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Opinion ARTICLE

Front. Plant Sci., 08 May 2018 | https://doi.org/10.3389/fpls.2018.00623

Is the G-Layer a Tertiary Cell Wall?

Bruno Clair1*, Annabelle Déjardin2, Gilles Pilate2 and Tancrède Alméras3
  • 1CNRS, UMR EcoFoG, AgroParisTech, Cirad, INRA, Université des Antilles, Université de Guyane, Kourou, France
  • 2BioForA, INRA, ONF, Orléans, France
  • 3LMGC, CNRS, Université de Montpellier, Montpellier, France

The G-Layer: an Example of Plant “Muscle”

Plant movements have fascinated scientists at least since Darwin's studies on this issue (Darwin and Darwin, 1880). These movements are enabled by various motor systems (Moulia et al., 2006; Forterre, 2013), and represent basic adaptations to the terrestrial environment since they are necessary to achieve adaptive movements or maintain the orientation of axes during growth (Moulia et al., 2006; Alméras and Fournier, 2009). To enable this function, a diversity of motor systems co-exists in the plant kingdom. In actively elongating organs, the mechanisms are generally based on differential growth. In non-growing soft tissues, a large variety of motor systems makes possible slow or rapid plant movements (Forterre, 2013). In woody stems, normal wood has contractile properties, named maturation strains (Archer, 1986). Combined with an eccentric secondary growth, these strains are able to induce changes in stem curvature (Alméras et al., 2005), sufficient to manage small mechanical disturbances. In the case of strong disturbances, trees generally produce reaction wood. In gymnosperms, the motor system is based on the swelling properties of a specific type of reaction wood named compression wood (Timell, 1986). In angiosperms, most species develop tension wood with fibers having a peculiar cell wall layer (Ghislain and Clair, 2017), historically named gelatinous layer or G-layer. This layer allows for the contraction of the fiber during its maturation, acting as a “muscle” to fulfill various mechanical needs, such as adjusting the shape and orientation of woody plant axes.

The underlying mechanism allowing G-layer to produce contraction, and therefore tensile stress, is not fully understood and still a matter of debate (Alméras and Clair, 2016; Gorshkova et al., 2018). The contraction occurs during cell wall thickening (Clair et al., 2011) synchronously with the swelling of the mesopores (Chang et al., 2015), suggesting a mechanism based on the swelling of the cell wall matrix that results in a strong tensile stress within the cellulosic lattice network (Alméras and Clair, 2016). Alternatively, a mechanism based on the entrapment of matrix material during cellulose aggregation has been proposed (Gorshkova et al., 2015). These two mechanisms may act together in a complementary manner (Alméras and Clair, 2016).

The G-layer was first described in 1860 by Hartig as a cellulosic, gelatinous, mucilaginous or cartilaginous layer. These names derived from its gelatinous aspect, often detached from the other layers of the fiber (after Sanio, 1860 cited by Potter, 1904). Anderson (1927) named this layer “tertiary wall” in a study on flax fibers. Wardrop and Dadswell (1948) used the term “tertiary layer” for tension wood in a single paper, but they later abandoned this term and named it G-layer. Onaka (1949) wrote the first reference monography on reaction wood, using the term G-layer, since then used by all the wood and tree community. In 1964, the International Association of Wood Anatomy Committee named this peculiar layer “G-layer” in the “Multilingual glossary of terms used in wood” (IAWA-Committee, 1964). Lately, in 2008, the G-layer was first described as having a mesoporous structure characteristic of a gel (Clair et al., 2008), providing a rational justification for the term “gelatinous.”

In 2012, Gorshkova and coworkers, working mainly on flax cortical fibers, have reintroduced the term “tertiary cell wall” in place of “G-layer,” giving more and more emphasis to this terminology in their articles (Gorshkova et al., 2012, 2015; Mellerowicz and Gorshkova, 2012; Mikshina et al., 2015), until their recent review paper entitled “Plant ‘muscles’: fibers with a tertiary cell wall” (Gorshkova et al., 2018). In the present paper, we wish to discuss the relevance to name the G-layer a “tertiary cell wall.”

