Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Anatomical and biochemical characterisation of a barrier to radial O2 loss in adventitious roots of two contrasting Hordeum marinum accessions

Lukasz Kotula A C E , Lukas Schreiber B , Timothy D. Colmer C D and Mikio Nakazono A C
+ Author Affiliations
- Author Affiliations

A Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa, Nagoya 464-8601, Japan.

B Department of Ecophysiology, Institute of Cellular and Molecular Botany, University of Bonn, Kirschallee 1, D-53115 Bonn, Germany.

C UWA School of Agriculture and Environment, Faculty of Science, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

D The UWA Institute of Agriculture, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

E Corresponding author. Email: lukasz.kotula@uwa.edu.au

Functional Plant Biology 44(9) 845-857 https://doi.org/10.1071/FP16327
Submitted: 22 September 2016  Accepted: 14 February 2017   Published: 29 March 2017

Abstract

A barrier to radial O2 loss (ROL) in roots is an adaptive trait of waterlogging-tolerant plants. Hordeum marinum Huds. is a waterlogging-tolerant species that, in contrast to its waterlogging-sensitive cultivated relatives, forms a tight barrier to ROL in basal root zones. To evaluate the nature of the barrier to ROL in roots, we combined measurements of ROL with histochemical and biochemical studies of two contrasting H. marinum accessions. H21 formed greater aerenchyma (up to 38% of cross-sectional area) and a tight barrier to ROL when grown under deoxygenated stagnant conditions, whereas the barrier was only partially formed in roots of H90 and aerenchyma was up to 26%. A tight barrier to ROL in roots of H21 corresponded with strong suberisation of the exodermis. In agreement with anatomical studies, almost all aliphatic suberin quantities were greater in roots of H21 grown under stagnant conditions compared with roots from aerated controls, and also to those in H90. By contrast to suberin, no differences in root lignification were observed between the two accessions raised in either aerated or stagnant conditions. These findings show that in adventitious roots of H. marinum, suberisation rather than lignification restricts ROL from the basal root zones.

Additional keywords: aerenchyma, apoplastic barrier, exodermis, suberin, waterlogging tolerance, wild Triticeae.


References

Abiko T, Kotula L, Shiono K, Malik AI, Colmer TD, Nakazono M (2012) Enhanced formation of aerenchyma and induction of a barrier to radial oxygen loss in adventitious roots of Zea nicaraguensis contribute to its waterlogging tolerance as compared with maize (Zea mays ssp. mays). Plant, Cell & Environment 35, 1618–1630.
Enhanced formation of aerenchyma and induction of a barrier to radial oxygen loss in adventitious roots of Zea nicaraguensis contribute to its waterlogging tolerance as compared with maize (Zea mays ssp. mays).CrossRef | 1:CAS:528:DC%2BC38XhtFKlsrrI&md5=187c472f4388108127c432802d039f7fCAS |

Armstrong W (1979) Aeration in higher plants. Advances in Botanical Research 7, 225–332.
Aeration in higher plants.CrossRef | 1:CAS:528:DyaL3cXhsVeiu7c%3D&md5=bd7ac671ff6c7a11056c42b86a2c3f67CAS |

Armstrong W (1994) Polarographic oxygen electrodes and their use in plant aeration studies. Proceedings of the Royal Society of Edinburgh Section B-Biological Sciences 102, 511–527.

Armstrong W, Wright EJ (1975) Radial oxygen loss from roots: the theoretical basis for the manipulation of flux data obtained by the cylindrical platinum electrode technique. Physiologia Plantarum 35, 21–26.
Radial oxygen loss from roots: the theoretical basis for the manipulation of flux data obtained by the cylindrical platinum electrode technique.CrossRef |

Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annual Review of Plant Biology 59, 313–339.
Flooding stress: acclimations and genetic diversity.CrossRef | 1:CAS:528:DC%2BD1cXntFaqsLc%3D&md5=d90a6c2ec0e60f70cf1ac88123e7f803CAS |

Boudet A-M (1998) A new view of lignification. Trends in Plant Science 3, 67–71.
A new view of lignification.CrossRef |

