Synchronized tissue polarization during regeneration or de novo vascular tissue formation is a plant-specific example of intercellular communication and coordinated development. According to the canalization hypothesis, the plant hormone auxin serves as polarizing signal that mediates directional channel formation underlying the spatio-temporal vasculature patterning. A necessary part of canalization is a positive feedback between auxin signaling and polarity of the intercellular auxin flow. The cellular and molecular mechanisms of this process are still poorly understood, not the least, because of a lack of a suitable model system. We show that the main genetic model plant, Arabidopsis (Arabidopsis thaliana) can be used to study the canalization during vascular cambium regeneration and new vasculature formation. We monitored localized auxin responses, directional auxin-transport channels formation, and establishment of new vascular cambium polarity during regenerative processes after stem wounding. The increased auxin response above and around the wound preceded the formation of PIN1 auxin transporter-marked channels from the primarily homogenous tissue and the transient, gradual changes in PIN1 localization preceded the polarity of newly formed vascular tissue. Thus, Arabidopsis is a useful model for studies of coordinated tissue polarization and vasculature formation after wounding allowing for genetic and mechanistic dissection of the canalization hypothesis.

Department of Cell Biology Faculty of Biology and Environmental Protection University of Silesia in Katowice 40 032 Katowice Jagiellońska 28 Poland

Institute of Science and Technology 3400 Klosterneuburg Austria

Mendel Centre for Plant Genomics and Proteomics Central European Institute of Technology CZ 62 500 Brno Czech Republic

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Scarpella E., Marcos D., Friml J. & Berleth T. Control of leaf vascular patterning by polar auxin transport. Genes Dev. 20, 1015–1027 (2006). PubMed PMC

Sauer M. PubMed PMC

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

Turing A. M. The chemical basis of morphogenesis. Philos. Trans. R. Soc. B-Biol. Sci. 237, 37–72 (1952).

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

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

Gälweiler PubMed

Friml J. PubMed

Friml J., Wiśniewska J., Benková E., Mendgen K. & Palme K. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in PubMed

Friml J. PubMed

Friml J. PubMed

Reinhardt D. PubMed

Petrášek J. PubMed

Wiśniewska J. PubMed

Benková E. PubMed

Dhonukshe P. PubMed

Paciorek T. PubMed

Robert S. PubMed PMC

Wabnik K. PubMed PMC

Grones P. PubMed

Wenzel C. L., Schuetz M., Yu Q. & Mattsson J. Dynamics of PubMed

Flaishman M. A., Loginovsky K. & Lev-Yadun S. Regenerative xylem in inflorescence stems of

Aloni R. & Sachs T. The three-dimensional structure of primary phloem systems. Planta 113, 345–353 (1973). PubMed

Aloni R. & Zimmermann M. H. Length, width, and pattern of regenerative vessels along strips of vascular tissue. Bot. Gaz. 145, 50–54 (1984).

Lev-Yadun S. Wound effects arrest wave phenomena in the secondary xylem of

Lev-Yadun S. The distance to which wound effects influence the structure of secondary xylem of decapitated PubMed

Philipson W. R., Ward J. M. & Butterfield B. G. The Vascular Cambium: Its Development and Activity. Chapman & Hall, London, United Kingdom (1971).

Uggla C., Moritz T., Sandberg G. & Sundberg B. Auxin as a positional signal in pattern formation in plants. Proc. Natl. Acad. Sci. USA 93, 9282–9286 (1996). PubMed PMC

Uggla C., Mellerowicz E. J. & Sundberg B. Indole-3-acetic acid controls cambial growth in Scots pine by positional signaling. Plant Physiol. 117, 113–121 (1998). PubMed PMC

Uggla C., Magel E., Moritz T. & Sundberg B. Function and dynamics of auxin and carbohydrates during earlywood/latewood transition in Scots pine. Plant Physiol. 125, 2029–2039 (2001). PubMed PMC

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

Wilson J. W. & Wilson P. M. W. The position of regenerating cambia, a new hypothesis. New Phytol. 60, 63–73 (1961).

Hejnowicz Z. Tensional stress in the cambium and its developmental significance. Am. J. Bot. 67, 1–5 (1980).

Jacobs W. P. The role of auxin in differentiation of xylem around a wound. Am. J. Bot. 39, 301–309 (1952).

Sachs T. Cell polarity and tissue patterning in plants. Development Suppl. 1, 83–93 (1991).

