Apoplastic barriers of Populus ×  canescens roots in reaction to different cultivation conditions and abiotic stress treatments

Abstract

Populus is an important tree genus frequently cultivated for economical purposes. However, the high sensitivity of poplars towards water deficit, drought, and salt accumulation significantly affects plant productivity and limits biomass yield. Various cultivation and abiotic stress conditions have been described to significantly induce the formation of apoplastic barriers (Casparian bands and suberin lamellae) in roots of different monocotyledonous crop species. Thus, this study aimed to investigate to which degree the roots of the dicotyledonous gray poplar (Populus ×  canescens) react to a set of selected cultivation conditions (hydroponics, aeroponics, or soil) and abiotic stress treatments (abscisic acid, oxygen deficiency) because a differing stress response could potentially help in explaining the observed higher stress susceptibility. The apoplastic barriers of poplar roots cultivated in different environments were analyzed by means of histochemistry and gas chromatography and compared to the available literature on monocotyledonous crop species. Overall, dicotyledonous poplar roots showed only a remarkably low induction or enhancement of apoplastic barriers in response to the different cultivation conditions and abiotic stress treatments. The genetic optimization (e.g., overexpression of biosynthesis key genes) of the apoplastic barrier development in poplar roots might result in more stress-tolerant cultivars in the future.

Keywords

Hydroponics / Aeroponics / Soil / Abscisic acid (ABA) / Oxygen deficiency / Poplar root suberin

References

[1] AbramoffMD, MagalhãesPJ, RamSJ. Image Processing with ImageJ, 2004, 11: 36-42

[2] AishanT, HalikÜ, KurbanA, CyffkaB, KubaM, BetzF, KeyimuM. Eco-morphological response of floodplain forests (Populus euphratica Oliv.) to water diversion in the lower Tarim River, northwest China. Environ Earth Sci, 2015, 73: 533-545

[3] Al AfasN, MarronN, CeulemansR. Clonal variation in stomatal characteristics related to biomass production of 12 poplar (Populus) clones in a short rotation coppice culture. Environ Exp Bot, 2006, 58: 279-286

[4] AllenSJ, HallRL, RosierPTW. Transpiration by two poplar varieties grown as coppice for biomass production. Tree Physiol, 1999, 19: 493-501

[5] Bagniewska-ZadwornaA, StelmasikA, MinickaJ. From birth to death - Populus trichocarpa fibrous roots functional anatomy. Biol Plant, 2014, 58: 551-560

[6] BallachHJ, WittigR. Reciprocal Effects of Platinum and Lead on the Water Household of Poplar Cuttings. Environ Sci Pollut Res, 1996, 3: 3-9

[7] BarberonM. The endodermis as a checkpoint for nutrients. New Phytol, 2017, 213: 1604-1610

[8] BelliniC, PăcurarDI, PerroneI. Adventitious Roots and Lateral Roots: Similarities and Differences. Annu Rev Plant Biol, 2014, 65: 639-666

[9] BoluWH, PolleA. Growth and stress reactions in roots and shoots of a salt-sensitive poplar species (Populus x canescens). Trop Ecol, 2004, 45: 161-171

[10] BrundrettMC, EnstoneDE, PetersonCA. A Berberine-Aniline Blue Fluorescent Staining Procedure for Suberin, Lignin, and Callose in Plant Tissue. Protoplasma, 1988, 146: 133-142

[11] BrundrettMC, KendrickB, PetersonCA. Efficient Lipid Staining in Plant Material with Sudan Red 7B or Fluoral Yellow 088 in Polyethylene Glycol-Glycerol. Biotech Histochem, 1991, 66: 111-116

[12] BrunnerI, HerzogC, DawesMA, ArendM, SperisenC. How tree roots respond to drought. Front Plant Sci, 2015, 6: 547

[13] ChenS, PolleA. Salinity tolerance of Populus. Plant Biol, 2010, 12: 317-333

[14] ChenYP, ChenYN, LiWH, XuCC. Characterization of photosynthesis of Populus euphratica grown in the arid region. Photosynthetica, 2006, 44: 622-626

