Skip to main content

Bidirectional Lateral Transport Barriers in Serving Plant Organs and Integral Plant Functioning: Localized Lignification, Suberinization, and Cutinization

  • Chapter
  • First Online:
Progress in Botany Vol. 82

Part of the book series: Progress in Botany ((BOTANY,volume 82))

  • 785 Accesses

Abstract

In their organs – roots, leaves, and stems – higher plants possess bidirectional barriers blocking apoplastic transport by diffusion of water and solutes. These are in the roots, (1) an endodermis (EN), (2) an exodermis (EX), and (3) EN-type cell layers in N2-fixing root nodules; in the leaves (4) envelopes of glands, gland hairs, and trichomes, (5) bundle sheaths, and (6) EN-type cell layers around the haustoria of rust fungi; (7) an EN-type cell layer in stems; and (8) a structurally invisible transport barrier in the root tip. Cell wall encrustations by lignin and adcrustations by suberin lamellae and by cutin prevent transport within the free spaces of the cell walls and transport across the cell walls. The latter is mediated by plasmodesmata.

Individually these transport barriers at strategic locations in the plant organs enforce switches between apoplastic and symplastic transport. These switches involve transport across membranes, and this ensures metabolic control over the solutes transported. Collectively the complement of the bidirectional transport barriers regulates the integrated harmonious functioning of the plants as whole entire organisms.

The cell wall structures of the apoplastic barriers in some cases, e.g., the root EN, have been shown not to be static anatomical elements but to be dynamic in response to internal development and environmental cues. Recent studies identify molecular signaling modules of developmental integrity of the radial cell wall encrustations in the Casparian strips in the root EN. Molecular studies also demonstrate hormonal control of reversible suberinization in response to environmental factors. The Scr gene and SCARECROW transcription factor regulate some of the barriers at distant locations within the plants. This opens a fascinating outlook for more work of plant molecular biology unraveling the integrated functioning of the transport-barrier complement.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

ABA:

Abscisic acid

AFS:

Apparent free space

BS:

Bundle sheath

CASP:

CASPRIAN STRIP MEMBRANE DOMAIN PROTEINS

CIF:

CASPARIAN STRIP INTEGRITY FACTORS

CL:

Cellulose layers

CS:

Casparian strip

DFS :

Donnan free space

EN:

Endodermis

EX:

Exodermis

M:

Mesophyll

PD:

Plasmodesmos, plasmodesmata

PEP:

Phosphoenolpyruvate

PEPC:

Phosphoenolpyruvate carboxylase

PM:

Plasma membrane

PW:

Primary cell wall

ROS:

Reactive oxygen species

RuBISCO:

Ribulosebisphosphate carboxylase/oxygenase

SGN:

SCHENGEN RECEPTOR LIKE KINASE

SL:

Suberin lamellae

WFS:

Water free space

References

  • Alassimone J, Fujita S, Doblas VG, Van Dop M, Barberon M, Kalmbach L, Vermeer JEM, Rojas-Murcia N, Santuari L, Hardtke SC, Geldner N (2016) Polarly localized kinase SGN1 is required for Casparian strip integrity and positioning. Nature Plants 2:16113

    CAS  PubMed  Google Scholar 

  • Arisz WH (1956) Significance of the symplasm theory for transport across the root. Protoplamsa 46:5–62

    Google Scholar 

  • Arisz WH (1960) Symplasmatischer Transport in Vallisneria-Blättern. Protoplasma 52:309–343

    Google Scholar 

  • Arisz WH (1969) Intercellular polar transport and the role of the plasmodesmata in coleoptiles and Vallisneria leaves. Acta Bot Neerl 18:14–38

    CAS  Google Scholar 

  • Arisz WH, Wiersema EP (1966) Symplasmatic long-distance transport in Vallisneria plants investigated by means of autoradiograms. Proc Kon Ned Akad Wetenschap Ser C 69:223–241

