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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

Abstract

Main conclusion

RG-I and AGP, but not XG, are associated to the building of the peculiar mechanical properties of tension wood.

Hardwood trees produce tension wood (TW) with specific mechanical properties to cope with environmental cues. Poplar TW fibers have an additional cell wall layer, the G-layer responsible for TW mechanical properties. We investigated, in two poplar hybrid species, the molecules potentially involved in the building of TW mechanical properties. First, we evaluated the distribution of the different classes of non-cellulosic polysaccharides during xylem fiber differentiation, using immunolocalization. In parallel, G-layers were isolated and their polysaccharide composition determined. These complementary approaches provided information on the occurrence of non-cellulosic polysaccharides during G-fiber differentiation. We found no evidence of the presence of xyloglucan (XG) in poplar G-layers, whereas arabinogalactan proteins (AGP) and rhamnogalacturonan type I pectins (RG-I) were abundant, with an apparent progressive loss of RG-I side chains during G-layer maturation. Similarly, the intensity of immunolabeling signals specific for glucomannans and glucuronoxylans varies during G-layer maturation. RG-I and AGP are best candidate matrix components to be responsible for TW mechanical properties.

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Abbreviations

AGP:

Arabinogalactan protein

HG:

Homogalacturonan

HPAEC-PAD:

High-performance anion exchange chromatography with pulsed amperometric detection

MALDI-TOF MS:

Matrix-assisted laser desorption ionization-time-of-flight mass spectrometry

ML:

Middle lamella

OW:

Opposite wood

PCW:

Primary cell wall

RG-I (II):

Rhamnogalacturonan type I (type II) pectin

TW:

Tension wood

XG:

Xyloglucan

XGO:

Xyloglucan oligomers

References

  • Almeras T, 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Almeras T, 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

    CAS  Article  PubMed  Google Scholar 

  • Anderson CT (2016) We be jammin’: an update on pectin biosynthesis, trafficking and dynamics. J Exp Bot 67:495–502

    CAS  Article  PubMed  Google Scholar 

  • Arend M (2008) Immunolocalization of (1,4)-beta-galactan in tension wood fibers of poplar. Tree Physiol 28:1263–1267

    CAS  Article  PubMed  Google Scholar 

  • Bamber RK (1987) The origin of growth stresses: a rebuttal. IAWA Bull 8:80–84

    Article  Google Scholar 

  • Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54:484–489

    CAS  Article  PubMed  Google Scholar 

  • Bowling AJ, Vaughn KC (2008) Immunocytochemical characterization of tension wood: gelatinous fibers contain more than just cellulose. Am J Bot 95:655–663

    Article  PubMed  Google Scholar 

  • Boyd JD (1972) Tree growth stresses—part V: evidence of an origin in differentiation and lignification. Wood Sci Technol 6:251–262

    Article  Google Scholar 

  • Chang SS, Quignard F, Almeras T, 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

    CAS  Article  PubMed  Google Scholar 

  • Clair B, Almeras T, Sugiyama J (2006) Compression stress in opposite wood of angiosperms: observations in chestnut, mani and poplar. Ann For Sci 63:507–510

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Clair B, Almeras T, Pilate G, Jullien D, Sugiyama J, Riekel C (2011) Maturation stress generation in poplar tension wood studied by synchrotron radiation microdiffraction. Plant Physiol 155:562–570

    CAS  Article  PubMed  Google Scholar 

  • Clausen MH, Willat WGT, Knox JP (2003) Synthetic methyl hexagalacturonate hapten inhibitors of antihomogalacturonan monoclonal antibodies LM7, JIM5 and JIM7. Carbohydr Res 338:1797–1800

    CAS  Article  PubMed  Google Scholar 

  • Decou R, Lhernould S, Laurans F, Sulpice E, Leplé JC, Déjardin A, Pilate G, Costa G (2009) Cloning and expression analysis of a wood-associated xylosidase gene (PtaBXL1) in poplar tension wood. Phytochemistry 70:163–172

