Endophytic fungi that colonize the plant root live in an environment with relative high concentrations of different sugars. Analyses of genome sequences indicate that such endophytes can secrete carbohydrate-related enzymes to compete for these sugars with the surrounding plant cells. We hypothesized that typical plant sugars can be used as carbon source by root endophytes and that these sugars also serve as signals to induce the expression and secretion of glycolytic enzymes. The plant-growth-promoting endophytes Serendipita indica and Serendipita herbamans were selected to first determine which sugars promote their growth and biomass formation. Secondly, particular sugars were added to liquid cultures of the fungi to induce intracellular and extracellular enzymatic activities which were measured in mycelia and culture supernatants. The results showed that both fungi cannot feed on melibiose and lactose, but instead use glucose, fructose, sucrose, mannose, arabinose, galactose and xylose as carbohydrate sources. These sugars regulated the cytoplasmic activity of glycolytic enzymes and also their secretion. The levels of induction or repression depended on the type of sugars added to the cultures and differed between the two fungi. Since no conventional signal peptide could be detected in most of the genome sequences encoding the glycolytic enzymes, a non-conventional protein secretory pathway is assumed. The results of the study suggest that root endophytic fungi translocate glycolytic activities into the root, and this process is regulated by the availability of particular plant sugars.

Department of Adaptive Biotechnologies Global Change Research Institute Czech Academy of Sciences 603 00 Brno Czech Republic

Department of Plant and Environmental Sciences University of Copenhagen 2630 Copenhagen Denmark

Institute of Biology Humboldt Universität zu Berlin Philippstrasse 13 10115 Berlin Germany

Leibniz Institute of Vegetable and Ornamental Crops Theodor Echtermeyer Weg 1 14979 Großbeeren Germany

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Weiß M., Waller F., Zuccaro A., Selosse M. Sebacinales—One thousand and one interactions with land plants. New Phytol. 2016;211:20–40. doi: 10.1111/nph.13977. PubMed DOI

Verma S., Varma A., Rexer K.-H., Hassel A., Kost G., Sarbhoy A., Bisen P., Butehorn B., Franken P. Piriformospora indica, gen. et sp. nov., a New Root-Colonizing Fungus. Mycologia. 1998;90:896. doi: 10.2307/3761331. DOI

Varma A., Verma S., Sahay N. Piriformospora Indica, Ble Plant-Growth-Promoting Root Endophyte. Appl. Environ. Microbiol. 1999;65:22–26. doi: 10.1128/AEM.65.6.2741-2744.1999. PubMed DOI PMC

Banhara A., Ding Y., Kühner R., Zuccaro A., Parniske M. Colonization of root cells and plant growth promotion by Piriformospora indica occurs independently of plant common symbiosis genes. Front. Plant Sci. 2015;6:667. doi: 10.3389/fpls.2015.00667. PubMed DOI PMC

Fakhro A., Andrade-Linares D.R., Von Bargen S., Bandte M., Büttner C., Grosch R., Schwarz D., Franken P. Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza. 2010;20:191–200. doi: 10.1007/s00572-009-0279-5. PubMed DOI

Gill S.S., Gill R., Trivedi D.K., Anjum N.A., Sharma K.K., Ansari M.W., Ansari A.A., Johri A.K., Prasad R., Pereira E., et al. Piriformospora indica: Potential and Significance in Plant Stress Tolerance. Front. Microbiol. 2016;7:332. doi: 10.3389/fmicb.2016.00332. PubMed DOI PMC

Varma A., Verma S., Sahay N., Tehorn B.B., Franken P., Varma A., Sahay N., Bütehorn B., Franken P.V.S.S. Piriformospora Indica, a Cultivable Plant-Growth-Promoting Root Endophyte. Appl. Environ. Microbiol. 1999;65:2741–2744. doi: 10.1128/AEM.65.6.2741-2744.1999. PubMed DOI PMC