    Google Scholar 

  • Barberon M, Vermeer JEM, de Bellis D, Wang P, Naseer S, Andersen TG, Humbel BM, Nawrath C, Takano J, Salt DE, Geldner N (2016) Adaptation of root function by nutrient-induced plasticity of endodermal differentiation. Cell 164:447–459

    CAS  PubMed  Google Scholar 

  • Bellasio C, Griffiths H (2013) Acclimation to low light by C4 maize: implications for bundle sheath leakiness. Plant Cell Environ 37:1046–1058

    PubMed  Google Scholar 

  • Benzing DH (1989) The mineral nutrition of epiphytes. In: Lüttge U (ed) Vascular plants as epiphytes. Evolution and ecology. Springer, Berlin, pp 167–199

    Google Scholar 

  • Benzing DH, Henderson K, Kessel B, Sulak J (1976) The absorptive capacities of bromeliad trichomes. Am J Bot 63:1009–1014

    Google Scholar 

  • Bilska A, Sowinski P (2010) Closure of plasmodesmata in maize (Zea mays) at low temperature: a new mechanism for inhibition of photosynthesis. Ann Bot 106:675–686

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen T, Cai X, Wu X, Karahara I, Schreiber L, Lin J (2011) Casparian strip development and its potential function in salt tolerance. Plant Signaling and Behavior 6:1499–1502

    CAS  PubMed  Google Scholar 

  • Danila FR, Quick WP, White RG, Furbank RT (2016) The metabolite pathway between bundle sheath and mesophyll: quantification of plasmodesmata in leaves of C3 and C4 monocots. Plant Cell 18:1461–1471

    Google Scholar 

  • De Simone O, Haase K, Müller E, Junk WJ, Hartmann K, Schreiber L, Schmidt W (2003) Apoplastic barriers and oxygen transport properties of hypodermal cell walls in roots from four Amazonian tree species. Plant Physiol 132:206–217

    PubMed  PubMed Central  Google Scholar 

  • Delrot S (1987) Phloem loading: apoplastic or symplastic? Plant Physiol Biochem 25:676–676

    Google Scholar 

  • Deng Y, Feng Z, Yuan F, Guo J, Suo S, Wang B (2015) Identification and functional analysis of the autofluorescent substance in Limonium bicolor salt glands. Plant Physiol Biochem 97:20–27

    CAS  PubMed  Google Scholar 

  • Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G et al (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86:423–433

    PubMed  Google Scholar 

  • Doblas VG, Smakowska-Luzan E, Fujita S, Alassimone J, Barberon M, Madalinski M, Belkhadir Y, Geldner N (2017a) Root diffusion barrier control by a vasculature-derived peptide binding to the SGN3 receptor. Science 355:280–284

    CAS  PubMed  Google Scholar 

  • Doblas VG, Geldner N, Barberon M (2017b) The endodermis, a tightly controlled barrier for nutrients. Curr Op Plant Biol 39:136–143

    CAS  Google Scholar 

  • Enstone DE, Peterson CA (1992) The apoplastic permeability of root apices. Can J Bot 70:1502–1512

    CAS  Google Scholar 

  • Enstone DE, Peterson CA (1997) Suberin position and band plasmolysis in the maize (Zea mays L.) root exodermis. Can J Bot 75:1188–1199

    Google Scholar 

  • Esau K (1953) Plant anatomy. Wiley, New York

    Google Scholar 

  • Feng Z, Sun Q, Deng Y, Sun S, Zhang J, Wang B (2014) Study on pathway and characteristics of ion secretion of salt glands of Limonium bicolor. Acta Physiol Plant. https://doi.org/10.1007/s11738-014-1644-3

  • Frey-Wyssling A (1935) Die Stoffausscheidungen der höheren Pflanzen. Springer, Berlin

    Google Scholar 

  • Frey-Wyssling A (1959) Die pflanzliche Zellwand. Springer, Berlin

    Google Scholar 

  • Frey-Wyssling A (1972) Elimination processes in higher plants. Saussurea 3:79–90

