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Cellular events during interfascicular cambium ontogenesis in inflorescence stems of Arabidopsis

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Abstract

Development of cambium and its activity is important for our knowledge of the mechanism of secondary growth. Arabidopsis thaliana emerges as a good model plant for such a kind of study. Thus, this paper reports on cellular events taking place in the interfascicular regions of inflorescence stems of A. thaliana, leading to the development of interfascicular cambium from differentiated interfascicular parenchyma cells (IPC). These events are as follows: appearance of auxin accumulation, PIN1 gene expression, polar PIN1 protein localization in the basal plasma membrane and periclinal divisions. Distribution of auxin was observed to be higher in differentiating into cambium parenchyma cells compared to cells within the pith and cortex. Expression of PIN1 in IPC was always preceded by auxin accumulation. Basal localization of PIN1 was already established in the cells prior to their periclinal division. These cellular events initiated within parenchyma cells adjacent to the vascular bundles and successively extended from that point towards the middle region of the interfascicular area, located between neighboring vascular bundles. The final consequence of which was the closure of the cambial ring within the stem. Changes in the chemical composition of IPC walls were also detected and included changes of pectic epitopes, xyloglucans (XG) and extensins rich in hydroxyproline (HRGPs). In summary, results presented in this paper describe interfascicular cambium ontogenesis in terms of successive cellular events in the interfascicular regions of inflorescence stems of Arabidopsis.

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References

  • Agusti J, Greb T (2013) Going with the wind – adaptive dynamics of plant secondary meristems. Mech Dev 130:34–44

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Agusti J, Lichtenberger R, Schwarz M, Nehlin L, Greb T (2011a) Characterization of transcriptome remodeling during cambium formation identifies MOL1 and RUL1 as opposing regulators of secondary growth. PLoS Genet 7:e1001312. doi:10.1371/journal.pgen.1001312

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Agusti J, Herold S, Schwartz M, Sanchez P, Ljung K, Dun EA, Brewer PB, Beveridge CA, Sieberer T, Sehr E, Greb T (2011b) Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. PNAS 7:1–6

    Google Scholar 

  • Aloni R, Zimmermann MH (1983) The control of vessel size and density along the plant axis – a new hypothesis. Differentiation 24:203–208

    Article  Google Scholar 

  • Altamura MM, Possenti M, Matteucci A, Baima S, Ruberti I, Morelli G (2001) Development of the vascular system in the inflorescence stem of Arabidopsis. New Phytol 151:81–389

    Article  Google Scholar 

  • Balla J, Kalousek P, Reinöhl V, Friml J, Procházka S (2011) Competitive canalization of PIN-dependent auxin flow from axillary buds controls pea bud outgrowth. Plant J 65:571–577

    Article  CAS  PubMed  Google Scholar 

  • Benitez-Alfonso Y, Faulkner C, Miyashima S, Helariutta Y, Maule A (2013) Symplastic intercellular connectivity regulates lateral root patterning. Dev Cell 26:136–147

    Article  CAS  PubMed  Google Scholar 

  • Benkova E, Ivanchenko MG, Friml J, Shishkova S, Dubrovsky JG (2009) A morphogenetic trigger: is there an emerging concept in plant developmental biology? Trends Plant Sci 14:189–193

    Google Scholar 

  • Bhalerao RP, Bennett MJ (2003) The case for morphogens in plants. Nat Cell Biol 5:939–943

    Article  CAS  PubMed  Google Scholar 

  • Blakeslee JJ, Bandyopadhyay A, Lee OR, Mravec J, Titapiwatanakun B, Sauer M, Makam SN, Cheng Y, Bouchard R, Adamec J, Geisler M, Nagashima A, Sakai T, Martinoia E, Friml J, Peer WA, Murphy AS (2007) Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell 19:131–147

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Busse JS, Evert RF (1999) Vascular differentiation and transition in the seedling of Arabidopsis thaliana (Brassicaceae). Int J Plant Sci 160:41–251

    Article  Google Scholar 

  • Campanoni P, Nick P (2005) Auxin-dependent cell division and cell elongation. 1-Naphtaleneacetic acid and 2,4-dichlorophenoxyacetic acid activate different pathways. Plant Physiol 137:939–948

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Carpita N, Tierney M, Campbell M (2001) Molecular biology of the plant cell wall: searching for the genes that define structure, architecture and dynamics. Plant Mol Biol 47:1–5

    Article  CAS  PubMed  Google Scholar 

  • Chaffey N (1999) Cambium: old challenges – new opportunities. Trees 13:138–151

    Article  Google Scholar 

  • Chaffey N (2002) Why is there so little research into the cell biology of the secondary vascular system of trees? New Phytol 153:213–223

