Пограничные клетки корневого апекса: роль в стратегиях адаптации и корневом иммунитете
- Authors: Пятина С.А.1, Шишацкая Е.И.1, Мензянова Н.Г.1
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Affiliations:
- Федеральное государственное автономное образовательное учреждение высшего образования “Сибирский федеральный университет”
- Issue: Vol 71, No 4 (2024)
- Pages: 398-408
- Section: ОБЗОРЫ
- URL: https://journals.rcsi.science/0015-3303/article/view/268072
- DOI: https://doi.org/10.31857/S0015330324040029
- EDN: https://elibrary.ru/MOHIPN
- ID: 268072
Cite item
Abstract
Пограничные клетки (ПК) – клеточная популяция корневого чехлика, которая в процессе дифференцировки отделяется от поверхности корневого апекса в форме одиночных клеток, небольших агрегатов или клеточных пластов, и переходит в ризосферное пространство. Функциональная активность ПК в ризосфере реализуется через продукцию экзометаболитов. В обзоре обсуждается роль ПК и формирующейся из их экзометаболитов корневой экстраклеточной ловушки в процессах адаптации корневой системы к различным абиотическим факторам и реакциях корневой иммунной системы.
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About the authors
С. А. Пятина
Федеральное государственное автономное образовательное учреждение высшего образования “Сибирский федеральный университет”
Author for correspondence.
Email: davcbetik@mail.ru
Russian Federation, Красноярск
Е. И. Шишацкая
Федеральное государственное автономное образовательное учреждение высшего образования “Сибирский федеральный университет”
Email: davcbetik@mail.ru
Russian Federation, Красноярск
Н. Г. Мензянова
Федеральное государственное автономное образовательное учреждение высшего образования “Сибирский федеральный университет”
Email: davcbetik@mail.ru
Russian Federation, Красноярск
References
- Hawes M.C., Gunawardena U., Miyasaka S., Zhao X. The role of root border cells in plant defense // Trends Plant Sci. 2000. V. 5. Р. 128. https://doi.org/10.1016/S1360-1385(00)01556-9
- Knudson L. Viability of detached root-cap cells // Am. J. Bot. 1919. V. 6. P. 309.
- Hawes M.C., Lin H.J. Correlation of pectolytic enzyme activity with the programmed release of cells from root caps of pea (Pisum sativum) // Plant Physiol. 1990. V. 94. P. 1855. https://doi.org/10.1104/pp.94.4.1855
- Hawes M.C., Pueppke S.G. Sloughed peripheral root cap cells: yield from different species and callus formation from single cells // Am. J. Bot. 1986. V. 73. P. 1466. https://doi.org/10.1002/j.1537-2197.1986.tb10892.x
- Mravec J., Guo X., Hansen A.R., Schückel J., Kračun S.K.I., Mikkelsen M.D., Mouille G., Johansen I.E., Ulvskov P., Domozych D.S., Willats W.G.T. Pea border cell maturation and release involve complex cell wall structural dynamics // Plant Physiol. 2017. V. 174. P. 1051. https://doi.org/10.1104/pp.16.00097
- Plancot B., Santaella C., Jaber R., Kiefer-Meyer M.C., Follet-Gueye M.L., Leprince J., Gattin I., Souc C., Driouich A., Vicré-Gibouin M. Deciphering the responses of root border-like cells of Arabidopsis and flax to pathogen-derived elicitors // Plant Physiol. 2013. V. 163. P. 1584. https://doi.org/10.1104/pp.113.222356
- Busont O., Durambur G., Bernard S., Plasson C., Joudiou C., Baude L., Chefdor F., Depierreux C., Héricourt F., Larcher M., Malik S., Boulogne I., Driouich A., Carpin S., Lamblin F. Black poplar (Populus nigra L.) root extracellular trap, structural and molecular remodeling in response to osmotic stress // Cells. 2023. V. 12. P. 858. https://doi.org/10.3390/cells12060858