    Google Scholar 

  • Furbank RT, Hatch MD (1987) Mechanism of C4 photosynthesis. Plant Physiol 85:958–964

    CAS  PubMed  PubMed Central  Google Scholar 

  • Geldner N (2013) The endodermis. Annu Rev Plant Biol 64:531–558

    CAS  PubMed  Google Scholar 

  • Giaquinta RT (1983) Phloem loading of sucrose. Ann Rev Plant Phys 54:892–898

    Google Scholar 

  • Givnish TJ, Burkhardt EL, Happel R, Weintraub J (1984) Carnivory in the bromeliad Brocchinia reducta, with a cost-benefit model for the general restriction of carnivorous plants to sunny, moist, nutrient-poor habitats. Am Nat 124:479–497

    Google Scholar 

  • Goh CJ, Kluge M (1989) Gas exchange and water relations in epiphytic orchids. In: Lüttge U (ed) Vascular plants as epiphytes. Evolution and ecology. Springer, Berlin, pp 139–166

    Google Scholar 

  • Gunning BES, Hughes JE (1976) Quantitative assessment of symplastic transport of pre-nectar into the trichomes of Abutilon nectaries. Aust J Plant Physiol 3:619–637

    Google Scholar 

  • Haas DL, Carothers ZB, Robins RR (1976) Observations of the phi-thickenings and casparian strips in Pelargonium roots. Am J Bot 63:863–867

    Google Scholar 

  • Heath MC (1976) Ultrastructural and functional similarity of the haustorial neck-band of rust fungi and the Casparian strip of vascular plants. Can J Bot 54:2484–2489

    Google Scholar 

  • Hill AE, Hill BS (1976) Elimination processes by glands. Mineral ions. In: Lüttge U, Pitman MG (eds) Transport in plants II. Part B tissues and organs. Encyclopedia of plant physiology, New Series vol 2. Springer, Berlin, pp 225–243

    Google Scholar 

  • Hose E, Clarkson DT, Steudle E, Schreiber L, Hartung W (2001) The exodermis: a variable apoplastic barrier. J Exp Bot 52:2245–2264

    CAS  PubMed  Google Scholar 

  • Karahara I, Shibaoka H (1994) The Casparian strip in pea epicotyls: effects of light on its development. Planta 192:269–275

    Google Scholar 

  • Karahara I, Ikeda A, Kondo T, Uetake Y (2004) Development of the Casparian strip in primary roots of maize under salt stress. Planta 219:41–47

    CAS  PubMed  Google Scholar 

  • Köster P, Wallrad L, Edel KH, Faisal M, Alatar AA, Kudla J (2019) The battle of two ions: Ca2+ signalling against Na+ stress. Plant Biol 21(Suppl 1):39–48

    PubMed  Google Scholar 

  • Krishnamurthy P, Ranathunge K, Franke R, Prakash HS, Schreiber L, Mathew MK (2009) The role of root apoplastic transport barriers in salt tolerance of rice (Oryza sativa L). Planta 230:119–134

    CAS  PubMed  Google Scholar 

  • Krishnamurthy P, Ranathunge K, Nayak S, Schreiber L, Mathew MK (2011) Root apoplastic barriers block Na+ transport to shoots in rice (Oryza sativa L.). J Exp Bot 62:4215–4228

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kromdijk J, Ubierna N, Cousins AB, Griffiths H (2014) Bundle-sheath leakiness in C4 photosynthesis: a careful balancing act between CO2 concentration and assimilation. J Exp Bot 65:3443–3457

    PubMed  Google Scholar 

  • Kuo J, O’Brien TB, Canny MJ (1974) Pit-field distribution, plasmodesmatal frequency, and assimilate flux in the mestome sheath cells of wheat leaves. Planta 121:97–118

    CAS  PubMed  Google Scholar 

  • Läuchli A (1976) Apoplasmic transport in tissues. In: Lüttge U, Pitman MG (eds) Transport in plants II. Part B tissues and organs. Encyclopedia of plant physiology, New Series vol 2. Springer, Berlin, pp 3–34

