Casparian bands and suberin lamellae in exodermis of lateral roots: an important trait of roots system response to abiotic stress factors
Jazyk angličtina Země Anglie, Velká Británie Médium print
Typ dokumentu časopisecké články
PubMed
28605408
PubMed Central
PMC5737840
DOI
10.1093/aob/mcx047
PII: 3866909
Knihovny.cz E-zdroje
- Klíčová slova
- Zea mays L., apoplastic barriers, endodermis, exodermis, lateral roots, permeability, root branching, stress,
- MeSH
- epidermis rostlin chemie růst a vývoj MeSH
- fyziologický stres * MeSH
- kořeny rostlin růst a vývoj MeSH
- kukuřice setá fyziologie MeSH
- lipidy chemie MeSH
- půda MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- lipidy MeSH
- půda MeSH
- suberin MeSH Prohlížeč
BACKGROUND AND AIMS: Root absorptive characteristics rely on the presence of apoplastic barriers. However, little is known about the establishment of these barriers within a complex root system, particularly in a major portion of them - the lateral roots. In Zea mays L., the exodermis differentiates under the influence of growth conditions. Therefore, the species presents a suitable model to elucidate the cross-talk among environmental conditions, branching pattern and the maturation of barriers within a complex root system involved in the definition of the plant-soil interface. The study describes the extent to which lateral roots differentiate apoplastic barriers in response to changeable environmental conditions. METHODS: The branching, permeability of the outer cell layers and differentiation of the endo- and exodermis were studied in primary roots and various laterals under different types of stress of agronomic importance (salinity, heavy metal toxicity, hypoxia, etc.). Histochemical methods, image analysis and apoplastic tracer assays were utilized. KEY RESULTS: The results show that the impact of growth conditions on the differentiation of both the endodermis and exodermis is modulated according to the type/diameter of the root. Fine laterals clearly represent that portion of a complex root system with a less advanced state of barrier differentiation, but with substantial ability to modify exodermis differentiation in response to environmental conditions. In addition, some degree of autonomy in exodermal establishment of Casparian bands (CBs) vs. suberin lamellae (SLs) was observed, as the absence of lignified exodermal CBs did not always fit with the lack of SLs. CONCLUSIONS: This study highlights the importance of lateral roots, and provides a first look into the developmental variations of apoplastic barriers within a complex root system. It emphasizes that branching and differentiation of barriers in fine laterals may substantially modulate the root system-rhizosphere interaction.
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Aloni R, Enstone DE, Peterson CA.. 1998. Indirect evidence for bulk water flow in root cortical cell walls of three dicotyledonous species. Planta 207: 1–7.
Andersen TG, Barberon M, Geldner N.. 2015. Suberization – the second life of an endodermal cell. Current Opinion in Plant Biology 28: 9–15. PubMed
Armstrong J, Armstrong W.. 2001. Rice and Phragmites: effects of organic acids on growth, root permeability, and radial oxygen loss to the rhizosphere. American Journal of Botany 88: 1359–1370. PubMed
Armstrong J, Armstrong W.. 2005. Rice: sulfide-induced barriers to root radial oxygen loss, Fe2+ and water uptake, and lateral root emergence. Annals of Botany 96: 625–38. PubMed PMC
Armstrong W, Cousins D, Armstrong J, Turner D, Beckett P.. 2000. Oxygen distribution in wetland plant roots and permeability barriers to gas-exchange with the rhizosphere: a microelectrode and modelling study with Phragmites australis. Annals of Botany 86: 687–703.
Bagniewska-Zadworna A, Stelmasik A, Minicka J.. 2014. From birth to death – Populus trichocarpa fibrous roots functional anatomy. Biologia Plantarum 58: 551–560.
Barberon M, Vermeer JEM, De Bellis D, et al.2016. Adaptation of root function by nutrient-induced plasticity of endodermal differentiation. Cell 164: 447–459. PubMed
Brundrett MC, Enstone DE, Peterson CA.. 1988. A berberine–aniline blue fluorescent staining procedure for suberin, lignin, and callose in plant tissue. Protoplasma 146: 133–142.