- Vicré M., Santaella C., Blanchet S., Gateau A., Driouich A. Root border-like cells of Arabidopsis. Microscopical characterization and role in the interaction with rhizobacteria // Plant Physiol. 2005. V. 138. P. 998. https://doi.org/10.1104/pp.104.051813
- Endo I., Tange T., Osawa H. 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. 2011. V. 108. P. 279. https://doi.org/10.1093/aob/mcr139
- Ropitaux M., Bernard S., Schapman D., Follet-Gueye M.L., Vicré M., Boulogne I., Driouich A. Root border cells and mucilage secretions of soybean, Glycine max (Merr) L.: characterization and role in interactions with the oomycete Phytophthora parasitica // Cells. 2020. V. 9. P. 2215. https://doi.org/10.3390/cells9102215
- Curlango-Rivera G., Huskey D.A., Mostafa A., Kessler J.O., Xiong Z., Hawes M.C. Intraspecies variation in cotton border cell production: rhizosphere microbiome implications // Am. J. Bot. 2013. V. 100. P. 1706. https://doi.org/10.3732/ajb.1200607
- Hawes M.C., Bengough G., Cassab G., Ponce G. Root caps and rhizosphere // J. Plant Growth Regul. 2002. V. 21. P. 352. https://doi.org/10.1007/s00344-002-0035-y
- Feng Y., Li H., Zhang X., Li X., Zhang J., Shi L., Chen X., Nong W., Wang C., Shabala S., Yu M. Effects of cadmium stress on root and root border cells of some vegetable species with different types of root meristem // Life. 2022. V. 12. P. 1401. https://doi.org/10.3390/life12091401
- Nagahashi G., Douds D.D. Isolated root caps, border cells, and mucilage from host roots stimulate hyphal branching of the arbuscular mycorrhizal fungus, Gigaspora gigantean // Mycol. Res. 2004. V. 108. P. 1079. https://doi.org/10.1017/S0953756204000693
- Berry A.M., Rasmussen U., Bateman K., Huss-Danell K., Lindwall S., Bergman B. Arabinogalactan proteins are expressed at the symbiotic interface in root nodules of Alnus spp // New Phytol. 2002. V. 155. P. 469. https://doi.org/10.1046/j.1469-8137.2002.00466.x
- Watson B.S., Bedair M.F., Urbanczyk-Wochniak E., Huhman D.V., Yang D.S., Allen S.N., Li W., Tang Y., Sumner L.W. Integrated metabolomics and transcriptomics reveal enhanced specialized metabolism in Medicago truncatula root border cells // Plant Physiol. 2015. V. 167. P. 1699. https://doi.org/10.1104/pp.114.253054
- Canellas L.P., Olivares F.L. Production of border cells and colonization of maize root tips by Herbaspirillum seropedicae are modulated by humic acid // Plant Soil. 2017. V. 417. P. 403. https://doi.org/10.1007/s11104-017-3267-0
- Hassan M.K., McInroy J.A., Kloepper J.W. The interactions of rhizodeposits with plant growth-promoting rhizobacteria in the rhizosphere: a review // Agriculture. 2019. V. 9. P. 142. https://doi.org/10.3390/agriculture9070142
- Shirakawa M., Matsushita N., Fukuda K. Visualization of root extracellular traps in an ectomycorrhizal woody plant (Pinus densiflora) and their interactions with root-associated bacteria // Planta. 2023. V. 258. P. 112. https://doi.org/10.1007/s00425-023-04274-1
- Ragland C.J., Shih K.Y., Dinneny J.R. Choreographing root architecture and rhizosphere interactions through synthetic biology // Nat. Commun. 2024. V. 15. P. 1370. https://doi.org/10.1038/s41467-024-45272-5
- Brigham L.A., Woo H.H., Wen F., Hawes M.C. Meristem-specific suppression of mitosis and a global switch in gene expression in the root cap of pea by endogenous signals // Plant Physiol. 1998. V. 118. P. 1223. https://doi.org/10.1104/pp.118.4.1223
- Bojun M., Jianwei P., Zhaojuan F., Pinghua Z., Muyuan Z. Development and influencing factors of soybean root border cell // Zuowu Xuebao. 2005. V. 31. P. 165.
