Comparative proteomic study of Arabidopsis mutants mpk4 and mpk6

. 2016 Jun 21 ; 6 () : 28306. [epub] 20160621

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu srovnávací studie, časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid27324189

Grantová podpora
P20 GM103476 NIGMS NIH HHS - United States

Arabidopsis MPK4 and MPK6 are implicated in different signalling pathways responding to diverse external stimuli. This was recently correlated with transcriptomic profiles of Arabidopsis mpk4 and mpk6 mutants, and thus it should be reflected also on the level of constitutive proteomes. Therefore, we performed a shot gun comparative proteomic analysis of Arabidopsis mpk4 and mpk6 mutant roots. We have used bioinformatic tools and propose several new proteins as putative MPK4 and MPK6 phosphorylation targets. Among these proteins in the mpk6 mutant were important modulators of development such as CDC48A and phospholipase D alpha 1. In the case of the mpk4 mutant transcriptional reprogramming might be mediated by phosphorylation and change in the abundance of mRNA decapping complex VCS. Further comparison of mpk4 and mpk6 root differential proteomes showed differences in the composition and regulation of defense related proteins. The mpk4 mutant showed altered abundances of antioxidant proteins. The examination of catalase activity in response to oxidative stress revealed that this enzyme might be preferentially regulated by MPK4. Finally, we proposed developmentally important proteins as either directly or indirectly regulated by MPK4 and MPK6. These proteins contribute to known phenotypic defects in the mpk4 and mpk6 mutants.

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Smékalová V., Doskočilová A., Komis G. & Šamaj J. Crosstalk between secondary messengers, hormones and MAPK modules during abiotic stress signalling in plants. Biotechnol. Adv. 32, 2–11 (2014). PubMed

Colcombet J. & Hirt H. Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem. J. 413, 217–226 (2008). PubMed

Teige M. et al. The MKK2 Pathway Mediates Cold and Salt Stress Signaling in Arabidopsis. Mol. Cell 15, 141–152 (2004). PubMed

Gao M. et al. MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res. 18, 1190–1198 (2008). PubMed

Asai T. et al. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977–983 (2002). PubMed

Liu Y. & Zhang S. Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16, 3386–3399 (2004). PubMed PMC

Takahashi F. et al. The Mitogen-Activated Protein Kinase Cascade MKK3–MPK6 Is an Important Part of the Jasmonate Signal Transduction Pathway in Arabidopsis. Plant Cell 19, 805–818 (2007). PubMed PMC

Kovtun Y., Chiu W. L., Tena G. & Sheen J. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl. Acad. Sci. USA 97, 2940–2945 (2000). PubMed PMC

Pitzschke A., Djamei A., Bitton F. & Hirt H. A major role of the MEKK1-MKK1/2-MPK4 pathway in ROS signalling. Mol. Plant 2, 120–137 (2009). PubMed PMC

Bush S. M. & Krysan P. J. Mutational evidence that the Arabidopsis MAP kinase MPK6 is involved in anther, inflorescence, and embryo development. J. Exp. Bot. 58, 2181–2191 (2007). PubMed

Bergmann D. C., Lukowitz W. & Somerville C. R. Stomatal Development and Pattern Controlled by a MAPKK Kinase. Science 304, 1494–1497 (2004). PubMed

Müller J. et al. Arabidopsis MPK6 is involved in cell division plane control during early root development, and localizes to the pre-prophase band, phragmoplast, trans-Golgi network and plasma membrane. Plant J. Cell Mol. Biol. 61, 234–248 (2010). PubMed

Beck M., Komis G., Muller J., Menzel D. & Šamaj J. Arabidopsis Homologs of Nucleus- and Phragmoplast-Localized Kinase 2 and 3 and Mitogen-Activated Protein Kinase 4 Are Essential for Microtubule Organization. Plant Cell 22, 755–771 (2010). PubMed PMC

Beck M., Komis G., Ziemann A., Menzel D. & Šamaj J. Mitogen-activated protein kinase 4 is involved in the regulation of mitotic and cytokinetic microtubule transitions in Arabidopsis thaliana. New Phytol. 189, 1069–1083 (2011). PubMed

Takáč T. & Šamaj J. Advantages and limitations of shot-gun proteomic analyses on Arabidopsis plants with altered MAPK signaling. Plant Proteomics 6, 107 (2015). PubMed PMC

Jensen L. J. et al. STRING 8–a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res. 37, D412–416 (2009). PubMed PMC

Conesa A. & Götz S. Blast2GO: A comprehensive suite for functional analysis in plant genomics. Int. J. Plant Genomics 2008, 619832 (2008). PubMed PMC