Waller F., Achatz B., Baltruschat H., Fodor J., Becker K., Fischer M., Heier T., Hückelhoven R., Neumann C., von Wettstein D., et al. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc. Natl. Acad. Sci. USA. 2005;102:13386–13391. doi: 10.1073/pnas.0504423102. PubMed DOI PMC

Riess K., Oberwinkler F., Bauer R., Garnica S. Communities of Endophytic Sebacinales Associated with Roots of Herbaceous Plants in Agricultural and Grassland Ecosystems Are Dominated by Serendipita herbamans sp. nov. PLoS ONE. 2014;9:e94676. doi: 10.1371/journal.pone.0094676. PubMed DOI PMC

Blechert O., Kost G., Hassel A., Rexer K.-H., Varma A. Mycorrhiza. Springer; Singapore: 1999. First Remarks on the Symbiotic Interaction Between Piriformospora indica and Terrestrial Orchids; pp. 683–688.

Vohník M., Pánek M., Fehrer J., Selosse M.-A. Experimental evidence of ericoid mycorrhizal potential within Serendipitaceae (Sebacinales) Mycorrhiza. 2016;26:831–846. doi: 10.1007/s00572-016-0717-0. PubMed DOI

Behie S.W., Bidochka M.J. Nutrient transfer in plant–fungal symbioses. Trends Plant Sci. 2014;19:734–740. doi: 10.1016/j.tplants.2014.06.007. PubMed DOI

Gianinazzi-Pearson V. Plant Cell Responses to Arbuscular Mycorrhizal Fungi: Getting to the Roots of the Symbiosis. Plant Cell. 1996;8:1871–1883. doi: 10.2307/3870236. PubMed DOI PMC

Parniske M. Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol. 2004;7:414–421. doi: 10.1016/j.pbi.2004.05.011. PubMed DOI

Harrison M.J. Signaling in the Arbuscular Mycorrhizal Symbiosis. Annu. Rev. Microbiol. 2005;59:19–42. doi: 10.1146/annurev.micro.58.030603.123749. PubMed DOI

Wang W., Shi J., Xie Q., Jiang Y., Yu N., Wang E. Nutrient Exchange and Regulation in Arbuscular Mycorrhizal Symbiosis. Mol. Plant. 2017;10:1147–1158. doi: 10.1016/j.molp.2017.07.012. PubMed DOI

Zuccaro A., Lahrmann U., Güldener U., Langen G., Pfiffi S., Biedenkopf D., Wong P., Samans B., Grimm C., Basiewicz M., et al. Endophytic Life Strategies Decoded by Genome and Transcriptome Analyses of the Mutualistic Root Symbiont Piriformospora indica. PLoS Pathog. 2011;7:e1002290. doi: 10.1371/journal.ppat.1002290. PubMed DOI PMC

Rani M., Raj S., Dayaman V., Kumar M., Dua M., Johri A.K. Functional Characterization of a Hexose Transporter from Root Endophyte Piriformospora indica. Front. Microbiol. 2016;7:1083. doi: 10.3389/fmicb.2016.01083. PubMed DOI PMC

Kaschuk G., Hungria M., Leffelaar P.A., Giller K.E., Kuyper T.W. Differences in photosynthetic behaviour and leaf senescence of soybean (Glycine max [L.] Merrill) dependent on N2 fixation or nitrate supply. Plant Biol. 2010;12:60–69. doi: 10.1111/j.1438-8677.2009.00211.x. PubMed DOI

Paul M.J., Pellny T.K. Carbon metabolite feedback regulation of leaf photosynthesis and development. J. Exp. Bot. 2003;54:539–547. doi: 10.1093/jxb/erg052. PubMed DOI

Paul M.J., Foyer C.H. Sink regulation of photosynthesis. J. Exp. Bot. 2001;52:1383–1400. doi: 10.1093/jexbot/52.360.1383. PubMed DOI

Ramon M., Rolland F., Sheen J. Sugar Sensing and Signaling. Arab. Book. 2008;6:e0117. doi: 10.1199/tab.0117. PubMed DOI PMC