[15] ColmerTD. Aerenchyma and an Inducible Barrier to Radial Oxygen Loss Facilitate Root Aeration in Upland, Paddy and Deep-water Rice (Oryza sativa L.). Ann Bot, 2003, 91: 301-309

[16] ColmerTD, GibberdMR, WiengweeraA, TinhTK. The barrier to radial oxygen loss from roots of rice (Oryza sativa L.) is induced by growth in stagnant solution. J Exp Bot, 1998, 49: 1431-1436

[17] Delude C, Vishwanath SJ, Rowland O, Domergue F (2017) Root Aliphatic Suberin Analysis Using Non-extraction or Solvent-extraction Methods. Bio-protocol 7:e2331. https://doi.org/10.21769/BioProtoc.2331

[18] DillenSY, RoodSB, CeulemansR. JanssonS, BhaleraoR, GrooverA. Growth and Physiology. Genetics and Genomics of Populus, 2010 Berlin, Heidelberg, New York Springer 39-63

[19] EckenwalderJE. StettlerRF, BradshawT, HeilmanP, HinckleyT. Systematics and evolution of Populus. Biology of Populus and its Implications for Management and Conservation, Part 1, 1996 Ottawa NRC Research Press 7-32

[20] EnstoneDE, PetersonCA. Suberin deposition and band plasmolysis in the corn (Zea mays L.) root exodermis. Can J Bot, 1997, 75: 1188-1199

[21] EnstoneDE, PetersonCA, MaF. Root Endodermis and Exodermis: Structure, Function, and Responses to the Environment. J Plant Growth Regul, 2003, 21: 335-351

[22] EsauK. Anatomy of Seed Plants, 1977 2 New York Wiley

[23] GambettaGA, FeiJ, RostTL, KnipferT, MatthewsMA, ShackelKA, WalkerMA, McElroneAJ. Water Uptake along the Length of Grapevine Fine Roots: Developmental Anatomy, Tissue-Specific Aquaporin Expression, and Pathways of Water Transport. Plant Physiol, 2013, 163: 1254-1265

[24] Grünhofer P, Schreiber L (2023) Cutinized and suberized barriers in leaves and roots: Similarities and differences. J Plant Physiol 282:153921. https://doi.org/10.1016/j.jplph.2023.153921

[25] GrünhoferP, GuoY, LiR, LinJ, SchreiberL. Hydroponic cultivation conditions allowing the reproducible investigation of poplar root suberization and water transport. Plant Methods, 2021, 17: 129

[26] GrünhoferP, HerzigL, SchreiberL. Leaf morphology, wax composition, and residual (cuticular) transpiration of four poplar clones. Trees, 2021, 36: 645-658

[27] GrünhoferP, SchreiberL, KresziesT. BaluškaF, MukherjeeS. Suberin in Monocotyledonous Crop Plants: Structure and Function in Response to Abiotic Stresses. Rhizobiology: Molecular Physiology of Plant Roots, 2021 Cham Springer International Publishing 333-378

[28] Grünhofer P, Stöcker T, Guo Y, Li R, Lin J, Ranathunge K, Schoof H, Schreiber L (2022) Populus × canescens root suberization in reaction to osmotic and salt stress is limited to the developing younger root tip region. Physiol Plant 174:e13765. https://doi.org/10.1111/ppl.13765

[29] Hoagland, D.R. & Arnon, D.I. (1950) The water-culture method for growing plants without soil. Circular, 347. Berkeley, University of California. https://doi.org/10.1111/ppl.13765

[30] HoseE, ClarksonDT, SteudleE, SchreiberL, HartungW. The exodermis: a variable apoplastic barrier. J Exp Bot, 2001, 52: 2245-2264

[31] IsebrandsJG, RichardsonJ. Poplars and Willows: Trees for Society and the Environment, 2014 Wallingford, UK CABI

