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Rhizoids and protonemata of characean algae: model cells for research on polarized growth and plant gravity sensing

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Summary.

Gravitropically tip-growing rhizoids and protonemata of characean algae are well-established unicellular plant model systems for research on gravitropism. In recent years, considerable progress has been made in the understanding of the cellular and molecular mechanisms underlying gravity sensing and gravity-oriented growth. While in higherplant statocytes the role of cytoskeletal elements, especially the actin cytoskeleton, in the mechanisms of gravity sensing is still enigmatic, there is clear evidence that in the characean cells actin is intimately involved in polarized growth, gravity sensing, and the gravitropic response mechanisms. The multiple functions of actin are orchestrated by a variety of actin-binding proteins which control actin polymerisation, regulate the dynamic remodelling of the actin filament architecture, and mediate the transport of vesicles and organelles. Actin and a steep gradient of cytoplasmic free calcium are crucial components of a feedback mechanism that controls polarized growth. Experiments performed in microgravity provided evidence that actomyosin is a key player for gravity sensing: it coordinates the position of statoliths and, upon a change in the cell’s orientation, directs sedimenting statoliths to specific areas of the plasma membrane, where contact with membrane-bound gravisensor molecules elicits short gravitropic pathways. In rhizoids, gravitropic signalling leads to a local reduction of cytoplasmic free calcium and results in differential growth of the opposite subapical cell flanks. The negative gravitropic response of protonemata involves actin-dependent relocation of the calcium gradient and displacement of the centre of maximal growth towards the upper flank. On the basis of the results obtained from the gravitropic model cells, a similar fine-tuning function of the actomyosin system is discussed for the early steps of gravity sensing in higher-plant statocytes.

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Abbreviations

ADF:

actin-depolymerizing factor

ER:

endoplasmic reticulum

References

  • R Aloni M Langhans E Aloni CI Ullrich (2004) ArticleTitleRole of cytokinin in the regulation of root gravitropism Planta 220 177–182 Occurrence Handle15365840 Occurrence Handle10.1007/s00425-004-1381-8 Occurrence Handle1:CAS:528:DC%2BD2cXptlSmurc%3D

    Article  PubMed  CAS  Google Scholar 

  • E Bartnik A Sievers (1988) ArticleTitleIn vivo observation of a spherical aggregate of endoplasmic reticulum and of Golgi vesicles in the tip of fast-growing Chara rhizoids Planta 176 1–9 Occurrence Handle10.1007/BF00392473

    Article  Google Scholar 

  • EB Blancaflor (2002) ArticleTitleThe cytoskeleton and gravitropism in higher plants J Plant Growth Regul 21 120–136 Occurrence Handle12024227 Occurrence Handle10.1007/s003440010041 Occurrence Handle1:CAS:528:DC%2BD38XltlOisL8%3D

    Article  PubMed  CAS  Google Scholar 

  • I Blilou J Xu M Wildwater V Willemsen I Paponov J Friml R Heidstra M Aida K Palme B Scheres (2005) ArticleTitleThe PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots Nature 433 39–44 Occurrence Handle15635403 Occurrence Handle10.1038/nature03184 Occurrence Handle1:CAS:528:DC%2BD2MXovFCj

    Article  PubMed  CAS  Google Scholar 

  • K Boonsirichai C Guan R Chen PH Masson (2002) ArticleTitleRoot gravitropism: an experimental tool to investigate basic cellular and molecular processes underlying mechanosensing and signal transmission in plants Annu Rev Plant Physiol Plant Mol Biol 53 421–447 Occurrence Handle1:CAS:528:DC%2BD38XlsVWhurg%3D

    CAS  Google Scholar 

  • M Braun (1996a) ArticleTitleImmunolocalization of myosin in rhizoids of Chara globularis Thuill Protoplasma 191 1–8 Occurrence Handle10.1007/BF01280820 Occurrence Handle1:CAS:528:DyaK28XjvFOrsbw%3D

