Phospholipase Dα1 (PLDα1) belongs to phospholipases, a large phospholipid hydrolyzing protein family. PLDα1 has a substrate preference for phosphatidylcholine leading to enzymatic production of phosphatidic acid, a lipid second messenger with multiple cellular functions. PLDα1 itself is implicated in biotic and abiotic stress responses. Here, we present a shot-gun differential proteomic analysis on roots of two Arabidopsis pldα1 mutants compared to the wild type. Interestingly, PLDα1 deficiency leads to altered abundances of proteins involved in diverse processes related to membrane transport including endocytosis and endoplasmic reticulum-Golgi transport. PLDα1 may be involved in the stability of attachment sites of endoplasmic reticulum to the plasma membrane as suggested by increased abundance of synaptotagmin 1, which was validated by immunoblotting and whole-mount immunolabelling analyses. Moreover, we noticed a robust abundance alterations of proteins involved in mitochondrial import and electron transport chain. Notably, the abundances of numerous proteins implicated in glucosinolate biosynthesis were also affected in pldα1 mutants. Our results suggest a broader biological involvement of PLDα1 than anticipated thus far, especially in the processes such as endomembrane transport, mitochondrial protein import and protein quality control, as well as glucosinolate biosynthesis.

Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University Šlechtitelů 2778371 Olomouc Czech Republic

Institute for Genomics Biocomputing and Biotechnology Mississippi Agricultural and Forestry Experiment Station Mississippi State University Starkville MS 39759 USA

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Wang X., editor. Phospholipases in Plant Signaling. Volume 20. Springer; Berlin/Heidelberg, Germany: 2014. (Signaling and Communication in Plants).

Hong Y., Zhao J., Guo L., Kim S.-C., Deng X., Wang G., Zhang G., Li M., Wang X. Plant phospholipases D and C and their diverse functions in stress responses. Prog. Lipid Res. 2016;62:55–74. doi: 10.1016/j.plipres.2016.01.002. PubMed DOI

Zhang Q., Lin F., Mao T., Nie J., Yan M., Yuan M., Zhang W. Phosphatidic acid regulates microtubule organization by interacting with MAP65-1 in response to salt stress in Arabidopsis. Plant Cell. 2012;24:4555–4576. doi: 10.1105/tpc.112.104182. PubMed DOI PMC

Testerink C., Munnik T. Molecular, cellular, and physiological responses to phosphatidic acid formation in plants. J. Exp. Bot. 2011;62:2349–2361. doi: 10.1093/jxb/err079. PubMed DOI

Zhang W., Qin C., Zhao J., Wang X. Phospholipase D alpha 1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling. Proc. Natl. Acad. Sci. USA. 2004;101:9508–9513. doi: 10.1073/pnas.0402112101. PubMed DOI PMC

Devaiah S.P., Roth M.R., Baughman E., Li M., Tamura P., Jeannotte R., Welti R., Wang X. Quantitative profiling of polar glycerolipid species from organs of wild-type Arabidopsis and a PHOSPHOLIPASE Dα1 knockout mutant. Phytochemistry. 2006;67:1907–1924. doi: 10.1016/j.phytochem.2006.06.005. PubMed DOI

Gao H.-B., Chu Y.-J., Xue H.-W. Phosphatidic Acid (PA) Binds PP2AA1 to Regulate PP2A Activity and PIN1 Polar Localization. Mol. Plant. 2013;6:1692–1702. doi: 10.1093/mp/sst076. PubMed DOI

Boutté Y., Moreau P. Modulation of endomembranes morphodynamics in the secretory/retrograde pathways depends on lipid diversity. Curr. Opin. Plant Biol. 2014;22:22–29. doi: 10.1016/j.pbi.2014.08.004. PubMed DOI

Dhonukshe P., Laxalt A.M., Goedhart J., Gadella T.W.J., Munnik T. Phospholipase d activation correlates with microtubule reorganization in living plant cells. Plant Cell. 2003;15:2666–2679. doi: 10.1105/tpc.014977. PubMed DOI PMC

Pleskot R., Potocký M., Pejchar P., Linek J., Bezvoda R., Martinec J., Valentová O., Novotná Z., Zárský V. Mutual regulation of plant phospholipase D and the actin cytoskeleton. Plant J. 2010;62:494–507. doi: 10.1111/j.1365-313X.2010.04168.x. PubMed DOI