[32] KavkaM, PolleA. Phosphate uptake kinetics and tissue-specific transporter expression profiles in poplar (Populus × canescens) at different phosphorus availabilities. BMC Plant Biol, 2016, 16: 206

[33] KnipferT, DanjouM, VionneC, FrickeW. Salt stress reduces root water uptake in barley (Hordeum vulgare L.) through modification of the transcellular transport path. Plant Cell Environ, 2020, 44: 1-18

[34] KotulaL, RanathungeK, SchreiberL, SteudleE. Functional and chemical comparison of apoplastic barriers to radial oxygen loss in roots of rice (Oryza sativa L.) grown in aerated or deoxygenated solution. J Exp Bot, 2009, 60: 2155-2167

[35] KresziesT, ShellakkuttiN, OsthoffA, YuP, BaldaufJA, Zeisler-DiehlVV, RanathungeK, HochholdingerF, SchreiberL. Osmotic stress enhances suberization of apoplastic barriers in barley seminal roots: analysis of chemical, transcriptomic and physiological responses. New Phytol, 2019, 221: 180-194

[36] KresziesT, EggelsS, KresziesV, OsthoffA, ShellakkuttiN, BaldaufJA, Zeisler-DiehlVV, HochholdingerF, RanathungeK, SchreiberL. Seminal roots of wild and cultivated barley differentially respond to osmotic stress in gene expression, suberization, and hydraulic conductivity. Plant Cell Environ, 2020, 43: 344-357

[37] KreuzwieserJ, HaubergJ, HowellKA, CarrollA, RennenbergH, MillarAH, WhelanJ. Differential Response of Gray Poplar Leaves and Roots Underpins Stress Adaptation during Hypoxia. Plant Physiol, 2009, 149: 461-473

[38] KrishnamurthyP, RanathungeK, FrankeR, PrakashHS, SchreiberL, MathewMK. The role of root apoplastic transport barriers in salt tolerance of rice (Oryza sativa L.). Planta, 2009, 230: 119-134

[39] KrishnamurthyP, RanathungeK, NayakS, SchreiberL, MathewMK. Root apoplastic barriers block Na⁺ transport to shoots in rice (Oryza sativa L.). J Exp Bot, 2011, 62: 4215-4228

[40] KrömerK. Wurzelhaut, Hypodermis und Endodermis der Angiospermenwurzel. Biblioth Bot, 1903, 59: 1-160

[41] LarchevêqueM, MaurelM, DesrochersA, LarocqueGR. How does drought tolerance compare between two improved hybrids of balsam poplar and an unimproved native species?. Tree Physiol, 2011, 31: 240-249

[42] MiyamotoN, SteudleE, HirasawaT, LafitteR. Hydraulic conductivity of rice roots. J Exp Bot, 2001, 52: 1835-1846

[43] NetzerF, MuellerCW, ScheererU, GrünerJ, Kögel-KnabnerI, HerschbachC, RennenbergH. Phosphorus nutrition of Populus × canescens reflects adaptation to high P-availability in the soil. Tree Physiol, 2018, 38: 6-24

[44] OttowEA, BrinkerM, TeichmannT, FritzE, KaiserW, BroschéM, KangasjärviJ, JiangX, PolleA. Populus euphratica Displays Apoplastic Sodium Accumulation, Osmotic Adjustment by Decreases in Calcium and Soluble Carbohydrates, and Develops Leaf Succulence under Salt Stress. Plant Physiol, 2005, 139: 1762-1772

[45] PedersenO, SauterM, ColmerTD, NakazonoM. Regulation of root adaptive anatomical and morphological traits during low soil oxygen. New Phytol, 2020, 229: 42-49

[46] PengY, ZhouZ, TongR, HuX, DuK. Anatomy and ultrastructure adaptations to soil flooding of two full-sib poplar clones differing in flood-tolerance. Flora, 2017, 233: 90-98

[47] PerumallaCJ, PetersonCA. Deposition of Casparian bands and suberin lamellae in the exodermis and endodermis of young corn and onion roots. Can J Bot, 1986, 64: 1873-1878

