Microorganisms produce volatile compounds (VCs) with molecular masses of less than 300 Da that promote plant growth and photosynthesis. Recently, we have shown that small VCs of less than 45 Da other than CO2 are major determinants of plant responses to fungal volatile emissions. However, the regulatory mechanisms involved in the plants' responses to small microbial VCs remain unclear. In Arabidopsis thaliana plants exposed to small fungal VCs, growth promotion is accompanied by reduction of the thiol redox of Calvin-Benson cycle (CBC) enzymes and changes in the levels of shikimate and 2-C-methyl-D-erythritol 4-phosphate (MEP) pathway-related compounds. We hypothesized that plants' responses to small microbial VCs involve post-translational modulation of enzymes of the MEP and shikimate pathways via mechanisms involving redox-activated photosynthesis signaling. To test this hypothesis, we compared the responses of wild-type (WT) plants and a cfbp1 mutant defective in a redox-regulated isoform of the CBC enzyme fructose-1,6-bisphosphatase to small VCs emitted by the fungal phytopathogen Alternaria alternata. Fungal VC-promoted growth and photosynthesis, as well as metabolic and proteomic changes, were substantially weaker in cfbp1 plants than in WT plants. In WT plants, but not in cfbp1 plants, small fungal VCs reduced the levels of both transcripts and proteins of the stromal Clp protease system and enhanced those of plastidial chaperonins and co-chaperonins. Consistently, small fungal VCs promoted the accumulation of putative Clp protease clients including MEP and shikimate pathway enzymes. clpr1-2 and clpc1 mutants with disrupted plastidial protein homeostasis responded weakly to small fungal VCs, strongly indicating that plant responses to microbial volatile emissions require a finely regulated plastidial protein quality control system. Our findings provide strong evidence that plant responses to fungal VCs involve chloroplast-to-nucleus retrograde signaling of redox-activated photosynthesis leading to proteostatic regulation of the MEP and shikimate pathways.

Centre for Research in Agricultural Genomics CSIC IRTA UAB UB Barcelona Spain

Department of Chemical Biology and Genetics Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University Olomouc Czechia

Instituto de Agrobiotecnología Mutilva Spain

Instituto de Hortofruticultura Subtropical y Mediterránea La Mayora Campus de Teatinos Málaga Spain

Laboratory of Growth Regulators Faculty of Science of Palackı University and Institute of Experimental Botany of the Czech Academy of Sciences Olomouc Czechia

Unidad de Proteómica Centro Nacional de Biotecnología Consejo Superior de Investigaciones Científicas Madrid Spain

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Ameztoy K., Baslam M., Sánchez-López ÁM., Muñoz F. J., Bahaji A., Almagro G., et al. (2019). Plant responses to fungal volatiles involve global post-translational thiol redox proteome changes that affect photosynthesis. PubMed DOI

Banerjee A., Wu Y., Banerjee R., Li Y., Yan H., Sharkey T. D. (2013). Feedback inhibition of deoxy-D-xylulose-5-phosphate synthase regulates the methylerythritol 4-phosphate pathway. PubMed DOI PMC

Carretero-Paulet L., Ahumada I., Cunillera N., Rodríguez-Concepción M., Ferrer A., Boronat A., et al. (2002). Expression and molecular analysis of the PubMed DOI PMC

Chan K. X., Phua S. Y., Crisp P., McQuinn R., Pogson B. J. (2016). Learning the languages of the chloroplast: retrograde signaling and beyond. PubMed DOI

Chen M., Galvão R. M., Li M., Burger B., Bugea J., Bolado J., et al. (2010). PubMed DOI PMC

Córdoba E., Salmi M., León P. (2009). Unravelling the regulatory mechanisms that modulate the MEP pathway in higher plants. PubMed DOI

Da Q., Wang P., Wang M., Sun T., Jin H., Liu B., et al. (2017). Thioredoxin and NADPH-dependent thioredoxin reductase c regulation of tetrapyrrole biosynthesis. PubMed DOI PMC

Ditengou F. A., Müller A., Rosenkranz M., Felten J., Lasok H., Van Doorn M. M., et al. (2015). Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogrammes root architecture. PubMed DOI PMC

Entus R., Poling M., Herrmann K. M. (2002). Redox regulation of PubMed DOI PMC

Estavillo G. M., Crisp P. A., Pornsiriwong W., Wirtz M., Collinge D., Carrie C., et al. (2011). Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in PubMed DOI PMC

Floková K., Tarkowská D., Miersch O., Strnad M., Wasternack C., Novák O. (2014). UHPLC-MS/MS based target profiling of stress-induced phytohormones. PubMed DOI

García-Gómez P., Almagro G., Sánchez-López ÁM., Bahaji A., Ameztoy K., Ricarte-Bermejo A., et al. (2019). Volatile compounds other than CO PubMed DOI

García-Gómez P., Bahaji A., Gámez-Arcas S., Muñoz F. J., Sánchez-lópez ÁM., Almagro G., et al. (2020). Volatiles from the fungal phytopathogen PubMed DOI