What Is a “Tertiary” Cell Wall?

Plant cell walls are often made of several layers. For example, the normal xylem fibers are made of a primary wall, and of three additional layers most often named S1, S2, and S3, usually gathered under the term “secondary cell wall.” The term “tertiary cell wall” was introduced a long time ago, but this terminology was from the beginning a matter of debate (Leise, 1963). From an ontogenic view, S1, S2, and S3 are all belonging to the secondary cell wall, whereas from a morphological view, S1 can be termed a transition layer, S2 the secondary wall, and S3 a tertiary wall (Wenzl, 1970). The IAWA glossary defined the tertiary wall as the “innermost layer of the cell wall next to the cell-lumen, often with warts” (IAWA-Committee, 1964). For some author, this “innermost layer” included the S3 layer which has a chemical composition different from the S1 and S2 layers (Leise, 1963). For this last author, the tertiary wall did not include the warty layer. The warty layer that develops during the last stages of cell differentiation, “is the remainder of the dying protoplast” (Leise, 1963). On the contrary, some authors propose to include this warty layer into the tertiary wall that is therefore made of two strata, the membranogenic stratum and the warty stratum (Frey-Wyssling, 1976). More recently, it was proposed to restrict the tertiary wall to the warty layer (Barnett and Jeronimidis, 2003). Following this last definition, the tertiary wall results from a post-mortem deposition and is therefore both morphologically and ontogenetically distinct from the secondary wall.

Gorshkova et al. (2018) propose that the G-layer is a tertiary cell wall with the following arguments: (i) “the G-layers are developed after the primary and secondary cell walls”, (ii) they “have distinct composition, architecture, and physical properties”, and (iii) “their formation is regulated by a set of transcription factors that differ from those of the primary and secondary cell walls.” Hereafter we discuss these arguments.

From an Ontogenic View, Is the G-Layer a “Tertiary” Cell Wall?

The terms “primary” and “secondary” bear particular meaning when referring to plant development. They refer to two distinct morphogenetic phases: a phase of extension, and a phase of thickening. This distinction applies to the growth of plant organs, where primary growth refers to organ extension achieved by primary meristems and secondary growth to organ thickening achieved by secondary meristems. It also applies at the tissue scale, where primary tissues developed from the primary meristem during organ elongation and secondary tissues developed from the secondary meristems during organ thickening. Current terminology makes it consistent with the cell wall scale, where extending cells have, most of the time, only a primary cell wall, while cell wall thickens during secondary cell wall deposition. From an ontogenic view, the term “tertiary” implicitly refers to a distinct phase of development, following cell wall extension and thickening. We believe that G-layer development is part of the phase of cell wall thickening, and in consequence, it should be considered as one layer of the secondary cell wall rather than a “tertiary” cell wall.

Indeed, secondary cell walls are always made of distinct layers. When a xylem fiber develops a G-layer, it develops it before the completion of the regular secondary cell wall: the G-layer replaces the S3 and part or all of the S2 layers (Saiki, 1971; Abedini et al., 2015). The differentiation of G-fibers occurs by a modification in the sequence of secondary layers deposition, rather than adding a third phase to the cell wall development. It is even more obvious in the G-fibers of the S1 + G type (without S2 layer). Higaki et al. (2017) have shown that, in this kind of G-fiber, the G-layer presents a smooth variation in organization and composition from the outer to the inner side. The outer part of the G-layer is characterized by a large microfibril angle, the presence of xylan and lignification, very similar to the composition of the S2 layer. The inner part exhibits the more typical G-layer characteristics: low microfibril angle, less xylan, and lignification. Moreover, this study emphasizes the continuity between S to G type in a single layer. Other interesting cases are the tension wood fibers (Ruelle et al., 2007; Ghislain et al., 2016) and phloem fibers (Nakagawa et al., 2012, 2014) of some angiosperm families exhibiting multi-layered cell walls. These multi-layered fibers result from alternating G-layers and S3 layers. The G-layer may not be called tertiary if it is formed before a S3 and again appears to be one of the successive layers of the secondary cell wall.