    CAS  Article  PubMed  Google Scholar 

  • Ding SY, Himmel ME (2006) The maize primary cell wall microfibril: a new model derived from direct visualization. J Agric Food Chem 54:597–606

    CAS  Article  PubMed  Google Scholar 

  • Donaldson LA, Knox JP (2012) Localization of cell wall polysaccharides in normal and compression wood of radiata pine: relationships with lignification and microfibril orientation. Plant Physiol 158:642–653

    CAS  Article  PubMed  Google Scholar 

  • Driouich A, Baskin TI (2008) Intercourse between cell wall and cytoplasm exemplified by arabinogalactan proteins and cortical microtubules. Am J Bot 95:1491–1497

    CAS  Article  PubMed  Google Scholar 

  • Ellis M, Egelund J, Schultz CJ, Bacic A (2010) Arabinogalactan proteins: key regulators at the cell surface. Plant Physiol 153:403–419

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Fujita M, Saiki H, Harada H (1974) Electron microscopy of microtubules and cellulose microfibrils in secondary wall formation of poplar tension wood fibers. Mokuzai Gakkaishi 20:147–156

    Google Scholar 

  • Galvez-Lopez D, Laurens F, Quemener B, Lahaye M (2011) Variability of cell wall polysaccharides composition and hemicellulose enzymatic profile in an apple progeny. Int J Biol Macromol 49:1104–1109

    CAS  Article  PubMed  Google Scholar 

  • Gens JS, Fujiki M, Pickard BG (2000) Arabinogalactan protein and wall-associated kinase in a plasmalemmal reticulum with specialized vertices. Protoplasma 212:115–134

    CAS  Article  PubMed  Google Scholar 

  • Gorshkova T, Mokshina NE, Chernova TE, Ibragimova NN, Salnikov VV, Mikshina PV, Tryfona T, Banasiak A, Immerzeel P, Dupree P, Mellerowicz E (2015) Aspen tension wood fibers contain β-(1 → 4)-galactans and acidic arabinogalactans retained by cellulose microfibrils in gelatinous walls. Plant Physiol 169:2048–2063

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goswami L, Dunlop JWC, Jungnikl K, Eder M, Gierlinger N, Coutand C, Jeronimidis G, Fratzl P, Burgert I (2008) Stress generation in the tension wood of poplar is based on the lateral swelling power of the G-layer. Plant J 56:531–538

    CAS  Article  PubMed  Google Scholar 

  • Gritsch C, Wan Y, Mitchell RAC, Shewry PR, Hanley SJ, Karp A (2015) G-fibre cell wall development in willow stems during tension wood induction. J Exp Bot 66:6447–6459. doi:10.1093/jxb/erv358

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Guillon F, Tranquet O, Quillien L, Utille JP, Ortiz JJO, Saulnier L (2004) Generation of polyclonal and monoclonal antibodies against arabinoxylans and their use for immunocytochemical location of arabinoxylans in cell walls of endosperm of wheat. J Cereal Sci 40:167–182

    CAS  Article  Google Scholar 

  • Hoebler C, Barry JL, David A, Delort-Laval J (1989) Rapid acid hydrolysis of plant cell wall polysaccharides and simplified quantitative determination of their neutral monosaccharides by gas-liquid chromatography. J Agric Food Chem 37:360–367

    CAS  Article  Google Scholar 

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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Jones L, Milne JL, Ashford D, McQueen-Mason SJ (2003) Cell wall arabinan is essential for guard cell function. Proc Natl Acad Sci USA 100:11783–11788

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Kaku T, Serada S, Baba K, Tanaka F, Hayashi T (2009) Proteomic analysis of the G-layer in poplar tension wood. J Wood Sci 55:250–257

    CAS  Article  Google Scholar 

  • Karas M, Ehring H, Nordhoff E, Stahl B, Strupat K, Hillenkamp F, Grehl M, Krebs B (1993) Matrix-assisted laser desorption/ionization mass spectrometry with additives to 2,5-dihydroxybenzoic acid. Org Mass Spectrom 28:1476–1481

