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Regulation of Intercellular Transport Through Plasmodesmata Under Abiotic Stresses

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Symplasmic Transport in Vascular Plants

Abstract

Plants are often subjected to environmental stresses. Except many responses, unfavourable conditions may affect intercellular communication by significantly changing the rate and efficiency of symplasmic transport. This can involve changes in the ultrastructure of plasmodesmata. Furthermore, the modification can concern the surroundings of plasmodesmata through deposition of callose. Thus, understanding the mechanisms that control permeability of plasmodesmata under stress conditions is of fundamental importance. This chapter presents structural changes of plasmodesmata in relation to the symplasmic transport efficiency under abiotic stress conditions. Responses of plasmodesmata to external stimuli are discussed in terms of plant acclimation to unfavourable conditions. The role of plasmodesmata in plant adaptation to different habitats is also considered.

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Abbreviations

ER:

Endoplasmic reticulum

PCA:

Primary carbon assimilation

PCR:

Primary carbon reduction

PD:

Plasmodesma/plasmodesmata

SEL:

Size exclusion limit

ROS:

Reactive oxygen species

References

  • Amiard V, Mueh KE, Demmig-Adams B, Ebbert V, Turgeon R, Adams WW. Anatomical and photosynthetic acclimation to the light environment in species with differing mechanisms of phloem loading. Proc Natl Acad Sci USA. 2005;102:12968–73.

    Article  PubMed  CAS  Google Scholar 

  • Anisimov AV, Egorov AG. Plasmodesmata as a modulator of osmotic water fluxes in plants. Russ J Plant Physiol. 2002;49:677–84.

    Article  CAS  Google Scholar 

  • Badelt K, White RG, Overall RL, Vesk M. Ultrastructural specializations of the cell wall sleeve around plasmodesmata. Am J Bot. 1994;81:1422–27.

    Article  Google Scholar 

  • Baluška F, Šamaj J, Napier R, Volkmann D. Maize calreticulin localizes preferentially to plasmodesmata in root apex. Plant J. 1999;19:481–8.

    Article  PubMed  Google Scholar 

  • Baluška F, Cvrčková F, Kendrick-Jones J, Volkmann D. Sink plasmodesmata as gateways for phloem unloading. Myosin VIII and calreticulin as molecular determinants of sink strength? Plant Physiol. 2001;126:39–46.

    Article  PubMed  Google Scholar 

  • Bell K, Oparka K. Imaging plasmodesmata. Protoplasma. 2011;248:9–25.

    Article  PubMed  Google Scholar 

  • Benitez-Alfonso Y, Jackson D. Redox homeostasis regulates plasmodesmal communication in Arabidopsis meristems. Plant Signal Behav. 2009;4:655–9.

    Article  PubMed  CAS  Google Scholar 

  • Benitez-Alfonso Y, Cilia M, Roman AS, Thomas C, Maule A, Hearn S, et al. Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proc Natl Acad Sci USA. 2009;106:3615–20.

    Article  PubMed  CAS  Google Scholar 

  • Benitez-Alfonso Y, Jackson D, Maule A. Redox regulation of intercellular transport. Protoplasma. 2011;248:131–40.

    Article  PubMed  CAS  Google Scholar 

  • Bilska A, Sowiński P. Closure of plasmodesmata in maize (Zea mays) at low temperature: a new mechanism for inhibition of photosynthesis. Ann Bot. 2010;106:675–86.

    Article  PubMed  CAS  Google Scholar 

  • Blackman LM, Overall RL. Structure and function of plasmodesmata. Aust J Plant Physiol. 2001;28:709–27.

    CAS  Google Scholar 

  • Blackman LM, Harper JDI, Overall RL. Localization of a centrin-like protein to higher plant plasmodesmata. Eur J Cell Biol. 1999;78:297–304.

    Article  PubMed  CAS  Google Scholar 

  • Botha CEJ, Cross RHM. Towards reconciliation of structure with function in plasmodesmata-who is the gatekeeper? Micron. 2000;31:713–21.