Each step in a given developmental process is governed by a whole battery of specific transcription factors. However, the cell is also able to respond to environmental cues thanks to the mobilization of some transcription factors. Specific transcription factors have been shown to be upregulated in spruce compression wood (Bedon et al., 2007). These transcription factors (MYB2, MYB4, MYB8) are likely to play a role in lignin metabolism. Likewise, a drought stress induces the expression of specific transcription factors, regulating a specific set of genes, resulting in the development of tissues with modified structure and properties (Fujita et al., 2005; Fichot et al., 2009). In tension wood, it is known that lignin metabolism is switched off when G-layers are deposited. In consequence, it is expected that the expression of related transcription factors is down-regulated. This is observed for example for MYB58 and MYB63 (Gorshkov et al., 2017), which are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation (Zhou et al., 2009). Therefore, the fact that some transcription factors appear differentially expressed between G-layer and S2 layer development is not sufficient to justify the differentiation of a tertiary layer.

From a Morphological View, Is the G-Layer a “Tertiary” Cell Wall?

Based on the similarity between G-layers of poplar tension wood and flax phloem fibers, Gorshkova and collaborators point the fact that “tertiary cell walls have unique chemical and architectural features,” namely that they have cellulose microfibrils aligned with the cell axis, are thick, devoid of lignin and xylan, but contain rhamnogalacturonan-I. In fact, this definition of the G-layer seems too restrictive. Recent publications indicated that the G-layer presents a larger diversity of morphological features: G-layers can be very thin (Fang et al., 2007); G-layers may remain unlignified or become lignified according to the tree species (Roussel and Clair, 2015; Ghislain and Clair, 2017; Higaki et al., 2017); xylans have been evidenced in poplar G-layers (Guedes et al., 2017).

The G-layer is not the only cell wall layer with peculiar features. For example, a conifer compression wood tracheid exhibits a rounded shape that generates intercellular spaces, while its thick internal layer also has many typical traits: an exceptionally high microfibril angle (Timell, 1986), the presence of a specific hemicellulose (Wloch and Hejnowicz, 1983), a high lignin content with a typical GH-type composition (Nimz et al., 1981; Koutaniemi et al., 2007), the occurrence of important amounts of β 1-4 galactan (Altaner et al., 2007), lower mannose (Timell, 1967; Kartal and Lebow, 2001). It also has specific physical properties and is regulated by a specific set of transcription factors (Bedon et al., 2007; Villalobos et al., 2012). Nevertheless, this layer is identified as one of the secondary wall layers. Similarly, we think that the specificity of the G-layer may not justify classifying it apart from the other secondary wall layers. The historical term “G-layer” (as opposed to S-layer) already points clearly enough to its particular nature.

How to Define a G-Layer?

Following the above discussion, we propose to dedicate the term tertiary cell wall to layers issued from a physiological process that fully differs from what happen in the secondary wall. Following Barnett and Jeronimidis (2003), we propose to name tertiary wall, what is built from a cell post-mortem process. This may include the warty layer as well as the late deposition of extractives (low molecular weight organic compounds, mainly terpenoids, alkaloids, or phenolic compounds, synthesized in living parenchyma cells) within the cell wall during heartwood formation.