Hord C. L. H. et al. Regulation of Arabidopsis early anther development by the mitogen-activated protein kinases, MPK3 and MPK6, and the ERECTA and related receptor-like kinases. Mol. Plant 1, 645–658 (2008). PubMed

Kosetsu K. et al. The MAP kinase MPK4 is required for cytokinesis in Arabidopsis thaliana. Plant Cell 22, 3778–3790 (2010). PubMed PMC

Meng X. & Zhang S. MAPK Cascades in Plant Disease Resistance Signaling. Annu. Rev. Phytopathol. 51, 245–266 (2013). PubMed

Doxey A. C., Yaish M. W. F., Moffatt B. A., Griffith M. & McConkey B. J. Functional Divergence in the Arabidopsis β-1,3-Glucanase Gene Family Inferred by Phylogenetic Reconstruction of Expression States. Mol. Biol. Evol. 24, 1045–1055 (2007). PubMed

Yamada K., Hara-Nishimura I. & Nishimura M. Unique Defense Strategy by the Endoplasmic Reticulum Body in Plants. Plant Cell Physiol. 52, 2039–2049 (2011). PubMed

Petersen M. et al. Arabidopsis MAP Kinase 4 Negatively Regulates Systemic Acquired Resistance. Cell 103, 1111–1120 (2000). PubMed

Lee S. M. et al. Pathogen inducible voltage-dependent anion channel (AtVDAC) isoforms are localized to mitochondria membrane in Arabidopsis. Mol. Cells 27, 321–327 (2009). PubMed

Hwang S.-G. et al. The Arabidopsis short-chain dehydrogenase/reductase 3, an ABSCISIC ACID DEFICIENT 2 homolog, is involved in plant defense responses but not in ABA biosynthesis. Plant Physiol. Biochem. 51, 63–73 (2012). PubMed

Li J., Brader G. & Palva E. T. Kunitz trypsin inhibitor: an antagonist of cell death triggered by phytopathogens and fumonisin b1 in Arabidopsis. Mol. Plant 1, 482–495 (2008). PubMed

Perl-Treves R., Foley R. C., Chen W. & Singh K. B. Early induction of the Arabidopsis GSTF8 promoter by specific strains of the fungal pathogen Rhizoctonia solani. Mol. Plant-Microbe Interact. MPMI 17, 70–80 (2004). PubMed

Park S.-C. et al. Characterization of a heat-stable protein with antimicrobial activity from Arabidopsis thaliana. Biochem. Biophys. Res. Commun. 362, 562–567 (2007). PubMed

Fujisaki K. & Ishikawa M. Identification of an Arabidopsis thaliana protein that binds to tomato mosaic virus genomic RNA and inhibits its multiplication. Virology 380, 402–411 (2008). PubMed

Dufresne P. J. et al. Heat shock 70 protein interaction with Turnip mosaic virus RNA-dependent RNA polymerase within virus-induced membrane vesicles. Virology 374, 217–227 (2008). PubMed

Noël L. D. et al. Interaction between SGT1 and cytosolic/nuclear HSC70 chaperones regulates Arabidopsis immune responses. Plant Cell 19, 4061–4076 (2007). PubMed PMC

Sun Q.-P., Guo Y., Sun Y., Sun D.-Y. & Wang X.-J. Influx of extracellular Ca2+ involved in jasmonic-acid-induced elevation of [Ca2+]cyt and JR1 expression in Arabidopsis thaliana. J. Plant Res. 119, 343–350 (2006). PubMed

He Y., Fukushige H., Hildebrand D. F. & Gan S. Evidence Supporting a Role of Jasmonic Acid in Arabidopsis Leaf Senescence. Plant Physiol. 128, 876–884 (2002). PubMed PMC

Voll L. M. et al. Loss of cytosolic NADP-malic enzyme 2 in Arabidopsis thaliana is associated with enhanced susceptibility to Colletotrichum higginsianum. New Phytol. 195, 189–202 (2012). PubMed

Niehl A. et al. Control of Tobacco mosaic virus Movement Protein Fate by CELL-DIVISION-CYCLE Protein48. Plant Physiol. 160, 2093–2108 (2012). PubMed PMC

Cheng Z. et al. Pathogen-secreted proteases activate a novel plant immune pathway. Nature 521, 213–216 (2015). PubMed PMC

Chen J.-G. et al. RACK1 mediates multiple hormone responsiveness and developmental processes in Arabidopsis. J. Exp. Bot. 57, 2697–2708 (2006). PubMed

Jarsch I. K. & Ott T. Perspectives on Remorin Proteins, Membrane Rafts, and Their Role During Plant–Microbe Interactions. Mol. Plant. Microbe Interact. 24, 7–12 (2010). PubMed