    Article  Google Scholar 

  • Chaffey N, Cholewa E, Regan S, Sundberg B (2002) Secondary xylem development in Arabidopsis: a model for wood formation. Physiol Plant 114:594–600

    Article  CAS  PubMed  Google Scholar 

  • Chen JG (2001) Dual auxin signaling pathways control cell elongation and division. J Plant Growth Regul 20:255–264

    Article  CAS  Google Scholar 

  • Darley CP, Forrester AM, McQueen-Mason SJ (2001) The molecular basis of plant cell wall extension. Plant Mol Biol 47:179–195

    Article  CAS  PubMed  Google Scholar 

  • Dettmer J, Elo A, Helariuta Y (2008) Hormone interactions during vascular development. Plant Mol Biol. doi:10.1007/s11103-008-9374-9

    PubMed  Google Scholar 

  • Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119:71–84

    CAS  PubMed  Google Scholar 

  • Dubois T, Guedira M, Dubois J, Vasseur J (1990) Direct somatic embryogenesis in roots of Cichorium: is callose an early marker? Ann Bot 65:539–545

    Google Scholar 

  • Dubrovsky JG, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml J, Shishkova S, Celenza J, Benkova E (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. PNAS 105:8790–8794

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Evert RF (2006) Esau’s plant anatomy: meristems, cells, and tissues of the structure, function, and development, 3rd edn. Wiley, New Jersey

    Book  Google Scholar 

  • Friml J (2010) Subcellular trafficking of PIN auxin carriers in auxin transport. EJCB 89:231–235

    CAS  Google Scholar 

  • Friml J, Wiśniewska J (2005) Auxin as an intercellular signal. Intercellular communication in plants. In: Fleming A (ed), Blackwell Publishing Limited, pp 1–25

  • Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish apical–basal axis of Arabidopsis. Nature 426:147–153

    Article  CAS  PubMed  Google Scholar 

  • Fukuda H (1997) Tracheary element differentiation. Plant Cell 9:1147–1156

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V, Bandyopadhyay A, Titapiwatanakun B, Peer WA, Bailly A, Richards EL, Ejendal KF, Smith AP, Baroux C, Grossniklaus U, Müller A, Hrycyna CA, Dudler R, Murphy AS, Martinoia E (2005) Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J 44:179–194

    Article  CAS  PubMed  Google Scholar 

  • Gonneau M, Höfte H, Vernhettes S (2012) Fluorescent tags to explore cell wall structure and dynamics. Front Plant Sci 3:1–6

    Article  Google Scholar 

  • Gray-Mitsumine M, Mellerowicz EJ, Abe H, Schrader J, Winzell A, Sterky F, Blomqvist K, McQueen-Mason S, Teeri TT, Sundberg B (2004) Expansins abundant in secondary xylem belong to subgroup A of the α-expansin gene family. Plant Physiol 135:1552–1564

    Article  Google Scholar 

  • Hayashi T, Kaida R (2011) Functions of xyloglucan in plant cells. Mol Plant 4:17–24

    Article  CAS  PubMed  Google Scholar 

  • Hellgren JM, Olofsson K, Sundberg B (2004) Patterns of auxin distribution during gravitational induction of reaction wood in poplar and pine. Plant Physiol 135:212–220

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: ß-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jose-Estanyol M, Puigdomenech P (2000) Plant cell wall glycoproteins and their genes. Plant Physiol Biochem 38:97–108

    CAS  Google Scholar 

  • Kitakura S, Vanneste S, Robert S, Löfke C, Teichmann T, Tanaka H, Friml J (2011) Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell 23:1920–1931

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Knox JP (1997) The use of antibodies to study the architecture and developmental regulation of plant cell walls. Int Rev Cytol 171:79–120

    Article  CAS  PubMed  Google Scholar 

  • Ko JH, Han KH (2004) Arabidopsis whole-transcriptome profiling defines the features of coordinated regulations that occur during secondary growth. Plant Mol Biol 55:433–453

    Article  CAS  PubMed  Google Scholar 

  • Ko JH, Han KH, Park S, Yang J (2004) Plant body weight-induced secondary growth in Arabidopsis and its transcription phenotype revealed by whole-transcriptome profiling. Plant Physiol 135:1069–1083

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kramer EM (2006) Wood grain pattern formation: a brief review. J Plant Growth Regul 25:290–301

    Article  CAS  Google Scholar 

  • Kurczyńska EU, Gaj MD, Ujczak A, Mazur E (2007) Histological analysis of direct somatic embryogenesis in Arabidopsis thaliana (L.) Heynh. Planta 226:619–628

    Article  PubMed  Google Scholar 

  • Larson PR (1994) The vascular cambium. Development and structure. Springer, Berlin

