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Effects of water stress on apoplastic barrier formation in soil grown roots differ from hydroponically grown roots: Histochemical, biochemical and molecular evidence.

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العنوان: Effects of water stress on apoplastic barrier formation in soil grown roots differ from hydroponically grown roots: Histochemical, biochemical and molecular evidence.
المؤلفون: Suresh K; Department of Ecophysiology, Institute of Cellular and Molecular Botany, University of Bonn, Bonn, Germany., Bhattacharyya S; Plant Cell Biology, Institute of Cellular and Molecular Botany, University of Bonn, Bonn, Germany., Carvajal J; Department of Ecophysiology, Institute of Cellular and Molecular Botany, University of Bonn, Bonn, Germany., Ghosh R; Department of Experimental Plant Biology, Charles University, Praha, Czech Republic., Zeisler-Diehl VV; Department of Ecophysiology, Institute of Cellular and Molecular Botany, University of Bonn, Bonn, Germany., Böckem V; Plant Sciences (IBG-2), Forschungszentrum Jülich GmbH, Jülich, Germany., Nagel KA; Plant Sciences (IBG-2), Forschungszentrum Jülich GmbH, Jülich, Germany., Wojciechowski T; Plant Sciences (IBG-2), Forschungszentrum Jülich GmbH, Jülich, Germany., Schreiber L; Department of Ecophysiology, Institute of Cellular and Molecular Botany, University of Bonn, Bonn, Germany.
المصدر: Plant, cell & environment [Plant Cell Environ] 2024 Aug 07. Date of Electronic Publication: 2024 Aug 07.
Publication Model: Ahead of Print
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: John Wiley & Sons Ltd Country of Publication: United States NLM ID: 9309004 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-3040 (Electronic) Linking ISSN: 01407791 NLM ISO Abbreviation: Plant Cell Environ Subsets: MEDLINE
أسماء مطبوعة: Publication: Hoboken, NJ : John Wiley & Sons Ltd.
Original Publication: Oxford, UK : Blackwell Scientific Publications
مستخلص: In root research, hydroponic plant cultivation is commonly used and soil experiments are rare. We investigated the response of 12-day-old barley roots, cultivated in soil-filled rhizotrons, to different soil water potentials (SWP) comparing a modern cultivar (cv. Scarlett) with a wild accession ICB181243 from Pakistan. Water potentials were quantified in soils with different relative water contents. Root anatomy was studied using histochemistry and microscopy. Suberin and lignin amounts were quantified by analytical chemistry. Transcriptomic changes were observed by RNA-sequencing. Compared with control with decreasing SWP, total root length decreased, the onset of endodermal suberization occurred much closer towards the root tips, amounts of suberin and lignin increased, and corresponding biosynthesis genes were upregulated in response to decreasing SWP. We conclude that decreasing water potentials enhanced root suberization and lignification, like osmotic stress experiments in hydroponic cultivation. However, in soil endodermal cell suberization was initiated very close towards the root tip, and root length as well as suberin amounts were about twofold higher compared with hydroponic cultivation.
(© 2024 The Author(s). Plant, Cell & Environment published by John Wiley & Sons Ltd.)
References: AghaKouchak, A., Cheng, L., Mazdiyasni, O. & Farahmand, A. (2014) Global warming and changes in risk of concurrent climate extremes: insights from the 2014 California drought. Geophysical Research Letters, 41, 8847–8852.
Ahmed, M.A., Passioura, J. & Carminati, A. (2018) Hydraulic processes in roots and the rhizosphere pertinent to increasing yield of water‐limited grain crops: a critical review. Journal of Experimental Botany, 69, 3255–3265.
Asong, Z.E., Wheater, H.S., Bonsal, B., Razavi, S. & Kurkute, S. (2018) Historical drought patterns over Canada and their teleconnections with large‐scale climate signals. Hydrology and Earth System Sciences, 22, 3105–3124.
Badr, A., M, K., Sch, R., Rabey, H.E., Effgen, S., Ibrahim, H.H. et al. (2000) On the origin and domestication history of barley (Hordeum vulgare). Molecular Biology and Evolution, 17, 499–510.
Bengough, A.G., McKenzie, B.M., Hallett, P.D. & Valentine, T.A. (2011) Root elongation, water stress, and mechanical impedance: a review of limiting stresses and beneficial root tip traits. Journal of Experimental Botany, 62, 59–68.