    Google Scholar 

  • Lee Y, Rubio MC, Alassimone J, Geldner N (2013) A mechanism for localized lignin deposition in the endodermis. Cell 1523:402–412

    Google Scholar 

  • Leegood RC (1985) The intercellular compartmentation of metabolites in leaves of Zea mays L. Planta 164:163–171

    CAS  PubMed  Google Scholar 

  • Lehmann H, Stelzer R, Holzamer S, Kunz U, Gierth M (2000) Analytical electron microscopical investigations on the apoplastic pathways of lanthanum transport in barley roots. Planta 211:816–822

    CAS  PubMed  Google Scholar 

  • Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta L et al (2010) The developmental dynamics of the maize leaf transcriptome. Nat Genet 42:1060–1067

    CAS  PubMed  Google Scholar 

  • Lim J, Helariutta Y, Specht CD, Jung J, Sims L, Bruce WB, Diehn S et al (2000) Molecular analysis of the SCARECROW gene in maize reveals a common basis for radial patterning in diverse meristems. Plant Cell 12:1307–1318

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lim J, Jung JW, Lim CE, Lee M-H, Kim BJ, Kim M et al (2005) Conservation and diversification of SCARECROW in maize. Plant Mol Biol 59:619–630

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lüttge U (1971) Structure and function of plant glands. Ann Rev Plant Physiol 22:23–44

    Google Scholar 

  • Lüttge U (2013) Whole-plant physiology: synergistic emergence rather than modularity. Progr Bot 74:165–190

    Google Scholar 

  • Lüttge U (2017) Faszination Pflanzen. Springer, Heidelberg

    Google Scholar 

  • Lüttge U (2019a) Plants: unitary organisms emerging from integration and self-organization of modules. In: Wegner LH, Lüttge U (eds) Emergence and modularity in life sciences. Springer, Heidelberg, pp 171–193

    Google Scholar 

  • Lüttge U (2019b) Elimination of salt by recretion: salt glands and gland-supported bladders in recretohalophytes. In: Hasanuzzaman M, Shabala S, Fujita M (eds) Halophytes and climate change: adaptive mechanisms and potential uses. CAB International, Wallingford, pp 223–239

    Google Scholar 

  • Lüttge U, Higinbotham N (1979) Transport in plants. Springer, New York

    Google Scholar 

  • Lüttge U, Schnepf E (1976) Elimination processes by glands. Organic substances. In: Lüttge U, Pitman MG (eds) Transport in plants II. Part B tissues and organs. Encyclopedia of plant physiology, New Series vol 2. Springer, Berlin, pp 245–277

    Google Scholar 

  • Lüttge U, Weigl J (1962) Mikroautoradiographische Untersuchungen der Aufnahme und des Transportes von 35SO4−− und 45Ca++ in Keimwurzeln von Zea mays L. und Pisum sativum L. Planta 58:113–126

    Google Scholar 

  • Ma F, Peterson CA (2001) Frequencies of plasmodesmata in Allium cepa L. roots: implications for solute transport pathways. J Exp Bot 52:1051–1061

    CAS  PubMed  Google Scholar 

  • Mackenzie KAD (1979) The development of the endodermis and phi layer of apple roots. Protoplasma 100:21–32

    Google Scholar 

  • Mertz RA, Brutnell TP (2014) Bundle sheath suberization in grass leaves: multiple barriers to characterization. J Exp Bot 65:3371–3380

    PubMed  Google Scholar 

  • Meyer CJ, Seago JL, Peterson CA (2009) Environmental effects on the maturation of the endodermis and multiseriate exodermis of Iris germanica roots. Ann Bot 103:687–702

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meyer CJ, Peterson CA, Steudle E (2011) Permeability of Iris germanica’s multiseriate exodermis to water, NaCl, and ethanol. J Exp Bot 62:1911–1926