We propose to define the G-layer as a part of the secondary wall, characterized by (i) an orientation of the cellulose microfibrils nearly parallel to the axis of the fiber, (ii) a matrix with high mesoporosity, and (iii) the ability to generate large contraction of the layer along the fiber axis during maturation, generating axial strain of the fiber or axial tensile stress if the strain is prevented. The G-layer may have microfibril angle in rupture with the surrounding S2 layer or be characterized by a continuous change in microfibril angle from S1 layer to G-layer. When the change in microfibril angle is abrupt, the G-layer is often observed detached from the S2 layer on cross sections. This detachment originates from the release of the high tensile stress in the G-layer during sectioning that produces a large strain in the G-layer, much larger than within the S2 layer. G-layer may be unlignified, partially lignified or fully lignified. Before lignification, the mesoporous texture gives the G-layer its gelatinous appearance, which has given the G-layer its name for more than a century and a half.

Author Contributions

All authors contributed equally to this work. They all participated to build the argumentation and write the paper. They all gave their final approval for publication.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

Authors are supported by a common project StressInTrees funded by the French National Research Agency (ANR-12-BS09-0004). BC and TA benefit from an Investissements d'Avenir grants managed by the French National Research Agency (CEBA, ref. ANR-10-LABX-25-01 and NUMEV, ref. ANR-10-LABX-20).

References

Abedini, R., Clair, B., Pourtahmasi, K., Laurans, F., and Arnould, O. (2015). Cell wall thickening in developing tension wood of artificially bent poplar trees. IAWA J. 36, 44–57. doi: 10.1163/22941932-00000084

CrossRef Full Text | Google Scholar

Alméras, T., and Clair, B. (2016). Critical review on the mechanisms of maturation stress generation in trees. J. R. Soc. Interface 13:20160550. doi: 10.1098/rsif.2016.0550

PubMed Abstract | CrossRef Full Text | Google Scholar

Alméras, T., and Fournier, M. (2009). Biomechanical design and long-term stability of trees: morphological and wood traits involved in the balance between weight increase and the gravitropic reaction. J. Theor. Biol. 256, 370–381. doi: 10.1016/j.jtbi.2008.10.011

PubMed Abstract | CrossRef Full Text | Google Scholar

Alméras, T., Thibaut, A., and Gril, J. (2005). Effect of circumferential heterogeneity of wood maturation strain, modulus of elasticity and radial growth on the regulation of stem orientation in trees. Trees 19, 457–467. doi: 10.1007/s00468-005-0407-6

CrossRef Full Text | Google Scholar

Altaner, C., Knox, J. P., and Jarvis, M. C. (2007). In situ detection of cell wall polysaccharides in Sitka spruce (Picea sitchensis (Bong.) Carrière) wood tissue. Bioresources 2, 284–295. Available online at: http://ojs.cnr.ncsu.edu/index.php/BioRes/article/view/BioRes_02_2_284_295_Altaner_KJ_CellWallPolysaccharides

Google Scholar

Anderson, D. B. (1927). A microchemical study of the structure and development of flax fibers. Am. J. Bot. 14, 187–211.

Google Scholar

Archer, R. R. (1986). Growth stresses and strains in trees. Berlin: Springer Verlag.

Barnett, J. R., and Jeronimidis, G. (2003). Wood Quality and Its Biological Basis. Oxford: Blackwell publishing/CRC Press.

Bedon, F., Grima-Pettenati, J., and Mackay, J. (2007). Conifer R2R3-MYB transcription factors: sequence analyses and gene expression in wood-forming tissues of white spruce (Picea glauca). BMC Plant Biol. 7:17. doi: 10.1186/1471-2229-7-17

PubMed Abstract | CrossRef Full Text | Google Scholar

Chang, S. S., Quignard, F., Alméras, T., and Clair, B. (2015). Mesoporosity changes from cambium to mature tension wood: a new step toward the understanding of maturation stress generation in trees. New Phytol. 205, 1277–1287. doi: 10.1111/nph.13126