[48] PolleA, ChenS. On the salty side of life: molecular, physiological and anatomical adaptation and acclimation of trees to extreme habitats. Plant Cell Environ, 2015, 38: 1794-1816

[49] PolleA, ChenSL, EckertC, HarfoucheA. Engineering Drought Resistance in Forest Trees. Front Plant Sci, 2019, 9: 1875

[50] QiuD, BaiS, MaJ, ZhangL, ShaoF, ZhangK, YangY, SunT, HuangJ, ZhouY, GalbraithDW, WangZ, SunG. The genome of Populus alba x Populus tremula var. glandulosa clone 84K. DNA Res, 2019, 26: 423-431

[51] RanathungeK, LinJ, SteudleE, SchreiberL. Stagnant deoxygenated growth enhances root suberization and lignifications, but differentially affects water and NaCl permeabilities in rice (Oryza sativa L.) roots. Plant Cell Environ, 2011, 34: 1223-1240

[52] RanathungeK, SchreiberL, FrankeR. Suberin research in the genomics era - New interest for an old polymer. Plant Sci, 2011, 180: 399-413

[53] RedjalaT, ZelkoI, SterckemanT, LeguéV, LuxA. Relationship between root structure and root cadmium uptake in maize. Environ Exp Bot, 2011, 71: 241-248

[54] ReinhardtDH, RostTL. Salinity accelerates endodermal development and induces an exodermis in cotton seedling roots. Environ Exp Bot, 1995, 35: 563-574

[55] RobisonDJ, RaffaKF. Productivity, drought tolerance and pest status of hybrid Populus: tree improvement and silvicultural implications. Biomass Bioenerg, 1998, 14: 1-20

[56] SannigrahiP, RagauskasAJ. Poplar as a feedstock for biofuels: A review of compositional characteristics. Biofuels, Bioprod Biorefin, 2010, 4: 209-226

[57] SchreiberL, FrankeRB. Endodermis and Exodermis in Roots, 2011 Chichester John Wiley & Sons, Ltd

[58] SchreiberL, FrankeR, HartmannK. Effects of NO₃ deficiency and NaCl stress on suberin deposition in rhizo- and hypodermal (RHCW) and endodermal cell walls (ECW) of castor bean (Ricinus communis L.) roots. Plant Soil, 2005, 269: 333-339

[59] ShionoK, AndoM, NishiuchiS, TakahashiH, WatanabeK, NakamuraM, MatsuoY, YasunoN, YamanouchiU, FujimotoM, TakanashiH, RanathungeK, FrankeRB, ShitanN, NishizawaNK, TakamureI, YanoM, TsutsumiN, SchreiberL, YazakiK, NakazonoM, KatoK. RCN1/OsABCG5, an ATP-binding cassette (ABC) transporter, is required for hypodermal suberization of roots in rice (Oryza sativa). Plant J, 2014, 80: 40-51

[60] SiemensJA, ZwiazekJJ. Effects of water deficit stress and recovery on the root water relations of trembling aspen (Populus tremuloides) seedlings. Plant Sci, 2003, 165: 113-120

[61] SilimS, NashR, ReynardD, WhiteB, SchroederW. Leaf gas exchange and water potential responses to drought in nine poplar (Populus spp.) clones with contrasting drought tolerance. Trees, 2009, 23: 959-969

[62] StolárikováM, VaculíkM, LuxA, BaccioD, MinnocciA, AndreucciA, SebastianiL. Anatomical differences of poplar (Populus × euramericana clone I-214) roots exposed to zinc excess. Biologia, 2012, 67: 483-489

[63] Stoláriková-VaculíkováM, RomeoS, MinnocciA, LuxováM, VaculíkM, LuxA, SebastianiL. Anatomical, biochemical and morphological responses of poplar Populus deltoides clone Lux to Zn excess. Environ Exp Bot, 2015, 109: 235-243

