effect of xyloglucan oligosaccharides on growth, viscoelastic properties, and long-term extension of pea shoots. Plant Physiol 113:103–109
Dong J, Kohel R, Zhang H (2001) Bacterial artificial chromosome (BAC) libraries constructed from the genetic standard of upland cotton. http://algodon.tamu.edu/htdocs-cotton/tm1bac.html
Eklöf JM, Brumer H (2010) The XTH gene family: an update on enzyme structure, function, and phylogeny in xyloglucan remodeling. Plant Physiol 153:456–466
Feinberg AP, Vogelstein B (1984) A technique for radio labeling DNA restriction fragments to a high specific activity. Anal Biochem 132:6–13
Fry SC, Smith RC, Renwick KF, Martin DJ, Hodge SK, Matthews KJ (1992) Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. Biochem J 282:821–828
Guo Y, Saha S, Yu JZ, Jenkins JN, Kohel RJ, Scheffler BE, Stelly DM (2008) BAC-derived SSR markers chromosome locations in cotton. Euphytica 161:361–370
Haigler CH, Zhang D, Wilkerson CG (2007) Biotechnological improvement of cotton fibre maturity. Physiol Plant 124:285–294
Herbers K, Lorences EP, Barrachina C, Sonnewald U (2001) Functional characterisation of Nicotiana tabacum xyloglucan endotransglycosylase (NtXET-1): generation of transgenic tobacco plants and changes in cell wall xyloglucan. Planta 212:279–287
Levy S, Maclachlan G, Staehelin LA (1997) Xyloglucan sidechains modulate binding to cellulose during in vitro binding assays as predicted by conformational dynamics simulations. Plant J 11:373–386
Li Y, Liu D, Tu L, Zhang X, Wang L, Zhu L, Tan J, Deng F (2009) Suppression of GhAGP4 gene expression repressed the initiation and elongation of cotton fiber. Plant Cell Rep 29:193–202
Link BM, Cosgrove DJ (1998) Acid-growth response and alpha-expansins in suspension cultures of bright yellow 2 tobacco. Plant Physiol 118:907–916
Luo M, **ao Y, Li X, Lu X, Deng W, Li D, Hou L, Hu M, Li Y, Pei Y (2007) GhDET2, a steroid 5alpha-reductase, plays an important role in cotton fiber cell initiation and elongation. Plant J 51:419–430
Machado A, Wu Y, Yang Y, Llewellyn DJ, Dennis ES (2009) The MYB transcription factor GhMYB25 regulates early fibre and trichome development. Plant J 59:52–62
Malinowski R, Filipecki M, Noyszewski A, Malepszy S (2004) Two xyloglucan endotrans-glucosylase/hydrolase related genes (CS-XTH1 and Cs-XTH3) expressed during cucumber (Cucumis sativus L.) somatic embryogenesis are also regulated by wounding and mechanical stimuli. Acta Physiol Plant 26:38–39
Maris A, Suslov D, Fry SC, Verbelen JP, Vissenberg K (2009) Enzymic characterization of two recombinant xyloglucan endotransglucosylase/hydrolase (XTH) proteins of Arabidopsis and their effect on root growth and cell wall extension. J Exp Bot 60:3959–3972
McQueen-Mason S, Cosgrove DJ (1994) Disruption of hydrogen bonding between plant cell wall polymers by proteins that induce wall extension. Proc Natl Acad Sci USA 91:6574–6578
McQueen-Mason SJ, Cosgrove DJ (1995) Expansin mode of action on cell walls Analysis of wall hydrolysis, stress relaxation, and binding. Plant Physiol 107:87–100
McQueen-Mason S, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4:1425–1433
McQueen-Mason SJ, Fry SC, Durachko DM, Cosgrove DJ (1993) The relationship between xyloglucan endotransglycosylase and in vitro cell wall extension in cucumber hypocotyls. Planta 190:327–331
Michailidis G, Argiriou A, Darzentas N, Tsaftaris A (2008) 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
Miedes E, Herbers K, Sonnewald U, Lorences EP (2010) Overexpression of a cell wall enzyme reduces xyloglucan depolymerization and softening of transgenic tomato fruits. J Agric Food Chem 58:5708–5713
Nishitani K, Vissenberg K (2007) Roles of the XTH family in the expanding cell. Springer, Berlin, pp 89–116
O’Neill MA, York WS (2003) The composition and structure of plant primary cell walls. In: Rose JKC (ed) The plant cell wall. CRC Press, Boca Raton, pp 1–54
Payton P, Allen RD, Trolinder NL, Holaday AS (1997) Over-expression of chloroplast-targeted Mn superoxide dismutase in cotton (Gossypium hirsutum L., cv. Coker 312) does not alter the reduction ofphotosynthesis after short exposures to low temperature and high light intensity. Photosyn Res 52:233–244
Payton P, Webb RP, Kornyeyev D, Allen RD, Holaday AS (2001) Protecting cotton photosynthesis during moderate chilling at high light intensity by increasing chloroplastic antioxidant enzyme activity. J Exp Bot 52:2345–2354
Pu L, Li Q, Fan X, Yang W, Xue Y (2008) The R2R3 MYB transcription factor GhMYB109 is required for cotton fiber development. Genetics 180:811–820
Quesada V, Dean C, Simpson GG (2005) Regulated RNA processing in the control of Arabidopsis flowering. Int J Dev Biol 49:773–780
Rose JKC, Bennett AB (1999) Cooperative disassembly of the cellulose–xyloglucan network of plant cell walls: parallels between cell expansion and fruit ripening. Trends Plant Sci 4:176–183
Rose JKC, Braam J, Fry SC, Nishitani K (2002) The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol 43:1421–1435