    CAS  PubMed  Google Scholar 

  • Naseer S, Lee Y, Lapierre C, Franke R, Nawrath C, Geldner N (2012) Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. Proc Natl Acad Sci U S A 209:10101–10106

    Google Scholar 

  • North GB, Nobel PS (1995) Hydraulic conductivity of concentric root tissues of Agave deserti Engelm. under wet and drying conditions. New Phytol 130:47–57

    Google Scholar 

  • Osmond CB (1971) Metabolite transport in C4 photosynthesis. Aust J Biol Sci 24:159–163

    CAS  PubMed  Google Scholar 

  • Pate JS (1976) Transport in symbiotic systems fixing nitrogen. In: Lüttge U, Pitman MG (eds) Transport in plants II. Part B tissues and organs. Encyclopedia of plant physiology, New Series vol 2. Springer, Berlin, pp 278–303

    Google Scholar 

  • Pate JS, Gunning BES, Briarty LG (1969) Ultrastructure and functioning of the transport system of the leguminous root nodule. Planta 85:11–34

    CAS  PubMed  Google Scholar 

  • Perumalla CJ, Peterson CA, Enstone DE (1990) A survey of angiosperm species to detect hypodermal Casparian bands. I. Roots with a uniseriate hypodermis and epidermis. Bot J Lin Soc 103:93–112

    Google Scholar 

  • Peterson CA (1987) The exodermal Casparian band of onion roots blocks the apoplastic movement of sulphate ions. J Exp Bot 38:2068–2081

    CAS  Google Scholar 

  • Peterson CA (1988) Exodermal Casparian bands: their significance for ion uptake by roots. Physiol Plant 72:204–208

    CAS  Google Scholar 

  • Peterson CA, Emanuel ME (1981) Pathway of movement of apoplastic fluorescent dye tracers through the endodermis at the site of secondary root formation in corn (Zea mays) and broad bean (Vicia faba). Can J Bot 59:618–625

    Google Scholar 

  • Peterson CA, Enstone DE (1996) Functions of passage cells in the endodermis and exodermis of roots. Physiol Plant 97:592–598

    CAS  Google Scholar 

  • Peterson CA, Perumalla CJ (1990) A survey of angiosperm species to detect hypodermal Casparian bands. II. Roots with a multiseriate hypodermis or epidermis. Bot J Lin Soc 103:113–125

    Google Scholar 

  • Peterson CA, Emanuel ME, Weerdenburg CA (1981) The permeability of phi thickenings in apple (Pyrus malus) and geranium (Pelargonium hortorum) roots to an apoplastic fluorescent dye tracer. Can J Bot 59:1107–1110

    Google Scholar 

  • Ranathunge K, Steudle E, Lafitte R (2005) A new precipitation technique provides evidence for the permeability of the Casparian band to ions in young roots of corn (Zea mays L.) and rice (Oryza sativa L.). Plant Cell Environ 28:1450–1462

    CAS  Google Scholar 

  • Ranathunge J, Lin J, Steudle E, Schreiber L (2011) Stagnant deoxygenated growth enhances root suberization and lignifications, but differentially affects water and NaCl permeabilities in rice (Oryza sativa L.) roots. Plant Cell Environ 34:1223–1240

    CAS  PubMed  Google Scholar 

  • Reinhardt DH, Rost TL (1995) Salinity accelerates endodermal development and induces an exodermis in cotton seedling roots. Environ Exp Bot 35:563–574

    CAS  Google Scholar 

  • Robards AW (1970) Electron microscopy and plant ultrastructure. McGraw-Hill, London

    Google Scholar 

  • Robards AW, Lucas WJ (1990) Plasmodesmata. Ann Rev Plant Physiol Plant Mol Biol 41:369–419

    Google Scholar 

  • Robards AW, Robb ME (1974) The entry of ions and molecules into roots: an investigation using electron-opaque tracers. Planta 120:1–12

    CAS  PubMed  Google Scholar 

  • Robards AW, Clarkson DT, Sanderson J (1979) Structure and permeability of the epidermal/hypodermal layers of the sand sedge (Carex arenaria L.). Protoplasma 101:331–347