Brundrett MC, Kendrick B, Peterson CA.. 1991. Efficient lipid staining in plant material with Sudan Red 7B or Fluoral Yellow 088 in polyethylene glycol–glycerol. Biotechnic and Histochemistry 66: 111–116. PubMed
Cahn M, Zobel R, Bouldin D.. 1989. Relationship between root elongation rate and diameter and duration of growth of lateral roots of maize. Plant and Soil 119: 271–279.
Casimiro I, Beeckman T, Graham N, et al.2003. Dissecting Arabidopsis lateral root development. Trends in Plant Science 8: 165–171. PubMed
Cassab GI, Eapen D, Campos ME.. 2013. Root hydrotropism: an update. American Journal of Botany 100: 14–24. PubMed
Clarkson D, Robards A, Stephens J, Stark M.. 1987. Suberin lamellae in the hypodermis of maize (Zea mays) roots; development and factors affecting the permeability of hypodermal layers. Plant, Cell & Environment 10: 83–93. PubMed
De Simone O, Haase K, Müller E, et al.2003. Apoplasmic barriers and oxygen transport properties of hypodermal cell walls in roots from four Amazonian tree species. Plant Physiology 132: 206–217. PubMed PMC
Drew M. 1975. Comparison of the effects of a localised supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytologist 75: 479–490.
Dubrovsky J, Gambetta G, Hernández-Barrera A, Shishkova S, González I.. 2006. Lateral root initiation in Arabidopsis: developmental window, spatial patterning, density and predictability. Annals of Botany 97: 903–915. PubMed PMC
Eapen D, Barroso ML, Ponce G, Campos ME, Cassab GI.. 2005. Hydrotropism: root growth responses to water. Trends in Plant Science 10: 44–50. PubMed
Enstone DE, Peterson CA.. 1997. Suberin deposition and band plasmolysis in the corn (Zea mays L.) root exodermis. Canadian Journal of Botany 75: 1188–1199.
Enstone DE, Peterson CA.. 1998. Effects of exposure to humid air on epidermal viability and suberin deposition in maize (Zea mays L.) roots. Plant, Cell & Environment 21: 837–844.
Enstone DE, Peterson CA.. 2005. Suberin lamella development in maize seedling roots grown in aerated and stagnant conditions. Plant, Cell & Environment 28: 444–455.
Enstone DE, Peterson CA, Ma F.. 2003. Root endodermis and exodermis: structure, function, and responses to the environment. Journal of Plant Growth Regulation 21: 335–351.
Esau K. 1953. Plant anatomy. New York: John Wiley & Sons, Inc.
Faiyue B, Al-Azzawi MJ, Flowers TJ.. 2010. The role of lateral roots in bypass flow in rice (Oryza sativa L.). Plant, Cell and Environment 33: 702–716. PubMed
Geldner N. 2013. The endodermis. Annual Review of Plant Biology 64: 531–558. PubMed
Henry A, Cal AJ, Batoto TC, Torres RO, Serraj R.. 2012. Root attributes affecting water uptake of rice (Oryza sativa) under drought. Journal of Experimental Botany 63: 4751–4763. PubMed PMC
Hochholdinger F. 2009. The maize root system: morphology, anatomy, and genetics In: Bennetzen JL, Hake SC, eds. Handbook of maize: its biology. New York: Springer, 145–160.
