Abstract
Main conclusion
Arabinogalactan protein content in both root extracellular trap and root exudates varies in three Sahelian woody plant species that are differentially tolerant to drought.
Abstract
At the root tip, mature root cap cells, mainly border cells (BCs)/border-like cells (BLCs) and their associated mucilage, form a web-like structure known as the “Root Extracellular Trap” (RET). Although the RET along with the entire suite of root exudates are known to influence rhizosphere function, their features in woody species is poorly documented. Here, RET and root exudates were analyzed from three Sahelian woody species with contrasted sensitivity to drought stress (Balanites aegyptiaca, Acacia raddiana and Tamarindus indica) and that have been selected for reforestation along the African Great Green Wall in northern Senegal. Optical and transmission electron microscopy show that Balanites aegyptiaca, the most drought-tolerant species, produces only BC, whereas Acacia raddiana and Tamarindus indica release both BCs and BLCs. Biochemical analyses reveal that RET and root exudates of Balanites aegyptiaca and Acacia raddiana contain significantly more abundant arabinogalactan proteins (AGPs) compared to Tamarindus indica, the most drought-sensitive species. Root exudates of the three woody species also differentially impact the plant soil beneficial bacteria Azospirillum brasilense growth. These results highlight the importance of root secretions for woody species survival under dry conditions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- AGP:
-
Arabinonogalactan protein
- AIR:
-
Alcohol insoluble residue
- BC:
-
Border cell
- BLC:
-
Border-like cell
- RAM:
-
Root apical meristem
- RET:
-
Root extracellular trap
References
Arnaud C, Bonnot C, Desnos T, Nussaume L (2010) The root cap at the forefront. C R Biol 333:335–343. https://doi.org/10.1016/j.crvi.2010.01.011
Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681. https://doi.org/10.1111/j.1365-3040.2009.01926.x
Bais HP, Weir TL, Perry LG et al (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266
Bashan Y, Puente ME, Rodriguez-Mendoza MN et al (1995) Survival of Azospirillum brasilense in the bulk soil and rhizosphere of 23 soil types. Appl Environ Microbiol 61:1938–1945
Beisson F, Li-Beisson Y, Pollard M (2012) Solving the puzzles of cutin and suberin polymer biosynthesis. Curr Opin Plant Biol 15:329–337. https://doi.org/10.1016/j.pbi.2012.03.003
Bennett T, van den Toorn A, Sanchez-Perez GF et al (2010) SOMBRERO, BEARSKIN1, and BEARSKIN2 regulate root cap maturation in Arabidopsis. Plant Cell 22:640–654. https://doi.org/10.1105/tpc.109.072272
Cai M-Z, Wang F-M, Li R-F et al (2011a) Response and tolerance of root border cells to aluminum toxicity in soybean seedlings. J Inorg Biochem 105:966–971. https://doi.org/10.1016/j.jinorgbio.2011.04.004
Cai M-Z, Zhang S-N, Xing C et al (2011b) Developmental characteristics and aluminum resistance of root border cells in rice seedlings. Plant Sci 180:702–708. https://doi.org/10.1016/j.plantsci.2011.01.017
Cannesan MA, Durand C, Burel C et al (2012) Effect of arabinogalactan proteins from the root caps of pea and Brassica napus on Aphanomyces euteiches zoospore chemotaxis and germination. Plant Physiol 159:1658–1670. https://doi.org/10.1104/pp.112.198507
Cannesan MA, Gangneux C, Lanoue A et al (2011) Association between border cell responses and localized root infection by pathogenic Aphanomyces euteiches. Ann Bot 108:459–469. https://doi.org/10.1093/aob/mcr177