    Article  CAS  Google Scholar 

  • M Braun (1996b) ArticleTitleAnomalous gravitropic response of Chara rhizoids during enhanced accelerations Planta 199 443–450 Occurrence Handle10.1007/BF00195738 Occurrence Handle1:STN:280:DC%2BD3MnlvFKnsA%3D%3D

    Article  CAS  Google Scholar 

  • M Braun (1997) ArticleTitleGravitropism in tip-growing cells Planta 203 S11–S19 Occurrence Handle11540318 Occurrence Handle10.1007/PL00008098 Occurrence Handle1:CAS:528:DyaK2sXlvVyjsb8%3D

    Article  PubMed  CAS  Google Scholar 

  • M Braun (2001) ArticleTitleAssociation of spectrin-like proteins with the actin-organized aggregate of endoplasmic reticulum in the Spitzenkörper of gravitropically tip-growing plant cells Plant Physiol 125 1611–1620 Occurrence Handle11299343 Occurrence Handle10.1104/pp.125.4.1611 Occurrence Handle1:CAS:528:DC%2BD3MXjtFKqtrc%3D

    Article  PubMed  CAS  Google Scholar 

  • M Braun (2002) ArticleTitleGravity perception requires statoliths settled on specific plasma-membrane areas in characean rhizoids and protonemata Protoplasma 219 150–159 Occurrence Handle12099215 Occurrence Handle10.1007/s007090200016

    Article  PubMed  Google Scholar 

  • M Braun P Richter (1999) ArticleTitleRelocalization of the calcium gradient and a dihydropyridine receptor is involved in upward bending by bulging of Chara protonemata, but not in downward bending by bowing of Chara rhizoids Planta 209 414–423 Occurrence Handle10550622 Occurrence Handle10.1007/s004250050744 Occurrence Handle1:CAS:528:DyaK1MXms1Sls7s%3D

    Article  PubMed  CAS  Google Scholar 

  • M Braun A Sievers (1993) ArticleTitleCentrifugation causes adaptation of microfilaments; studies on the transport of statoliths in gravity sensing Chara rhizoids Protoplasma 174 50–61 Occurrence Handle11541080 Occurrence Handle10.1007/BF01404042 Occurrence Handle1:STN:280:DC%2BD3MnlvFKmsA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • M Braun A Sievers (1994) ArticleTitleRole of the microtubule cytoskeleton in gravisensing Chara rhizoids Eur J Cell Biol 63 289–298 Occurrence Handle8082653 Occurrence Handle1:STN:280:ByuA28vjtlM%3D

    PubMed  CAS  Google Scholar 

  • M Braun GO Wasteneys (1998a) ArticleTitleReorganization of the actin and microtubule cytoskeleton throughout blue-light-induced differentiation of characean protonemata into multicellular thalli Protoplasma 202 38–53 Occurrence Handle10.1007/BF01280873

    Article  Google Scholar 

  • M Braun GO Wasteneys (1998b) ArticleTitleDistribution and dynamics of the cytoskeleton in graviresponding protonemata and rhizoids of characean algae: exclusion of microtubules and a convergence of actin filaments in the apex suggest an actin-mediated gravitropism Planta 205 39–50 Occurrence Handle10.1007/s004250050294 Occurrence Handle1:CAS:528:DyaK1cXislGitrs%3D

    Article  CAS  Google Scholar 

  • M Braun GO Wasteneys (2000) Actin in characean rhizoids and protonemata. Tip growth, gravity sensing and photomorphogenesis CJ Staiger F Baluska D Volkmann PW Barlow (Eds) Actin: a dynamic framework for multiple plant cell functions Kluwer Dordrecht 237–258

    Google Scholar 

  • M Braun B Buchen A Sievers (2002) ArticleTitleActomyosin-mediated statolith positioning in gravisensing plant cells studied in microgravity J Plant Growth Regul 21 137–145 Occurrence Handle12016508 Occurrence Handle10.1007/s003440010052 Occurrence Handle1:CAS:528:DC%2BD38XltlOisLw%3D