    CAS  Google Scholar 

  • Sack FD (1987) The structure of the stem endodermis in etiolated pea seedlings. Can J Bot 65:1514–1519

    CAS  PubMed  Google Scholar 

  • Schreiber L, Hartmann K, Skrabs M, Zeier L (1999) Apoplastic barriers in roots: chemical composition of endodermal and hypodermal cell walls. J Exp Bot 50:1267–1280

    CAS  Google Scholar 

  • Schreiber L, Franke R, Hartmann KD, Ranathunge K, Steudle E (2005) The chemical composition of suberin in apoplastic barriers affects radial hydraulic conductivity differently in the roots of rice (Oryza sativa L. cv. IR64) and corn (Zea mays L. cv. Helix). J Exp Bot 56:1427–1436

    CAS  PubMed  Google Scholar 

  • Schröder M, Kunz U, Stelzer R, Lehmann H (2002) On the evidence of a diffusion barrier in the outer cortex apoplast of cress roots (Lepidium sativum), demonstrated by analytical electron microscopy. J Plant Phys 159:1197–1204

    Google Scholar 

  • Slewinski TL, Anderson AA, Zhang CK, Turgeon R (2012) Scarecrow plays a role in establishing Kranz anatomy in maize leaves. Plant Cell Phys 53:2030–2037

    CAS  Google Scholar 

  • Steudle E (1994) Water transport across roots. Plant Soil 167:79–90

    CAS  Google Scholar 

  • Steudle E (2000) Water uptake by plant roots: an integration of views. Plant Soil 226:45–56

    CAS  Google Scholar 

  • Steudle E (2011) Hydraulic architecture of vascular plants. In: Lüttge U, Beck E, Bartels D (eds) Plant desiccation tolerance. Ecological studies, vol 215. Springer, Berlin, pp 185–207

    Google Scholar 

  • Steudle E, Peterson CA (1998) How does water get through roots? J Exp Bot 49:775–788

    CAS  Google Scholar 

  • van Bel AJE (1987) The apoplast concept of phloem loading has no universal validity. Plant Physiol Biochem 25:677–686

    Google Scholar 

  • van Bel AJE (1993) Strategies of phloem loading. Ann Rev Plant Physiol Plant Mol Biol 44:253–281

    Google Scholar 

  • van Bel AJE, Gamalei YV (1992) Ecophysiology of phloem loading in source leaves. Plant Cell Environ 15:265–270

    Google Scholar 

  • van Bel AJE, van Kesteren WJP, Papenhuijzen C (1988) Ultrastructural indications for coexistence of symplastic and apoplastic phloem loading in Commelina benghalensis leaves. Difference in ontogenic development, spatial arrangement and symplastic connections of the two sieve tubes in the minor vein. Planta 176:159–172

    PubMed  Google Scholar 

  • van Bel AJE, Gamalei YV, Ammerlaan A, Bik LPM (1992) Dissimilar phloem loading in leaves with symplasmic or apoplasmic minor-vein configurations. Planta 186:518–525

    PubMed  Google Scholar 

  • van Bel AJE, Ammerlaan A, van Dijk AA (1994) A three-step screening procedure to identify the mode of phloem loading in intact leaves. Evidence for symplasmic and apoplasmic phloem loading associated with the type of companion cell. Planta 192:31–39

    Google Scholar 

  • van Fleet DS (1961) Histochemistry and function of the endodermis. Bot Rev 27:165–220

    Google Scholar 

  • Walker NA, Pitman MG (1976) Mesurement of fluxes across membranes. In: Lüttge U, Pitman MG (eds) Transport in plants II. Part A cells. Encyclopedia of plant physiology, New Series vol 2. Springer, Berlin, pp 93–126

    Google Scholar 

  • White PJ (2001) The pathways of calcium movement to the xylem. J Exp Bot 52:891–899