Benjamini, Y. & Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B: Statistical Methodology, 57, 289–300.
Boudiar, R., Casas, A.M., Gioia, T., Fiorani, F., Nagel, K.A. & Igartua, E. (2020) Effects of low water availability on root placement and shoot development in landraces and modern barley cultivars. Agronomy, 10, 134.
Brundrett, M.C., Kendrick, B. & Peterson, C.A. (1991) Efficient lipid staining in plant material with Sudan red 7B or fluorol [correction of fluoral] yellow 088 in polyethylene glycol‐glycerol. Biotechnic & Histochemistry, 66, 111–116.
Cabané, M., Pireaux, J.‐C., Léger, E., Weber, E., Dizengremel, P., Pollet, B. et al. (2004) Condensed lignins are synthesized in poplar leaves exposed to ozone. Plant Physiology, 134, 586–594.
Cai, K., Chen, X., Han, Z., Wu, X., Zhang, S., Li, Q. et al. (2020) Screening of worldwide barley collection for drought tolerance: the assessment of various physiological measures as the selection criteria. Frontiers in Plant Science, 11, 1159.
Chen, S., Wang, S., Altman, A. & Huttermann, A. (1997) Genotypic variation in drought tolerance of poplar in relation to abscisic acid. Tree Physiology, 17, 797–803.
Dara, A., Moradi, B.A., Vontobel, P. & Oswald, S.E. (2015) Mapping compensating root water uptake in heterogeneous soil conditions via neutron radiography. Plant and Soil, 397, 273–287.
Dasauni, K. & Nailwal, T.K. (2020) Chapter 3 ‐ Zinc finger proteins: novel sources of genes for abiotic stress tolerance in plants. In: Wani, S.H. (Ed.) Transcription factors for abiotic stress tolerance in plants. Academic Press, pp. 29–45.
Dawson, I.K., Russell, J., Powell, W., Steffenson, B., Thomas, W.T.B. & Waugh, R. (2015) Barley: a translational model for adaptation to climate change. New Phytologist, 206, 913–931.
Dutta, P., Bandopadhyay, P. & Bera, A.K. (2016) Identification of leaf based physiological markers for drought susceptibility during early seedling development of mungbean. American Journal of Plant Sciences, 07, 1921–1936.
Ellis, R.P., Forster, B.P., Robinson, D., Handley, L.L., Gordon, D.C., Russell, J.R. et al. (2000) Wild barley: a source of genes for crop improvement in the 21st century? Journal of Experimental Botany, 51, 9–17.
Enstone, D.E., Peterson, C.A. & Ma, F. (2002) Root endodermis and exodermis: structure, function, and responses to the environment. Journal of Plant Growth Regulation, 21, 335–351.
Esau, K. (1953) Plant anatomy. Soil Science, 75, 407.
Fan, L., Linker, R., Gepstein, S., Tanimoto, E., Yamamoto, R. & Neumann, P.M. (2006) Progressive inhibition by water deficit of cell wall extensibility and growth along the elongation zone of maize roots is related to increased lignin metabolism and progressive stelar accumulation of wall phenolics. Plant Physiology, 140, 603–612.
Foster, C.E., Martin, T.M. & Pauly, M. (2010) Comprehensive compositional analysis of plant cell walls (Lignocellulosic biomass) part I: lignin. Journal of Visualized Experiments, 37, e1745.
Franke, R. & Schreiber, L. (2007) Suberin — a biopolyester forming apoplastic plant interfaces. Current Opinion in Plant Biology, 10, 252–259.
Gambetta, G.A., Knipfer, T., Fricke, W. & McElrone, A.J. (2017) Aquaporins and root water uptake. In: Chaumont, F. & Tyerman, S.D. (Eds.) Plant aquaporins: from transport to signaling (Signaling and Communication in Plants). Springer International Publishing, pp. 133–153.
Gangola, M.P. & Ramadoss, B.R. (2020) Chapter 2 ‐ WRKY transcription factors for biotic and abiotic stress tolerance in plants. In: Wani, S.H. (Ed.) Transcription factors for abiotic stress tolerance in plants. Academic Press, pp. 15–28.
Ge, S.X., Jung, D. & Yao, R. (2020) ShinyGO: a graphical gene‐set enrichment tool for animals and plants. Bioinformatics, 36, 2628–2629.