Carminati A, Vetterlein D (2013) Plasticity of rhizosphere hydraulic properties as a key for efficient utilization of scarce resources. Ann Bot 112:277–290. https://doi.org/10.1093/aob/mcs262
Chaboud A (1983) Isolation, purification and chemical composition of maize root cap slime. Plant Soil 73:395–402
Chen R, Rosen E, Masson PH (1999) Gravitropism in higher plants. Plant Physiol 120:343–350
Cho SK, Kim JE, Park J-A et al (2006) Constitutive expression of abiotic stress-inducible hot pepper CaXTH3, which encodes a xyloglucan endotransglucosylase/hydrolase homolog, improves drought and salt tolerance in transgenic Arabidopsis plants. FEBS Lett 580:3136–3144. https://doi.org/10.1016/j.febslet.2006.04.062
Cohen AC, Bottini R, Pontin M et al (2015) Azospirillum brasilense ameliorates the response of Arabidopsis thaliana to drought mainly via enhancement of ABA levels. Physiol Plant 153:79–90. https://doi.org/10.1111/ppl.12221
Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861. https://doi.org/10.1038/nrm1746
Driouich A, Durand C, Cannesan M-A et al (2010) Border cells versus border-like cells: are they alike? J Exp Bot 61:3827–3831. https://doi.org/10.1093/jxb/erq216
Driouich A, Durand C, Vicré-Gibouin M (2007) Formation and separation of root border cells. Trends Plant Sci 12:14–19. https://doi.org/10.1016/j.tplants.2006.11.003
Driouich A, Follet-Gueye M-L, Bernard S et al (2012) Golgi-mediated synthesis and secretion of matrix polysaccharides of the primary cell wall of higher plants. Front Plant Sci 3:79. https://doi.org/10.3389/fpls.2012.00079
Driouich A, Follet-Gueye M-L, Vicré-Gibouin M, Hawes M (2013) Root border cells and secretions as critical elements in plant host defense. Curr Opin Plant Biol 16:489–495. https://doi.org/10.1016/j.pbi.2013.06.010
Durand C, Vicré-Gibouin M, Follet-Gueye ML et al (2009) The organization pattern of root border-like cells of Arabidopsis is dependent on cell wall homogalacturonan. Plant Physiol 150:1411–1421. https://doi.org/10.1104/pp.109.136382
Endo I, Tange T, Osawa H (2011) A cell-type-specific defect in border cell formation in the Acacia mangium root cap developing an extraordinary sheath of sloughed-off cells. Ann Bot 108:279–290. https://doi.org/10.1093/aob/mcr139
Fendrych M, Van Hautegem T, Van Durme M et al (2014) Programmed cell death controlled by ANAC033/SOMBRERO determines root cap organ size in Arabidopsis. Curr Biol 24:931–940. https://doi.org/10.1016/j.cub.2014.03.025
Fincher GB, Stone BA, Clarke AE (1983) Arabinogalactan-proteins: structure, biosynthesis, and function. Annu Rev Plant Physiol 34:47–70
Griffin GJ, Hale MG, Shay FJ (1976) Nature and quantity of sloughed organic matter produced by roots of axenic peanut plants. Soil Biol Biochem 8:29–32
Gunawardena U (2005) Tissue-specific localization of pea root infection by Nectria haematococca. Mechanisms and consequences. Plant Physiol 137:1363–1374. https://doi.org/10.1104/pp.104.056366
Hamamoto L, Hawes MC, Rost TL (2006) The production and release of living root cap border cells is a function of root apical meristem type in dicotyledonous angiosperm plants. Ann Bot 97:917–923. https://doi.org/10.1093/aob/mcj602
Hawes MC, Bengough G, Cassab G, Ponce G (2002) Root caps and rhizosphere. J Plant Growth Regul 21:352–367. https://doi.org/10.1007/s00344-002-0035-y
Hawes MC, Curlango-Rivera G, Wen F et al (2011) Extracellular DNA: the tip of root defenses? Plant Sci 180:741–745. https://doi.org/10.1016/j.plantsci.2011.02.007