    Article  PubMed  CAS  Google Scholar 

  • Botha CEJ, Hartley BJ, Cross RHM. The ultrastructure and computer-enhanced digital image analysis of plasmodesmata at the Kranz mesophyll-bundle sheath interface of Themeda triandra var. imberbis (Retz) A. Camus in conventionally-fixed blades. Ann Bot. 1993;72:255–61.

    Article  Google Scholar 

  • Botha CEJ, Cross RHM, Liu L. Comparative structure of specialised monocotyledonous leaf blade plasmodesmata. In: Oparka KJ, editor. Plasmodesmata. Oxford: Blackwell Publishing Ltd.; 2005. p. 73–89.

    Chapter  Google Scholar 

  • Bowler C, Fluhr R. The role of calcium and activated oxygens as signals for controlling cross-tolerance. Trends Plant Sci. 2000;5:241–6.

    Article  PubMed  CAS  Google Scholar 

  • Brecknock S, Dibbayawan T, Vesk M, Vesk PA, Faulkner C, Barton DA, et al. High resolution scanning electron microscopy of plasmodesmata. Planta. 2011;234:749–58.

    Article  PubMed  CAS  Google Scholar 

  • Brown AH. Circumnutations: from Darwin to space flights. Plant Physiol. 1993;101:345–8.

    PubMed  CAS  Google Scholar 

  • Cessna SG, Matsumoto TK, Lamb GN, Rice SJ, Hochstedler WW. The externally derived portion of the hyperosmotic shock-activated cytosolic calcium pulse mediates adaptation to ionic stress in suspension-cultured tobacco cells. J Plant Physiol. 2007;164:815–23.

    Article  PubMed  CAS  Google Scholar 

  • Chen XY, Kim JY. Callose synthesis in higher plants. Plant Signal Behav. 2009;4:489–92.

    Article  PubMed  CAS  Google Scholar 

  • Close TJ. Dehydrins: a commonality in the response of plants to dehydration and low temperature. Physiol Plant. 1997;100:291–6.

    Article  CAS  Google Scholar 

  • Davidson A, Keller F, Turgeon R. Phloem loading, plant growth form, and climate. Protoplasma. 2011;248:153–63.

    Article  PubMed  CAS  Google Scholar 

  • Ding B, Turgeon R, Parthasarathy MV. Substructure of freeze-substituted plasmodesmata. Protoplasma. 1992;169:28–41.

    Article  Google Scholar 

  • Drake GA, Carr DJ, Anderson WP. Plasmolysis, plasmodesmata, and the electrical coupling of oat coleoptile cells. J Exp Bot. 1978;29:1205–14.

    Article  Google Scholar 

  • Ehlers K, Kollmann R. Primary and secondary plasmodesmata: structure, origin, and functioning. Protoplasma. 2001;216:1–30.

    Article  PubMed  CAS  Google Scholar 

  • Epel BL, Erlanger MA. Light regulates symplastic communication in etiolated corn seedlings. Physiol Plant. 1991;83:149–53.

    Article  CAS  Google Scholar 

  • Evert RF, Eschrich W, Heyser W. Distribution and structure of the plasmodesmata in mesophyll and bundle-sheath cells of Zea mays L. Planta. 1977;136:77–89.

    Article  Google Scholar 

  • Faulkner C, Maule A. Opportunities and successes in the search for plasmodesmal proteins. Protoplasma. 2011;248:27–38.

    Article  PubMed  CAS  Google Scholar 

  • Frohnmeyer H, Bowler C, Zhu J-k, Yamagata H, Schäfer E, Chua N-h. Different roles for calcium and calmodulin in phytochrome- and UV-regulated expression of chalcone synthase. Plant J. 1998;13:763–72.

    Article  CAS  Google Scholar 

  • Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR. Control of Ascorbate Peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. Plant J. 2003;33:691–705.