Pleskot R., Li J., Žárský V., Potocký M., Staiger C.J. Regulation of cytoskeletal dynamics by phospholipase D and phosphatidic acid. Trends Plant Sci. 2013;18:496–504. doi: 10.1016/j.tplants.2013.04.005. PubMed DOI

Novák D., Vadovič P., Ovečka M., Šamajová O., Komis G., Colcombet J., Šamaj J. Gene expression pattern and protein localization of Arabidopsis Phospholipase D Alpha 1 revealed by advanced light-sheet and super-resolution microscopy. Front. Plant Sci. 2018;9:371. doi: 10.3389/fpls.2018.00371. PubMed DOI PMC

Mishra G., Zhang W., Deng F., Zhao J., Wang X. A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis. Science. 2006;312:264–266. doi: 10.1126/science.1123769. PubMed DOI

Zhang Y., Zhu H., Zhang Q., Li M., Yan M., Wang R., Wang L., Welti R., Zhang W., Wang X. Phospholipase Dα1 and Phosphatidic Acid Regulate NADPH Oxidase Activity and Production of Reactive Oxygen Species in ABA-Mediated Stomatal Closure in Arabidopsis. Plant Cell. 2009;21:2357–2377. doi: 10.1105/tpc.108.062992. PubMed DOI PMC

Guo L., Mishra G., Markham J.E., Li M., Tawfall A., Welti R., Wang X. Connections between sphingosine kinase and phospholipase D in the abscisic acid signaling pathway in Arabidopsis. J. Biol. Chem. 2012;287:8286–8296. doi: 10.1074/jbc.M111.274274. PubMed DOI PMC

Roy Choudhury S., Pandey S. The role of PLDα1 in providing specificity to signal-response coupling by heterotrimeric G-protein components in Arabidopsis. Plant J. 2016;86:50–61. doi: 10.1111/tpj.13151. PubMed DOI

Roy Choudhury S., Pandey S. Phosphatidic acid binding inhibits RGS1 activity to affect specific signaling pathways in Arabidopsis. Plant J. 2017;90:466–477. doi: 10.1111/tpj.13503. PubMed DOI

Hong Y., Zheng S., Wang X. Dual functions of phospholipase Dalpha1 in plant response to drought. Mol. Plant. 2008;1:262–269. doi: 10.1093/mp/ssm025. PubMed DOI

Huo C., Zhang B., Wang H., Wang F., Liu M., Gao Y., Zhang W., Deng Z., Sun D., Tang W. Comparative Study of Early Cold-Regulated Proteins by Two-Dimensional Difference Gel Electrophoresis Reveals a Key Role for Phospholipase Dα1 in Mediating Cold Acclimation Signaling Pathway in Rice. Mol. Cell. Proteom. 2016;15:1397–1411. doi: 10.1074/mcp.M115.049759. PubMed DOI PMC

Lu S., Bahn S.C., Qu G., Qin H., Hong Y., Xu Q., Zhou Y., Hong Y., Wang X. Increased expression of phospholipase Dα1 in guard cells decreases water loss with improved seed production under drought in Brassica napus. Plant Biotechnol. J. 2013;11:380–389. doi: 10.1111/pbi.12028. PubMed DOI

Uraji M., Katagiri T., Okuma E., Ye W., Hossain M.A., Masuda C., Miura A., Nakamura Y., Mori I.C., Shinozaki K., et al. Cooperative function of PLDδ and PLDα1 in abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol. 2012;159:450–460. doi: 10.1104/pp.112.195578. PubMed DOI PMC

Devaiah S.P., Pan X., Hong Y., Roth M., Welti R., Wang X. Enhancing seed quality and viability by suppressing phospholipase D in Arabidopsis: Phospholipase D in seed aging. Plant J. 2007;50:950–957. doi: 10.1111/j.1365-313X.2007.03103.x. PubMed DOI

Ufer G., Gertzmann A., Gasulla F., Röhrig H., Bartels D. Identification and characterization of the phosphatidic acid-binding A. thaliana phosphoprotein PLDrp1 that is regulated by PLDα1 in a stress-dependent manner. Plant J. 2017;92:276–290. doi: 10.1111/tpj.13651. PubMed DOI