Brundrett MC, Kendrick B, Peterson CA (1991) Efficient lipid staining in plant material with sudan red 7B or fluorol yellow 088 in polyethylene glycol-glycerol. Biotechnic & Histochemistry 66, 111–116.
Efficient lipid staining in plant material with sudan red 7B or fluorol yellow 088 in polyethylene glycol-glycerol.CrossRef | 1:STN:280:DyaK3MzmtlCktg%3D%3D&md5=604d2779f56ae7ae3ff37d631844845cCAS |

Campbell MM, Sederoff RR (1996) Variation in lignin content and composition: mechanism of control and implications for the genetic improvements of plants. Plant Physiology 110, 3–13.
Variation in lignin content and composition: mechanism of control and implications for the genetic improvements of plants.CrossRef | 1:CAS:528:DyaK28XltFGgtA%3D%3D&md5=a0af8c9e96dab6fcf3a2a5674f9529adCAS |

Colmer TD (2003) Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant, Cell & Environment 26, 17–36.
Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots.CrossRef | 1:CAS:528:DC%2BD3sXhtlKrtLs%3D&md5=7cd6e1d97585c4a75886b1021b03461fCAS |

Colmer TD, Voesenek LACJ (2009) Flooding tolerance: suits of plant traits in variable environments. Functional Plant Biology 36, 665–681.
Flooding tolerance: suits of plant traits in variable environments.CrossRef |

Colmer TD, Gibberd MR, Wiengweera A, Tinh TK (1998) The barrier to radial oxygen loss from roots of rice (Oryza sativa L.) is induced by growth in stagnant solution. Journal of Experimental Botany 49, 1431–1436.
The barrier to radial oxygen loss from roots of rice (Oryza sativa L.) is induced by growth in stagnant solution.CrossRef | 1:CAS:528:DyaK1cXlsVOkt7k%3D&md5=bfeba989d15b1340ebac6bb292201742CAS |

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 Physiology 132, 206–217.
Apoplastic barriers and oxygen transport properties of hypodermal cell walls in roots from four Amazonian tree species.CrossRef | 1:CAS:528:DC%2BD3sXktVGgsL0%3D&md5=ad3728da374592ea197a3bdf48cfc954CAS |

Enstone ED, Peterson CA (2005) Suberin lamellae development in maize seedling roots grown in aerated and stagnant conditions. Plant, Cell & Environment 28, 444–455.
Suberin lamellae development in maize seedling roots grown in aerated and stagnant conditions.CrossRef |

Freudenberg K (1965) Lignin: its composition and formation from p-hydroxycinnamyl alcohols. Science 148, 595–600.
Lignin: its composition and formation from p-hydroxycinnamyl alcohols.CrossRef | 1:CAS:528:DyaF2MXktFWnsr8%3D&md5=8145a5b1cea8382b73923785261ed878CAS |

Garthwaite AJ, von Bothmer R, Colmer TD (2003) Diversity in root aeration traits associated with waterlogging tolerance in the genus Hordeum. Functional Plant Biology 30, 875–889.
Diversity in root aeration traits associated with waterlogging tolerance in the genus Hordeum.CrossRef |

Garthwaite AJ, Armstrong W, Colmer TD (2008) Assessment of O2 diffusivity across the barrier to radial O2 loss in adventitious roots of Hordeum marinum. New Phytologist 179, 405–416.
Assessment of O2 diffusivity across the barrier to radial O2 loss in adventitious roots of Hordeum marinum.CrossRef | 1:CAS:528:DC%2BD1cXpsVOgtL8%3D&md5=d4fcd9c3513e432311ce063320187ff1CAS |

Herzog M, Striker GG, Colmer TD, Pedersen O (2016) Mechanisms of waterlogging tolerance in wheat – a review of root and shoot physiology. Plant, Cell & Environment 39, 1068–1086.
Mechanisms of waterlogging tolerance in wheat – a review of root and shoot physiology.CrossRef | 1:CAS:528:DC%2BC28XlvVaitLg%3D&md5=508e5fcf5d45eb9688a05ead789d2847CAS |