Graça, J. (2015) Suberin: the biopolyester at the frontier of plants. Frontiers in Chemistry, 3, 62.
Groenevelt, P.H. & Grant, C.D. (2004) A new model for the soil‐water retention curve that solves the problem of residual water contents. European Journal of Soil Science, 55, 479–485.
Grünhofer, P., Heimerich, I., Herzig, L., Pohl, S. & Schreiber, L. (2023) Apoplastic barriers of Populus × canescens roots in reaction to different cultivation conditions and abiotic stress treatments. Stress Biology, 3, 24.
Grünhofer, P., Stöcker, T., Guo, Y., Li, R., Lin, J., Ranathunge, K. et al. (2022) Populus×canescensroot suberization in reaction to osmotic and salt stress is limited to the developing younger root tip region. Physiologia Plantarum, 174, e13765.
Hewelke, P., Gratowski, T., Hewelke, E., Żakowicz, S. & Tyszka, J. (2015) Analysis of water retention capacity for select forest soils in Poland. Polish Journal of Environmental Studies, 24, 1013–1019.
Holbein, J., Franke, R.B., Marhavý, P., Fujita, S., Górecka, M., Sobczak, M. et al. (2019) Root endodermal barrier system contributes to defence against plant‐parasitic cyst and root‐knot nematodes. The Plant Journal, 100, 221–236.
Izanloo, A., Condon, A.G., Langridge, P., Tester, M. & Schnurbusch, T. (2008) Different mechanisms of adaptation to cyclic water stress in two South Australian bread wheat cultivars. Journal of Experimental Botany, 59, 3327–3346.
Kirkham, M.B. (2005) Chapter 8 ‐ Field capacity, wilting point, available water, and the non‐limiting water range. In: Kirkham, M.B. (Ed.) Principles of soil and plant water relations. Academic Press, pp. 101–115.
Koevoets, I.T., Venema, J.H., Elzenga, J.T.M. & Testerink, C. (2016) Roots withstanding their environment: exploiting root system architecture responses to abiotic stress to improve crop tolerance. Frontiers in Plant Science, 7, 1335.
Kováč, J., Lux, A. & Vaculík, M. (2018) Formation of a subero‐lignified apical deposit in root tip of radish (Raphanus sativus) as a response to copper stress. Annals of Botany, 122, 823–831.
Kreszies, T., Eggels, S., Kreszies, V., Osthoff, A., Shellakkutti, N., Baldauf, J.A. et al. (2020) Seminal roots of wild and cultivated barley differentially respond to osmotic stress in gene expression, suberization, and hydraulic conductivity. Plant, Cell & Environment, 43, 344–357.
Kreszies, T., Shellakkutti, N., Osthoff, A., Yu, P., Baldauf, J.A., Zeisler‐Diehl, V.V., et al. (2019) Osmotic stress enhances suberization of apoplastic barriers in barley seminal roots: analysis of chemical, transcriptomic and physiological responses. New Phytologist, 221, 180–194.
Kumari, V.V., Banerjee, P., Verma, V.C., Sukumaran, S., Chandran, M.A.S., Gopinath, K.A. et al. (2022) Plant nutrition: an effective way to alleviate abiotic stress in agricultural crops. International Journal of Molecular Sciences, 23, 8519.
Lanoue, A., Burlat, V., Henkes, G.J., Koch, I., Schurr, U. & Röse, U.S.R. (2010) De novo biosynthesis of defense root exudates in response to Fusarium attack in barley. New Phytologist, 185, 577–588.
Lens, F., Picon‐Cochard, C., Delmas, C.E., Signarbieux, C., Buttler, A. & Cochard, H. et al. (2016) Herbaceous angiosperms are not more vulnerable to drought‐induced embolism than angiosperm trees. Plant Physiology, 172, 661–667.
Li, N., Li, Y., Yoo, C.G., Yang, X., Lin, X., Ralph, J. et al. (2018) An uncondensed lignin depolymerized in the solid state and isolated from lignocellulosic biomass: a mechanistic study. Green Chemistry, 20, 4224–4235.
Liao, Y., Smyth, G.K. & Shi, W. (2014) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics, 30, 923–930.
Liao, Y., Smyth, G.K. & Shi, W. (2019) The R package Rsubread is easier, faster, cheaper and better for alignment and quantification of RNA sequencing reads. Nucleic Acids Research, 47, e47.
