Developmental features of cotton fibre middle lamellae in relation to cell adhesion and cell detachment in cultivars with distinct fibre qualities
© The Author(s). 2017
Received: 1 September 2016
Accepted: 24 March 2017
Published: 31 March 2017
Cotton fibre quality traits such as fibre length, strength, and degree of maturation are determined by genotype and environment during the sequential phases of cotton fibre development (cell elongation, transition to secondary cell wall construction and cellulose deposition). The cotton fibre middle lamella (CFML) is crucial for both cell adhesion and detachment processes occurring during fibre development. To explore the relationship between fibre quality and the pace at which cotton fibres develop, a structural and compositional analysis of the CFML was carried out in several cultivars with different fibre properties belonging to four commercial species: Gossypium hirsutum, G. barbadense, G. herbaceum and G. arboreum.
Cotton fibre cell adhesion, through the cotton fibre middle lamella (CFML), is a developmentally regulated process determined by genotype. The CFML is composed of de-esterified homogalacturonan, xyloglucan and arabinan in all four fibre-producing cotton species: G. hirsutum, G. barbadense, G. herbaceum and G. arboreum. Conspicuous paired cell wall bulges are a feature of the CFML of two G. hirsutum cultivars from the onset of fibre cell wall detachment to the start of secondary cell wall deposition. Xyloglucan is abundant in the cell wall bulges and in later stages pectic arabinan is absent from these regions.
The CFML of cotton fibres is re-structured during the transition phase. Paired cell wall bulges, rich in xyloglucan, are significantly more evident in the G. hirsutum cultivars than in other cotton species.
KeywordsCotton fibre Middle lamella CFML Cell adhesion Cell wall Gossypium spp. Polysaccharides
Cotton fibres are single-cells and individual fibres start elongating from the seed surface as separate entities. The fibres then adhere together for the fibre elongation phase and detach again during later stages of fibre development. This makes cotton fibre cells an exceptional model to study cytokinesis-independent processes of plant cell adhesion and cell detachment as such processes are rarely present in the same developmental system. Cotton fibre cell development is a very finely regulated process which commences at the day of anthesis and commonly lasts between 50 and 60 days. Fibre development is usually divided into five sequential and overlapping stages: initiation, elongation, transition, secondary cell wall synthesis and desiccation (often misleadingly referred as maturation).
At the initiation stage (from 0 to 3–5 dpa) epidermal cells arise from certain cells at the seed surface with fibre initials and non-fibre cells in a 1:3.7 ratio . One seed can generate approximately 14,500 lint (long) fibres , giving a fibre density of up to 1300 fibres/mm2 . Considering that the flower ovary encloses 4 to 5 carpels (locules) which commonly contain 8 seeds (ovules) each it has been hypothesized that cotton fibres become adhered as a requirement in the highly packed environment inside the locule so that space can be optimised and high turgor pressure maintained during a coordinated fibre elongation phase. At this stage cotton fibres acquire a conical tip shape and elongate in adhered groups in a spiral-like manner [3, 4].
The matrix of polymers between two adhered plant cells is referred to as the middle lamella and the cotton fibre middle lamella (CFML) was first described by Singh et al.  in Gossypium hirsutum, one of the most commercialised species for fibre production. The CFML is a specialized outer layer of primary cell walls that mediates cell adhesion and links several fibres together into tissue-like bundles. The CFML therefore does not originate from the cell plate formed after cytokinesis but upon cell contact between cells at the beginning of the cell elongation phase. This is developmentally distinct from what is commonly considered as plant cell middle lamellae that mediate cell adhesion between daughter cells and that is established from cell plates during cytokinesis [5–9]. Similarly to the cell-plate-derived middle lamellae, the CFML was found to be rich in xyloglucan and de-esterified homogalacturonan polysaccharides using monoclonal antibodies . As fibres elongate, they turn and fold over themselves in a grouped and ordered manner due to the adhesive properties of the CFML until the start of secondary cell wall deposition .