Justin SHFW, Armstrong W (1987) The anatomical characteristics of roots and plant response to soil flooding. New Phytologist 106, 465–495.
The anatomical characteristics of roots and plant response to soil flooding.CrossRef |

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.
Functional and chemical comparison of apoplastic barriers to radial oxygen loss in roots of rice (Oryza sativa L.) grown in aerated or deoxygenated solution.CrossRef | 1:CAS:528:DC%2BD1MXmtFSjtLo%3D&md5=2cf8b47dbda71a7b0304cd95bddc6955CAS |

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.
Effects of organic acids on the formation of the barrier to radial oxygen loss in roots of Hordeum marinum.CrossRef | 1:CAS:528:DC%2BC2cXjtFOlsA%3D%3D&md5=d3343e6ce380222ca70e7260b7c841a4CAS |

Kotula L, Clode PL, Striker GG, Pedersen O, Läuchli A, Shabala S, Colmer TD (2015) Oxygen deficiency and salinity affect cell-specific ion concentrations in adventitious roots of barley (Hordeum vulgare). New Phytologist 208, 1114–1125.
Oxygen deficiency and salinity affect cell-specific ion concentrations in adventitious roots of barley (Hordeum vulgare).CrossRef | 1:CAS:528:DC%2BC2MXhvVWqs7bI&md5=fcc50248d8437cead7b7b555250f6199CAS |

Lux A, Morita S, Abe J, Ito K (2005) An improved method for clearing and staining free-hand sections and whole-mount samples. Annals of Botany 96, 989–996.
An improved method for clearing and staining free-hand sections and whole-mount samples.CrossRef |

Malik AI, English JP, Colmer TD (2009) Tolerance of Hordeum marinum accessions to O2 deficiency, salinity and these stresses combined. Annals of Botany 103, 237–248.
Tolerance of Hordeum marinum accessions to O2 deficiency, salinity and these stresses combined.CrossRef | 1:CAS:528:DC%2BD1MXjsFCktbc%3D&md5=72f8bd80fad65d5eb8883aa1daa87777CAS |

Malik AI, Islam AKMR, Colmer TD (2011) Transfer of the barrier to radial oxygen loss in roots of Hordeum marinum to wheat (Triticum aestivum): evaluation of four H. marinum-wheat amphiploids. New Phytologist 190, 499–508.
Transfer of the barrier to radial oxygen loss in roots of Hordeum marinum to wheat (Triticum aestivum): evaluation of four H. marinum-wheat amphiploids.CrossRef | 1:STN:280:DC%2BC3MzjvFaruw%3D%3D&md5=fe4779c83550ce29003208c03015b52aCAS |

McDonald MP, Galwey NW, Colmer TD (2001) Waterlogging tolerance in the tribe Triticeae: the adventitious roots of Critesion marinum have a relatively high porosity and a barrier to radial oxygen loss. Plant, Cell & Environment 24, 585–596.
Waterlogging tolerance in the tribe Triticeae: the adventitious roots of Critesion marinum have a relatively high porosity and a barrier to radial oxygen loss.CrossRef |

Ranathunge K, Lin J, Steudle E, Schreiber L (2011) Stagnant deoxygenated growth enhances root suberization and lignification, but differentially affects water and NaCl permeabilities in rice (Oryza sativa L.) roots. Plant, Cell & Environment 34, 1223–1240.
Stagnant deoxygenated growth enhances root suberization and lignification, but differentially affects water and NaCl permeabilities in rice (Oryza sativa L.) roots.CrossRef | 1:CAS:528:DC%2BC3MXhtVOntbrO&md5=ba0dd505edabd976dce9e2c967811b7aCAS |

Schreiber L, Hartmann K, Skrabs M, Zeier J (1999) Apoplastic barriers on roots; chemical composition of endodermal and hypodermal cell walls. Journal of Experimental Botany 50, 1267–1280.