Gajiwala K.S., Burley S.K. Winged helix proteins. Curr. Opin. Struct. Biol. 2000;10:110–116. doi: 10.1016/S0959-440X(99)00057-3. PubMed DOI

Rodriguez L., Gonzalez-Guzman M., Diaz M., Rodrigues A., Izquierdo-Garcia A.C., Peirats-Llobet M., Fernandez M.A., Antoni R., Fernandez D., Marquez J.A., et al. C2-domain abscisic acid-related proteins mediate the interaction of PYR/PYL/RCAR abscisic acid receptors with the plasma membrane and regulate abscisic acid sensitivity in Arabidopsis. Plant Cell. 2014;26:4802–4820. doi: 10.1105/tpc.114.129973. PubMed DOI PMC

Zhang Q., Berkey R., Blakeslee J.J., Lin J., Ma X., King H., Liddle A., Guo L., Munnik T., Wang X., et al. Arabidopsis phospholipase Dα1 and Dδ oppositely modulate EDS1- and SA-independent basal resistance against adapted powdery mildew. J. Exp. Bot. 2018;69:3675–3688. doi: 10.1093/jxb/ery146. PubMed DOI PMC

Pleskot R., Pejchar P., Staiger C.J., Potocký M. When fat is not bad: The regulation of actin dynamics by phospholipid signaling molecules. Front. Plant Sci. 2014;5:5. doi: 10.3389/fpls.2014.00005. PubMed DOI PMC

Steinborn K. The Arabidopsis PILZ group genes encode tubulin-folding cofactor orthologs required for cell division but not cell growth. Genes Dev. 2002;16:959–971. doi: 10.1101/gad.221702. PubMed DOI PMC

Du Y., Cui M., Qian D., Zhu L., Wei C., Yuan M., Zhang Z., Li Y. AtTFC B is involved in control of cell division. Front. Biosci. Elite Ed. 2010;2:752–763. PubMed

Dhonukshe P., Bargmann B.O.R., Gadella T.W.J. Arabidopsis Tubulin Folding Cofactor B Interacts with α-Tubulin In Vivo. Plant Cell Physiol. 2006;47:1406–1411. doi: 10.1093/pcp/pcl001. PubMed DOI

Gu Y., Deng Z., Paredez A.R., DeBolt S., Wang Z.-Y., Somerville C. Prefoldin 6 is required for normal microtubule dynamics and organization in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2008;105:18064–18069. doi: 10.1073/pnas.0808652105. PubMed DOI PMC

Nishimura N., Sarkeshik A., Nito K., Park S.-Y., Wang A., Carvalho P.C., Lee S., Caddell D.F., Cutler S.R., Chory J., et al. PYR/PYL/RCAR family members are major in-vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J. Cell Mol. Biol. 2010;61:290–299. doi: 10.1111/j.1365-313X.2009.04054.x. PubMed DOI PMC

Postaire O., Tournaire-Roux C., Grondin A., Boursiac Y., Morillon R., Schäffner A.R., Maurel C. A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis. Plant Physiol. 2010;152:1418–1430. doi: 10.1104/pp.109.145326. PubMed DOI PMC

McLoughlin F., Arisz S.A., Dekker H.L., Kramer G., de Koster C.G., Haring M.A., Munnik T., Testerink C. Identification of novel candidate phosphatidic acid-binding proteins involved in the salt-stress response of Arabidopsis thaliana roots. Biochem. J. 2013;450:573–581. doi: 10.1042/BJ20121639. PubMed DOI

Bellati J., Champeyroux C., Hem S., Rofidal V., Krouk G., Maurel C., Santoni V. Novel Aquaporin Regulatory Mechanisms Revealed by Interactomics. Mol. Cell. Proteom. 2016;15:3473–3487. doi: 10.1074/mcp.M116.060087. PubMed DOI PMC

Wang Y., Carrie C., Giraud E., Elhafez D., Narsai R., Duncan O., Whelan J., Murcha M.W. Dual location of the mitochondrial preprotein transporters B14.7 and Tim23-2 in complex I and the TIM17:23 complex in Arabidopsis links mitochondrial activity and biogenesis. Plant Cell. 2012;24:2675–2695. doi: 10.1105/tpc.112.098731. PubMed DOI PMC

Neupert W. A Perspective on Transport of Proteins into Mitochondria: A Myriad of Open Questions. J. Mol. Biol. 2015;427:1135–1158. doi: 10.1016/j.jmb.2015.02.001. PubMed DOI