Hose E, Clarkson D, Steudle E, Schreiber L, Hartung W.. 2001. The exodermis: a variable apoplastic barrier. Journal of Experimental Botany 52: 2245–2264. PubMed
Hosmani PS, Kamiya T, Danku J, et al.2013. Dirigent domain-containing protein is part of the machinery required for formation of the lignin-based Casparian strip in the root. Proceedings of the National Academy of Sciences, USA 110: 14498–14503. PubMed PMC
Jansen L, Roberts I, De Rycke R, Beeckman T.. 2012. Phloem-associated auxin response maxima determine radial positioning of lateral roots in maize. Philosophical Transactions of the Royal Society B: Biological Sciences 367: 1525–1533. PubMed PMC
Kadam N, Yin X, Bindraban P, Struik P, Jagadish K.. 2015. Does morphological and anatomical plasticity during the vegetative stage make wheat more tolerant of water-deficit stress than rice? Plant Physiology 167: 1389–1401. PubMed PMC
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. PubMed
Kotula L, Ranathunge K, Schreiber L, Steudle E.. 2009. Functional and chemical comparison of apoplastic barriers to radial oxygen loss in roots of rice (Oryza sativa L.) grown in aerated or deoxygenated solution. Journal of Experimental Botany 60: 2155–2167. PubMed
Kotula L, Colmer TD, Nakazono M.. 2014. Effects of organic acids on the formation of the barrier to radial oxygen loss in roots of Hordeum marinum. Functional Plant Biology 41: 187–202. PubMed
Krishnamurthy P, Ranathunge K, Franke R, Prakash H, Schreiber L, Mathew M.. 2009. The role of root apoplastic transport barriers in salt tolerance of rice (Oryza sativa L.). Planta 230: 119–134. PubMed
Kroemer K. 1903. Wurzelhaut, Hypodermis und Endodermis der Angiospermenwurzel. Bibliotheca Botanica 59: 1–160.
Lux A, Šottníková A, Opatrná J, Greger M.. 2004. Differences in structure of adventitious roots in Salix clones with contrasting characteristics of cadmium accumulation and sensitivity. Physiologia Plantarum 120: 537–545. PubMed
Lux A, Martinka M, Vaculik M, White PJ.. 2011. Root responses to cadmium in the rhizosphere: a review. Journal of Experimental Botany 62: 21–37. PubMed
Meyer CJ, Seago JL Jr., Peterson CA.. 2009. Environmental effects on the maturation of the endodermis and multiseriate exodermis of Iris germanica roots. Annals of Botany 103: 687–702. PubMed PMC
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. Proceedings of the National Academy of Sciences, USA 109: 10101–10106. PubMed PMC
Orman-Ligeza B, Parizot B, Gantet PP, Beeckman T, Bennett MJ, Draye X.. 2013. Post-embryonic root organogenesis in cereals: branching out from model plants. Trends in Plant Science 18: 459–467. PubMed
Pagès L, Pellerin S.. 1994. Evaluation of parameters describing the root system architecture of field grown maize plants (Zea mays L.). Plant and Soil 164: 169–176.
Pearse A. 1968. Histochemistry (theoretical and applied). London: J. A. Churchill Ltd.
Pecková E, Tylová E, Soukup A.. 2016. Tracing root permeability: comparison of tracer methods. Biologia Plantarum 60: 695–705.
Perumalla C, Peterson CA.. 1986. Deposition of Casparian bands and suberin lamellae in the exodermis and endodermis of young corn and onion roots. Canadian Journal of Botany 64: 1873–1878.
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. Botanical Journal of the Linnean Society 103: 93–112.
Postma JA, Dathe A, Lynch JP.. 2014. The optimal lateral root branching density for maize depends on nitrogen and phosphorus availability. Plant Physiology 166: 590–602. PubMed PMC
Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MA.. 2007. Stress-induced morphogenic responses: growing out of trouble? Trends in Plant Science 12: 98–105. PubMed
Redjala T, Zelko I, Sterckeman T, Legué V, Lux A.. 2011. Relationship between root structure and root cadmium uptake in maize. Environmental and Experimental Botany 71: 241–248.
Reinhardt D, Rost T.. 1995. Salinity accelerates endodermal development and induces an exodermis in cotton seedling roots. Environmental and Experimental Botany 35: 563–574.