    Article  PubMed  CAS  Google Scholar 

  • M Braun J Hauslage A Czogalla C Limbach (2004) ArticleTitleTip-localized actin polymerization and remodeling, reflected by the localization of ADF, profilin and villin, are fundamental for gravity-sensing and polarized growth of characean rhizoids Planta 219 379–388 Occurrence Handle15060825 Occurrence Handle10.1007/s00425-004-1235-4 Occurrence Handle1:CAS:528:DC%2BD2cXlsVCktbY%3D

    Article  PubMed  CAS  Google Scholar 

  • B Buchen M Braun Z Hejnowicz A Sievers (1993) ArticleTitleStatoliths pull on microfilaments: experiments under microgravity Protoplasma 172 38–42 Occurrence Handle11541056 Occurrence Handle10.1007/BF01403719 Occurrence Handle1:STN:280:DC%2BD3MnlvFKhug%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • Buchen B, Braun M, Sievers A (1997) Statoliths, cytoskeletal elements and cytoplasmic streaming of Chara rhizoids under reduced gravity during TEXUS flights. In: Life sciences experiments performed on sounding rockets (1985–1994). Scientific/technical publications, SP-1206. European Space Agency Publications Division, Noordwijk, pp 71–75

  • W Cai M Braun A Sievers (1997) ArticleTitleDisplacement of statoliths in Chara rhizoids during horizontal rotation on clinostats Acta Biol Exp Sin 30 147–155 Occurrence Handle1:STN:280:DC%2BD3MnlsFCltg%3D%3D

    CAS  Google Scholar 

  • D Driss-Ecole B Jeune M Prouteau P Julianus G Perbal (2000) ArticleTitleLentil root statoliths reach a stable state in microgravity Planta 211 396–405 Occurrence Handle10987559 Occurrence Handle10.1007/s004250000298 Occurrence Handle1:CAS:528:DC%2BD3cXlsVWqsLo%3D

    Article  PubMed  CAS  Google Scholar 

  • BK Drobak VE Franklin-Tong CJ Staiger (2004) ArticleTitleThe role of the actin cytoskeleton in plant cell signaling New Phytol 163 13–30 Occurrence Handle10.1111/j.1469-8137.2004.01076.x Occurrence Handle1:CAS:528:DC%2BD2cXmtVOhsLg%3D

    Article  CAS  Google Scholar 

  • A Geitmann AM Emons (2000) ArticleTitleThe cytoskeleton in plant and fungal cell tip growth J Microsc 198 218–245 Occurrence Handle10849200 Occurrence Handle10.1046/j.1365-2818.2000.00702.x Occurrence Handle1:CAS:528:DC%2BD3cXkslygtro%3D

    Article  PubMed  CAS  Google Scholar 

  • Z Hejnowicz A Sievers (1981) ArticleTitleRegulation of the position of statoliths in Chara rhizoids Protoplasma 108 117–137 Occurrence Handle11540622 Occurrence Handle10.1007/BF01276887 Occurrence Handle1:STN:280:DC%2BD3MnlvFWqsg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • Z Hejnowicz B Heinemann A Sievers (1977) ArticleTitleTip growth: pattern of growth rate and stress in the Chara rhizoid Z Pflanzenphysiol 81 409–424

    Google Scholar 

  • PK Hepler L Vidali AY Cheung (2001) ArticleTitlePolarized cell growth in higher plants Annu Rev Cell Dev Biol 17 159–187 Occurrence Handle11687487 Occurrence Handle10.1146/annurev.cellbio.17.1.159 Occurrence Handle1:CAS:528:DC%2BD3MXos1OmsLs%3D

    Article  PubMed  CAS  Google Scholar 

  • D Hodick (1994) ArticleTitleNegative gravitropism in Chara protonemata: a model integrating the opposite gravitropic responses of protonemata and rhizoids Planta 195 43–49 Occurrence Handle11541071 Occurrence Handle10.1007/BF00206290 Occurrence Handle1:CAS:528:DyaK2MXit1yjt74%3D