Garnica-Vergara A., Barrera-Ortiz S., Muñoz-Parra E., Raya-González J., Méndez-Bravo A., Macías-Rodríguez L., et al. (2016). The volatile 6-pentyl-2H-pyran-2-one from PubMed DOI

Ghirardo A., Wright L. P., Bi Z., Rosenkranz M., Pulido P., Rodríguez-Concepción M., et al. (2014). Metabolic flux analysis of plastidic isoprenoid biosynthesis in poplar leaves emitting and nonemitting isoprene. PubMed DOI PMC

Ghirardo A., Zimmer I., Brüggemann N., Schnitzler J. P. (2010). Analysis of 1-deoxy-d-xylulose 5-phosphate synthase activity in Grey poplar leaves using isotope ratio mass spectrometry. PubMed DOI

Guo Y., Jud W., Ghirardo A., Antritter F., Benz J. P., Schnitzler J.-P., et al. (2020). Sniffing fungi – phenotyping of volatile chemical diversity in PubMed DOI

Henkes S., Sonnewald U., Badur R., Flachmann R., Stitt M. (2001). A small decrease of plastid transketolase activity in antisense tobacco transformants has dramatic effects on photosynthesis and phenylpropanoid metabolism. PubMed DOI PMC

Hernández-Verdeja T., Strand Å. (2018). Retrograde signals navigate the path to chloroplast development. PubMed DOI PMC

Hooper C. M., Castleden I. R., Tanz S. K., Aryamanesh N., Millar A. H. (2017). SUBA4: The interactive data analysis centre for PubMed DOI PMC

Kessler F., Blobel G. (1996). Interaction of the protein import and folding machineries in the chloroplast. PubMed DOI PMC

Li J., Ezquer I., Bahaji A., Montero M., Ovecka M., Baroja-Fernández E., et al. (2011). Microbial volatile-induced accumulation of exceptionally high levels of starch in PubMed DOI

Lichtenthaler H. K. (1987). Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. DOI

Llamas E., Pulido P., Rodríguez-Concepción M. (2017). Interference with plastome gene expression and Clp protease activity in PubMed DOI PMC

Long S. P., Bernacchi C. J. (2003). Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. PubMed DOI

Megger D. A., Pott L. L., Ahrens M., Padden J., Bracht T., Kuhlmann K., et al. (2014). Comparison of label-free and label-based strategies for proteome analysis of hepatoma cell lines. PubMed DOI

Melonek J., Oetke S., Krupinska K. (2016). Multifunctionality of plastid nucleoids as revealed by proteome analyses. PubMed DOI

Michelet L., Zaffagnini M., Morisse S., Sparla F., Pérez-Pérez M. E., Francia F., et al. (2013). Redox regulation of the Calvin-Benson cycle: something old, something new. PubMed DOI PMC

Moreno J. C., Martínez-Jaime S., Schwartzmann J., Karcher D., Tillich M., Graf A., et al. (2018). Temporal proteomics of inducible RNAi lines of Clp protease subunits identifies putative protease substrates. PubMed DOI PMC

Naranjo B., Diaz-Espejo A., Lindahl M., Cejudo F. J. (2016). Type- PubMed DOI PMC

Nishimura K., Asakura Y., Friso G., Kim J., Oh S. H., Rutschow H., et al. (2013). ClpS1 is a conserved substrate selector for the chloroplast Clp protease system in PubMed DOI PMC

Nishimura K., Kato Y., Sakamoto W. (2017). Essentials of proteolytic machineries in chloroplasts. PubMed DOI

Novák O., Hauserová E., Amakorová P., Doležal K., Strnad M. (2008). Cytokinin profiling in plant tissues using ultra-performance liquid chromatography-electrospray tandem mass spectrometry. PubMed DOI

Okegawa Y., Motohashi K. (2015). Chloroplastic thioredoxin PubMed DOI

Pěnčík A., Rolčík J., Novák O., Magnus V., Barták P., Buchtík R., et al. (2009). Isolation of novel indole-3-acetic acid conjugates by immunoaffinity extraction. PubMed DOI

Perlaza K., Toutkoushian H., Boone M., Lam M., Iwai M., Jonikas M. C., et al. (2019). The Mars1 kinase confers photoprotection through signaling in the chloroplast unfolded protein response. PubMed DOI PMC

Phua S. Y., Yan D., Chan K. X., Estavillo G. M., Nambara E., Pogson B. J. (2018). The Arabidopsis SAL1-PAP pathway: a case study for integrating chloroplast retrograde, light and hormonal signaling in modulating plant growth and development? PubMed DOI PMC

Pokhilko A., Bou-Torrent J., Pulido P., Rodríguez-Concepción M., Ebenhöh O. (2015). Mathematical modelling of the diurnal regulation of the MEP pathway in Arabidopsis. PubMed DOI

Pulido P., Llamas E., Llorente B., Ventura S., Wright L. P., Rodríguez-Concepción M. (2016). Specific Hsp100 chaperones determine the fate of the first enzyme of the plastidial isoprenoid pathway for either refolding or degradation by the stromal Clp protease in PubMed DOI PMC