    CAS  Article  Google Scholar 

  • Kim JS, Daniel G (2012) Distribution of glucomannans and xylans in poplar xylem and their changes under tension stress. Planta 236:35–50

    CAS  Article  PubMed  Google Scholar 

  • Knox JP, Linstead J, Peart J, Cooper C, Roberts K (1991) Developmentally regulated epitopes of cell surface arabinogalactan proteins and their relation to root tissue pattern formation. Plant J 1:317–326

    CAS  Article  PubMed  Google Scholar 

  • Knox JP, Peart J, Neill SJ (1995) Identification of novel cell surface epitopes using leaf epidermal strip assay system. Planta 196:266–270

    CAS  Google Scholar 

  • Koutaniemi S, Guillon F, Tranquet O, Bouchet B, Tuomainen P, Virkki L, Petersen HL, Willats WG, Saulnier L, Tenkanen M (2012) Substituent-specific antibody against glucuronoxylan reveals close association of glucuronic acid and acetyl substituents and distinct labeling patterns in tree species. Planta 236:739–751

    CAS  Article  PubMed  Google Scholar 

  • Lafarguette F, Leplé JC, Déjardin A, Laurans F, Costa G, Lesage-Descauses MC, Pilate G (2004) Poplar genes encoding fasciclin-like arabinogalactan proteins are highly expressed in tension wood. New Phytol 164:107–121

    CAS  Article  Google Scholar 

  • Lahaye M, Quemener B, Causse M, Seymour GB (2012) Hemicellulose fine structure is affected differently during ripening of tomato lines with contrasted texture. Int J Biol Macromol 51:462–470

    CAS  Article  PubMed  Google Scholar 

  • Lamport DTA, Varnai P (2013) Periplasmic arabinogalactan glycoproteins act as a calcium capacitor that regulates plant growth and development. New Phytol 197:58–64

    CAS  Article  PubMed  Google Scholar 

  • Lamport DTA, Kieliszewski MJ, Showalter AM (2006) Salt stress upregulates periplasmic arabinogalactan-proteins: using salt stress to analyse AGP function. New Phytol 169:479–492

    CAS  Article  PubMed  Google Scholar 

  • Lee KJD, Cornuault V, Manfield IW, Ralet MC, Knox JP (2013) Multi-scale spatial heterogeneity of pectic rhamnogalacturonan I (RG-I) structural features in tobacco seed endosperm cell walls. Plant J 75:1018–1027

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Macquet A, Ralet MC, Loudet O, Kronenberger J, Mouille G, Marion-Poll A, North HM (2007) A naturally occurring mutation in an Arabidopsis accession affects a beta-d-galactosidase that increases the hydrophilic potential of rhamnogalacturonan I in seed mucilage. Plant Cell 19:3990–4006

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Maekaji K (1974) The mechanism of gelation of konjac mannan. Agric Biol Chem 38:315–321

    CAS  Article  Google Scholar 

  • Marcus SE, Verhertbruggen Y, Herve C, Ordaz-Ortiz JJ, Farkas V, Pedersen HL, Willats WGT, Knox JP (2008) Pectic homogalacturonan masks abundant sets of xyloglucan epitopes in plant cell walls. BMC Plant Biol 8:60

    Article  PubMed  PubMed Central  Google Scholar 

  • Marcus SE, Blake AW, Benians TAS, Lee KJD, Poyser C, Donaldson L, Leroux O, Rogowski A, Petersen HL, Boraston A, Gilbert HJ, Willats WGT, Knox JP (2010) Restricted access of proteins to mannan polysaccharides in intact plant cell walls. Plant J 64:191–203

    CAS  Article  PubMed  Google Scholar 

  • McCartney L, Steele-Kingy CG, Jordan E, Knox JP (2003) Cell wall pectic (1-4)-beta-d-galactan marks the acceleration of cell elongation in the Arabidopsis seedling root meristem. Plant J 33:447–454