    Article  PubMed  CAS  Google Scholar 

  • D Hodick A Sievers (1998) ArticleTitleHypergravity can reduce but not enhance the gravitropic response of Chara globularis protonemata Protoplasma 204 145–154 Occurrence Handle11542591 Occurrence Handle10.1007/BF01280321 Occurrence Handle1:STN:280:DC%2BD3MnmtFWltQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • D Hodick B Buchen A Sievers (1998) ArticleTitleStatolith positioning by microfilaments in Chara rhizoids and protonemata Adv Space Res 21 1183–1189 Occurrence Handle11541370 Occurrence Handle10.1016/S0273-1177(97)00633-9 Occurrence Handle1:STN:280:DC%2BD3MnlvF2nsQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • T Hoson S Kamisaka Y Masuda M Yamashita B Buchen (1997) ArticleTitleEvaluation of the three-dimensional clinostat as a simulator of weightlessness Planta 203 S187–S197 Occurrence Handle9299798 Occurrence Handle10.1007/PL00008108 Occurrence Handle1:CAS:528:DyaK2sXlvVyjt7w%3D

    Article  PubMed  CAS  Google Scholar 

  • G Hou VL Kramer Y-S Wang R Chen G Perbal S Gilroy EB Blancaflor (2004) ArticleTitleThe promotion of gravitropism in Arabidopsis roots upon actin disruption is coupled with the extended alkalinization of the columella cytoplasm and a persistent lateral auxin gradient Plant J 39 113–125 Occurrence Handle15200646 Occurrence Handle10.1111/j.1365-313X.2004.02114.x Occurrence Handle1:CAS:528:DC%2BD2cXms1yku78%3D

    Article  PubMed  CAS  Google Scholar 

  • JZ Kiss (2000) ArticleTitleMechanisms of the early phases of plant gravitropism Crit Rev Plant Sci 19 551–573 Occurrence Handle11806421 Occurrence Handle10.1016/S0735-2689(01)80008-3 Occurrence Handle1:STN:280:DC%2BD38%2FotVarsg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • V Legué E Blancaflor C Wymer G Perbal D Fantin S Gilroy (1997) ArticleTitleCytoplasmic free Ca2+ in Arabidopsis roots changes in response to touch but not gravity Plant Physiol 114 789–800 Occurrence Handle9232870 Occurrence Handle10.1104/pp.114.3.789

    Article  PubMed  Google Scholar 

  • MS Ladinsky DN Mastronarde JR McIntosh KE Howell LA Staehelin (1999) ArticleTitleGolgi structure in three dimensions: functional insights from the normal rat kidney cell J Cell Biol 144 1135–1149 Occurrence Handle10087259 Occurrence Handle10.1083/jcb.144.6.1135 Occurrence Handle1:CAS:528:DyaK1MXitVKjtLk%3D

    Article  PubMed  CAS  Google Scholar 

  • G Leitz E Schnepf KO Greulich (1995) ArticleTitleMicromanipulation of statoliths in gravity-sensing Chara rhizoids by optical tweezers Planta 197 278–288 Occurrence Handle11540723 Occurrence Handle10.1007/BF00202648 Occurrence Handle1:CAS:528:DyaK2MXovVyrsL0%3D

    Article  PubMed  CAS  Google Scholar 

  • C Limbach J Hauslage C Schaefer M Braun (2005) ArticleTitleHow to activate a plant gravireceptor: early mechanisms of gravity sensing studied in characean rhizoids during parabolic flights Plant Physiol 139 1–11 Occurrence Handle10.1104/pp.105.068106

    Article  Google Scholar 

  • A Lovy-Wheeler KL Wilsen TI Baskin PK Hepler (2005) ArticleTitleEnhanced fixation reveals the apical cortical fringe of actin filaments as a consistent feature of the pollen tube Planta 221 95–104 Occurrence Handle15747143 Occurrence Handle10.1007/s00425-004-1423-2 Occurrence Handle1:CAS:528:DC%2BD2MXjtl2lu7c%3D