Cotton fibres do not stop elongating abruptly but undergo a transition phase characterized by an increase in the rate of cellulose synthesis  and the formation of the winding layer (similar to the S1 layer in xylem vessels) which is the first of the secondary cell wall layers to be deposited internal to the primary cell wall . It is at this stage that fibres detach from each other at the onset of the major phase of secondary cell wall deposition. The timing of these developmental events depends on the genotype and is also influenced by temperature and environmental conditions during fibre growth [12–15]. Cotton fibre length is a major trait for the textile and derivative industries. Most of the fibre elongation occurs once cells are adhered and before they are detached from each other and secondary cell walls start being deposited. The amount of time that fibres are in the elongation phase partly determines final fibre length. Therefore understanding the mechanisms behind CFML mediation of cell adherence and detachment is important knowledge with the potential to be applied to the improvement of fibre quality.
Many aspects of the CFML remain to be uncovered, such as a comprehensive understanding of its structure and composition and a comparative analysis of the developmental timing for cell adhesion and detachment processes through the CFML in different cotton genotypes. These questions have been addressed here and the different timings of cell adhesion and cell detachment between genotypes with very different fibre qualities (fibre quality parameters described in ) have been determined. Moreover, two distinctive cell wall structural features of the CFML in G. hirsutum cultivars have been identified which may be determinants of the extent of fibre cell elongation in this species. Using immunochemistry techniques we have identified the polysaccharide arabinan to be part of the CFML in addition to pectic HG and xyloglucan. Taken together these results suggest that the timings of cell adhesion and cell detachment mediated by the CFML are different between genotypes, potentially affecting fibre quality traits.
The plants, and associated fibre properties, used in this study were the same as those described . In short, seeds from six domesticated inbred cotton lines (FM966 and Coker312 - G. hirsutum, JFW15 - G. arboreum, Krasnyj - G. herbaceum, China10 and PimaS7 - G. barbadense) were sown in soil compost to which 30 g of Osmocote® 11 N + 11P + 18 K+ 2MgO + TE (working duration 5–6 months) was added to each pot and grown at Bayer Cropscience, Ghent. The settings for the day temperature were 24–26 °C and temperature increased with warm weather up to 30–35 °C with a 16 h photoperiod, except when outside light was >0.25 μmol m−2 s−1. All cotton flowers were tagged on the day of anthesis so that bolls could be harvested at the desired dpa. In one case ovule culture was used. Cotton ovaries were harvested at 1 or 2 dpa and sterilized in 70% ethanol for 5 min and washed with sterile water. All ovules of same ovary were transferred to a Petri dish under sterile conditions. Each Petri dish contained 12 ml of media (MS medium 4 (M0238), macronutrients (50 mM KNO3 as unique nitrogen source, 2 mM KH2PO4, 2 mM MGSO4), vitamins (4 μM nicotinic acid, 4 μM pyridoxine-HCl, 4 μM thiamine-HCl, 1 μM myo-inositol), pH 5, 100 mM glucose, 20 mM fructose, 10 μM IAA and 0.5 μM GA3). Ovules were cultured in the dark at 28 °C and media was changed every 3–5 days.
Resin-embedding of plant materials
Immediately after collection, small regions of fibre tissues were carefully dissected from cotton bolls, causing minimal tissue disruption, and submerged in 4% (v/v) paraformaldehyde in PEM (0.1 M PIPES pH 6.95, 2 mM EGTA, 1 mM MgSO4) buffer. Fixed developing fibres were dehydrated, resin-embedded and sectioned as described previously .
Monoclonal antibodies (mAbs)
Microscopy and immunochemistry procedures
Resin sections were used for immunofluorescence detection of cell wall epitopes. PBS with 5% (w/v) milk protein was added for 30 min at room temperature to prevent non-specific binding. Primary antibodies were used at a 1:5 dilution (except for directly coupled LM19, see below, which was used at 1:1000) in 5% milk/PBS for 1.5 h. Goat anti-rat, anti-mouse or ant-rat IgG Alexa Fluor488 (Life Technologies) were used as secondary antibodies in a 1:100 dilution in 5% milk/PBS and samples were incubated for 1 h. Calcofluor White (Sigma–Aldrich) was used at 0.02 mg/ml in PBS for 5 min for visualization of cell walls. Anti-fade reagent Citifluor glycerol/PBS (Agar Scientific) was used to mount slides. Immunofluorescence imaging was performed using an Olympus BX61 microscope (http://www.olympus-global.com/) equipped with epifluorescence irradiation. Micrographs were obtained with a Hamamatsu ORCA285 camera (Hamamastu, http://www.hamamatsu.com) and PerkinElmer Volocity software. All related and comparative micrographs were captured using equivalent settings, and relevant micrographs were processed in equivalent ways for the generation of datasets. In all cases the area shown in each micrograph is representative of the fibre tissue seen in at least 3 sections analysed from one plant. In the case the FM966 line the micrographs are representative of the analysis of more than 3 plants.