Teixeira P.F., Glaser E. Processing peptidases in mitochondria and chloroplasts. Biochim. Biophys. Acta Mol. Cell Res. 2013;1833:360–370. doi: 10.1016/j.bbamcr.2012.03.012. PubMed DOI

Van Aken O., Whelan J., Van Breusegem F. Prohibitins: Mitochondrial partners in development and stress response. Trends Plant Sci. 2010;15:275–282. doi: 10.1016/j.tplants.2010.02.002. PubMed DOI

Piechota J., Bereza M., Sokołowska A., Suszyński K., Lech K., Jańska H. Unraveling the functions of type II-prohibitins in Arabidopsis mitochondria. Plant Mol. Biol. 2015;88:249–267. doi: 10.1007/s11103-015-0320-3. PubMed DOI

Ahn C.S., Lee J.H., Reum Hwang A., Kim W.T., Pai H.-S. Prohibitin is involved in mitochondrial biogenesis in plants. Plant J. 2006;46:658–667. doi: 10.1111/j.1365-313X.2006.02726.x. PubMed DOI

Donaldson J.G. Phospholipase D in endocytosis and endosomal recycling pathways. Biochim. Biophys. Acta. 2009;1791:845–849. doi: 10.1016/j.bbalip.2009.05.011. PubMed DOI PMC

Antonescu C.N., Danuser G., Schmid S.L. Phosphatidic Acid Plays a Regulatory Role in Clathrin-mediated Endocytosis. Mol. Biol. Cell. 2010;21:2944–2952. doi: 10.1091/mbc.e10-05-0421. PubMed DOI PMC

Li G., Xue H.-W. Arabidopsis PLD 2 Regulates Vesicle Trafficking and Is Required for Auxin Response. Plant Cell. 2007;19:281–295. doi: 10.1105/tpc.106.041426. PubMed DOI PMC

Roth M.G. Molecular mechanisms of PLD function in membrane traffic. Traffic. 2008;9:1233–1239. doi: 10.1111/j.1600-0854.2008.00742.x. PubMed DOI

Thakur R., Panda A., Coessens E., Raj N., Yadav S., Balakrishnan S., Zhang Q., Georgiev P., Basak B., Pasricha R., et al. Phospholipase D activity couples plasma membrane endocytosis with retromer dependent recycling. eLife. 2016;5:e18515. doi: 10.7554/eLife.18515. PubMed DOI PMC

Schumacher K., Krebs M. The V-ATPase: Small cargo, large effects. Curr. Opin. Plant Biol. 2010;13:724–730. doi: 10.1016/j.pbi.2010.07.003. PubMed DOI

Fujiwara M., Uemura T., Ebine K., Nishimori Y., Ueda T., Nakano A., Sato M.H., Fukao Y. Interactomics of Qa-SNARE in Arabidopsis thaliana. Plant Cell Physiol. 2014;55:781–789. doi: 10.1093/pcp/pcu038. PubMed DOI

Mayer A., Wickner W., Haas A. Sec18p (NSF)-Driven Release of Sec17p (α-SNAP) Can Precede Docking and Fusion of Yeast Vacuoles. Cell. 1996;85:83–94. doi: 10.1016/S0092-8674(00)81084-3. PubMed DOI

Wang T., Li L., Hong W. SNARE proteins in membrane trafficking. Traffic. 2017;18:767–775. doi: 10.1111/tra.12524. PubMed DOI

Uemura T., Ueda T., Ohniwa R.L., Nakano A., Takeyasu K., Sato M.H. Systematic analysis of SNARE molecules in Arabidopsis: Dissection of the post-Golgi network in plant cells. Cell Struct. Funct. 2004;29:49–65. doi: 10.1247/csf.29.49. PubMed DOI

Wang C., Yan X., Chen Q., Jiang N., Fu W., Ma B., Liu J., Li C., Bednarek S.Y., Pan J. Clathrin Light Chains Regulate Clathrin-Mediated Trafficking, Auxin Signaling, and Development in Arabidopsis. Plant Cell. 2013;25:499–516. doi: 10.1105/tpc.112.108373. PubMed DOI PMC

Fan L., Li R., Pan J., Ding Z., Lin J. Endocytosis and its regulation in plants. Trends Plant Sci. 2015;20:388–397. doi: 10.1016/j.tplants.2015.03.014. PubMed DOI