Ruan YL, Llewellyn DJ, Furbank RT (2003) Suppression of sucrose synthase gene expression represses cotton fiber cell initiation, elongation, and seed development. Plant Cell 15:952–964
Saladié M, Rose JK, Cosgrove DJ, Catalá C (2006) Characterization of a new xyloglucan endotransglucosylase/hydrolase (XTH) from ripening tomato fruit and implications for the diverse modes of enzymic action. Plant J 47:282–295
Schmidt R (2002) Plant genome evolution: lessons from comparative genomics at the DNA level. Plant Mol Biol 48:21–37
Shin YK, Yum H, Kim ES, Cho H, Gothandam KM, Hyun J, Chung YY (2006) BcXTH1, a Brassica campestris homologue of Arabidopsis XTH9, is associated with cell expansion. Planta 224:32–41
Sulova Z, lednicka M, Farkas V (1995) A colorimetric assay for xyloglucan-endotransglycosylase from germinating seeds. Anal Biochem 229:80–85
Thompson JE, Fry SC (2001) Restructuring of wall-bound xyloglucan by transglycosylation in living plant cells. Plant J 26:23–34
Tian B, Pan Z, Lee JY (2007) Widespread mRNA polyadenylation events in introns indicate dynamic interplay between polyadenylation and splicing. Genome Res 17:156–165
Tiwari SC, Wilkins TA (1995) Cotton (Gossypium hirsutum) seed trichomes expand via diffuse growing mechanism. Can J Bot 73:746–757
Van Sandt VS, Suslov D, Verbelen JP, Vissenberg K (2007) Xyloglucan endotransglucosylase activity loosens a plant cell wall. Ann Bot 100:1467–1473
Vissenberg K, Fry SC, Verbelen J-P (2001) Root hair initiation is coupled to a highly localized increase of xyloglucan endotransglycoslyase action in Arabidopsis roots. Plant Physiol 127:1125–1135
Vissenberg K, Van Sandt V, Fry SC, Verbelen J-P (2003) Xyloglucan endotransglucosylase action is high in the root elongation zone and in trichoblasts of all vascular plants from Selaginella to Zea mays. J Exp Bot 54:335–344
Vissenberg K, Fry SC, Pauly M, Hofte H, Verbelen JP (2005a) XTH acts at the microfibril–matrix interface during cell elongation. J Exp Bot 56:673–683
Vissenberg K, Oyama M, Osato Y, Yokoyama R, Verbelen J-P, Nishitani K (2005b) Differential expression of AtXTH17, -18, -19 and -20 genes in Arabidopsis roots. Physiological roles in specification in cell wall construction. Plant Cell Physiol 46:192–200
Wagstaff C, Clarkson GJ, Zhang F, Rothwell SD, Fry SC, Taylor G, Dixon MS (2010) Modification of cell wall properties in lettuce improves shelf life. J Exp Bot 61:1239–1248
Wan CH, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem 223:7–12
Wang HY, Wang J, Gao P, Jiao GL, Zhao PM, Li Y, Wang GL, **a GX (2009) Down-regulation of GhADF1 gene expression affects cotton fibre properties. Plant Biotechnol J 7:13–23
Wang H, Guo Y, Lv F, Zhu H, Wu S, Jiang Y, Li F, Zhou B, Guo W, Zhang T (2010a) The essential role of GhPEL gene, encoding a pectate lyase, in cell wall loosening by depolymerization of the de-esterified pectin during fiber elongation in cotton. Plant Mol Biol 72:397–406
Wang J, Wang HY, Zhao PM, Han LB, Jiao GL, Zheng YY, Huang SJ, **a GX (2010b) Over-expression of a profilin (GhPFN2) promotes the progression of developmental phases in cotton fibers. Plant Cell Physiol. doi:10.1093/pcp/pcq086
**ao YH, Li DM, Yin MH, Li XB, Zhang M, Wang YJ, Dong J, Zhao J, Luo M, Luo XY, Hou L, Hu L, Pei Y (2010) Gibberellin 20-oxidase promotes initiation and elongation of cotton fibers by regulating gibberellin synthesis. J. Plant Physiol 167:829–837
Yokoyama R, Nishitani K (2001) A comprehensive expression analysis of all members of a gene family encoding cell-wall enzymes allowed us to predict cis-regulatory regions involved in cell-wall construction in specific organs of Arabidopsis. Plant Cell Physiol 42:1025–1033
Yokoyama R, Rose JKC, Nishitani K (2004) A surprising diversity and abundance of xyloglucan endotranglucosylase/hydrolases in rice Classification and expression analysis. Plant Physiol 134:1088–1099
Zenoni S, Reale L, Tornielli GB, Lanfaloni L, Porceddu A, Ferrarini A, Moretti C, Zamboni A, Speghini A, Ferranti F, Pezzotti M (2004) Downregulation of the Petunia hybrida alpha-expansin gene PhEXP1 reduces the amount of crystalline cellulose in cell walls and leads to phenotypic changes in petal limbs. Plant Cell 16:295–308
Acknowledgments
This work is dedicated to the memory of Ms. Jeanie Heinen who worked tirelessly on the development of transgenic cotton plants used in this study. Jeanie succumbed to cancer, after a courageous battle. The authors also thank Dr. Norma Trolinder and Mr. Greg Cartwright for help with cotton transformation procedures, Dr. Phat Dang for technical assistance, and Dr. John Yu for providing the cotton BAC library filters, BAC clones and DNA samples. This work was supported, in part, by a research contract from the Toyobo Research Institute to RDA.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lee, J., Burns, T.H., Light, G. et al. Xyloglucan endotransglycosylase/hydrolase genes in cotton and their role in fiber elongation. Planta 232, 1191–1205 (2010). https://doi.org/10.1007/s00425-010-1246-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-010-1246-2