- Kumar N., Iyer-Pascuzzi A.S. Shedding the last layer: mechanisms of root cap cell release // Plants. 2020. V. 9. P. 308. https://doi.org/10.3390/plants9030308
- Bozhkov A.I., Kuznetsova Y.A., Menzyanova N.G. Effect of sodium fluoride on the root apex border cells in one-day-old wheat seedlings // Russ. J. Plant Physiol. 2009. V. 56. P. 480. https://doi.org/10.1134/S1021443709040062
- Xiao Z., Liang Y. Silicon prevents aluminum from entering root tip by promoting formation of root border cells in rice // Plant Physiol. Biochem. 2022. V. 175. P. 12. https://doi.org/10.1016/j.plaphy.2022.02.003
- Shishatskaya E., Menzyanova N., Zhila N., Prudnikova S., Volova T., Thomas S. Toxic effects of the fungicide tebuconazole on the root system of fusarium-infected wheat plants // Plant Physiol. Biochem. 2018. V. 132. P. 400. https://doi.org/10.1016/j.plaphy.2018.09.025
- Menzyanova N.G., Pyatina S.A., Shabanov A.V., Shishatskaya E.I. Dose-dependent effects of nanoscale forms of humic acids in a hydroponic culture of Triticum aestivum: induction of oxidative stress and an increase in the number of border cells // J. Sib. Fed. Univ. Biol. 2023. V. 16. P. 64.
- Zhao X., Misaghi I.J., Hawes M.C. Stimulation of border cell production in response to increased carbon dioxide levels // Plant Physiol. 2000. V. 122. P. 181. https://doi.org/10.1104/pp.122.1.181
- Cannesan M.A., Gangneux C., Lanoue A., Giron D., Laval K., Hawes M., Driouich A., Vicré-Gibouin M. Association between border cell responses and localized root infection by pathogenic Aphanomyces euteiches // Ann. Bot. 2011. V. 108. P. 459. https://doi.org/10.1093/aob/mcr177
- Wen F., VanEtten H.D., Tsaprailis G., Hawes M.C. Extracellular proteins in pea root tip and border cell exudates // Plant Physiol. 2007. V. 143. P. 773. https://doi.org/10.1104/pp.106.091637
- Woo H.H., Hirsch A.M., Hawes M.C. Altered susceptibility to infection by Sinorhizobium meliloti and Nectria haematococca in alfalfa roots with altered cell cycle // Plant Cell Rep. 2004. V. 22. P. 967. https://doi.org/10.1007/s00299-004-0787-x
- Wormit A., Usadel B. The multifaceted role of pectin methylesterase inhibitors (PMEIs) // Int. J. Mol. Sci. 2018. V. 19. P. 2878. https://doi.org/10.3390/ijms19102878
- Driouich A., Durand C., Vicré-Gibouin M. Formation and separation of root border cells // Trends Plant Sci. 2007. V. 12. P. 14. https://doi.org/10.1016/j.tplants.2006.11.003
- Babu Y., Bayer M. Plant polygalacturonases involved in cell elongation and separation – the same but different? // Plants. 2014. V. 3. P. 613. https://doi.org/10.3390/plants3040613
- Yan J., Zhu J., Zhou J., Xing C., Song H., Wu K., Cai M. Using brefeldin A to disrupt cell wall polysaccharide components in rice and nitric oxide to modify cell wall structure to change aluminum tolerance // Front. Plant Sci. 2022. V. 13. P. 948212. https://doi.org/10.3389/fpls.2022.948212
- Schmidt R., Kunkowska A.B., Schippers J.H. Role of reactive oxygen species during cell expansion in leaves // Plant Physiol. 2016. V. 172. P. 2098. https://doi.org/10.1104/pp.16.00426
- Majda M., Robert S. The role of auxin in cell wall expansion // Int. J. Mol. Sci. 2018. V. 19. P. 951. https://doi.org/10.3390/ijms19040951