Hawes MC, Gunawardena U, Miyasaka S, Zhao X (2000) The role of root border cells in plant defense. Trends Plant Sci 5:128–133
Hawes MC, Lin H-J (1990) Correlation of pectolytic enzyme activity with the programmed release of cells from root caps of pea (Pisum sativum). Plant Physiol 94:1855–1859
Hawes MC, Pueppke SG (1986) Sloughed peripheral root cap cells: yield from different species and callus formation from single cells. Am J Bot 73:1466. https://doi.org/10.2307/2443851
Heimsch C, Seago JL (2008) Organization of the root apical meristem in angiosperms. Am J Bot 95:1–21
Jones L, Seymour GB, Knox JP (1997) Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1[- >]4)-[beta]-D-galactan. Plant Physiol 113:1405. https://doi.org/10.1104/pp.113.4.1405
Kamiya M, Higashio S-Y, Isomoto A et al (2016) Control of root cap maturation and cell detachment by BEARSKIN transcription factors in Arabidopsis. Development 143:4063–4072. https://doi.org/10.1242/dev.142331
Karve R, Suárez-Román F, Iyer-Pascuzzi AS (2016) The transcription factor NIN-LIKE PROTEIN7 controls border-like cell release. Plant Physiol 171:2101–2111. https://doi.org/10.1104/pp.16.00453
Kitazawa K, Tryfona T, Yoshimi Y et al (2013) β-Galactosyl yariv reagent binds to the β-1,3-galactan of arabinogalactan proteins. Plant Physiol 161:1117–1126. https://doi.org/10.1104/pp.112.211722
Knox JP, Linstead PJ, Peart JCC, Roberts K (1991) Developmentally regulated epitopes of cell surface arabinogalactan proteins and their relation to root tissue pattern formation. Plant J 1:317–326. https://doi.org/10.1046/j.1365-313X.1991.t01-9-00999.x
Koroney AS, Plasson C, Pawlak B et al (2016) Root exudate of Solanum tuberosum is enriched in galactose-containing molecules and impacts the growth of Pectobacterium atrosepticum. Ann Bot 118:797–808. https://doi.org/10.1093/aob/mcw128
Logbo J, Diouf M, Ngaryo F et al (2013) Effet du stress hydrique sur l’architecture racinaire de jeunes plants d’Acacia tortilis (Forsk.), de Balanites aegyptiaca (L) Del., et de Zizyphus mauritiana Lam. Int J Biol Chem Sci 7:1011. https://doi.org/10.4314/ijbcs.v7i3.10
Lu H, Chen M, Showalter AM (2001) Developmental expression and perturbation of arabinogalactan-proteins during seed germination and seedling growth in tomato. Physiol Plant 112:442–450. https://doi.org/10.1034/j.1399-3054.2001.1120319.x
Marcus SE, Verhertbruggen Y, Hervé C et al (2008) Pectic homogalacturonan masks abundant sets of xyloglucan epitopes in plant cell walls. BMC Plant Biol 8:60. https://doi.org/10.1186/1471-2229-8-60
McCabe PF, Valentine TA, Forsberg LS, Pennell RI (1997) Soluble signals from cells identified at the cell wall establish a developmental pathway in carrot. Plant Cell 9:2225. https://doi.org/10.1105/tpc.9.12.2225
Miyasaka SC, Hawes MC (2001) Possible role of root border cells in detection and avoidance of aluminum toxicity. Plant Physiol 125:1978–1987
Moller I, Marcus SE, Haeger A et al (2007) High-throughput screening of monoclonal antibodies against plant cell wall glycans by hierarchical clustering of their carbohydrate microarray binding profiles. Glycoconj J 25:37–48. https://doi.org/10.1007/s10719-007-9059-7
Mravec J, Guo X, Hansen AR et al (2017) Pea border cell maturation and release involve complex cell wall structural dynamics. Plant Physiol 174:1051–1066. https://doi.org/10.1104/pp.16.00097
Ndiaye O (2013) Carcactéristiques des sols, de la flore et de la végétation du Ferlo, Sénégal. PhD, Université Cheikh Anta Diop (UCAD), 30 Décembre 2013. http://bibnum.ucad.sn/viewer.php?c=ths&d=ths_2015_0027.