PubMed Abstract | CrossRef Full Text | Google Scholar

Clair, B., Alméras, T., Pilate, G., Jullien, D., Sugiyama, J., and Riekel, C. (2011). Maturation stress generation in poplar tension wood studied by synchrotron radiation microdiffraction. Plant Physiol. 155, 562–570. doi: 10.1104/pp.110.167270

PubMed Abstract | CrossRef Full Text | Google Scholar

Clair, B., Gril, J., Di Renzo, F., Yamamoto, H., and Quignard, F. (2008). Characterization of a gel in the cell wall to elucidate the paradoxical shrinkage of tension wood. Biomacromolecules 9, 494–498. doi: 10.1021/bm700987q

PubMed Abstract | CrossRef Full Text | Google Scholar

Darwin, C., and Darwin, F. (1880). The Power of Movements in Plants. London: Murray.

Fang, C.-H., Clair, B., Gril, J., and Alméras, T. (2007). Transverse shrinkage in G-fibers as a function of cell wall layering and growth strain. Wood Sci. Technol. 41, 659–671. doi: 10.1007/s00226-007-0148-3

CrossRef Full Text | Google Scholar

Fichot, R., Laurans, F., Monclus, R., Moreau, A., Pilate, G., and Brignolas, F. (2009). Xylem anatomy correlates with gas exchange, water-use efficiency and growth performance under contrasting water regimes: evidence from Populus deltoides x Populus nigra hybrids. Tree Physiol. 29, 1537–1549. doi: 10.1093/treephys/tpp087

PubMed Abstract | CrossRef Full Text | Google Scholar

Forterre, Y. (2013). Slow, fast and furious: understanding the physics of plant movements. J. Exp. Bot. 64, 4745–4760. doi: 10.1093/jxb/ert230

PubMed Abstract | CrossRef Full Text | Google Scholar

Frey-Wyssling, A. (1976). The plant Cell Wall. Berlin: Borntraeger.

Google Scholar

Fujita, Y., Fujita, M., Satoh, R., Maruyama, K., Parvez, M. M., Seki, M., et al. (2005). AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17, 3470–3488. doi: 10.1105/tpc.105.035659

PubMed Abstract | CrossRef Full Text | Google Scholar

Ghislain, B., and Clair, B. (2017). Diversity in the organisation and lignification of tension wood fibre walls - a review. IAWA J. 38, 245–265. doi: 10.1163/22941932-20170170

CrossRef Full Text | Google Scholar

Ghislain, B., Nicolini, E. A., Romain, R., Ruelle, J., Yoshinaga, A., Alford, M. H., et al. (2016). Multilayered structure of tension wood cell walls in Salicaceae sensu lato and its taxonomic significance. Bot. J. Linn. Soc. 182, 744–756. doi: 10.1111/boj.12471

CrossRef Full Text | Google Scholar

Gorshkov, O., Mokshina, N., Gorshkov, V., Chemikosova, S., Gogolev, Y., and Gorshkova, T. (2017). Transcriptome portrait of cellulose-enriched flax fibres at advanced stage of specialization. Plant Mol. Biol. 93, 431–449. doi: 10.1007/s11103-016-0571-7

PubMed Abstract | CrossRef Full Text | Google Scholar

Gorshkova, T., Brutch, N., Chabbert, B., Deyholos, M., Hayashi, T., Lev-Yadun, S., et al. (2012). Plant fiber formation: State of the art, recent and expected progress, and open questions. Crit. Rev. Plant Sci. 31, 201–228. doi: 10.1080/07352689.2011.616096

CrossRef Full Text | Google Scholar

Gorshkova, T., Chernova, T., Mokshina, N., Ageeva, M., and Mikshina, P. (2018). Plant ‘muscles’: fibers with a tertiary cell wall. New Phytol. 218, 66–72. doi: 10.1111/nph.14997