    CAS  Article  PubMed  Google Scholar 

  • McCartney L, Marcus SE, Knox JP (2005) Monoclonal antibodies to plant cell wall xylans and arabinoxylans. J Histochem Cytochem 53:543–546

    CAS  Article  PubMed  Google Scholar 

  • Mellerowicz EJ, Immerzeel P, Hayashi T (2008) Xyloglucan: the molecular muscle of trees. Ann Bot 102:659–665

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Mikshina PV, Idiyatullin BZ, Petrova AA, Shashkov AS, Zuev YF, Gorshkova TA (2015) Physicochemical properties of complex rhamnogalacturonan I from gelatinous cell walls of flax fibers. Carbohydr Polym 117:853–861

    CAS  Article  PubMed  Google Scholar 

  • Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11:266–277

    CAS  Article  PubMed  Google Scholar 

  • Nishikubo N, Awano T, Banasiak A, Bourquin V, Ibatullin F, Funada R, Brumer H, Teeri TT, Hayashi T, Sundberg B, Mellerowicz EJ (2007) Xyloglucan endo-transglycosylase (XET) functions in gelatinous layers of tension wood fibers in poplar—a glimpse into the mechanism of the balancing act of trees. Plant Cell Physiol 48:843–855

    CAS  Article  PubMed  Google Scholar 

  • Norberg PH, Meier H (1966) Physical and chemical properties of the gelatinous layer in tension wood fibres of aspen (Populus tremula L.). Holzforschung 20:174–178

    CAS  Article  Google Scholar 

  • Pauly M, Gille S, Liu L, Mansoori N, de Souza A, Schultink A, Xiong G (2013) Hemicellulose biosynthesis. Planta 238:627–642

    CAS  Article  PubMed  Google Scholar 

  • Peaucelle A, Braybrook SA, Le Guillou L, Bron E, Kuhlemeier C, Höfte H (2011) Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. Curr Biol 21:1720–1726

    CAS  Article  PubMed  Google Scholar 

  • Pennell RI, Knox JP, Scofield GN, Selvendran RR, Roberts K (1989) A family of abundant plasma membrane-associated glycoproteins related to the arabinogalactan proteins is unique to flowering plants. J Cell Biol 108:1967–1977

    CAS  Article  PubMed  Google Scholar 

  • Pennell RI, Janniche L, Kjellbom P, Scofield GN, Peart JM, Roberts K (1991) Developmental regulation of a plasma membrane arabinogalactan protein epitope in oilseed rape flowers. Plant Cell 3:1317–1326

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Pilate G, Chabbert B, Cathala B, Yoshinaga A, Leplé J-C, Laurans F, Lapierre C, Ruel K (2004) Lignification and tension wood. CR Biol 327:889–901

    CAS  Article  Google Scholar 

  • Puhlmann J, Bucheli E, Swain MJ, Dunning N, Albersheim P, Darvill AG, Hahn MG (1994) 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 104:699–710

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  • Richardson KC, Jarett L, Finke EH (1960) Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Biotech Histochem 35:313–323

    CAS  Google Scholar 

  • Roach MJ, Mokshina NY, Badhan A, Snegireva AV, Hobson N, Deyholos MK, Gorshkova TA (2011) Development of cellulosic secondary walls in flax fibers requires beta-galactosidase. Plant Physiol 156:1351–1363

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289

    CAS  Article  PubMed  Google Scholar 

  • Seifert GJ, Roberts K (2007) The biology of arabinogalactan proteins. Annu Rev Plant Biol 58:137–161

    CAS  Article  PubMed  Google Scholar 

  • Shinohara N, Sunagawa N, Tamura S, Yokoyama R, Ueda M, Igarashi K, Nishitani K (2017) The plant cell-wall enzyme AtXTH3 catalyses covalent cross-linking between cellulose and cello-oligosaccharide. Sci Rep 7:46099