    Article  PubMed  CAS  Google Scholar 

  • Gamalei Y. Structure and function of leaf minor veins in trees and herbs. Trees. 1989;3:96–110.

    Article  Google Scholar 

  • Gamalei Y. Phloem loading and its development related to plant evolution from trees to herbs. Trees. 1991;5:50–64.

    Article  Google Scholar 

  • Hepler PK. Endoplasmic reticulum in the formation of the cell plate and plasmodesmata. Protoplasma. 1982;111:121–33.

    Article  Google Scholar 

  • Herrmann MM, Pinto S, Kluth J, Wienand U, Lorbiecke R. The PTI1-like kinase ZmPti1a from maize (Zea mays L.) co-localizes with callose at the plasma membrane of pollen and facilitates a competitive advantage to the male gametophyte. BMC Plant Biol. 2006;6:22.

    Article  PubMed  Google Scholar 

  • Holdaway-Clarke TL, Walker NA, Hepler PK, Overall RL. Physiological elevations in cytoplasmic free calcium by cold or ion injection result in transient closure of higher plant plasmodesmata. Planta. 2000;210:329–35.

    Article  PubMed  CAS  Google Scholar 

  • Karlson DT, Fujino T, Kimura S, Baba K, Itoh T, Ashworth EN. Novel plasmodesmata association of dehydrin-like proteins in cold-acclimated red-osier dogwood (Cornus sericea). Tree Physiol. 2003;23:759–67.

    Article  PubMed  CAS  Google Scholar 

  • Kerstiens G, Possell M. Is competence for isoprene emission related to the mode of phloem loading? New Phytol. 2001;152:368–72.

    Google Scholar 

  • Kosová K, Vítámvás P, Prášil IT. The role of dehydrins in plant response to cold. Biol Plant. 2007;51:601–17.

    Article  Google Scholar 

  • Lee SC, Lee MY, Kim SJ, Jun SH, An G, Kim SR. Characterization of an abiotic stress-inducible dehydrin gene, OsDhn1, in rice (Oryza sativa L.). Mol Cells. 2005;19:212–18.

    PubMed  CAS  Google Scholar 

  • Levitt J. Responses of plants to environmental stresses. 2nd ed. New York: Academic; 1980.

    Google Scholar 

  • Levy A, Erlanger M, Rosenthal M, Epel BL. A plasmodesmata-associated β-1,3-glucanase in Arabidopsis. Plant J. 2007;49:669–82.

    Article  PubMed  CAS  Google Scholar 

  • Logan BA, Monson RK, Potosnak MJ. Biochemistry and physiology of foliar isoprene production. Trends Plant Sci. 2000;5:477–81.

    Article  PubMed  CAS  Google Scholar 

  • Lucas WJ, Lee J-Y. Plasmodesmata as a supracellular control network in plants. Nat Rev Mol Cell Biol. 2004;5:712–26.

    Article  PubMed  CAS  Google Scholar 

  • Lucas WJ, Ding B, Van der Schoot C. Plasmodesmata and the supracellular nature of plants. New Phytol. 1993;125:435–76.

    Article  Google Scholar 

  • McIntosh R, Nicastro D, Mastronarde D. New views of cells in 3D: an introduction to electron tomography. Trends Cell Biol. 2005;15:43–51.

    Article  PubMed  CAS  Google Scholar 

  • Morris DA. Hormonal regulation of source–sink relationships: an overview of potential control mechanisms. In: Zamski E, Schaffer AA, editors. Photoassimilate distribution in plants and crops. Sourcesink Relationships. New York: Marcel Dekker, Inc.; 1996. p. 441–65.

    Google Scholar 

  • Neuhaus G, Bowler C, Hiratsuka K, Yamagata H, Chua NH. Phytochrome-regulated repression of gene expression requires calcium and cGMP. EMBO J. 1997;16:2554–64.

    Article  PubMed  CAS  Google Scholar 

  • Northote DH, Lewis DR. Freeze-etched surfaces of membranes and organelles in the cells of pea root tips. J Cell Sci. 1968;3:199–206.