Jang J.C., Sheen J. Sugar Sensing in Higher Plants. Trends Plant Sci. 1997;15:773–785. doi: 10.1016/S1360-1385(97)89545-3. DOI

Hu X., Shi Y., Zhang P., Miao M., Zhang T., Jiang B. d-Mannose: Properties, Production, and Applications: An Overview. Compr. Rev. Food Sci. Food Saf. 2016;15:773–785. doi: 10.1111/1541-4337.12211. PubMed DOI

Engel J., Schmalhorst P., Routier F.H. Biosynthesis of the Fungal Cell Wall Polysaccharide Galactomannan Requires Intraluminal GDP-mannose. J. Biol. Chem. 2012;287:44418–44424. doi: 10.1074/jbc.M112.398321. PubMed DOI PMC

Kawaguchi H., Sasaki M., Vertès A.A., Inui M., Yukawa H. Identification and Functional Analysis of the Gene Cluster for l-Arabinose Utilization in Corynebacterium glutamicum. Appl. Environ. Microbiol. 2009;75:3419–3429. doi: 10.1128/AEM.02912-08. PubMed DOI PMC

Xiao H., Gu Y., Ning Y., Yang Y., Mitchell W.J., Jiang W., Yang S. Confirmation and Elimination of Xylose Metabolism Bottlenecks in Glucose Phosphoenolpyruvate-Dependent Phosphotransferase System-Deficient Clostridium acetobutylicum for Simultaneous Utilization of Glucose, Xylose, and Arabinose. Appl. Environ. Microbiol. 2011;77:7886–7895. doi: 10.1128/AEM.00644-11. PubMed DOI PMC

Saltman P. Hexokinase in Higher Plants. J. Biol. Chem. 1953;200:145–154. doi: 10.1016/S0021-9258(18)38447-3. PubMed DOI

Bessell E.M., Foster A.B., Westwood J.H. The use of deoxyfluoro-d-glucopyranoses and related compounds in a study of yeast hexokinase specificity. Biochem. J. 1972;128:199–204. doi: 10.1042/bj1280199. PubMed DOI PMC

Conesa A., Punt P.J., Van Luijk N., van den Hondel C.A.M.J.J. The Secretion Pathway in Filamentous Fungi: A Biotechnoloical View. Fungal Genet. Biol. 2001;33:155–171. doi: 10.1006/fgbi.2001.1276. PubMed DOI

Miura N., Ueda M. Evaluation of Unconventional Protein Secretion by Saccharomyces cerevisiae and other Fungi. Cells. 2018;7:128. doi: 10.3390/cells7090128. PubMed DOI PMC

Gil-Bona A., Llama-Palacios A., Parra C.M., Vivanco F., Nombela C., Monteoliva L., Gil C. Proteomics Unravels Extracellular Vesicles as Carriers of Classical Cytoplasmic Proteins in Candida albicans. J. Proteome Res. 2015;14:142–153. doi: 10.1021/pr5007944. PubMed DOI

Oliveira D.L., Nakayasu E.S., Joffe L.S., Guimarães A.J., Sobreira T.J.P., Nosanchuk J.D., Cordero R.J.B., Frases S., Casadevall A., Almeida I.C., et al. Characterization of Yeast Extracellular Vesicles: Evidence for the Participation of Different Pathways of Cellular Traffic in Vesicle Biogenesis. PLoS ONE. 2010;5:e11113. doi: 10.1371/journal.pone.0011113. PubMed DOI PMC

Vallejo M.C., Nakayasu E.S., Matsuo A.L., Sobreira T.J.P., Longo L.V.G., Ganiko L., Almeida I.C., Puccia R. Vesicle and Vesicle-Free Extracellular Proteome of Paracoccidioides brasiliensis: Comparative Analysis with Other Pathogenic Fungi. J. Proteome Res. 2012;11:1676–1685. doi: 10.1021/pr200872s. PubMed DOI PMC