    Article  PubMed  PubMed Central  Google Scholar 

  • Steffan W, Kovac P, Albersheim P, Darvill AG, Hahn MG (1995) Characterization of a monoclonal antibody that recognizes an arabinosylated (1-6)-beta-d-galactan epitope in plant complex carbohydrates. Carbohydr Res 275:295–307

    CAS  Article  PubMed  Google Scholar 

  • Tan L, Eberhard S, Pattathil S, Warder C, Glushka J, Yuan CH, Hao ZY, Zhu X, Avci U, Miller JS, Baldwin D, Pham C, Orlando R, Darvill A, Hahn MG, Kieliszewski MJ, Mohnen D (2013) An Arabidopsis cell wall proteoglycan consists of pectin and arabinoxylan covalently linked to an arabinogalactan protein. Plant Cell 25:270–287

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Thimm JC, Burritt DJ, Ducker WA, Melton LD (2000) Celery (Apium graveolens L.) parenchyma cell walls examined by atomic force microscopy: effect of dehydration on cellulose microfibrils. Planta 212:25–32

    CAS  Article  PubMed  Google Scholar 

  • Thimm JC, Burritt DJ, Ducker WA, Melton LD (2009) Pectins influence microfibril aggregation in celery cell walls: an atomic force microscopy study. J Struct Biol 168:337–344

    CAS  Article  PubMed  Google Scholar 

  • Timell TE (1969) The chemical composition of tension wood. Sven Papperstidn 72:173–181

    CAS  Google Scholar 

  • Ulvskov P, Wium H, Bruce D, Jorgensen B, Qvist KB, Skjot M, Hepworth D, Borkhardt B, Oxenbøll Sørensen S (2005) Biophysical consequences of remodeling the neutral side chains of rhamnogalacturonan I in tubers of transgenic potatoes. Planta 220:609–620

    CAS  Article  PubMed  Google Scholar 

  • Verhertbruggen Y, Marcus SE, Haeger A, Ordaz-Ortiz JJ, Knox JP (2009) An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohydr Res 344:1858–1862

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  • Willats WGT, Gilmartin PM, Mikkelsen JD, Knox JP (1999) Cell wall antibodies without immunization: generation and use of de-esterified homogalacturonan block-specific antibodies from a naive phage display library. Plant J 18:57–65

    CAS  Article  PubMed  Google Scholar 

  • Yamamoto H (2004) Role of the gelatinous layer on the origin of the physical properties of the tension wood. J Wood Sci 50:197–208

    CAS  Article  Google Scholar 

  • Zykwinska A, Gaillard C, Buleon A, Pontoire B, Garnier C, Thibault JF, Ralet MC (2007a) Assessment of in vitro binding of isolated pectic domains to cellulose by adsorption isotherms, electron microscopy, and X-ray diffraction methods. Biomacromol 8:223–232

    CAS  Article  Google Scholar 

  • Zykwinska A, Thibault JF, Ralet MC (2007b) Organization of pectic arabinan and galactan side chains in association with cellulose microfibrils in primary cell walls and related models envisaged. J Exp Bot 58:1795–1802

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

This work was partly supported by the “Stress in Trees” Project ANR-12-BS09-0004. FTP Guedes was funded by CAPES (Ministry of Education, Brazil). We would like to thank Pierre-Ivan Raynal (Electron Microscopy Facility, François Rabelais University and University Hospital of Tours, France) for technical support for MET observations. Confocal microscopy was carried out in Xylobiotech Facility funded by the IA project “Xyloforest” (ANR-10-EQPX-16).

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Guedes, F.T.P., Laurans, F., Quemener, B. et al. 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 (2017). https://doi.org/10.1007/s00425-017-2737-1

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Keywords

  • Cellulose aggregation
  • G-fiber maturation
  • Hemicellulose
  • Hydrogel formation
  • Mechanical strain
  • Pectin