Nagahashi G, Douds DD (2004) Isolated root caps, border cells, and mucilage from host roots stimulate hyphal branching of the arbuscular mycorrhizal fungus, Gigaspora gigantea. Mycol Res 108:1079–1088. https://doi.org/10.1017/S0953756204000693
Nguema-Ona E, Coimbra S, Vicre-Gibouin M et al (2012) Arabinogalactan proteins in root and pollen-tube cells: distribution and functional aspects. Ann Bot 110:383–404. https://doi.org/10.1093/aob/mcs143
Nguema-Ona E, Vicré-Gibouin M, Cannesan M-A, Driouich A (2013) Arabinogalactan proteins in root–microbe interactions. Trends Plant Sci 18:440–449. https://doi.org/10.1016/j.tplants.2013.03.006
Nguema-Ona E, Vicré-Gibouin M, Gotté M et al (2014) Cell wall O-glycoproteins and N-glycoproteins: aspects of biosynthesis and function. Front Plant Sci 5:499. https://doi.org/10.3389/fpls.2014.00499
Olmos E, García De La Garma J, Gomez-Jimenez MC, Fernandez-Garcia N (2017) Arabinogalactan proteins are involved in salt-adaptation and vesicle trafficking in tobacco by-2 cell cultures. Front Plant Sci 8:1092. https://doi.org/10.3389/fpls.2017.01092
Pennell RI, Janniche L, Kjellbom P et al (1991) Developmental regulation of a plasma membrane arabinogalactan protein epitope in oilseed rape flowers. Plant Cell 3:1317. https://doi.org/10.1105/tpc.3.12.1317
Pollard M, Beisson F, Li Y, Ohlrogge JB (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 13:236–246. https://doi.org/10.1016/j.tplants.2008.03.003
Radwan UAA (2007) Photosynthetic and leaf anatomical characteristics of the drought-resistant Balanites aegyptiaca (L.) Del. seedlings. Am-Eurasian J Agric Environ Sci 2:680–688
Rodríguez-Salazar J, Suárez R, Caballero-Mellado J, Iturriaga G (2009) Trehalose accumulation in Azospirillum brasilense improves drought tolerance and biomass in maize plants. FEMS Microbiol Lett 296:52–59. https://doi.org/10.1111/j.1574-6968.2009.01614.x
Ropitaux M, Bernard S, Follet-Gueye M-L et al (2019) Xyloglucan and cellulose form molecular cross-bridges connecting root border cells in pea (Pisum sativum). Plant Physiol Biochem 139:191–196. https://doi.org/10.1016/j.plaphy.2019.03.023
Rost TL (2011) The organization of roots of dicotyledonous plants and the positions of control points. Ann Bot 107:1213–1222. https://doi.org/10.1093/aob/mcq229
Sasse J, Martinoia E, Northen T (2018) Feed your friends: Do plant exudates shape the root microbiome? Trends Plant Sci 23:25–41. https://doi.org/10.1016/j.tplants.2017.09.003
Seifert GJ, Roberts K (2007) The biology of arabinogalactan proteins. Annu Rev Plant Biol 58:137–161. https://doi.org/10.1146/annurev.arplant.58.032806.103801
Sénéchal F, Wattier C, Rustérucci C, Pelloux J (2014) Homogalacturonan-modifying enzymes: structure, expression, and roles in plants. J Exp Bot 65:5125–5160. https://doi.org/10.1093/jxb/eru272
Showalter AM (2001) Arabinogalactan-proteins: structure, expression and function. Cell Mol Life Sci 58:1399–1417
Smallwood M, Martin H, Knox JP (1995) An epitope of rice threonine- and hydroxyproline-rich glycoprotein is common to cell wall and hydrophobic plasma-membrane glycoproteins. Planta 196:510–522. https://doi.org/10.1007/BF00203651
Smallwood M, Yates EA, Willats WGT et al (1996) Immunochemical comparison of membrane-associated and secreted arabinogalactan-proteins in rice and carrot. Planta 198:452–459. https://doi.org/10.1007/BF00620063
Thevis M, Opfermann G, Schänzer W (2000) Mass spectrometry of partially methylated alditol acetates derived from hydroxyethyl starch. J Mass Spectrom 35:77–84. https://doi.org/10.1002/(SICI)1096-9888(200001)35:1%3c77:AID-JMS916%3e3.0.CO;2-L
Van Doorn WG (2011) Classes of programmed cell death in plants, compared to those in animals. J Exp Bot 62:4749–4761. https://doi.org/10.1093/jxb/err196
van Holst G-J, Clarke AE (1986) Organ-specific arabinogalactan-proteins of Lycopersicon peruvianum (Mill) demonstrated by crossed electrophoresis. Plant Physiol 80:786–789. https://doi.org/10.1104/pp.80.3.786