McKinney E. C., Kandasamy M. K. & Meagher R. B. Small changes in the regulation of one Arabidopsis profilin isovariant, PRF1, alter seedling development. Plant Cell 13, 1179–1191 (2001). PubMed PMC

Abu-Abied M. et al. Identification of plant cytoskeleton-interacting proteins by screening for actin stress fiber association in mammalian fibroblasts. Plant J. 48, 367–379 (2006). PubMed

Konopka-Postupolska D., Clark G. & Hofmann A. Structure, function and membrane interactions of plant annexins: An update. Plant Sci. 181, 230–241 (2011). PubMed

Zhang Q. et al. Phosphatidic acid regulates microtubule organization by interacting with MAP65-1 in response to salt stress in Arabidopsis. Plant Cell 24, 4555–4576 (2012). PubMed PMC

Yu L. et al. Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol. 188, 762–773 (2010). PubMed

Rancour D. M., Dickey C. E., Park S. & Bednarek S. Y. Characterization of AtCDC48. Evidence for Multiple Membrane Fusion Mechanisms at the Plane of Cell Division in Plants. Plant Physiol. 130, 1241–1253 (2002). PubMed PMC

Ishiguro S. et al. SHEPHERD is the Arabidopsis GRP94 responsible for the formation of functional CLAVATA proteins. EMBO J. 21, 898–908 (2002). PubMed PMC

Goeres D. C. et al. Components of the Arabidopsis mRNA Decapping Complex Are Required for Early Seedling Development. Plant Cell Online 19, 1549–1564 (2007). PubMed PMC

Frei dit Frey N. et al. Functional analysis of Arabidopsis immune-related MAPKs uncovers a role for MPK3 as negative regulator of inducible defences. Genome Biol. 15, R87 (2014). PubMed PMC

Park S., Rancour D. M. & Bednarek S. Y. In planta analysis of the cell cycle-dependent localization of AtCDC48A and its critical roles in cell division, expansion, and differentiation. Plant Physiol. 148, 246–258 (2008). PubMed PMC

Smékalová V. et al. Involvement of YODA and mitogen activated protein kinase 6 in Arabidopsis post-embryogenic root development through auxin up-regulation and cell division plane orientation. New Phytol. 203, 1175–1193 (2014). PubMed PMC

Hoehenwarter W. et al. Identification of novel in vivo MAP kinase substrates in Arabidopsis thaliana through use of tandem metal oxide affinity chromatography. Mol. Cell. Proteomics MCP 12, 369–380 (2013). PubMed PMC

Popescu S. C. et al. MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev. 23, 80–92 (2009). PubMed PMC

Chang R., Jang C. J. H., Branco-Price C., Nghiem P. & Bailey-Serres J. Transient MPK6 activation in response to oxygen deprivation and reoxygenation is mediated by mitochondria and aids seedling survival in Arabidopsis. Plant Mol. Biol. 78, 109–122 (2012). PubMed

Yoo S.-D., Cho Y.-H., Tena G., Xiong Y. & Sheen J. Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451, 789–795 (2008). PubMed PMC

Lassowskat I., Böttcher C., Eschen-Lippold L., Scheel D. & Lee J. Sustained mitogen-activated protein kinase activation reprograms defense metabolism and phosphoprotein profile in Arabidopsis thaliana. Front. Plant Sci. 5, 554 (2014). PubMed PMC

Beckers G. J. M. et al. Mitogen-Activated Protein Kinases 3 and 6 Are Required for Full Priming of Stress Responses in Arabidopsis thaliana. Plant Cell 21, 944–953 (2009). PubMed PMC

Yamada K., Nagano A. J., Nishina M., Hara-Nishimura I. & Nishimura M. Identification of Two Novel Endoplasmic Reticulum Body-Specific Integral Membrane Proteins. Plant Physiol. 161, 108–120 (2013). PubMed PMC

Matsushima R., Kondo M., Nishimura M. & Hara-Nishimura I. A novel ER-derived compartment, the ER body, selectively accumulates a beta-glucosidase with an ER-retention signal in Arabidopsis. Plant J. Cell Mol. Biol. 33, 493–502 (2003). PubMed

Berriri S. et al. Constitutively active mitogen-activated protein kinase versions reveal functions of Arabidopsis MPK4 in pathogen defense signaling. Plant Cell 24, 4281–4293 (2012). PubMed PMC

Xing Y. et al. MKK5 regulates high light-induced gene expression of Cu/Zn superoxide dismutase 1 and 2 in Arabidopsis. Plant Cell Physiol. 54, 1217–1227 (2013). PubMed