- Zhang J., Qian Y., Chen Z., Amee M., Niu H., Du D., Yao J., Chen K., Chen L., Sun J. Lead-induced oxidative stress triggers root cell wall remodeling and increases lead absorption through esterification of cell wall polysaccharide // J. Hazard. Mater. 2020. V. 385. P. 121524. https://doi.org/10.1016/j.jhazmat.2019.121524
- Pieczywek P.M., Leszczuk A., Kurzyna-Szklarek M., Cybulska J., Jóźwiak Z., Rutkowski K., Zdunek A. Apple metabolism under oxidative stress affects plant cell wall structure and mechanical properties // Sci. Rep. 2023. V. 13. P. 13879. https://doi.org/10.1038/s41598-023-40782-6
- Wen F., Brigham L.A., Curlango-Rivera G., Xiong Z., Hawes M.C. Altered growth and root tip morphology in Pisum sativum L. in response to altered expression of a gene expressed in border cells // Plant Soil. 2014. V. 377. P. 179. https://doi.org/10.1007/s11104-013-1995-3
- Wen F., Celoy R., Price I., Ebolo J.J., Hawes M.C. Identification and characterization of a rhizosphere β-galactosidase from Pisum sativum L. // Plant Soil. 2008. V. 304. P. 133. https://doi.org/10.1007/s11104-007-9528-6
- Chuberre C., Plancot B., Driouich A., Moore J.P., Bardor M., Gügi B., Vicré M. Plant immunity is compartmentalized and specialized in roots // Front. Plant Sci. 2018. V. 9. P. 1692. https://doi.org/10.3389/fpls.2018.01692
- Driouich A., Gaudry A., Pawlak B., Moore J.P. Root cap – derived cells and mucilage: a protective network at the root tip // Protoplasma. 2021. V. 258. P. 1179. https://doi.org/10.1007/s00709-021-01660-y
- Hawes M., Allen C., Turgeon B.G., Curlango-Rivera G., Minh Tran T., Huskey D.A., Xiong Z. Root border cells and their role in plant defense // Annu. Rev. Phytopathol. 2016. V. 54. P. 143. https://doi.org/10.1146/annurev-phyto-080615-100140
- Driouich A., Smith C., Ropitaux M., Chambard M., Boulogne I., Bernard S., Follet-Gueye M., Vicré M., Moore J. Root extracellular traps versus neutrophil extracellular traps in host defence, a case of functional convergence? // Biol. Rev. 2019. V. 94. P. 1685. https://doi.org/10.1111/brv.12522
- Driouich A., Follet-Gueye M.L., Vicré-Gibouin M., Hawes M. Root border cells and secretions as critical elements in plant host defense // Curr. Opin. Plant Biol. 2013. V. 16. P. 489. https://doi.org/10.1016/j.pbi.2013.06.010
- Carreras A., Bernard S., Durambur G., Gügi B., Loutelier C., Pawlak B., Boulogne I., Vicré M., Driouich A., Goffner D., Follet-Gueye M.L. In vitro characterization of root extracellular trap and exudates of three Sahelian woody plant species // Planta. 2020. V. 251. P. 1. https://doi.org/10.1007/s00425-019-03302-3
- Vincent D., Rafiqi M., Job D. The multiple facets of plant–fungal interactions revealed through plant and fungal secretomics // Front. Plant Sci. 2020. V. 10. P. 1626. https://doi.org/10.3389/fpls.2019.01626
- Hartman K., Schmid M.W., Bodenhausen N., Bender S.F., Valzano-Held A.Y., Schlaeppi K., van der Heijden M.G. A symbiotic footprint in the plant root microbiome // Environ. Microbiome. 2023. V. 18. P. 65. https://doi.org/10.1186/s40793-023-00521-w
- Li J., Yang Z.L., Ding T., Song Y.J., Li H.C., Li D.Q., Chen S., Xu F. The role of surface functional groups of pectin and pectin-based materials on the adsorption of heavy metal ions and dyes // Carbohydr. Polym. 2022. V. 276. P. 118789. https://doi.org/10.1016/j.carbpol.2021.118789