Yang C.-K., Ewis H.E., Zhang X., Lu C.-D., Hu H.-J., Pan Y., Abdelal A.T., Tai P.C. Nonclassical Protein Secretion by Bacillus subtilis in the Stationary Phase Is Not Due to Cell Lysis. J. Bacteriol. 2011;193:5607–5615. doi: 10.1128/JB.05897-11. PubMed DOI PMC

Yang C.-K., Zhang X.-Z., Lu C.-D., Tai P.C. An internal hydrophobic helical domain of Bacillus subtilis enolase is essential but not sufficient as a non-cleavable signal for its secretion. Biochem. Biophys. Res. Commun. 2014;446:901–905. doi: 10.1016/j.bbrc.2014.03.032. PubMed DOI PMC

de Oliveira A.R., Oliveira L.N., Chaves E., Weber S.S., Bailão A.M., Parente-Rocha J.A., Baeza L.C., Soares C.M.D.A., Borges C.L. Characterization of extracellular proteins in members of the Paracoccidioides complex. Fungal Biol. 2018;122:738–751. doi: 10.1016/j.funbio.2018.04.001. PubMed DOI

Nizam S., Qiang X., Wawra S., Nostadt R., Getzke F., Schwanke F., Dreyer I., Langen G., Zuccaro A. Serendipita indica E5′ NT modulates extracellular nucleotide levels in the plant apoplast and affects fungal colonization. EMBO Rep. 2019;20:47430. doi: 10.15252/embr.201847430. PubMed DOI PMC

Thürich J., Meichsner D., Furch A.C.U., Pfalz J., Krüger T., Kniemeyer O., Brakhage A., Oelmüller R. Arabidopsis thaliana responds to colonisation of Piriformospora indica by secretion of symbiosis-specific proteins. PLoS ONE. 2018;13:e0209658. doi: 10.1371/journal.pone.0209658. PubMed DOI PMC

Jammer A., Gasperl A., Luschin-Ebengreuth N., Heyneke E., Chu H., Cantero-Navarro E., Großkinsky D.K., Albacete A.A., Stabentheiner E., Franzaring J., et al. Simple and robust determination of the activity signature of key carbohydrate metabolism enzymes for physiological phenotyping in model and crop plants. J. Exp. Bot. 2015;66:5531–5542. doi: 10.1093/jxb/erv228. PubMed DOI

Pontecorvo G., Roper J., Chemmons L., Macdonald K., Bufton A. The Genetics of Aspergillus nidulans. Adv. Genet. 1953;5:141–238. doi: 10.1016/s0065-2660(08)60408-3. PubMed DOI

Bonfig K.B., Gabler A., Simon U.K., Luschin-Ebengreuth N., Hatz M., Berger S., Muhammad N., Zeier J., Sinha A.K., Roitsch T. Post-Translational Derepression of Invertase Activity in Source Leaves via Down-Regulation of Invertase Inhibitor Expression Is Part of the Plant Defense Response. Mol. Plant. 2010;3:1037–1048. doi: 10.1093/mp/ssq053. PubMed DOI

Deshmukh S., Huckelhoven R., Schäfer P., Imani J., Sharma M., Weiss M., Waller F., Kogel K.-H. The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proc. Natl. Acad. Sci. USA. 2006;103:18450–18457. doi: 10.1073/pnas.0605697103. PubMed DOI PMC

Slewinski T.L. Diverse Functional Roles of Monosaccharide Transporters and Their Homologs in Vascular Plants: A Physiological Perspective. Mol. Plant. 2011;4:641–662. doi: 10.1093/mp/ssr051. PubMed DOI

Seifert G., Barber C., Wells B., Dolan L., Roberts K. Galactose Biosynthesis in Arabidopsis: Genetic Evidence for Substrate Channeling from UDP-D-Galactose into Cell Wall Polymers. Curr. Biol. 2002;12:1840–1845. doi: 10.1016/S0960-9822(02)01260-5. PubMed DOI

Friese C., Allen M. Tracking the fates of exotic and local VA mycorrhizal fungi: Methods and patterns. Agric. Ecosyst. Environ. 1991;34:87–96. doi: 10.1016/0167-8809(91)90096-G. DOI

Morton J.B., Koske R.E., Stürmer S.L., Bentivenga S.P. Biodiversity of Fungi: Inventory and Monitoring Methods. Elsevier; Amsterdam, The Netherlands: 2004. Mutualistic Arbuscular Endomycorrhizal Fungi; pp. 317–336.