Vanstockem M, Michiels K, Vanderleyden J, Van Gool AP (1987) Transposon mutagenesis of Azospirillum brasilense and Azospirillum lipoferum: physical analysis of Tn5 and Tn5-Mob insertion mutants. Appl Environ Microbiol 53:410–415
Verhertbruggen Y, Marcus SE, Haeger A et al (2009) An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohydr Res 344:1858–1862. https://doi.org/10.1016/j.carres.2008.11.010
Vicré M, Santaella C, Blanchet S et al (2005) Root border-like cells of Arabidopsis. Microscopical characterization and role in the interaction with rhizobacteria. Plant Physiol 138:998–1008. https://doi.org/10.1104/pp.104.051813
Wade TI, Ndiaye O, Mauclaire M et al (2018) Biodiversity field trials to inform reforestation and natural resource management strategies along the African Great Green Wall in Senegal. New For. https://doi.org/10.1007/s11056-017-9623-3
Wang P, Chen X, Goldbeck C et al (2017) A distinct class of vesicles derived from the trans-Golgi mediates secretion of xylogalacturonan in the root border cell. Plant J 92:596–610. https://doi.org/10.1111/tpj.13704
Watson BS, Bedair MF, Urbanczyk-Wochniak E et al (2015) Integrated metabolomics and transcriptomics reveal enhanced specialized metabolism in Medicago truncatula root border cells. Plant Physiol 167:1699–1716. https://doi.org/10.1104/pp.114.253054
Wen F, VanEtten HD, Tsaprailis G, Hawes MC (2007) Extracellular proteins in pea root tip and border cell exudates. Plant Physiol 143:773–783. https://doi.org/10.1104/pp.106.091637
Wen F, White GJ, VanEtten HD et al (2009) Extracellular DNA is required for root tip resistance to fungal infection. Plant Physiol 151:820–829. https://doi.org/10.1104/pp.109.142067
Wen F, Zhu Y, Hawes MC (1999) Effect of pectin methylesterase gene expression on pea root development. Plant Cell 11:1129–1140
Willats WGT, McCartney L, Knox JP (2001) In-situ analysis of pectic polysaccharides in seed mucilage and at the root surface of Arabidopsis thaliana. Planta 213:37–44
Willats WGT, McCartney L, Steele-King CG et al (2004) A xylogalacturonan epitope is specifically associated with plant cell detachment. Planta 218:673–681. https://doi.org/10.1007/s00425-003-1147-8
Willemsen V, Bauch M, Bennett T et al (2008) The NAC domain transcription factors FEZ and SOMBRERO control the orientation of cell division plane in Arabidopsis root stem cells. Dev Cell 15:913–922. https://doi.org/10.1016/j.devcel.2008.09.019
Yan Y, Takáč T, Li X et al (2015) Variable content and distribution of arabinogalactan proteins in banana (Musa spp.) under low temperature stress. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00353
Yates EA, Valdor J-F, Haslam SM et al (1996) Characterization of carbohydrate structural features recognized by anti-arabinogalactan-protein monoclonal antibodies. Glycobiology 6:131–139
Acknowledgements
This work was supported by the Labex DRIIHM (Dispositif de Recherche Interdisciplinaire sur les Interactions Hommes-Milieux) (ANR-11-LABX-0010), the OHMi (Observatoire Hommes-Milieux) Tessekéré and by the « Structure Fédérative de Recherche, SFR Normandie-Végétale (FED-4277); the authors wish to thank them. Images were obtained on PRIMACEN (http://www.primacen.fr), the Cell Imaging Platform of Normandy, IRIB, Faculty of Sciences, University of Rouen, 76821 Mont Saint Aignan. A. brasilense was provided by Geneviève Grundmann and Claire Pringent-Combaret from CNRS, UMR 5557, Ecologie Microbienne, Villeurbanne, France.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Carreras, A., Bernard, S., Durambur, G. et al. In vitro characterization of root extracellular trap and exudates of three Sahelian woody plant species. Planta 251, 19 (2020). https://doi.org/10.1007/s00425-019-03302-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-019-03302-3