    Book  Google Scholar 

  • Lev-Yadun S (1994) Induction of sclereid differentiation in the pith of Arabidopsis thaliana (L.) Heynh. J Exp Bot 45:1845–1849

    Article  CAS  Google Scholar 

  • Lev-Yadun S (1997) Fibres and fibre-sclereids in wild-type Arabidopsis thaliana. Ann Bot 80:125–129

    Article  Google Scholar 

  • Lev-Yadun S, Flaishman MA (2001) The effect of submergence on ontogeny of cambium and secondary xylem and on fiber lignification in inflorescence stems of Arabidopsis. IAWA J 22:159–169

    Article  Google Scholar 

  • Little CHA, Wareing PF (1981) Control of cambial activity and dormancy in Picea sitchensis by indol-3-ylacetic and abscisic acids. Can J Bot 59:1480–1493

    Article  CAS  Google Scholar 

  • Little CHA, MacDonald JE, Olsson O (2002) Involvement of indole-3-acetic acid in fascicular and interfascicular cambial growth and interfascicular extraxylary fiber differentiation in Arabidopsis thaliana inflorescence stems. Int J Sci 163:519–529

    CAS  Google Scholar 

  • Mazur E, Kurczynska EU (2012) Rays, intrusive growth and storied cambium in Arabidopsis thaliana. Protoplasma 249:217–220

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mellerowicz EJ, Baucher M, Sundberg B, Boerjan W (2001) Unravelling cell wall formation in the woody dicot stem. Plant Mol Biol 47:239–274

    Article  CAS  PubMed  Google Scholar 

  • Nieminen KM, Kauppinen L, Helariutta Y (2004) A weed for wood? Arabidopsis as a genetic model for xylem development. Plant Physiol 135:653–659

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nishikubo N, Takahashi J, Roos AA, Derba-Maceluch M, Piens K, Brumer H, Teeri TT, Stälbrand H, Mellerowicz EJ (2011) Xyloglucan endo-transglycosylase-mediated xyloglucan rearrangement in developing wood of hybrid aspen. Plant Physiol 155:399–413

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • O’Brien TP, McCully ME (1981) The study of plant structure. Principles and selected methods. Termarcarphi Pty Ltd, Melbourne

    Google Scholar 

  • Oh S, Park S, Han KH (2003) Transcriptional regulation of secondary growth in Arabidopsis thaliana. J Exp Bot 393:2709–2722

    Article  Google Scholar 

  • Paciorek T, Sauer M, Balla J, Wiśniewska J, Friml J (2006) Immunocytochemical technique for protein localization in sections of plant tissues. Nat Protoc 1:104–107

    Article  CAS  PubMed  Google Scholar 

  • Paul-Victor C, Rowe N (2011) Effect of mechanical perturbation on the biomechanics, primary growth and secondary tissue development of inflorescence stems of Arabidopsis thaliana. Ann Bot 107:209–218

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pedroso MC, Pais MS (1992) A scanning electron microscope and x-ray microanalysis study during induction of morphogenesis in Camellia japonica L. Plant Sci 87:99–108

    Article  CAS  Google Scholar 

  • Petrašek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertova D, Wiśniewska J, Tadele Z, Kubeš M, Čovanova M, Dhonukshe P, Skupa P, Benkova E, Perry L, Křecek P, Lee OR, Fink GR, Giesler M, Murphy AS, Luschnig C, Zažimalova E, Friml J (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312:914–918

    Article  PubMed  Google Scholar 

  • Philipson WR, Ward JM, Butterfield BG (1971) The vascular cambium. Its development and activity. Chapman and Hall, London

    Google Scholar 

  • Romberger JA, Hejnowicz Z, Hill JF (1993) The vascular cambium. Plant structure: function and development. Springer, Berlin, pp 354–385

    Google Scholar 

  • Sachs T (1975) The induction of transport channels by auxin. Planta 127:201–206

    Article  CAS  PubMed  Google Scholar 

  • Sachs T (1981) The control of the patterned differentiation of vascular tissues. Adv Bot Res 9:151–262

    Article  Google Scholar 

  • Sauer M, Balla J, Luschnig C, Wiśniewska J, Reinöhl V, Friml J, Benkova E (2006) Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev 20:2902–2911

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schrader J, Baba K, May ST, Palme K, Bennett M, Bhalerao RP, Sandberg G (2003) Polar auxin transport in the wood-forming tissues of hybrid aspen is under simultaneous control of development and environmental signals. Proc Natl Acad Sci 100:10096–10101

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sehr EM, Agusti J, Lehner R, Farmer EE, Schwartz M, Greb T (2010) Analysis of secondary growth in Arabidopsis shoot reveals a positive role of jasmonate signalling in cambium formation. Plant J 63:811–822