Sachs T. & Cohen D. Circular vessels and the control of vascular differentiation in plants. Differentiation 21, 22–26 (1982).

Hejnowicz Z. & Kurczyńska E. U. Occurrence of circular vessels above axillary buds in stems of woody plants. Acta Soc. Bot. Pol. 56, 415–419 (1987).

Lev-Yadun S. & Aloni R. Vascular differentiation in branch junctions of trees: circular patterns and functional significance. Trees 4, 49–54 (1990).

Ko J. H., Han K. H., Park S. & Yang J. Plant body weight-induced secondary growth in Arabidopsis and its transcription phenotype revealed by whole-transcriptome profiling. Plant Physiol. 135, 1069–1083 (2004). PubMed PMC

Mazur E., Kurczyńska E. U. & Friml J. Cellular events during interfascicular cambium ontogenesis in inflorescence stems of PubMed

Busse J. S. & Evert R. F. Vascular differentiation and transition in the seedling of

Chaffey N., Cholewa E., Regan S. & Sundberg B. Secondary xylem development in PubMed

Ragni L. & Hardtke C. S. Small but thick enough, the Arabidopsis hypocotyl as a model to study secondary growth. Physiol. Plant. 151, 164–171 (2014). PubMed

Lev-Yadun S. & Flaishman M. A. 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 (2001).

Sehr E. M. PubMed PMC

Agusti J. PubMed PMC

Paul-Victor C. & Rowe N. Effect of mechanical perturbation on the biomechanics, primary growth and secondary tissue development in inflorescence stems of PubMed PMC

Sanchez P., Nehlin L. & Greb T. From thin to thick: major transitions during stem development. Trends Plant Sci. 17, 113–121 (2012). PubMed PMC

Mazur E. & Kurczyńska E. U. Rays, intrusive growth, and storied cambium in the inflorescence stems of PubMed PMC

Baima S. PubMed

Baima S. PubMed PMC

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

Altamura

Lev-Yadun S. Fibres and fibre-sclereids in wild-type

Nieminen K. M., Kauppinen L. & Helariutta Y. A weed for wood? Arabidopsis as a genetic model for xylem development. Plant Physiol. 135, 653–659 (2004). PubMed PMC

Melnyk C. W., Schuster C., Leyser O. & Meyerowitz E. M. A Developmental Framework for Graft Formation and Vascular Reconnection in PubMed PMC

Rolland-Lagan A. G. & Prusinkiewicz P. Reviewing models of auxin canalization in the context of leaf vein pattern formation in PubMed

Parry G. & Estelle M. Auxin receptors: a new role for F-box proteins. Curr. Opin. Cell Biol. 18, 152–156 (2006). PubMed

Kelley D. R. & Estelle M. Ubiquitin-mediated control of plant hormone signaling. Plant Physiol. 160, 47–55 (2012). PubMed PMC

Vieten A. PubMed

Xu T. PubMed PMC

Michalko J., Dravecká M., Bollenbach T. & Friml J. Embryo-lethal phenotypes in early PubMed PMC

Kurczyńska E. U. & Hejnowicz Z. Differentiation of circular vessels in isolated segments of

Lev-Yadun S. Circular vessels in the secondary xylem of

Barnett J. R. & Harris J. M. Early stages of bordered pit formation in radiata pine. Wood Sci. Technol. 9, 233–241 (1975).

Leitch M. A. & Savidge R. A. Evidence for auxin regulation of bordered-pit positioning during tracheid differentiation in

O’Brien T. P. & McCully M. E. The Study of Plant Structure: Principles and Selected Methods, 1st Ed. Termarcarphi 1981, Melbourne, Australia (1981).

Jefferson R. A., Kavanagh T. A. & Bevan M. W. GUS fusions: ß-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901–3907 (1987). PubMed PMC

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

ABP1-TMK auxin perception for global phosphorylation and auxin canalization

Receptor kinase module targets PIN-dependent auxin transport during canalization

Strigolactones inhibit auxin feedback on PIN-dependent auxin transport canalization

Auxin canalization and vascular tissue formation by TIR1/AFB-mediated auxin signaling in Arabidopsis

Mechanistic framework for cell-intrinsic re-establishment of PIN2 polarity after cell division

PID/WAG-mediated phosphorylation of the Arabidopsis PIN3 auxin transporter mediates polarity switches during gravitropism

WRKY23 is a component of the transcriptional network mediating auxin feedback on PIN polarity