Love, M.I., Huber, W. & Anders, S. (2014) Moderated estimation of fold change and dispersion for RNA‐seq data with DESeq. 2. Genome Biology, 15, 550.
Lynch, J.P. & Wojciechowski, T. (2015) Opportunities and challenges in the subsoil: pathways to deeper rooted crops. Journal of Experimental Botany, 66, 2199–2210.
Martin, M. (2011) Cutadapt removes adapter sequences from high‐throughput sequencing reads. EMBnet. Journal, 17, 10–12.
Nagel, K.A., Putz, A., Gilmer, F., Heinz, K., Fischbach, A., Pfeifer, J. et al. (2012) GROWSCREEN‐Rhizo is a novel phenotyping robot enabling simultaneous measurements of root and shoot growth for plants grown in soil‐filled rhizotrons. Functional Plant Biology, 39, 891–904.
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, 109, 10101–10106.
Naz, A.A., Arifuzzaman, M., Muzammil, S., Pillen, K. & Léon, J. (2014) Wild barley introgression lines revealed novel QTL alleles for root and related shoot traits in the cultivated barley (Hordeum vulgare L.). BMC Genetics, 15, 107.
Newton, A.C., Flavell, A.J., George, T.S., Leat, P., Mullholland, B., Ramsay, L. et al. (2011) Crops that feed the world 4. Barley: a resilient crop? Strengths and weaknesses in the context of food security. Food Security, 3, 141–178.
Nimah, M.N. & Hanks, R.J. (1973) Model for estimating soil water, plant, and atmospheric interrelations: I. Description and sensitivity. Soil Science Society of America Journal, 37, 522–527.
North, G.B. & Nobel, P.S. (1995) Hydraulic conductivity of concentric root tissues of Agave deserti Engelm. under wet and drying conditions. New Phytologist, 130, 47–57.
Or, D., Wraith, J.M. & Warrick, A. (2002) Soil water content and water potential relationships. Soil Physics Companion, 1, 49–84.
Ouyang, W., Yin, X., Yang, J. & Struik, P.C. (2020) Comparisons with wheat reveal root anatomical and histochemical constraints of rice under water‐deficit stress. Plant and Soil, 452, 547–568.
Paschen, B., Wrage‐Mönnig, N., Fritz, C. & Wichern, F. (2022) Ability of cereal species for nitrogen uptake from cover crop rhizodeposits is not related to domestication level. Journal of Plant Nutrition and Soil Science, 185, 589–602.
Ramadoss, B.R., Gangola, M.P. & Gurunathan, S. (2020) Chapter 4 ‐ NAC transcription factor family in rice: recent advancements in the development of stress‐tolerant rice. In: Wani, S.H. (Ed.) Transcription factors for abiotic stress tolerance in plants. Academic Press, pp. 47–61.
Ranathunge, K., Kim, Y.X., Wassmann, F., Kreszies, T., Zeisler, V. & Schreiber, L. (2017) The composite water and solute transport of barley (Hordeum vulgare) roots: effect of suberized barriers. Annals of Botany, 119, mcw252.
Ranathunge, K., Schreiber, L., Bi, Y.‐M. & Rothstein, S.J. (2016) Ammonium‐induced architectural and anatomical changes with altered suberin and lignin levels significantly change water and solute permeabilities of rice (Oryza sativa L.) roots. Planta, 243, 231–249.
Ritchie, M.E., Phipson, B., Wu, D., Hu, Y., Law, C.W., Shi, W. et al. (2015) limma powers differential expression analyses for RNA‐sequencing and microarray studies. Nucleic Acids Research, 43, e47.
Robinson, M.D., McCarthy, D.J. & Smyth, G.K. (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26, 139–140.
Rolando, C., Monties, B. & Lapierre, C. (1992) Thioacidolysis. In: Lin, S.Y. & Dence, C.W. (Eds.) Methods in lignin chemistry. Springer series in wood science. Springer, pp. 334–349.
Sahnoune, M., Adda, A., Soualem, S., Harch, M.K. & Merah, O. (2004) Early water‐deficit effects on seminal roots morphology in barley. Comptes Rendus Biologies, 327, 389–398.
Sato, K. (2020) History and future perspectives of barley genomics. DNA Research, 27, dsaa023.