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Suer S, Agusti J, Sanchez P, Schwartz M, Greb T (2011) WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell 23:3247–3259

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sundberg B, Uggla C, Tuominen H (2000) Auxin gradients and cambial growth. In: Savidge R, Barnett J, Napier R (eds) Cell and molecular biology of wood formation (SEB Experimental Biology Reviews). BIOS, Oxford, pp 169–188

    Google Scholar 

  • Takeda T, Furuta Y, Awano K, Mitsuishi Y, Hayashi T (2002) Suppression and acceleration of cell elongation by integration of xyloglucans in pea stem segments. PNAS 99:9055–9060

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tchorbadjieva MI (2005) Protein markers for somatic embryogenesis. Plant Cell Monogr (2). In: Mujib A, Šamaj J (eds) Somatic embryogenesis. Springer, Berlin, pp 215–233

    Google Scholar 

  • Tuominen H, Puech L, Regan S, Fink S, Olsson O, Sundberg B (2000) Cambial-region-specific expression of the Agrobacterium iaa genes in transgenic aspen visualized by a linked uidA reporter gene. Plant Physiol 123:531–542

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Uggla C, Moritz T, Sandberg G, Sundberg B (1996) Auxin as a positional signal in pattern formation in plants. Proc Natl Acad Sci 93:9282–9296

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Uggla C, Mellerowicz EJ, Sundberg B (1998) Indole-3-acetic acid controls cambial growth in Scots pine by positional signaling. Plant Physiol 117:113–121

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Gulifoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vatén A, Dettmer J, Wu S, Stierhof YD, Miyashima S, Yadav SR, Roberts CJ, Campilho A, Bulone V, Lichtenberger R, Lehesranta S, Mahönen AP, Kim JY, Jokitalo E, Sauer N, Scheres B, Nakajima K, Carlsbecker A, Gallangher KL, Helariutta Y (2011) Callose biosynthesis regulates symplastic trafficking during root development. Dev Cell 21:1144–1155

    Article  PubMed  Google Scholar 

  • Vieten A, Vanneste S, Wiśniewska J, Benkova E, Benjamins R, Beeckman T, Luschnig C, Friml J (2005) Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development 132:4521–4531

    Article  CAS  PubMed  Google Scholar 

  • Wabnik K, Kleine-Vehn J, Balla J, Sauer M, Naramoto S, Reinöhl V, Merks RMH, Govaerts W, Friml J (2010) Emergence of tissue polarization from synergy of intracellular and extracellular auxin signaling. Mol Syst Biol 6:1–15

    Article  Google Scholar 

  • Wang X, Sager R, Cui W, Zhang C, Lee JY (2013) Salicylic acid regulates plasmodesmata closure during innate immune responses in Arabidopsis. Plant Cell. doi:10.1105/tpc.113.110676

    Google Scholar 

  • Willats WGT, Steele-King CG, McCartney L, Orfila C, Marcus SE, Knox JP (2000) Making and using antibody probes to study plant cell walls. Plant Physiol Biochem 38:27–36

    CAS  Google Scholar 

  • Ye ZH, Varner JE (1991) Tissue-Specific Expression of Cell Wall Proteins in Developing Soybean Tissues. Plant Cell 3:23–37

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ye ZH, Song YR, Marcus A, Varner JE (1991) Comparative localization of three classes of cell wall proteins. Plant J 1:175–183

    Article  CAS  PubMed  Google Scholar 

  • Zhao C, Johnson BJ, Kositsup B, Beers EP (2000) Exploiting secondary growth in Arabidopsis. Construction of xylem and bark cDNA libraries and cloning of three xylem endopeptidases. Plant Physiol 123:1185–1196

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We express our gratitude to Professor Paul Knox for the anti-extensin LM1 antibody probe for HRGPs detection and Dr. Timothy C. Baldwin (University of Wolverhampton) for his assistance in the preparation of the English version of this manuscript.

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The authors declare that they have no conflict of interest.

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  1. Laboratory of Cell Biology, Faculty of Biology and Environmental Protection, University of Silesia, Jagiellońska 28, 40-032, Katowice, Poland

    Ewa Mazur & Ewa U. Kurczyńska

  2. Institute of Science and Technology (IST), 3400, Klosterneuburg, Austria

    Jiři Friml

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  1. Ewa Mazur
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Mazur, E., Kurczyńska, E.U. & Friml, J. Cellular events during interfascicular cambium ontogenesis in inflorescence stems of Arabidopsis . Protoplasma 251, 1125–1139 (2014). https://doi.org/10.1007/s00709-014-0620-5

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