Giardina B.J., Stanley B.A., Chiang H.-L. Glucose induces rapid changes in the secretome of Saccharomyces cerevisiae. Proteome Sci. 2014;12:9. doi: 10.1186/1477-5956-12-9. PubMed DOI PMC

Stein K., Chiang H.L. Exocytosis and Endocytosis of Small Vesicles across the Plasma Membrane in Saccharomyces Cerevisiae. Membranes. 2014;4:608–629. doi: 10.3390/membranes4030608. PubMed DOI PMC

Büttner M. The Arabidopsis sugar transporter (AtSTP) family: An update. Plant Biol. 2010;12:35–41. doi: 10.1111/j.1438-8677.2010.00383.x. PubMed DOI

Rottmann T.M., Klebl F., Schneider S., Kischka D., Rüscher D., Sauer N., Stadler R. Sugar Transporter STP7 Specificity for l-Arabinose and d-Xylose Contrasts with the Typical Hexose Transporters STP8 and STP12. Plant Physiol. 2018;176:2330–2350. doi: 10.1104/pp.17.01493. PubMed DOI PMC

O’Leary B., Neale H.C., Geilfus C.-M., Jackson R., Arnold D.L., Preston G.M. Early changes in apoplast composition associated with defence and disease in interactions Phaseolus Vulgaris and the Halo Blight Pathogen Pseudomonas Syringae Pv. Phaseolicola. Plant Cell Environ. 2016;39:2172–2184. doi: 10.1111/pce.12770. PubMed DOI PMC

Lee E.-J., Matsumura Y., Soga K., Hoson T., Koizumi N. Glycosyl Hydrolases of Cell Wall are Induced by Sugar Starvation in Arabidopsis. Plant Cell Physiol. 2007;48:405–413. doi: 10.1093/pcp/pcm009. PubMed DOI

Quirino B.F., Reiter W.-D., Amasino R.D. One of two tandem Arabidopsis genes homologous to monosaccharide transporters is senescence-associated. Plant Mol. Biol. 2001;46:447–457. doi: 10.1023/A:1010639015959. PubMed DOI

Schüßler A., Martin H., Cohen D., Fitz M., Wipf D. Arbuscular MycorrhizaMycorrhiza—Studies on the Geosiphon Symbiosis Lead to the Characterization of the First Glomeromycotan Sugar Trans-porter. Plant Signal. Behav. 2007;2:431–434. doi: 10.4161/psb.2.5.4465. PubMed DOI PMC

Helber N., Wippel K., Sauer N., Schaarschmidt S., Hause B., Requena N. A Versatile Monosaccharide Transporter That Operates in the Arbuscular Mycorrhizal Fungus Glomus sp Is Crucial for the Symbiotic Relationship with Plants. Plant Cell. 2011;23:3812–3823. doi: 10.1105/tpc.111.089813. PubMed DOI PMC

Martchenko M., Levitin A., Hogues H., Nantel A., Whiteway M. Transcriptional Rewiring of Fungal Galactose-Metabolism Circuitry. Curr. Biol. 2007;17:1007–1013. doi: 10.1016/j.cub.2007.05.017. PubMed DOI PMC

Bacon C.W., White J.F. Biotechnology of Endophytic Fungi of Grasses. CRC Press; Boca Raton, FL, USA: 2018.