Schneider, H.M., Strock, C.F., Hanlon, M.T., Vanhees, D.J., Perkins, A.C., Ajmera, I.B. et al. (2021) Multiseriate cortical sclerenchyma enhance root penetration in compacted soils. Proceedings of the National Academy of Sciences, 118, e2012087118.
Schreiber, L. (1996) Chemical composition of Casparian strips isolated from Clivia miniata Reg. roots: evidence for lignin. Planta, 199, 596–601.
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.
Schreiber, L., Hartmann, K., Skrabs, M. & Zeier, J. (1999) Apoplastic barriers in roots: chemical composition of endodermal and hypodermal cell walls. Journal of Experimental Botany, 50, 1267–1280.
Sharma, N.K., Gupta, S.K., Dwivedi, V. & Chattopadhyay, D. (2020) Lignin deposition in chickpea root xylem under drought. Plant Signaling & Behavior, 15, 1754621.
Steudle, E. (2000a) Water uptake by roots: effects of water deficit. Journal of Experimental Botany, 51, 1531–1542.
Steudle, E. (2000b) Water uptake by plant roots: an integration of views. Plant and Soil, 226, 45–56.
Steudle, E. & Peterson, C.A. (1998) How does water get through roots? Journal of Experimental Botany, 49, 775–788.
Tian, T., Liu, Y., Yan, H., You, Q., Yi, X., Du, Z. et al. (2017) agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Research, 45, W122–W129.
Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R. et al. (2012) Differential gene and transcript expression analysis of RNA‐seq experiments with TopHat and Cufflinks. Nature Protocols, 7, 562–578.
Vazquez‐Cooz, I. & Meyer, R.W. (2002) A differential staining method to identify lignified and unlignified tissues. Biotechnic & Histochemistry, 77, 277–282.
Wald, A. (1943) Tests of statistical hypotheses concerning several parameters when the number of observations is large. Transactions of the American Mathematical Society, 54, 426–482.
Wang, H., Cheng, X., Yin, D., Chen, D., Luo, C., Liu, H. et al. (2023) Advances in the research on plant WRKY transcription factors responsive to external stresses. Current Issues in Molecular Biology, 45, 2861–2880.
Yamaguchi, M., Valliyodan, B., Zhang, J., Lenoble, M.E., Yu, O., Rogers, E.E. et al. (2010) Regulation of growth response to water stress in the soybean primary root. I. Proteomic analysis reveals region‐specific regulation of phenylpropanoid metabolism and control of free iron in the elongation zone. Plant, Cell & Environment, 33, 223–243.
Yang, L., Wang, C.C., Guo, W.D., Li, X.B., Lu, M. & Yu, C.L. (2006) Differential expression of cell wall related genes in the elongation zone of rice roots under water deficit. Russian Journal of Plant Physiology, 53, 390–395.
Zeier, J., Goll, A., Yokoyama, M., Karahara, I. & Schreiber, L. (1999) Structure and chemical composition of endodermal and rhizodermal/hypodermal walls of several species. Plant, Cell & Environment, 22, 271–279.
Zeier, J., Ruel, K., Ryser, U. & Schreiber, L. (1999) 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.
Zeier, J. & Schreiber, L. (1997) Chemical composition of hypodermal and endodermal cell walls and xylem vessels isolated from Clivia miniata (Identification of the Biopolymers Lignin and Suberin). Plant Physiology, 113, 1223–1231.
Zeier, J. & Schreiber, L. (1998) 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, 206, 349–361.
Zhao, J., Sun, H., Dai, H., Zhang, G. & Wu, F. (2010) Difference in response to drought stress among Tibet wild barley genotypes. Euphytica, 172, 395–403.
Zhou, Z., Ding, Y., Fu, Q., Wang, C., Wang, Y. & Cai, H. et al. (2022) Comprehensive evaluation of vegetation responses to meteorological drought from both linear and nonlinear perspectives. Frontiers in Earth Science, 10, 953805.
معلومات مُعتمدة: Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) - Projektnummer: 511193270; POF-Funding of the Helmholtz Association
فهرسة مساهمة: Keywords: apoplastic root barrier; lignin; soil water potential; soil water stress; soil‐grown barley root; suberin
تواريخ الأحداث: Date Created: 20240807 Latest Revision: 20240807
رمز التحديث: 20240807
DOI: 10.1111/pce.15067
PMID: 39110071
قاعدة البيانات: MEDLINE
الوصف
تدمد:1365-3040
DOI:10.1111/pce.15067