Reyes-Hernández BJ, Srivastava AC, Ugartechea-Chirino Y, et al.2014. The root indeterminacy-to-determinacy developmental switch is operated through a folate-dependent pathway in Arabidopsis thaliana. New Phytologist 202: 1223–1236. PubMed
Robbins NE, Trontin C, Duan L, Dinneny JR.. 2014. Beyond the barrier: communication in the root through the endodermis. Plant Physiology 166: 551–559. PubMed PMC
Shishkova S, Las Peñas ML, Napsucialy-Mendivil S, et al.2013. Determinate primary root growth as an adaptation to aridity in Cactaceae: towards an understanding of the evolution and genetic control of the trait. Annals of Botany 112: 239–252. PubMed PMC
Schreiber L, Hartmann KD, Skrabs M, Zeier J.. 1999. Apoplastic barriers in roots: chemical composition of endodermal and hypodermal cell walls. Journal of Experimental Botany 50: 1267–1280.
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). Journal of Experimental Botany 56: 1427–1436. PubMed
Soukup A. 2014. Selected simple methods of plant cell wall histochemistry and staining for light microscopy. Methods in Molecular Biology 1080: 25–40. PubMed
Soukup A, Votrubová O, Čížková H.. 2002. Development of anatomical structure of roots of Phragmites australis. New Phytologist 153: 277–287.
Soukup A, Armstrong W, Schreiber L, Franke R, Votrubova O.. 2007. Apoplastic barriers to radial oxygen loss and solute penetration: a chemical and functional comparison of the exodermis of two wetland species, Phragmites australis and Glyceria maxima. New Phytologist 173: 264–278. PubMed
Svistoonoff S, Creff A, Reymond M, et al.2007. Root tip contact with low-phosphate media reprograms plant root architecture. Nature Genetics 39: 792–796. PubMed
Thomas R, Fang X, Ranathunge K, Anderson TR, Peterson CA, Bernards MA.. 2007. Soybean root suberin: anatomical distribution, chemical composition, and relationship to partial resistance to Phytophthora sojae. Plant Physiology 144: 299–311. PubMed PMC
Varney G, McCully M.. 1991. The branch roots of Zea. II. Developmental loss of the apical meristem in field-grown roots. New Phytologist 118: 535–546.
Waisel Y, Eshel A.. 2002. Functional diversity of various constituents of a single root system In: Waisel Y, Eshel A, Kafkafi U, eds. Plant roots: the hidden half, 3rd edn. New York: Marcel Dekker, Inc, 243–268.
Walch-Liu P, Ivanov II, Filleur S, Gan Y, Remans T, Forde BG.. 2006. Nitrogen regulation of root branching. Annals of Botany 97: 875–881. PubMed PMC
Wang X, McCully M, Canny M.. 1995. Branch roots of Zea. 5: structural features that may influence water and nutrient transport. Botanica Acta 108: 209–219.
Zadworny M, Eissenstat DM.. 2011. Contrasting the morphology, anatomy and fungal colonization of new pioneer and fibrous roots. New Phytologist 190: 213–21. PubMed
Zeier J, Goll A, Yokoyama M, Karahara I, Schreiber L.. 1999a. Structure and chemical composition of endodermal and rhizodermal/hypodermal walls of several species. Plant, Cell and Environment, 22: 271–279.
Zeier J, Ruel K, Ryser U, Schreiber L.. 1999b. Chemical analysis and immunolocalisation of lignin and suberin in endodermal and hypodermal/rhizodermal cell walls of developing maize (Zea mays L.) primary roots. Planta 209: 1–12. PubMed
Zimmermann HM, Steudle E.. 1998. Apoplastic transport across young maize roots: effect of the exodermis. Planta 206: 7–19.
Zimmermann HM, Hartmann K, Schreiber L, Steudle E.. 2000. Chemical composition of apoplastic transport barriers in relation to radial hydraulic conductivity of corn roots (Zea mays L.). Planta 210: 302–311. PubMed
Exodermis and Endodermis Respond to Nutrient Deficiency in Nutrient-Specific and Localized Manner