Yamaoka S., Shimono Y., Shirakawa M., Fukao Y., Kawase T., Hatsugai N., Tamura K., Shimada T., Hara-Nishimura I. Identification and dynamics of Arabidopsis adaptor protein-2 complex and its involvement in floral organ development. Plant Cell. 2013;25:2958–2969. doi: 10.1105/tpc.113.114082. PubMed DOI PMC

Zelazny E., Santambrogio M., Pourcher M., Chambrier P., Berne-Dedieu A., Fobis-Loisy I., Miège C., Jaillais Y., Gaude T. Mechanisms Governing the Endosomal Membrane Recruitment of the Core Retromer in Arabidopsis. J. Biol. Chem. 2013;288:8815–8825. doi: 10.1074/jbc.M112.440503. PubMed DOI PMC

Kang H., Kim S.Y., Song K., Sohn E.J., Lee Y., Lee D.W., Hara-Nishimura I., Hwang I. Trafficking of Vacuolar Proteins: The Crucial Role of Arabidopsis Vacuolar Protein Sorting 29 in Recycling Vacuolar Sorting Receptor. Plant Cell. 2012;24:5058–5073. doi: 10.1105/tpc.112.103481. PubMed DOI PMC

Nodzyński T., Feraru M.I., Hirsch S., De Rycke R., Niculaes C., Boerjan W., Van Leene J., De Jaeger G., Vanneste S., Friml J. Retromer Subunits VPS35A and VPS29 Mediate Prevacuolar Compartment (PVC) Function in Arabidopsis. Mol. Plant. 2013;6:1849–1862. doi: 10.1093/mp/sst044. PubMed DOI

Hino T., Tanaka Y., Kawamukai M., Nishimura K., Mano S., Nakagawa T. Two Sec13p Homologs, AtSec13A and AtSec13B, Redundantly Contribute to the Formation of COPII Transport Vesicles in Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 2011;75:1848–1852. doi: 10.1271/bbb.110331. PubMed DOI

Fridmann-Sirkis Y., Siniossoglou S., Pelham H.R.B. TMF is a golgin that binds Rab6 and influences Golgi morphology. BMC Cell Biol. 2004;5:18. doi: 10.1186/1471-2121-5-18. PubMed DOI PMC

Latijnhouwers M., Gillespie T., Boevink P., Kriechbaumer V., Hawes C., Carvalho C.M. Localization and domain characterization of Arabidopsis golgin candidates. J. Exp. Bot. 2007;58:4373–4386. doi: 10.1093/jxb/erm304. PubMed DOI

Wang P., Richardson C., Hawkins T.J., Sparkes I., Hawes C., Hussey P.J. Plant VAP27 proteins: Domain characterization, intracellular localization and role in plant development. New Phytol. 2016;210:1311–1326. doi: 10.1111/nph.13857. PubMed DOI

Saravanan R.S., Slabaugh E., Singh V.R., Lapidus L.J., Haas T., Brandizzi F. The targeting of the oxysterol-binding protein ORP3a to the endoplasmic reticulum relies on the plant VAP33 homolog PVA12. Plant J. Cell Mol. Biol. 2009;58:817–830. doi: 10.1111/j.1365-313X.2009.03815.x. PubMed DOI

Siao W., Wang P., Voigt B., Hussey P.J., Baluska F. Arabidopsis SYT1 maintains stability of cortical endoplasmic reticulum networks and VAP27-1-enriched endoplasmic reticulum–plasma membrane contact sites. J. Exp. Bot. 2016;67:6161–6171. doi: 10.1093/jxb/erw381. PubMed DOI PMC

Takáč T., Pechan T., Richter H., Müller J., Eck C., Böhm N., Obert B., Ren H., Niehaus K., Šamaj J. Proteomics on brefeldin A-treated Arabidopsis roots reveals profilin 2 as a new protein involved in the cross-talk between vesicular trafficking and the actin cytoskeleton. J. Proteome Res. 2011;10:488–501. doi: 10.1021/pr100690f. PubMed DOI

Takáč T., Pechan T., Šamajová O., Ovečka M., Richter H., Eck C., Niehaus K., Šamaj J. Wortmannin treatment induces changes in Arabidopsis root proteome and post-Golgi compartments. J. Proteome Res. 2012;11:3127–3142. doi: 10.1021/pr201111n. PubMed DOI