[64] StrohmM, EiblmeierM, LangebartelsC, JouaninL, PolleA, SandermannH, RennenbergH. Responses of transgenic poplar (Populus tremula × P. alba) overexpressing glutathione synthetase or glutathione reductase to acute ozone stress: visible injury and leaf gas exchange. J Exp Bot, 1999, 50: 365-374

[65] TaylorG. Populus: Arabidopsis for Forestry. Do We Need a Model Tree?. Ann Bot, 2002, 90: 681-689

[66] TsaiC-J, HardingSA, TschaplinskiTJ, LindrothRL, YuanY. Genome-wide analysis of the structural genes regulating defense phenylpropanoid metabolism in Populus. New Phytol, 2006, 172: 47-62

[67] TuskanGA, DifazioS, JanssonS, BohlmannJ, GrigorievI, HellstenU, PutnamN, RalphS, RombautsS, SalamovA. The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray). Science, 2006, 313: 1596-1604

[68] TylováE, PeckováE, BlascheováZ, SoukupA. Casparian bands and suberin lamellae in exodermis of lateral roots: an important trait of roots system response to abiotic stress factors. Ann Bot, 2017, 120: 71-85

[69] van LooM, JosephJA, HeinzeB, FayMF, LexerC. Clonality and spatial genetic structure in Populus x canescens and its sympatric backcross parent P. alba in a Central European hybrid zone. New Phytol, 2008, 177: 506-516

[70] VishwanathSJ, DeludeC, DomergueF, RowlandO. Suberin: biosynthesis, regulation, and polymer assembly of a protective extracellular barrier. Plant Cell Rep, 2015, 34: 573-586

[71] VoicuMC, ZwiazekJJ. Cycloheximide inhibits root water flow and stomatal conductance in aspen (Populus tremuloides) seedlings. Plant Cell Environ, 2004, 27: 199-208

[72] WanX, ZwiazekJJ. Root water flow and leaf stomatal conductance in aspen (Populus tremuloides) seedlings treated with abscisic acid. Planta, 2001, 213: 741-747

[73] WangP, WangC-M, GaoL, CuiY-N, YangH-L, de SilvaNDG, MaQ, FlowersTJ, RowlandO, WangS-M. Aliphatic suberin confers salt tolerance to Arabidopsis by limiting Na⁺ influx, K⁺ efflux and water backflow. Plant Soil, 2020, 448: 603-620

[74] XuX, XiaoL, FengJ, ChenN, ChenY, SongB, XueK, ShiS, ZhouY, JenksMA. Cuticle lipids on heteromorphic leaves of Populus euphratica Oliv. growing in riparian habitats differing in available soil moisture. Physiol Plant, 2016, 158: 318-330

[75] Zeier J (1998) Pflanzliche Abschlussgewebe der Wurzel: Chemische Zusammensetzung und Feinstruktur der Endodermis in Abhängigkeit von Entwicklung und äußeren Faktoren. Doctoral Thesis. Julius-Maximilians-University, Würzburg. https://doi.org/10.1007/978-3-030-84985-6_19

[76] ZeierJ, SchreiberL. Chemical Composition of Hypodermal and Endodermal Cell Walls and Xylem Vessels Isolated from Clivia miniata. Plant Physiol, 1997, 113: 1223-1231

[77] ZeierJ, SchreiberL. Comparative investigation of primary and tertiary endodermal cell walls isolated from the roots of five monocotyledoneous species: chemical composition in relation to fine structure. Planta, 1998, 206: 349-361

[78] ZhouHH, ChenYN, LiWH, ChenYP. Photosynthesis of Populus euphratica in relation to groundwater depths and high temperature in arid environment, northwest China. Photosynthetica, 2010, 48: 257-268

[79] ZimmermannHM, HartmannK-D, SchreiberL, SteudleE. Chemical composition of apoplastic transport barriers in relation to radial hydraulic conductivity of corn roots (Zea mays L.). Planta, 2000, 210: 302-311

Funding

Deutsche Forschungsgemeinschaft(391657309)