Schreiber L, Franke R, Hartmann K-D, 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.
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).CrossRef | 1:CAS:528:DC%2BD2MXksVKmt7o%3D&md5=8eb90ac03b9bbe1c949163362bb8fa10CAS |

Setter TL, Waters I (2003) Review of prospects for germplasm improvement for waterlogging tolerance in wheat, barley and oats. Plant and Soil 253, 1–34.
Review of prospects for germplasm improvement for waterlogging tolerance in wheat, barley and oats.CrossRef | 1:CAS:528:DC%2BD3sXltVemsb4%3D&md5=7473c39317add5fab1cf03665dbbbd5aCAS |

Shiono K, Yamauchi T, Yamazaki S, Mohanty B, Malik AI, Nagamura Y, Nishizawa NK, Tsutsumi N, Colmer TD, Nakazono M (2014) Microarray analysis of laser-microdissected tissues indicates the biosynthesis of suberin in the outer part of roots during formation of a barrier to radial oxygen loss in rice (Oryza sativa). Journal of Experimental Botany 65, 4795–4806.
Microarray analysis of laser-microdissected tissues indicates the biosynthesis of suberin in the outer part of roots during formation of a barrier to radial oxygen loss in rice (Oryza sativa).CrossRef | 1:CAS:528:DC%2BC2MXitl2gtbw%3D&md5=5f0e24f6280165f2113bb0612b10975bCAS |

Soukup A, Votrubova O, Cizkova H (2002) Development of anatomical structure of root of Phragmites australis. New Phytologist 153, 277–287.
Development of anatomical structure of root of Phragmites australis.CrossRef |

Soukup A, Armstrong W, Schreiber L, Franke R, Votrubová 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.
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.CrossRef | 1:CAS:528:DC%2BD2sXhvVSltbc%3D&md5=b2861058cdf430f17d5caa53bd42f683CAS |

Striker GG, Insausti P, Grimoldi AA, Vega AS (2007) Trade-off between root porosity and mechanical strength in species with different types of aerenchyma. Plant, Cell & Environment 30, 580–589.
Trade-off between root porosity and mechanical strength in species with different types of aerenchyma.CrossRef | 1:STN:280:DC%2BD2s3gsVOqsg%3D%3D&md5=972da6cff3c7ef18c1d1f2be48e0737aCAS |

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.
Soybean root suberin: anatomical distribution, chemical composition, and relationship to partial resistance to Phytophthora sojae.CrossRef | 1:CAS:528:DC%2BD2sXls1Kjtbw%3D&md5=63038b8249707f7785ca93877d07845dCAS |

Wiengweera A, Greenway H, Thomson CJ (1997) The use of agar nutrient solution to simulate lack of convection in waterlogged soils. Annals of Botany 80, 115–123.
The use of agar nutrient solution to simulate lack of convection in waterlogged soils.CrossRef |

Zeier J, Schreiber L (1997) Chemical composition of hypodermal and endodermal cell walls and xylem vessels isolated from Clivia miniata. Plant Physiology 113, 1223–1231.
Chemical composition of hypodermal and endodermal cell walls and xylem vessels isolated from Clivia miniata.CrossRef | 1:CAS:528:DyaK2sXis1Gktro%3D&md5=55af07dc2457ba76b741474bc78d141aCAS |

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 & Environment 22, 271–279.
Structure and chemical composition of endodermal and rhizodermal/hypodermal walls of several species.CrossRef | 1:CAS:528:DyaK1MXjt1Wru74%3D&md5=ff013effd0409c4a2904341d8ffcd3e4CAS |

Zeier J, Ruel K, Ryser U, Schreiber L (1999b) Chemical analysis and immunolocalisation of lignin and suberin in endodermal and hypoermal/rhizodermal cell walls of developing maize (Zea mays L.) primary roots. Planta 209, 1–12.
Chemical analysis and immunolocalisation of lignin and suberin in endodermal and hypoermal/rhizodermal cell walls of developing maize (Zea mays L.) primary roots.CrossRef | 1:CAS:528:DyaK1MXkvVCltLY%3D&md5=982d5deed0e65869796e1ab8af7a44b2CAS |



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