Vascular cambium regeneration and vessel formation in wounded inflorescence stems of Arabidopsis
Language English Country England, Great Britain Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
27649687
PubMed Central
PMC5030676
DOI
10.1038/srep33754
PII: srep33754
Knihovny.cz E-resources
- MeSH
- Arabidopsis physiology MeSH
- Cambium physiology MeSH
- Indoleacetic Acids metabolism MeSH
- Regeneration MeSH
- Plant Stems physiology MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Indoleacetic Acids MeSH
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.
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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. et al. Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev. 20, 2902–2911 (2006). 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 et al. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226–2230 (1998). PubMed
Friml J. et al. AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108, 661–673 (2002a). PubMed
Friml J., Wiśniewska J., Benková E., Mendgen K. & Palme K. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806–809 (2002b). PubMed
Friml J. et al. Efflux-dependent auxin gradients establish the apical--basal axis of Arabidopsis. Nature 426, 147–153 (2003). PubMed
Friml J. et al. A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306, 862–865 (2004). PubMed
Reinhardt D. et al. Regulation of phyllotaxis by polar auxin transport. Nature 426, 255–260 (2003). PubMed
Petrášek J. et al. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312, 914–918 (2006). PubMed
Wiśniewska J. et al. Polar PIN localization directs auxin flow in plants. Science 312, 883–883 (2006). PubMed
Benková E. et al. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602 (2003). PubMed
Dhonukshe P. et al. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol. 17, 520–527 (2007). PubMed
Paciorek T. et al. Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435, 1251–1256 (2005). PubMed
Robert S. et al. ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 143, 111–121 (2010). PubMed PMC
Wabnik K. et al. Emergence of tissue polarization from synergy of intracellular and extracellular auxin signaling. Mol. Syst. Biol. 6, 447 (2010). PubMed PMC
Grones P. et al. Auxin-binding pocket of ABP1 is crucial for its gain-of-function cellular and developmental roles. J. Exp. Bot. 66, 5055–5065 (2015). PubMed
Wenzel C. L., Schuetz M., Yu Q. & Mattsson J. Dynamics of MONOPTEROS and PIN-FORMED1 expression during leaf vein pattern formation in Arabidopsis thaliana. Plant J. 49, 387–398 (2007). PubMed
Flaishman M. A., Loginovsky K. & Lev-Yadun S. Regenerative xylem in inflorescence stems of Arabidopsis thaliana. J. Plant Growth Regul. 22, 253–258 (2003).
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 Rhamnus alaternus (Rhamnaceae). IAWA J. 22, 295–300 (2001).
Lev-Yadun S. The distance to which wound effects influence the structure of secondary xylem of decapitated Pinus pinea. J. Plant Growth Regul. 21, 191–196 (2002). 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 Arabidopsis. Protoplasma 251, 1125–1139 (2014). PubMed
Busse J. S. & Evert R. F. Vascular differentiation and transition in the seedling of Arabidopsis thaliana (Brassicaceae). Int. J. Plant Sci. 160, 241–251(1999).
Chaffey N., Cholewa E., Regan S. & Sundberg B. Secondary xylem development in Arabidopsis: a model for wood formation. Physiol. Plant. 114, 594–600 (2002). 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. et al. Analysis of secondary growth in the Arabidopsis shoot reveals a positive role of jasmonate signalling in cambium formation. Plant J. 63, 811–822 (2010). PubMed PMC
Agusti J. et al. Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc. Natl. Acad. Sci. USA 108, 20242–20247 (2011). PubMed PMC
Paul-Victor C. & Rowe N. Effect of mechanical perturbation on the biomechanics, primary growth and secondary tissue development in inflorescence stems of Arabidopsis thaliana. Ann. Bot. 107, 209–218 (2011). 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 Arabidopsis thaliana (L.) Heynh. Protoplasma 249, 217–220 (2012). PubMed PMC
Baima S. et al. The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Development 121, 4171–4182 (1995). PubMed
Baima S. et al. The Arabidopsis ATHB-8 HD-Zip protein acts as a differentiation-promoting transcription factor of the vascular meristems. Plant Physiol. 126, 643–655 (2001). 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 et al. Development of the vascular system in the inflorescence stem of Arabidopsis. New Phytol. 151, 381–389 (2001).
Lev-Yadun S. Fibres and fibre-sclereids in wild-type Arabidopsis thaliana. Ann. Bot. 80, 125–129 (1997).
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 Arabidopsis thaliana. Curr. Biol. 25, 1306–1318 (2015). PubMed PMC
Rolland-Lagan A. G. & Prusinkiewicz P. Reviewing models of auxin canalization in the context of leaf vein pattern formation in Arabidopsis. Plant J. 44, 854–865 (2005). 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. et al. Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development 132, 4521–4531 (2005). PubMed
Xu T. et al. Cell surface- and Rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143, 99–110 (2010). PubMed PMC
Michalko J., Dravecká M., Bollenbach T. & Friml J. Embryo-lethal phenotypes in early abp1 mutants are due to disruption of the neighboring BSM gene. F1000Research 4, 1104, (doi: 10.12688/f1000 research.7143.1) (October 23, 2015). PubMed PMC
Kurczyńska E. U. & Hejnowicz Z. Differentiation of circular vessels in isolated segments of Fraxinus excelsior. Physiol. Plant. 83, 275–280 (1991).
Lev-Yadun S. Circular vessels in the secondary xylem of Arabidopsis thaliana (Brassicaceae). IAWA J. 17, 31–35 (1996).
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 Larix laricina. IAWA J. 16, 289–297 (1995).
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
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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
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