    Article  PubMed  CAS  Google Scholar 

  • DN Mastronarde (1997) ArticleTitleDual-axis tomography: an approach with alignment methods that preserve resolution J Struct Biol 120 343–352 Occurrence Handle9441937 Occurrence Handle10.1006/jsbi.1997.3919 Occurrence Handle1:STN:280:DyaK1c7htVaqsQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • I Ottenschläger P Wolff C Wolverton RP Bhalerao G Sandberg H Ishikawa M Evans K Palme (2003) ArticleTitleGravity-regulated differential auxin transport from columella to lateral root cap cells Proc Natl Acad Sci USA 100 2987–2991 Occurrence Handle12594336 Occurrence Handle10.1073/pnas.0437936100

    Article  PubMed  Google Scholar 

  • G Perbal A Lefrance B Jeune D Driss-Ecole (2004) ArticleTitleMechanotransduction in root gravity sensing cells Physiol Plant 120 303–311 Occurrence Handle14974478 Occurrence Handle10.1111/j.0031-9317.2004.0233.x Occurrence Handle1:CAS:528:DC%2BD2cXhtFSlt7g%3D

    Article  PubMed  CAS  Google Scholar 

  • A Sievers B Heinemann MI Rodriguez-Garcia (1979) ArticleTitleNachweis des subapikalen differentiellen Flankenwachstums im Chara-Rhizoid während der Graviresponse Z Pflanzenphysiol 91 435–442 Occurrence Handle1:STN:280:DC%2BD3MnlvFKrtQ%3D%3D

    CAS  Google Scholar 

  • A Sievers B Buchen D Volkmann Z Hejnowicz (1991a) Role of the cytoskeleton in gravity perception CW Lloyd (Eds) The cytoskeletal basis for plant growth and form Academic Press London 169–182

    Google Scholar 

  • A Sievers M Kramer-Fischer M Braun B Buchen (1991b) ArticleTitleThe polar organization of the growing Chara rhizoid and the transport of statoliths are actin-dependent Bot Acta 104 103–109 Occurrence Handle1:STN:280:DC%2BD3MnlvFymtA%3D%3D

    CAS  Google Scholar 

  • A Sievers B Buchen D Hodick (1996) ArticleTitleGravity sensing in tip-growing cells Trends Plant Sci 1 273–279 Occurrence Handle11539828 Occurrence Handle10.1016/1360-1385(96)10028-5 Occurrence Handle1:STN:280:DC%2BD3MnlvVeqtw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • A Sievers B Braun GB Monshausen (2002) The root cap: structure and function Y Waisel A Eshel U Kafkafi (Eds) Plant roots – the hidden half EditionNumber3 Marcel Dekker New York 33–47

    Google Scholar 

  • D Volkmann B Buchen Z Hejnowicz M Tewinkel A Sievers (1991) ArticleTitleOriented movement of statoliths studied in a reduced gravitational field during parabolic flights of rockets Planta 185 153–161 Occurrence Handle11538120 Occurrence Handle10.1007/BF00194056 Occurrence Handle1:STN:280:DC%2BD3Mnls1Kltw%3D%3D

    Article  PubMed  CAS  Google Scholar 

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  1. Gravitationsbiologie, Institut für Molekulare Physiologie und Biotechnologie der Pflanzen, Universität Bonn, Bonn

    M. Braun & C. Limbach

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  1. M. Braun
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  2. C. Limbach
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Correspondence to M. Braun.

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Correspondence and reprints: Gravitationsbiologie, Institut für Molekulare Physiologie und Biotechnologie der Pflanzen, Universität Bonn, Kirschallee 1, 53115 Bonn, Federal Republic of Germany.

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Braun, M., Limbach, C. Rhizoids and protonemata of characean algae: model cells for research on polarized growth and plant gravity sensing. Protoplasma 229, 133–142 (2006). https://doi.org/10.1007/s00709-006-0208-9

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