    Google Scholar 

  • Olesen P. The neck constriction in plasmodesmata. Planta. 1979;144:349–58.

    Article  Google Scholar 

  • Olesen P, Robards AW. The neck region of plasmodesmata: general architecture and some functional aspects. In: Robards AW, Lucas WJ, Pitts JD, Jongsma HJ, Spray DC, editors. Parallels in cell-to-cell junctions in plants and animals. Berlin: Springer; 1990. p. 145–70.

    Chapter  Google Scholar 

  • Oparka KJ, Prior DAM. Direct evidence for pressure-generated closure of plasmodesmata. Plant J. 1992;2:741–50.

    Article  Google Scholar 

  • Overall RL, Blackman LM. A model of the macromolecular structure of plasmodesmata. Trends Plant Sci. 1996;1:307–11.

    Google Scholar 

  • Overall RL, Wolfe J, Gunning BES. Intercellular communication in Azolla roots: I. Ultrastructure of plasmodesmata. Protoplasma. 1982;111:134–50.

    Article  Google Scholar 

  • Pearcy RW, Ehleringer J. Comparative ecophysiology of C3 and C4 plants. Plant Cell Environ. 1984;7:1–13.

    Article  CAS  Google Scholar 

  • Piršelová B, Mistríková V, Libantová J, Moravčíková J, Matušíková I. Study on metal-triggered callose deposition in roots of maize and soybean. Biologia. 2012;67:698–705.

    Article  Google Scholar 

  • Radford JE, White RG. Effects of tissue-preparation-induced callose synthesis on estimates of plasmodesma size exclusion limits. Protoplasma. 2001;216:47–55.

    Article  PubMed  CAS  Google Scholar 

  • Radford JE, Vesk M, Overall RL. Callose deposition at plasmodesmata. Protoplasma. 1998;201:30–7.

    Article  CAS  Google Scholar 

  • Raffaele S, Bayer E, Lafarge D, Cluzet S, German Retana S, Boubekeur T, et al. Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs potato virus X movement. Plant Cell Online. 2009;21:1541–55.

    Article  CAS  Google Scholar 

  • Rinne PL, van der Schoot C. Symplasmic fields in the tunica of the shoot apical meristem coordinate morphogenetic events. Development. 1998;125:1477–85.

    PubMed  CAS  Google Scholar 

  • Rinne PLH, Kaikuranta PM, van der Schoot C. The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy. Plant J. 2001;26:249–64.

    Article  PubMed  CAS  Google Scholar 

  • Rinne PLH, van den Boogaard R, Mensink MGJ, Kopperud C, Kormelink R, Goldbach R, et al. Tobacco plants respond to the constitutive expression of the tospovirus movement protein NSM with a heat-reversible sealing of plasmodesmata that impairs development. Plant J. 2005;43:688–707.

    Article  PubMed  CAS  Google Scholar 

  • Ritzenthaler C, Findlay K, Roberts K, Maule AJ. Rapid detection of plasmodesmata in purified cell walls. Protoplasma. 2000;211:165–71.

    Article  Google Scholar 

  • Robards AW. A new interpretation of plasmodesmatal ultrastructure. Planta. 1968;82:200–10.

    Article  Google Scholar 

  • Roberts AG, Oparka KJ. Plasmodesmata and the control of symplastic transport. Plant Cell Environ. 2003;26:103–24.

    Article  Google Scholar 

  • Robinson-Beers K, Evert RF. Fine structure of plasmodesmata in mature leaves of sugarcane. Planta. 1991;184:307–18.

    Google Scholar 

  • Rorat T. Plant dehydrins—tissue location, structure and function. Cell Mol Biol Lett. 2006;11:536–56.

    Article  PubMed  CAS  Google Scholar 

  • Russin WA, Evert RF, Vanderveer PJ, Sharkey TD, Briggs SP. Modification of a specific class of plasmodesmata and loss of sucrose export ability in the sucrose export defective1 maize mutant. Plant Cell. 1996;8:645–58.