Hadacek F. Plant root carbohydrates affect growth behaviour of endophytic microfungi. FEMS Microbiol. Ecol. 2002;41:161–170. doi: 10.1111/j.1574-6941.2002.tb00977.x. PubMed DOI

Boldt K., Pörs Y., Haupt B., Bitterlich M., Kühn C., Grimm B., Franken P. Photochemical processes, carbon assimilation and RNA accumulation of sucrose transporter genes in tomato arbuscular mycorrhiza. J. Plant Physiol. 2011;168:1256–1263. doi: 10.1016/j.jplph.2011.01.026. PubMed DOI

Bitterlich M., Krügel U., Boldt-Burisch K., Franken P., Kühn C. The sucrose transporter Sl SUT 2 from tomato interacts with brassinosteroid functioning and affects arbuscular mycorrhiza formation. Plant J. 2014;78:877–889. doi: 10.1111/tpj.12515. PubMed DOI

Seiboth B., Pakdaman B.S., Hartl L., Kubicek C.P. Lactose Metabolism in Filamentous Fungi: How to Deal with an Unknown Substrate. Fungal Biol. Rev. 2007;21:42–48. doi: 10.1016/j.fbr.2007.02.006. DOI

Kennedy J.F., Quinton L. Essentials of Carbohydrate Chemistry and Biochemistry. Carbohydr. Polym. 2002;47:87. doi: 10.1016/S0144-8617(01)00274-0. DOI

de Queiroz C.B., Santana M.F. Prediction of the secretomes of endophytic and nonendophytic fungi reveals similarities in host plant infection and colonization strategies. Mycologia. 2020;112:491–503. doi: 10.1080/00275514.2020.1716566. PubMed DOI

Ehlert C., Plassard C., Cookson S.J., Tardieu F., Simonneau T. Do pH changes in the leaf apoplast contribute to rapid inhibition of leaf elongation rate by water stress? Comparison of stress responses induced by polyethylene glycol and down-regulation of root hydraulic conductivity. Plant Cell Environ. 2011;34:1258–1266. doi: 10.1111/j.1365-3040.2011.02326.x. PubMed DOI

Grignon C., Sentenac H. PH and Ionic Conditions in the Apoplast. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1991;98:451–463. doi: 10.1146/annurev.pp.42.060191.000535. DOI

Williams A.M., MacLean D.J., Scott K.J. Cellular Location and Properties of Invertase in Mycelium of Puccinia Graminis. New Phytol. 1984;98:451–463. doi: 10.1111/j.1469-8137.1984.tb04138.x. DOI

Nelson J.M., Anderson R.S. Glucose and Fructose Retardation of Invertase Action. J. Biol. Chem. 1926;69:443–448. doi: 10.1016/S0021-9258(18)84561-6. DOI

Dynesen J., Smits H.P., Olsson L., Nielsen J. Carbon catabolite repression of invertase during batch cultivations of Saccharomyces cerevisiae: The role of glucose, fructose, and mannose. Appl. Microbiol. Biotechnol. 1998;50:579–582. doi: 10.1007/s002530051338. PubMed DOI

Zhang D. Post-translational inhibitory regulation of acid invertase induced by fructose and glucose in developing apple fruit. Sci. China Ser. C Life Sci. 2002;45:309–321. doi: 10.1360/02yc9034. PubMed DOI

Longo L.V.G., Da Cunha J.P.C., Sobreira T.J.P., Puccia R. Proteome of cell wall-extracts from pathogenic Paracoccidioides brasiliensis: Comparison among morphological phases, isolates, and reported fungal extracellular vesicle proteins. EuPA Open Proteom. 2014;3:216–228. doi: 10.1016/j.euprot.2014.03.003. DOI

Weisser P., Krämer R., A Sprenger G. Expression of the Escherichia coli pmi gene, encoding phosphomannose-isomerase in Zymomonas mobilis, leads to utilization of mannose as a novel growth substrate, which can be used as a selective marker. Appl. Environ. Microbiol. 1996;62:4155–4161. doi: 10.1128/aem.62.11.4155-4161.1996. PubMed DOI PMC

Schnarrenberger C. Characterization and compartmentation, in green leaves, of hexokinases with different specificities for glucose, fructose, and mannose and for nucleoside triphosphates. Planta. 1990;181:249–255. doi: 10.1007/BF02411547. PubMed DOI