Janda M., Šašek V., Chmelařová H., Andrejch J., Nováková M., Hajšlová J., Burketová L., Valentová O. Phospholipase D affects translocation of NPR1 to the nucleus in Arabidopsis thaliana. Front. Plant Sci. 2015;6:59. doi: 10.3389/fpls.2015.00059. PubMed DOI PMC

Kravets V.S., Kretinin S.V., Kolesnikov Y.S., Getman I.A., Romanov G.A. Cytokinins evoke rapid activation of phospholipase D in sensitive plant tissues. Dokl. Biochem. Biophys. 2009;428:264–267. doi: 10.1134/S1607672909050111. PubMed DOI

Fan L., Zheng S., Wang X. Antisense suppression of phospholipase D alpha retards abscisic acid- and ethylene-promoted senescence of postharvest Arabidopsis leaves. Plant Cell. 1997;9:2183. doi: 10.1105/tpc.9.12.2183. PubMed DOI PMC

Testerink C., Larsen P.B., van der Does D., van Himbergen J.A.J., Munnik T. Phosphatidic acid binds to and inhibits the activity of Arabidopsis CTR1. J. Exp. Bot. 2007;58:3905–3914. doi: 10.1093/jxb/erm243. PubMed DOI

Malka S.K., Cheng Y. Possible Interactions between the Biosynthetic Pathways of Indole Glucosinolate and Auxin. Front. Plant Sci. 2017;8:2131. doi: 10.3389/fpls.2017.02131. PubMed DOI PMC

Sønderby I.E., Geu-Flores F., Halkier B.A. Biosynthesis of glucosinolates--gene discovery and beyond. Trends Plant Sci. 2010;15:283–290. doi: 10.1016/j.tplants.2010.02.005. PubMed DOI

Skirycz A., Reichelt M., Burow M., Birkemeyer C., Rolcik J., Kopka J., Zanor M.I., Gershenzon J., Strnad M., Szopa J., et al. DOF transcription factor AtDof1.1 (OBP2) is part of a regulatory network controlling glucosinolate biosynthesis in Arabidopsis. Plant J. Cell Mol. Biol. 2006;47:10–24. doi: 10.1111/j.1365-313X.2006.02767.x. PubMed DOI

Petersen A., Wang C., Crocoll C., Halkier B.A. Biotechnological approaches in glucosinolate production. J. Integr. Plant Biol. 2018;60:1231–1248. doi: 10.1111/jipb.12705. PubMed DOI PMC

Takáč T., Šamajová O., Pechan T., Luptovčiak I., Šamaj J. Feedback microtubule control and microtubule-actin cross-talk in arabidopsis revealed by integrative proteomic and cell biology analysis of KATANIN 1 mutants. Mol. Cell. Proteom. 2017;16:1591–1609. doi: 10.1074/mcp.M117.068015. PubMed DOI PMC

Takáč T., Vadovič P., Pechan T., Luptovčiak I., Šamajová O., Šamaj J. Comparative proteomic study of Arabidopsis mutants mpk4 and mpk6. Sci. Rep. 2016;6:28306. doi: 10.1038/srep28306. PubMed DOI PMC

Conesa A., Götz S. Blast2GO: A comprehensive suite for functional analysis in plant genomics. Int. J. Plant Genom. 2008;2008:619832. doi: 10.1155/2008/619832. PubMed DOI PMC

Fukasawa Y., Tsuji J., Fu S.-C., Tomii K., Horton P., Imai K. MitoFates: Improved prediction of mitochondrial targeting sequences and their cleavage sites. Mol. Cell. Proteom. 2015;14:1113–1126. doi: 10.1074/mcp.M114.043083. PubMed DOI PMC

Šamajová O., Komis G., Šamaj J. Immunofluorescent Localization of MAPKs and Colocalization with Microtubules in Arabidopsis Seedling Whole-Mount Probes. In: Komis G., Šamaj J., editors. Plant MAP Kinases: Methods and Protocols. Springer; New York, NY, USA: 2014. pp. 107–115. PubMed

Phosphatidic Acid in Plant Hormonal Signaling: From Target Proteins to Membrane Conformations

Recent Advances in the Cellular and Developmental Biology of Phospholipases in Plants