PubMed Abstract | CrossRef Full Text | Google Scholar

Gorshkova, T., Mokshina, N., Chernova, T., Ibragimova, N., Salnikov, V., Mikshina, P., et al. (2015). Aspen tension wood fibers contain beta-(1—> 4)-galactans and acidic arabinogalactans retained by cellulose microfibrils in gelatinous walls. Plant Physiol. 169, 2048–2063. doi: 10.1104/pp.15.00690

PubMed Abstract | CrossRef Full Text | Google Scholar

Guedes, F. T. P., Laurans, F., Quemener, B., Assor, C., Lainé-Prade, V., Boizot, N., et al. (2017). Non-cellulosic polysaccharide distribution during G-layer formation in poplar tension wood fibers: abundance of rhamnogalacturonan I and arabinogalactan proteins but no evidence of xyloglucan. Planta 246, 857–878. doi: 10.1007/s00425-017-2737-1

PubMed Abstract | CrossRef Full Text | Google Scholar

Higaki, A., Yoshinaga, A., and Takabe, K. (2017). Heterogeneous distribution of xylan and lignin in tension wood G-layers of the S1+G type in several Japanese hardwoods. Tree Physiol. 37, 1767–1775. doi: 10.1093/treephys/tpx144

PubMed Abstract | CrossRef Full Text | Google Scholar

IAWA-Committee (1964). Multilingual Glossary of Terms Used in Wood. Winterthur: Konkordia.

Kartal, S. N., and Lebow, S. T. (2001). Effect of compression wood on leaching and fixation of CCA-C treated red pine. Wood Fiber Sci. 33, 182–192. Available online at: https://wfs.swst.org/index.php/wfs/article/view/674

Google Scholar

Koutaniemi, S., Warinowski, T., Kärkönen, A., Alatalo, E., Fossdal, C. G., Säränpaa, P., et al. (2007). Expression profiling of the lignin biosynthetic pathway in Norway spruce using EST sequencing and real-time RT-PCR. Plant Mol. Biol. 65, 311–328. doi: 10.1007/s11103-007-9220-5

PubMed Abstract | CrossRef Full Text | Google Scholar

Leise, W. (1963). Tertiary wall and warty layer in wood cells. J. Polym. Sci. C 2, 213–219.

Google Scholar

Mellerowicz, E. J., and Gorshkova, T. A. (2012). Tensional stress generation in gelatinous fibres: a review and possible mechanism based on cell-wall structure and composition. J. Exp. Bot. 63, 551–565. doi: 10.1093/jxb/err339

PubMed Abstract | CrossRef Full Text | Google Scholar

Mikshina, P. V., Petrova, A. A., Faizullin, D. A., Zuev, Y. F., and Gorshkova, T. A. (2015). Tissue-specific rhamnogalacturonan I forms the gel with hyperelastic properties. Biochemistry 80, 915–924. doi: 10.1134/S000629791507010X

PubMed Abstract | CrossRef Full Text | Google Scholar

Moulia, B., Coutand, C., and Lenne, C. (2006). Posture control and skeletal mechanical acclimation in terrestrial plants: implications for mechanical modeling of plant architecture. Am. J. Bot. 93, 1477–1489. doi: 10.3732/ajb.93.10.1477

PubMed Abstract | CrossRef Full Text

Nakagawa, K., Yoshinaga, A., and Takabe, K. (2012). Anatomy and lignin distribution in reaction phloem fibres of several Japanese hardwoods. Ann. Bot. 110, 897–904. doi: 10.1093/aob/mcs144

PubMed Abstract | CrossRef Full Text | Google Scholar

Nakagawa, K., Yoshinaga, A., and Takabe, K. (2014). Xylan deposition and lignification in the multi-layered cell walls of phloem fibres in Mallotus japonicus (Euphorbiaceae). Tree Physiol. 34, 1018–1029. doi: 10.1093/treephys/tpu061

PubMed Abstract | CrossRef Full Text | Google Scholar

Nimz, H. H., Robert, D., Faix, O., and Nemr, M. (1981). Carbon-13 NMR Spectra of Lignins, 8. Structural differences between lignins of hardwoods, softwoods, grasses and compression wood. Holzforschung 35, 16–26.