Pulido P., Toledo-Ortiz G., Phillips M. A., Wright L. P., Rodríguez-Concepción M. (2013). Arabidopsis J-Protein J20 delivers the first enzyme of the plastidial isoprenoid pathway to protein quality control. PubMed DOI PMC

Rodríguez-Concepción M., D’Andrea L., Pulido P. (2019). Control of plastidial metabolism by the Clp protease complex. PubMed DOI

Rojas-González J. A., Soto-Súarez M., García-Díaz Á, Romero-Puertas M. C., Sandalio L. M., Mérida Á, et al. (2015). Disruption of both chloroplastic and cytosolic FBPase genes results in a dwarf phenotype and important starch and metabolite changes in PubMed DOI PMC

Rudella A., Friso G., Alonso J. M., Ecker J. R., Van Wijk K. J. (2006). Downregulation of ClpR2 leads to reduced accumulation of the ClpPRS protease complex and defects in chloroplast biogenesis in PubMed DOI PMC

Ryu C.-M., Farag M. A., Hu C.-H., Reddy M. S., Wei H.-X., Pare P. W., et al. (2003). Bacterial volatiles promote growth in PubMed DOI PMC

Sánchez-López ÁM., Bahaji A., De Diego N., Baslam M., Li J., Muñoz F. J., et al. (2016a). Arabidopsis responds to PubMed DOI PMC

Sánchez-López ÁM., Baslam M., De Diego N., Muñoz F. J., Bahaji A., Almagro G., et al. (2016b). Volatile compounds emitted by diverse phytopathogenic microorganisms promote plant growth and flowering through cytokinin action. PubMed DOI

Serrato A. J., Yubero-Serrano E. M., Sandalio L. M., Muñoz-Blanco J., Chueca A., Caballero J. L., et al. (2009). cpFBPaseII, a novel redox-independent chloroplastic isoform of fructose-1,6-bisphosphatase. PubMed DOI

Teow C. C., Truong V., Den McFeeters R. F., Thompson R. L., Pecota K. V., Yencho G. C. (2007). Antioxidant activities, phenolic and β-carotene contents of sweet potato genotypes with varying flesh colours. DOI

Thimm O., Bläsing O., Gibon Y., Nagel A., Meyer S., Krüger P., et al. (2004). MAPMAN: A user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. PubMed DOI

Tsai Y. C. C., Mueller-Cajar O., Saschenbrecker S., Hartl F. U., Hayer-Hartl M. (2012). Chaperonin cofactors, Cpn10 and Cpn20, of green algae and plants function as hetero-oligomeric ring complexes. PubMed DOI PMC

Tzin V., Malitsky S., Zvi M. M., Ben Bedair M., Sumner L., Aharoni A., et al. (2012). Expression of a bacterial feedback-insensitive 3-deoxy-d-arabino-heptulosonate 7-phosphate synthase of the shikimate pathway in PubMed DOI

Vogel M. O., Moore M., König K., Pecher P., Alsharafa K., Lee J., et al. (2014). Fast retrograde signaling in response to high light involves metabolite export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ERF transcription factors in PubMed DOI PMC

von Caemmerer S., Farquhar G. D. (1981). Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. PubMed DOI

Vranová E., Coman D., Gruissem W. (2013). Network analysis of the MVA and MEP pathways for isoprenoid synthesis. PubMed DOI

Welsch R., Zhou X., Yuan H., Álvarez D., Sun T., Schlossarek D., et al. (2018). Clp protease and OR directly control the proteostasis of phytoene synthase, the crucial enzyme for carotenoid biosynthesis in PubMed DOI

Wright L. P., Rohwer J. M., Ghirardo A., Hammerbacher A., Ortiz-Alcaide M., Raguschke B., et al. (2014). Deoxyxylulose 5-phosphate synthase controls flux through the methylerythritol 4-phosphate pathway in PubMed DOI PMC

Xiao Y., Savchenko T., Baidoo E. E. K., Chehab W. E., Hayden D. M., Tolstikov V., et al. (2012). Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes. PubMed DOI

Yin R., Messner B., Faus-Kessler T., Hoffmann T., Schwab W., Hajirezaei M. R., et al. (2012). Feedback inhibition of the general phenylpropanoid and flavonol biosynthetic pathways upon a compromised flavonol-3-O-glycosylation. PubMed DOI PMC

Zhang H., Xie X., Kim M. S., Kornyeyev D. A., Holaday S., Paré P. W. (2008). Soil bacteria augment PubMed DOI

Zhao Q., Liu C. (2018). Chloroplast chaperonin: an intricate protein folding machine for photosynthesis. PubMed DOI PMC

Zheng B., Halperin T., Hruskova-Heidingsfeldova O., Adam Z., Clarke A. K. (2002). Characterization of chloroplast Clp proteins in PubMed DOI

Zybailov B., Friso G., Kim J., Rudella A., Rodríguez V. R., Asakura Y., et al. (2009). Large scale comparative proteomics of a chloroplast Clp protease mutant reveals folding stress, altered protein homeostasis, and feedback regulation of metabolism. PubMed DOI PMC

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