- Nagayama T., Nakamura A., Yamaji N., Satoh S., Furukawa J., Iwai H. Changes in the distribution of pectin in root border cells under aluminum stress // Front. Plant Sci. 2019. V. 10. P. 1216. https://doi.org/10.3389/fpls.2019.01216
- Zhang Y., Wu Y., Xu G., Song J., Wu T., Mei X., Liu P. Effects of iron toxicity on the morphological and biological characteristics of rice root border cells // J. Plant Nutr. 2017. V. 40. P. 332. https://doi.org/10.1080/01904167.2016.1240193
- Dolinska J., Holdynski M., Pieta P., Lisowski W., Ratajczyk T., Palys B., Jablonska A., Opallo M. Noble metal nanoparticles in pectin matrix. Preparation, film formation, property analysis, and application in electrocatalysis // ACS Omega. 2020. V. 5. P. 23909. https://doi.org/10.1021/acsomega.0c03167
- Feng L., Xu N., Qu Q., Zhang Z., Ke M., Lu T., Qian H. Synergetic toxicity of silver nanoparticle and glyphosate on wheat (Triticum aestivum L.) // Sci. Total Environ. 2021. V. 797. P. 149200. https://doi.org/10.1016/j.scitotenv.2021.149200
- Park H.J., Wang W., Curlango-Rivera G., Xiong Z., Lin Z., Huskey D.A., Hawes M.C., VanEtten H.D., Turgeon B.G. A DNase from a fungal phytopathogen is a virulence factor likely deployed as counter defense against host-secreted extracellular DNA // MBio. 2019. V. 10. P. 10. https://doi.org/10.1128/mbio.02805-18
- Wen F., White G.J., VanEtten H.D., Xiong Z., Hawes M.C. Extracellular DNA is required for root tip resistance to fungal infection // Plant Physiol. 2009. V. 151. P. 820. https://doi.org/10.1104/pp.109.142067
- Chambard M., Plasson C., Derambure C., Coutant S., Tournier I., Lefranc B., Leprince J., Kiefer-Meyer M.C., Driouich A., Follet-Gueye M.L., Boulogne I. New insights into plant extracellular DNA. A study in soybean root extracellular trap // Cells. 2021. V. 10. P. 69. https://doi.org/10.3390/cells10010069
- Zhou W., Saran R., Liu J. Metal sensing by DNA // Chem. Rev. 2017. V. 117. P. 8272. https://doi.org/10.1021/acs.chemrev.7b00063
- Karimi-Maleh H., Liu Y., Li Z., Darabi R., Orooji Y., Karaman C., Karimi F., Baghayeri M., Rouhi J., Fu L., Rostamnia S., Rajendran S., Sanati A.L., Sadeghifar H., Ghalkhani M. Calf thymus ds-DNA intercalation with pendimethalin herbicide at the surface of ZIF-8/Co/rGO/C3N4/ds-DNA/SPCE; a bio-sensing approach for pendimethalin quantification confirmed by molecular docking study // Chemosphere. 2023. V. 332. P. 138815. https://doi.org/10.1016/j.chemosphere.2023.138815
- Avellan A., Yun J., Zhang Y., Spielman-Sun E., Unrine J.M., Thieme J., Li J., Lombi E., Bland G., Lowry G.V. Nanoparticle size and coating chemistry control foliar uptake pathways, translocation, and leaf-to-rhizosphere transport in wheat // ACS Nano. 2019. V. 13. P. 5291. https://doi.org/10.1021/acsnano.8b09781
- Oota M., Toyoda S., Kotake T., Wada N., Hashiguchi M., Akashi R., Ishikawa H., B. Favery, Tsai A.Y., Sawa S. Rhamnogalacturonan-I as a nematode chemoattractant from Lotus corniculatus L. super-growing root culture // Front. Plant Sci. 2023. V. 13. P. 1008725. https://doi.org/10.3389/fpls.2022.1008725
- Vaghela B., Vashi R., Rajput K., Joshi R. Plant chitinases and their role in plant defense: a comprehensive review // Enzyme Microb. Technol. 2022. V. 159. P. 110055. https://doi.org/10.1016/j.enzmictec.2022.110055