Google Scholar

Onaka, F. (1949). Studies on compression and tension wood. Wood Res. 1, 1–88.

Google Scholar

Potter, M. C. (1904). On the occurrence of cellulose in the xylem of woody stems. Ann. Bot. 18, 121–140.

Google Scholar

Roussel, J. R., and Clair, B. (2015). Evidence of the late lignification of the G-layer in Simarouba tension wood, to assist understanding how non-G-layer species produce tensile stress. Tree Physiol. 35, 1366–1377. doi: 10.1093/treephys/tpv082

PubMed Abstract | CrossRef Full Text | Google Scholar

Ruelle, J., Yoshida, M., Clair, B., and Thibaut, B. (2007). Peculiar tension wood structure in Laetia procera (Poepp.) Eichl. (Flacourtiaceae). Trees 21, 345–355. doi: 10.1007/s00468-007-0128-0

CrossRef Full Text | Google Scholar

Saiki, H. (1971). Cell wall organization of gelatinous fibers in tension wood. Bull. Kyoto Univ. For. 42, 210–220.

Google Scholar

Sanio, C. (1860). Einige Bemerkungen über den Bau des Holzes - I. Ueber den Bau des Týpfels und Hofes. Bot. Zeitung 18, 193–200.

Timell, T. E. (1967). Recent progress in the chemistry of wood hemicelluloses. Wood Sci. Technol. 1, 45–70.

Google Scholar

Timell, T. E. (1986). Compression Wood in Gymnosperms. 2. Occurence of Stem, Branch and Root. Compression Woods, Factors Causing Formation of Compression Wood, Gravitropism and Compression Wood, Physiology of Compression Wood Formaion, Inheritance of Compression Wood. Berlin: Springer Verlag.

Villalobos, D. P., Díaz-Moreno, S. M., Said el, S. S., Cañas, R. A., Osuna, D., Van Kerckhoven, S. H., et al. (2012). Reprogramming of gene expression during compression wood formation in pine: coordinated modulation of S-adenosylmethionine, lignin and lignan related genes. BMC Plant Biol. 12:100. doi: 10.1186/1471-2229-12-100

PubMed Abstract | CrossRef Full Text | Google Scholar

Wardrop, A. B., and Dadswell, H. E. (1948). The nature of reaction wood I - The structure and properties of tension wood fibres. Aust. J. Sci. Res. Ser. B 1, 3–16.

Google Scholar

Wenzl, H. F. J. (1970). The Chemical Technology of Wood. New York, NY: Academic press.

Google Scholar

Wloch, W., and Hejnowicz, Z. (1983). Location of laricinian in compression wood tracheids. Acta Soc. Bot. Polon 52, 201–203.

Google Scholar

Zhou, J., Lee, C., Zhong, R., and Ye, Z. H. (2009). MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21, 248–266. doi: 10.1105/tpc.108.063321

PubMed Abstract | CrossRef Full Text | Google Scholar

Keywords: gelatinous layer, G-layer, secondary cell wall, tertiary cell wall, tension wood, flax, maturation stress

Citation: Clair B, Déjardin A, Pilate G and Alméras T (2018) Is the G-Layer a Tertiary Cell Wall? Front. Plant Sci. 9:623. doi: 10.3389/fpls.2018.00623

Received: 09 February 2018; Accepted: 19 April 2018;
Published: 08 May 2018.

Edited by:

Peter Ulvskov, University of Copenhagen, Denmark

Reviewed by:

Simcha Lev-Yadun, University of Haifa, Israel
Stuart Thompson, University of Westminster, United Kingdom

Copyright © 2018 Clair, Déjardin, Pilate and Alméras. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Bruno Clair, bruno.clair@cnrs.fr