Two distinctive features of cell walls/CFML in cotton fibre tissues
Enlarged CFML regions could be seen in both longitudinal and transversal fibre sections, indicating that they are large three dimensional structures, oval-shaped and filled with particles as stained by Calcofluor White (arrowheads in Fig. 1d). On the other hand, CFML bulges could be followed in serial cross sections indicating that each CFML bulge has the form of a stripe along the fibre as observed in longitudinal sections (arrow in Fig. 1d). Equivalent paired CFML bulges were also present in fibres grown from cultured ovules of FM966 (Fig. 1c) suggesting that their occurrence does not require developing fibres to be inside a locule and, moreover, that the arrangement of paired bulges must be defined by adjacent fibre cells and not by other vegetative parts of the boll.
The pace of cotton fibre development is determined by cotton genotype
Remarkable differences were observed in the pace of fibre development between the cotton species during five sequential time points post anthesis (5, 10, 17 and 25 dpa and mature fibres) when grown under the same conditions as shown in Fig. 1a. The term developmental pace is used here to indicate the speed at which common developmental features, i.e. cell wall adhesion and detachment and secondary cell wall deposition, appeared in different cotton lines. Fibre cell adhesion was obvious by 5 dpa in China10 and FM966 only and enlarged regions of the CFML were already observed in the fibre tissue of these lines (see arrowheads 5 dpa top panels) whereas cell adhesion at the same dpa was incomplete in PimaS7, Krasnyj and JFW15. At 10 dpa all lines showed complete cell adhesion and enlarged regions of the CFML filled with particles were widely present throughout the tissue, except for the JFW15 fibre tissue which showed much fewer enlarged CFML regions. At 17 dpa, the start of cell wall detachment was visible in China10, Krasnyj and JFW15, however fibres in PimaS7 and FM966 were still highly adhered. Cell wall detachment was delayed in the FM966 line compared to the other lines that were observed to start fibre detachment by 17 dpa. Similar cell wall detachment is observed in FM966 only at 25 dpa. Moreover, clear differences in the start and rate of secondary cell wall deposition were also observed. Higher cellulose deposition was seen in the JFW15 line at 17 dpa and, while FM966 fibres showed thinner cell walls compared to any other line at 25 dpa, JFW15 and Krasnyj had extra-thickened cell walls. The higher rate of cellulose deposition in the JFW15 line was very evident at maturation. While the G. arboreum (JFW15) and G. herbaceum (Krasnyj) cultivars showed an early start to secondary cell wall thickening and higher cellulose deposition rates, the G. hirsutum FM966 cultivar showed prolonged cell attachment and specific CFML patterns with a lower cellulose deposition rate than even the G. barbadense lines (China10 and PimaS7). Shorter cell adhesion time and a prolonged secondary cell wall deposition in the JFW15 and Krasnyj cultivars may be correlated with lower quality fibres. It is possible that the timing of fibre elongation and the transition phase (that may be linked to cell adhesion and cell detachment) may ultimately influence the degree of maturation and length of cotton fibres.
CFML dynamics and cell wall glycan composition during fibre development
The CFML from G. barbadense cultivars, as analysed , was found to differ in composition compared to G. hirsutum since fucosylated xyloglucan could not be detected. In our hands, the occurrence of fucosylated xyloglucan in the CFML in G. barbadense as well as in G. hirsutum cultivars was detected by the CCRC-M1 probe  as shown in Fig. 3b. Moreover, treatment of fibre sections with xyloglucanase efficiently removed the xyloglucan LM15 epitope, however it did not abolish Calcofluor White staining (Fig. 3c) suggesting that other β-glycans are present in the CFML currently not detected by any of the available probes.