- Perrot T., Pauly M., Ramírez V. Emerging roles of β-glucanases in plant development and adaptative responses // Plants. 2022. V. 11. P. 1119. https://doi.org/10.3390/plants11091119
- du Toit A. Defence and counter defence // Nat. Rev. Microbiol. 2019. V. 17. P. 267. https://doi.org/10.1038/s41579-019-0185-6
- Jensen J.K., Sørensen S.O., Harholt J., Geshi N., Sakuragi Y., Møller I., J. Zandleven, Bernal A.J., Jensen N.B., Sørensen C., Pauly M., Beldman G., Willats W.G.T., Scheller H.V. Identification of a xylogalacturonan xylosyltransferase involved in pectin biosynthesis in Arabidopsis // Plant Cell. 2008. V. 20. P. 1289. https://doi.org/10.1105/tpc.107.050906
- Tran T.M., MacIntyre A., Hawes M., Allen C. Escaping underground nets: extracellular DNases degrade plant extracellular traps and contribute to virulence of the plant pathogenic bacterium Ralstonia solanacearum // PLoS Pathog. 2016. V. 12. P. e1005686. https://doi.org/10.1371/journal.ppat.1005686
- Ramos-Martínez E., Hernández-González L., Ramos-Martínez I., Perez-Campos Mayoral L., López-Cortés G.I., Pérez-Campos E., Andrade G.M., Hernández-Huerta M.T., José M.V. Multiple origins of extracellular DNA traps // Front. Immunol. 2021. V. 12. P. 621311. https://doi.org/10.3389/fimmu.2021.621311
- Mutua V., Gershwin L.J. A review of neutrophil extracellular traps (NETs) in disease: potential anti-NETs therapeutics // Clin. Rev. Allergy Immunol. 2021. V. 61. P. 194. https://doi.org/10.1007/s12016-020-08804-7
- Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D.S., Weinrauch Y., Zychlinsky A. Neutrophil extracellular traps kill bacteria // Science. 2004. V. 303. P. 1532. https://doi.org/10.1126/science.1092
- Reichel M., Muñoz-Caro T., Contreras G.S., García A.R., Magdowski G., Gärtner U., Taubert A., Hermosilla C. Harbour seal (Phoca vitulina) PMN and monocytes release extracellular traps to capture the apicomplexan parasite Toxoplasma gondii // Dev. Comp. Immunol. 2015. V. 50. P. 106. https://doi.org/10.1016/j.dci.2015.02.002
- Yang H., Biermann M.H., Brauner J.M., Liu Y., Zhao Y., Herrmann M. New insights into neutrophil extracellular traps: mechanisms of formation and role in inflammation // Front. Immunol. 2016. V. 7. P. 302. https://doi.org/10.3389/fimmu.2016.00302
- Zhang X., Zhuchenko O., Kuspa A., Soldati T. Social amoebae trap and kill bacteria by casting DNA nets // Nat. Commun. 2016. V. 7. P. 10938. https://doi.org/10.1038/ncomms10938
- Wiszniewska A. Priming strategies for benefiting plant performance under toxic trace metal exposure // Plants. 2021. V. 10. P. 623. https://doi.org/10.3390/plants10040623
- Chen H.H., Chen X.F., Zheng Z.C., Huang W.L., Guo J., Yang L.T., Chen L.S. Characterization of copper-induced-release of exudates by Citrus sinensis roots and their possible roles in copper-tolerance // Chemosphere. 2022. V. 308. P. 136348. https://doi.org/10.1016/j.chemosphere.2022.136348
- Slobodiuk S., Niven C., Arthur G., Thakur S., Ercumen A. Does irrigation with treated and untreated wastewater increase antimicrobial resistance in soil and water: a systematic review // Int. J. Environ. Res. Public Health 2021. V. 18. P. 11046. https://doi.org/10.3390/ijerph182111046
- Mordor Intelligence (2024) https://www.mordorintelligence.com/industry-reports/hydroponics-market. Cited 6 May 2024.
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