    PubMed  CAS  Google Scholar 

  • Sage R, Pearcy R. The physiological ecology of C4 photosynthesis. In: Leegood R, Sharkey T, von Caemmerer S, editors. Photosynthesis, physiology and metabolism. Dordrecht: Kluwer Academic Publishers; 2000. p. 497–532.

    Google Scholar 

  • Salmon MS, Bayer EMF. Dissecting plasmodesmata molecular composition by mass spectrometry-based proteomics. Front Plant Sci. 2013;3:1–8.

    Article  Google Scholar 

  • Samardakiewicz S, Krzeslowska M, Bilski H, Bartosiewicz R, Woźny A. Is callose a barrier for lead ions entering Lemna minor L. root cells? Protoplasma. 2012;249:347–51.

    Article  PubMed  CAS  Google Scholar 

  • Sattler SE, Cahoon EB, Coughlan SJ, DellaPenna D. Characterization of tocopherol cyclases from higher plants and cyanobacteria. Evolutionary implications for tocopherol synthesis and function. Plant Physiol. 2003;132:2184–95.

    Article  PubMed  CAS  Google Scholar 

  • Schulz A. Plasmodesmal widening accompanies the short-term increase in symplasmic phloem unloading in pea root tips under osmotic stress. Protoplasma. 1995;188:22–37.

    Article  Google Scholar 

  • Sharkey TD, Yeh S. Isoprene emission from plants. Annu Rev Plant Physiol Plant Mol Biol. 2001;52:407–36.

    Article  PubMed  CAS  Google Scholar 

  • Sivaguru M, Fujiwara T, Šamaj J, Baluška F, Yang Z, Osawa H, et al. Aluminum-induced 1→3-β-d-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata. A new mechanism of aluminum toxicity in plants. Plant Physiol. 2000;124:991–1006.

    Article  PubMed  CAS  Google Scholar 

  • Sowiński P, Rudzińska-Langwald A, Kobus P. Changes in plasmodesmata frequency in vascular bundles of maize seedling leaf induced by growth at sub-optimal temperatures in relation to photosynthesis and assimilate export. Environ Exp Bot. 2003;50:183–96.

    Article  Google Scholar 

  • Sowiński P, Bilska A, Barańska K, Fronk J, Kobus P. Plasmodesmata density in vascular bundles in leaves of C4 grasses grown at different light conditions in respect to photosynthesis and photosynthate export efficiency. Environ Exp Bot. 2007;61:74–84.

    Article  Google Scholar 

  • Stolarz M. Circumnutation as a visible plant action and reaction. Plant Signal Behav. 2009;4:380–87.

    Article  PubMed  CAS  Google Scholar 

  • Stonebloom S, Burch-Smith T, Kim I, Meinke D, Mindrinos M, Zambryski P. Loss of the plant DEAD-box protein ISE1 leads to defective mitochondria and increased cell-to-cell transport via plasmodesmata. Proc Natl Acad Sci USA. 2009;106:17229–34.

    Article  PubMed  CAS  Google Scholar 

  • Stonebloom S, Brunkard JO, Cheung AC, Jiang K, Feldman L, Zambryski P. Redox states of plastids and mitochondria differentially regulate intercellular transport via plasmodesmata. Plant Physiol. 2012;158:190–9.

    Article  PubMed  CAS  Google Scholar 

  • Thomson WW, Platt-Aloia K. The ultrastructure of the plasmodesmata of the salt glands of Tamarix as revealed by transmission and freeze-fracture electron microscopy. Protoplasma. 1985;125:13–23.

    Article  Google Scholar 

  • Tilney LG, Cooke TJ, Connelly PS, Tilney MS. The structure of plasmodesmata as revealed by plasmolysis, detergent extraction, and protease digestion. J Cell Biol. 1991;112:739–47.