Cotton fibres possess a middle lamella that does not originate from cytokinesis after cell plate formation but after the cell-to-cell contact of elongating cotton fibres. The CFML brings fibre cells together and helps them to turn and fold for an optimised packing of cells in the very restrictive volume of the cotton locule during the fast cell elongation phase. Comparison of cell and tissue morphologies in five cotton lines at several dpa, indicated that the timing of cell adherence and the transition phase, as well as the speed at which cellulose is deposited in the secondary cell wall were major morphological variables during fibre development. This work has revealed novel features of the CFML: particle-filled enlarged regions and CFML bulges (mostly paired in the G. hirsutum cultivars). Screening with monoclonal antibodies against cell wall polysaccharides revealed the presence of several xyloglucan epitopes including fucosylated xyloglucan (CCRC-M1) in the enlarged CFML regions of both G. hirsutum and G. barbadense lines as well as arabinan in addition to the previously reported de-esterified HG . In contrast, only xyloglucan was abundantly detected in the CFML bulges.
The origin of the particles in the enlarged CFML regions could be the result of the combined action of several cell wall loosening enzymes such as expansins, endoglucanases and endotransglycosylases that release fragments of the cell wall allowing the cells to expand. The degradation of XG-cellulose tethers is essential in cell wall loosening and this degradation can be done by xyloglucanases and xyloglucan endotransglucosylases/hydrolases (XTH) [28–30]. Literature on cotton fibres has repeatedly reported gene upregulation and peak activities of cell wall remodelling enzymes during fibre elongation which then declines during the transition phase [31–34]. Xyloglucan in the CFML regions could be the result of this extensive enzymatic activity in the cell walls that digest and release polymers into the intercellular spaces to create an adhesive middle lamella. In tomato fruit, xyloglucan has been reported to take part in cell adhesion in the pericarp parenchyma . The observations may indicate a role for the re-modelling of xyloglucan and pectin in the control of fibre cohesiveness.
The paired CFML bulges are perhaps best thought of as linear longitudinal cell wall regions and are a clear case of cell wall heterogeneity. The striking pattern of paired bulges was prominent at the transition phase in FM966 and Coker312 cultivars belonging to G. hirsutum species. How the cell regulates the formation of this specific cell wall pattern and for what purpose are intriguing questions. It appears that the CFML organization into a paired pattern is specific to G. hirsutum species and although not essential for fibre development, as it is not obvious in other species, these regular structures along elongating axes may somehow be involved in maintaining axial cell elongation. The paired bulges may be linked in some way to the relatively greater elongation rates of G. hirsutum lines or alternatively they may perhaps facilitate cell wall detachment at the onset of the phase of secondary cell wall deposition as in several cases they appear to mark the extent of an early stage of intercellular space formation. In this they are reminiscent of the electron dense regions of maize leaf palisade cells during development of mesophyll air spaces .
This work provides the first comprehensive in situ biochemical analysis of the processes of cell adhesion and detachment associated with the CFML that take place during cotton fibre development, and identifies two cell wall features in relation to the CFML; enlarged CFML regions and CFML bulges, the latter with a unique paired pattern in cultivars of G. hirsutum species. In conclusion, this work has identified cell wall domains and aspects of cell wall glycan heterogeneity that appear to be linked with fibre cell adhesion and detachment processes which may impact upon fibre quality.
We thank Sue Marcus for providing the monoclonal antibodies used in this study and Martin Fuller for helping with the sectioning of some of the cultivars.
This work was supported by the European Union Seventh Framework Programme [(FP7 2007–2013) under 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.
Availability of data and materials
The datasets during and/or analysed during the current study available from the corresponding author on reasonable request.