    CAS  PubMed  Google Scholar 

  • Wu X, Lin JX, Lin QQ, Wang J, Schreiber L (2005) Casparian strips in needles are more solute-permeable than endodermal transport barriers in roots of Pinus bungeana. Plant Cell Physiol 46:1799–1808

    CAS  PubMed  Google Scholar 

  • Yuan F, Chen M, Leng BY, Wang BS (2013) An efficient autofluorescence method for screening Limonium bicolor mutants for abnormal salt gland density and salt secretion. S Afr J Bot 88:110–117

    CAS  Google Scholar 

  • Yuan F, Amy Lu M-J, Leng B-Y, Zheng GY, Feng Z-T, Li P-H, Zhu X-G, Wang BS (2015) Comparative transcriptome analysis of developmental stages of the Limonium bicolor leaf generates insights into salt gland differentiation. Plant Cell Environ 38:1637–1657

    CAS  PubMed  Google Scholar 

  • Yuan F, Leng B, Wang B (2016a) Progress in studying salt secretion from the salt glands in recretohalophytes: how do plants secrete salt? Frontiers Plant Sci 7:1–12

    Google Scholar 

  • Yuan F, Amy Lyu MJ, Leng B-Y, Zhu X-G, Wang B-S (2016b) The transcriptome of NaCl-treated Limonium bicolor leaves reveals the genes controlling salt secretion of salt gland. Plant Mol Biol 91:241–256

    CAS  PubMed  Google Scholar 

  • Zeier J, Schreiber L (1999) Fourier transform infrared-spectroscopic characterization of isolated endodermal cell walls from plant roots: chemical nature in relation to anatomical development. Planta 209:537–542

    CAS  PubMed  Google Scholar 

  • Zeier J, Goll A, Yokoyama M, Karahara I, Schreiber L (1999a) Structure and chemical compostition of endodermal and rhizodermal/hypodermal walls of several species. Plant Cell Environ 22:271–279

    CAS  Google Scholar 

  • Zeier J, Ruel K, Ryser U, Schreiber L (1999b) Chemical analysis and immunolocalistion of lignin and suberin in endodermal and hypodermal/rhizodermal cell walls of developing maize (Zea mays L.) primary roots. Planta 209:1–12

    CAS  PubMed  Google Scholar 

  • Ziegler H, Lüttge U (1967) Die Salzdrüsen von Limonium vulgare. II Mitteilung Die Lokalisierung des Chlorids. Planta 74:1–17

    CAS  PubMed  Google Scholar 

  • Ziegler H, Weigl J, Lüttge U (1963) Mikroautoradiographischer Nachweis der Wanderung von 35SO4−− durch die Tertiärendodermis der Iris-Wurzel. Protoplasma 56:362–370

    CAS  Google Scholar 

  • Zimmermann HM, Steudle E (1998) Apoplastic transport across young maize roots: effect of the exodermis. Planta 206:7–19

    CAS  Google Scholar 

  • Zimmermann HM, Hartmann K, Schreiber L, Steudle E (2000) Chemical composition of apoplastic transport barriers in relation to radial hydraulic conductivity of maize roots (Zea mays L.). Planta 210:302–311

    CAS  PubMed  Google Scholar 

Download references

Acknowledgment

I thank C. Barry Osmond for his help with the literature on the mesophyll/bundle sheath interface in the leaves of C4 plants. I am grateful to Rainer Matyssek for reading a draft of the essay and making valuable comments and to Francisco Cánovas for editing the essay.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ulrich Lüttge .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Lüttge, U. (2019). Bidirectional Lateral Transport Barriers in Serving Plant Organs and Integral Plant Functioning: Localized Lignification, Suberinization, and Cutinization. In: Cánovas, F.M., Lüttge, U., Risueño, MC., Pretzsch, H. (eds) Progress in Botany Vol. 82. Progress in Botany, vol 82. Springer, Cham. https://doi.org/10.1007/124_2019_36

Download citation

Publish with us

Policies and ethics