Peripheral membrane proteins modulate stress tolerance by safeguarding cellulose synthases

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  • Kesten, Christopher
  • Álvaro García-Moreno
  • Vítor Amorim-Silva
  • Alexandra Menna
  • Araceli G. Castillo
  • Francisco Percio
  • Laia Armengot
  • Noemi Ruiz-Lopez
  • Yvon Jaillais
  • Clara Sánchez-Rodríguez
  • Miguel A. Botella

Controlled primary cell wall remodeling allows plant growth under stressful conditions, but how these changes are conveyed to adjust cellulose synthesis is not understood. Here, we identify the TETRATRICOPEPTIDE THIOREDOXIN-LIKE (TTL) proteins as new members of the cellulose synthase complex (CSC) and describe their unique and hitherto unknown dynamic association with the CSC under cellulose-deficient conditions. We find that TTLs are essential for maintaining cellulose synthesis under high-salinity conditions, establishing a stress-resilient cortical microtubule array, and stabilizing CSCs at the plasma membrane. To fulfill these functions, TTLs interact with CELLULOSE SYNTHASE 1 (CESA1) and engage with cortical microtubules to promote their polymerization. We propose that TTLs function as bridges connecting stress perception with dynamic regulation of cellulose biosynthesis at the plasma membrane.

OriginalsprogEngelsk
Artikelnummereabq6971
TidsskriftScience Advances
Vol/bind8
Udgave nummer46
Antal sider14
ISSN2375-2548
DOI
StatusUdgivet - 2022

Bibliografisk note

Funding Information:
Acknowledgments:W earegra teful toK.ScklodowskiforgeneratingtheCESAconstructsused fortheY2HassaysandtoO.Voinnetforcriticalreadingofthemanuscript.Live-cellimagingwas performedwithequipmentmaintainedbytheScientificCenterforOpticalandElectron Microscopy(ScopeM,ETH-Zürich)andbytheCenterforAdvancedBioimaging(CAB)Denmark. Funding:ThisworkwasfundedbytheSpanishMinistryforScienceandInnovation(MCIN/AEI/ 10.13039/501100011033,PGC2018-098789-B-I00,andPID2019-107657RB-C22toM.A.B.,N.R.-L., and A.G.C., respectively), the Andalusian Research Plan cofinanced by the European Union (PAIDI2020-PY20_00084andUMA20-FEDERJA-023)toM.A.B.andJuntadeAndalucíaUMA-FEDERproject(UMA18-FEDERJA-154)toN.R.-L.,andtheSwissNationalfoundationtoC.S.-R. (SNF31003A_163065/1toAM).C.K.wassupportedbyaPeterundTr audl Engelhorn-Stiftung fellowship,anETHCareerSeedGrant(SEED-0519-2)oftheETHFoundation,anEmerging Investiga tor grant(NNF20OC0060564)oftheNovoNordiskFoundation,andanExperiment grant(R346-2020-1546)oftheLundbeckfoundation.Á.G.-M.wassupportedbyBES-2015-071256andEMBOShort-T erm 7632Fellowships.F .P .wassupportedbyandFPU19/02219 fellowship. V .A.-S. was supported by an Emerging Investigator research project (UMA20-FEDERJA-007)andcofinancedbythe“ProgramaOperativoFEDER2014-2020”andbythe “ConsejeríadeEconomíayConocimientodelaJuntadeAndalucía”.Y .J. wasfundedbythe Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program(grantagreementno.101001097).Authorcontributions:M.A.B.,C.S.-R.,C.K.,Á.G.-M., and V .A.-S. designed the research. C.K. conducted imaging and image analysis, heterologous proteinexpression,andmicrotubule-basedassays.Á.G.-M.andV .A.-S. generatedtheplantlines andthephysiologicalandthebiochemicaldata.A.M.conductedcellulosemeasurements. A.G.C.performedY2Hstudies.F .P .performedthephysiologicalandthephylogeneticanalysis. L.A.andY .J. contributedtolinesgeneration.N.R.-L.contributedtobiochemicalanalyses.Data analyseswereledbyC.K.,Á.G.-M.,V .A.-S., C.S.-R.,andM.A.B.C.K.,V .A.-S., C.S.-R.,andM.A.B.wrote themanuscriptwithmajorcontributionfromY .J. Allauthorsreadandpro vided feedbackonthe manuscript.Competinginterests:Theauthorsdeclarethattheyhav enocompetinginterests. Dataandmaterialsavailability:Alldataneededtoevaluatetheconclusionsinthepaperare presentinthepaperand/ortheSupplementaryMaterials.

Funding Information:
This work was funded by the Spanish Ministry for Science and Innovation (MCIN/AEI/ 10.13039/501100011033, PGC2018-098789-B-I00, and PID2019-107657RB-C22 to M.A.B., N.R.L., and A.G.C., respectively), the Andalusian Research Plan cofinanced by the European Union (PAIDI 2020-PY20_00084 and UMA20-FEDERJA-023) to M.A.B. and Junta de Andalucía UMAFEDER project (UMA18-FEDERJA-154) to N.R.-L., and the Swiss National foundation to C.S.-R. (SNF 31003A_163065/1 to AM). C.K. was supported by a Peter und Traudl Engelhorn-Stiftung fellowship, an ETH Career Seed Grant (SEED-05 19-2) of the ETH Foundation, an Emerging Investigator grant (NNF20OC0060564) of the Novo Nordisk Foundation, and an Experiment grant (R346-2020-1546) of the Lundbeck foundation. Á.G.-M. was supported by BES-2015-071256 and EMBO Short-Term 7632 Fellowships. F.P. was supported by and FPU19/02219 fellowship. V.A.-S. was supported by an Emerging Investigator research project (UMA20-FEDERJA-007) and cofinanced by the “Programa Operativo FEDER 2014-2020” and by the “Consejería de Economía y Conocimiento de la Junta de Andalucía”. Y.J. was funded by the Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement no. 101001097).

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