MCHG collected cotton fibre materials, performed immunochemical assays, analysed and interpreted data and wrote the manuscript. JLR collected cotton fibre materials and contributed to the data analysis and interpretation of data. FM provided the cotton plants used in this study, guided this work, and contributed to the data analysis and interpretation of the data. JPK guided this work, contributed to the data analysis and interpretation of the data and was a major contributor in the writing of this manuscript. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Consent for publication
Ethics approval and consent to participate
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Stewart JM. Fiber initiation on the cotton ovule (Gossypium hirsutum). Am J Bot. 1975;62(7):723–30.View ArticleGoogle Scholar
- Bowman DT, Van ESbroeck GA, Van’t Hof J, Jividen GM. Ovule fiber cell numbers in modern upland cottons. J Cotton Sci. 2001;5(2):81–3.Google Scholar
- Paiziev AA, Krakhmalev VA. Self-organization phenomena during developing of cotton fibers. Curr Opin Solid St M. 2004;8(2):127–33.View ArticleGoogle Scholar
- Singh B, Avci U, Eichler Inwood SE, Grimson MJ, Landgraf J, Mohnen D, Sorensen I, Wilkerson CG, Willats WG, Haigler CH. A specialized outer layer of the primary cell wall joins elongating cotton fibers into tissue-like bundles. Plant Physiol. 2009;150(2):684–99.View ArticlePubMedPubMed CentralGoogle Scholar
- Nishitani K, Demura T. Editorial: an emerging view of plant cell walls as an Apoplastic intelligent system. Plant Cell Physiol. 2015;56(2):177–9.View ArticlePubMedGoogle Scholar
- Matar D, Catesson AM. Cell plate development and delayed formation of the pectic middle lamella in root meristems. Protoplasma. 1988;146(1):10–7.View ArticleGoogle Scholar
- Albersheim P, Darvill A, Roberts K, Sederoff R, Staehelin A. Plant cell walls. New York: Garland Sciences; 2011.Google Scholar
- Knox JP. Cell adhesion, cell separation and plant morphogenesis. Plant J. 1992;2(2):137–41.View ArticleGoogle Scholar
- Daher FB, Braybrook SA. How to let go: pectin and plant cell adhesion. Front Plant Sci. 2015;6:523.View ArticlePubMedPubMed CentralGoogle Scholar
- Meinert MC, Delmer DP. Changes in biochemical composition of the cell wall of the cotton fiber during development. Plant Physiol. 1977;59(6):1088–97.View ArticlePubMedPubMed CentralGoogle Scholar
- Flint EA. The structure and development of the cotton fibre. Biol Rev. 1950;25(4):414–34.View ArticleGoogle Scholar
- Munger P, Bleiholder H, Hack H, Hess M, Stauß R, van den Boom T, Weber E. Phenological growth stages of the cotton plant (Gossypium hirsutum L.): codification and description according to the BBCH Scale 1. J Agron Crop Sci. 1998;180(3):143–9.View ArticleGoogle Scholar
- Thaker VS, Saroop S, Vaishnav PP, Singh YD. Genotypic variations and influence of diurnal temperature on cotton fibre development. Field Crop Res. 1989;22(2):129–41.View ArticleGoogle Scholar
- Roberts EM, Rao NR, Huang JY, Trolinder NL, Haigler CH. Effects of cycling temperatures on fiber metabolism in cultured cotton ovules. Plant Physiol. 1992;100(2):979–86.View ArticlePubMedPubMed CentralGoogle Scholar
- Liakatas A, Roussopoulos D, Whittington W. Controlled-temperature effects on cotton yield and fibre properties. J Agric Sci. 1998;130(04):463–71.View ArticleGoogle Scholar
- Hernandez-Gomez MC, Runavot J-L, Guo X, Bourot S, Benians TAS, Willats WGT, Meulewaeter F, Knox JP. 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. 2015;56(9):1786–97.View ArticlePubMedPubMed CentralGoogle Scholar
- Lee KD, Knox JP. Resin embedding, sectioning, and immunocytochemical analyses of plant cell walls in hard tissues. In: Žárský V, Cvrčková F, editors. Plant Cell Morphogenesis, vol. 1080. New York: Humana Press; 2014. p. 41–52.View ArticleGoogle Scholar
- Marcus SE, Verhertbruggen Y, Herve C, Ordaz-Ortiz JJ, Farkas V, Pedersen HL, Willats WG, Knox JP. Pectic homogalacturonan masks abundant sets of xyloglucan epitopes in plant cell walls. BMC Plant Biol. 2008;8:60.View ArticlePubMedPubMed CentralGoogle Scholar