Domsch W.K., Gams T.A. Compendium of Soil Fungi. Institute of Soil Biology. Fed. Agric. Res. Cent. 1993 doi: 10.1111/j.1365-2389.2008.01052_1.x. DOI

Adomako D., Kaye A.G., Lewis D.H. Carbohydrate Metabolism in Chaetomium Globosum. II. Some Properties of Kinases and Isomerases Initiating the Utilization of Sugars. New Phytol. 1971;70:699–712. doi: 10.1111/j.1469-8137.1971.tb02571.x. DOI

Kaffarnik F.A.R., Jones A., Rathjen J., Peck S.C. Effector Proteins of the Bacterial Pathogen Pseudomonas syringae Alter the Extracellular Proteome of the Host Plant, Arabidopsis thaliana. Mol. Cell. Proteom. 2009;8:145–156. doi: 10.1074/mcp.M800043-MCP200. PubMed DOI

Floerl S., Majcherczyk A., Possienke M., Feussner K., Tappe H., Gatz C., Feussner I., Kües U., Polle A. Verticillium longisporum Infection Affects the Leaf Apoplastic Proteome, Metabolome, and Cell Wall Properties in Arabidopsis thaliana. PLoS ONE. 2012;7:e31435. doi: 10.1371/journal.pone.0031435. PubMed DOI PMC

Cheng F.-Y., Blackburn K., Lin Y.-M., Goshe M.B., Williamson J.D. Absolute Protein Quantification by LC/MSE for Global Analysis of Salicylic Acid-Induced Plant Protein Secretion Responses. J. Proteome Res. 2009;8:82–93. doi: 10.1021/pr800649s. PubMed DOI

Gould S.J., Keller G.-A., Schneider M., Howell S.H., Garrard L.J., Goodman J.M., Distel B., Tabak H. Subramani Peroxisomal Protein Import Is Conserved between Yeast, Plants, Insects and Mammals. Trends Genet. 1990;6:73. doi: 10.1016/0168-9525(90)90086-l. PubMed DOI PMC

Gould S.J., Keller G.A., Subramani S. Identification of peroxisomal targeting signals located at the carboxy terminus of four peroxisomal proteins. J. Cell Biol. 1988;107:897–905. doi: 10.1083/jcb.107.3.897. PubMed DOI PMC

Gould S.J., Keller G.-A., Hosken N., Wilkinson J., Subramani S. A conserved tripeptide sorts proteins to peroxisomes. J. Cell Biol. 1989;108:1657–1664. doi: 10.1083/jcb.108.5.1657. PubMed DOI PMC

McCommis K.S., Finck B.N. Mitochondrial pyruvate transport: A historical perspective and future research directions. Biochem. J. 2015;466:443–454. doi: 10.1042/BJ20141171. PubMed DOI PMC

Kwon Y., Oh J.E., Noh H., Hong S.-W., Bhoo S.H., Lee H. The ethylene signaling pathway has a negative impact on sucrose-induced anthocyanin accumulation in Arabidopsis. J. Plant Res. 2010;124:193–200. doi: 10.1007/s10265-010-0354-1. PubMed DOI

Chivasa S., Murphy A.M., Hamilton J.M., Lindsey K., Carr J.P., Slabas A.R. Extracellular ATP is a regulator of pathogen defence in plants. Plant J. 2009;60:436–448. doi: 10.1111/j.1365-313X.2009.03968.x. PubMed DOI

Kwon H.-K., Yokoyama R., Nishitani K. A Proteomic Approach to Apoplastic Proteins Involved in Cell Wall Regeneration in Protoplasts of Arabidopsis Suspension-cultured Cells. Plant Cell Physiol. 2005;46:843–857. doi: 10.1093/pcp/pci089. PubMed DOI

Kehr J., Kragler F. Long distance RNA movement. New Phytol. 2018;218:29–40. doi: 10.1111/nph.15025. PubMed DOI