    Article  PubMed  CAS  Google Scholar 

  • Tilsner J, Amari K, Torrance L. Plasmodesmata viewed as specialised membrane adhesion sites. Protoplasma. 2011;248:39–60.

    Article  PubMed  CAS  Google Scholar 

  • Trzcinska-Danielewicz J, Bilska A, Fronk J, Zielenkiewicz P, Jarochowska E, Roszczyk M, et al. Global analysis of gene expression in maize leaves treated with low temperature: I. Moderate chilling (14°C). Plant Sci. 2009;177:648–58.

    Article  CAS  Google Scholar 

  • Tucker EB. Calcium-loaded 1,2-bis(2-aminophenoxy)ethane-N, N, N′,N′-tetraacetic acid blocks cell-to-cell diffusion of carboxyfluorescein in staminal hairs of Setcreasea purpurea. Planta. 1990;182:34–8.

    Article  CAS  Google Scholar 

  • Tucker EB, Boss WF. Mastoparan-induced intracellular Ca2+ fluxes may regulate cell-to-cell communication in plants. Plant Physiol. 1996;111:459–67.

    PubMed  CAS  Google Scholar 

  • Turner A, Wells B, Roberts K. Plasmodesmata of maize root tips: structure and composition. J Cell Sci. 1994;107:3351–61.

    PubMed  CAS  Google Scholar 

  • Ueki S, Citovsky V. Identification of an interactor of cadmium ion-induced glycine-rich protein involved in regulation of callose levels in plant vasculature. Proc Natl Acad Sci USA. 2005;102:12089–94.

    Article  PubMed  CAS  Google Scholar 

  • Vatén A, Dettmer J, Wu S, Stierhof Y-D, Miyashima S, Yadav SR, et al. Callose biosynthesis regulates symplastic trafficking during root development. Dev Cell. 2011;21:1144–55.

    Article  PubMed  Google Scholar 

  • Willison JHM. Plasmodesmata: a freeze-fracture view. Can J Bot. 1976;54:2842–7.

    Article  Google Scholar 

  • Wojtaszek P, Anielska-Mazur A, Gabryś H, Baluška F, Volkmann D. Recruitment of myosin VIII towards plastid surfaces is root-cap specific and provides the evidence for actomyosin involvement in root osmosensing. Funct Plant Biol. 2005;32:721–36.

    Article  CAS  Google Scholar 

  • Wright KM, Wood NT, Roberts AG, Chapman S, Boevink P, MacKenzie KM, et al. Targeting of TMV movement protein to plasmodesmata requires the actin/ER network; Evidence from FRAP. Traffic. 2007;8:21–31.

    Article  PubMed  CAS  Google Scholar 

  • Zambryski P, Crawford K. Plasmodesmata: gatekeepers for cell-to-cell transport of developmental signals in plants. Annu Rev Cell Dev Biol. 2000;16:393–421.

    Article  PubMed  CAS  Google Scholar 

  • Zavaliev R, Ueki S, Epel BL, Citovsky V. Biology of callose (β-1,3-glucan) turnover at plasmodesmata. Protoplasma. 2011;248:117–30.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

I am grateful to Prof. P. Sowiński for helpful comments, advice and encouragement, and Dr. J. Fronk for critical reading of the manuscript. I thank S. Suski and H. Bilski from the Nencki Institute of Experimental Biology, PAS, for help in electron tomography, and the TEWI Platform Team, especially K. Świrski and K. Dróżka for CAD software support. Special thanks to H. Kos for help with the 3D plasmodesmata models. Financial support for the preparation of this manuscript came from the Ministry of Science and Higher Education, Poland (0036/IP1/2011/71), and the National Science Centre, Poland (5496/B/P01/2010/39).

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Bilska, A. (2013). Regulation of Intercellular Transport Through Plasmodesmata Under Abiotic Stresses. In: Sokołowska, K., Sowiński, P. (eds) Symplasmic Transport in Vascular Plants. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-7765-5_3

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