- Pedersen HL, Fangel JU, McCleary B, Ruzanski C, Rydahl MG, Ralet M-C, Farkas V, von Schantz L, Marcus SE, Andersen MCF, et al. Versatile high resolution oligosaccharide microarrays for plant glycobiology and cell wall research. J Biol Chem. 2012;287(47):39429–38.View ArticlePubMedPubMed CentralGoogle Scholar
- Puhlmann J, Bucheli E, Swain MJ, Dunning N, Albersheim P, Darvill AG, Hahn MG. Generation of monoclonal antibodies against plant cell-wall polysaccharides. I. Characterization of a monoclonal antibody to a terminal alpha-(1-->2)-linked fucosyl-containing epitope. Plant Physiol. 1994;104(2):699–710.View ArticlePubMedPubMed CentralGoogle Scholar
- Jones L, Seymour GB, Knox JP. Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1[−>]4)-[beta]-D-Galactan. Plant Physiol. 1997;113(4):1405–12.View ArticlePubMedPubMed CentralGoogle Scholar
- Willats WGT, Knox JP. Immunoprofiling of pectic polysaccharides. Anal Biochem. 1999;268(1):143–6.View ArticlePubMedGoogle Scholar
- Willats WG, Marcus SE, Knox JP. Generation of monoclonal antibody specific to (1-->5)-alpha-L-arabinan. Carbohydr Res. 1998;308(1–2):149–52.View ArticlePubMedGoogle Scholar
- Moller I, Marcus SE, Haeger A, Verhertbruggen Y, Verhoef R, Schols H, Ulvskov P, Mikkelsen JD, Knox JP, Willats W. High-throughput screening of monoclonal antibodies against plant cell wall glycans by hierarchical clustering of their carbohydrate microarray binding profiles. Glycoconj J. 2008;25(1):37–48.View ArticlePubMedGoogle Scholar
- Verhertbruggen Y, Marcus SE, Haeger A, Verhoef R, Schols HA, McCleary BV, McKee L, Gilbert HJ, Paul Knox J. Developmental complexity of arabinan polysaccharides and their processing in plant cell walls. Plant J. 2009;59(3):413–25.View ArticlePubMedGoogle Scholar
- Verhertbruggen Y, Marcus SE, Haeger A, Ordaz-Ortiz JJ, Knox JP. An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohydr Res. 2009;344(14):1858–62.View ArticlePubMedGoogle Scholar
- Avci U, Pattathil S, Singh B, Brown VL, Hahn MG, Haigler CH. Cotton fiber cell walls of Gossypium hirsutum and Gossypium barbadense have differences related to loosely-bound xyloglucan. PLoS ONE. 2013;8(2):14.View ArticleGoogle Scholar
- Cosgrove DJ. Loosening of plant cell walls by expansins. Nature. 2000;407(6802):321–6.View ArticlePubMedGoogle Scholar
- Fry SC, Smith RC, Renwick KF, Martin DJ, Hodge SK, Matthews KJ. Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. Biochem J. 1992;282(Pt 3):821–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Hayashi T, Kaida R. Functions of xyloglucan in plant cells. Mol Plant. 2011;4(1):17–24.View ArticlePubMedGoogle Scholar
- Shimizu Y, Aotsuka S, Hasegawa O, Kawada T, Sakuno T, Sakai F, Hayashi T. Changes in levels of mRNAs for cell wall-related enzymes in growing cotton fiber cells. Plant Cell Physiol. 1997;38(3):375–8.View ArticlePubMedGoogle Scholar
- Orford SJ, Timmis JN. Specific expression of an expansin gene during elongation of cotton fibres. Biochim Biophys Acta. 1998;1398(3):342–6.View ArticlePubMedGoogle Scholar
- Michailidis G, Argiriou A, Darzentas N, Tsaftaris A. Analysis of xyloglucan endotransglycosylase/hydrolase (XTH) genes from allotetraploid (Gossypium hirsutum) cotton and its diploid progenitors expressed during fiber elongation. J Plant Physiol. 2009;166(4):403–16.View ArticlePubMedGoogle Scholar
- Shao MY, Wang XD, Ni M, Bibi N, Yuan SN, Malik W, Zhang HP, Liu YX, Hua SJ. Regulation of cotton fiber elongation by xyloglucan endotransglycosylase/hydrolase genes. Genet Mol Res. 2011;10(4):3771–82.View ArticlePubMedGoogle Scholar
- Ordaz-Ortiz JJ, Marcus SE, Knox JP. Cell wall microstructure analysis implicates hemicellulose polysaccharides in cell adhesion in tomato fruit pericarp parenchyma. Mol Plant. 2009;2(5):910–21.View ArticlePubMedGoogle Scholar
- Kollöffel C, Linssen PWT. The formation of intercellular spaces in the cotyledons of developing and germinating pea seeds. Protoplasma. 1984;120(1):12–9.View ArticleGoogle Scholar