Xing Y., Chen W., Jia W. & Zhang J. Mitogen-activated protein kinase kinase 5 (MKK5)-mediated signalling cascade regulates expression of iron superoxide dismutase gene in Arabidopsis under salinity stress. J. Exp. Bot. 66, 5971–5981 (2015). PubMed PMC

Xing Y., Jia W. & Zhang J. AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J. 54, 440–451 (2008). PubMed

Takáč T. et al. Proteomic and Biochemical Analyses Show a Functional Network of Proteins Involved in Antioxidant Defense of the Arabidopsis anp2anp3 Double Mutant. J. Proteome Res. 13, 5347–5361 (2014). PubMed PMC

Baluska F. et al. Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. Dev. Biol. 227, 618–632 (2000). PubMed

Li J., Blanchoin L. & Staiger C. J. Signaling to actin stochastic dynamics. Annu. Rev. Plant Biol. 66, 415–440 (2015). PubMed

Murashige T. & Skoog F. A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures. Physiol. Plant. 15, 473–497 (1962).

López-Bucio J. S. et al. Arabidopsis thaliana mitogen-activated protein kinase 6 is involved in seed formation and modulation of primary and lateral root development. J. Exp. Bot. 65, 169–183 (2014). PubMed PMC

Takáč T., Pechan T., Šamajová O. & Šamaj J. Integrative chemical proteomics and cell biology methods to study endocytosis and vesicular trafficking in Arabidopsis. Methods Mol. Biol. Clifton NJ 1209, 265–283 (2014). PubMed

Dinkel H. et al. ELM 2016-data update and new functionality of the eukaryotic linear motif resource. Nucleic Acids Res. 44, D294–300 (2016). PubMed PMC

Xue Y. et al. GPS: a comprehensive www server for phosphorylation sites prediction. Nucleic Acids Res. 33, W184–187 (2005). PubMed PMC

Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976). PubMed

Aebi H. Catalase in vitro. Methods Enzymol. 105, 121–126 (1984). PubMed

Liu C. & Mehdy M. C. A nonclassical arabinogalactan protein gene highly expressed in vascular tissues, AGP31, is transcriptionally repressed by methyl jasmonic acid in Arabidopsis. Plant Physiol. 145, 863–874 (2007). PubMed PMC

Hooks M. A. et al. Selective induction and subcellular distribution of ACONITASE 3 reveal the importance of cytosolic citrate metabolism during lipid mobilization in Arabidopsis. Biochem. J. 463, 309–317 (2014). PubMed

Taylor N. L., Heazlewood J. L., Day D. A. & Millar A. H. Lipoic acid-dependent oxidative catabolism of alpha-keto acids in mitochondria provides evidence for branched-chain amino acid catabolism in Arabidopsis. Plant Physiol. 134, 838–848 (2004). PubMed PMC

Xu J., Yang J.-Y., Niu Q.-W. & Chua N.-H. Arabidopsis DCP2, DCP1, and VARICOSE Form a Decapping Complex Required for Postembryonic Development. Plant Cell 18, 3386–3398 (2006). PubMed PMC

Winter G., Todd C. D., Trovato M., Forlani G. & Funck D. Physiological implications of arginine metabolism in plants. Front Plant Sci 6, 534 (2015). PubMed PMC

Sung D. Y., Vierling E. & Guy C. L. Comprehensive Expression Profile Analysis of the Arabidopsis Hsp70 Gene Family. Plant Physiol. 126, 789–800 (2001). PubMed PMC

Guo Y., Xiong L., Ishitani M. & Zhu J.-K. An Arabidopsis mutation in translation elongation factor 2 causes superinduction of CBF/DREB1 transcription factor genes but blocks the induction of their downstream targets under low temperatures. Proc. Natl. Acad. Sci. USA 99, 7786–7791 (2002). PubMed PMC

Gookin T. E. & Assmann S. M. Significant reduction of BiFC non-specific assembly facilitates in planta assessment of heterotrimeric G-protein interactors. Plant J. 80, 553–567 (2014). PubMed PMC

Park S., Rancour D. M. & Bednarek S. Y. In planta analysis of the cell cycle-dependent localization of AtCDC48A and its critical roles in cell division, expansion, and differentiation. Plant Physiol. 148, 246–258 (2008). PubMed PMC

Heeg C. et al. Analysis of the Arabidopsis O-acetylserine(thiol)lyase gene family demonstrates compartment-specific differences in the regulation of cysteine synthesis. Plant Cell 20, 168–185 (2008). PubMed PMC

Mayfield J. D., Paul A.-L. & Ferl R. J. The 14-3-3 proteins of Arabidopsis regulate root growth and chloroplast development as components of the photosensory system. J. Exp. Bot. 63, 3061–3070 (2012). PubMed PMC

Deyholos M. K. et al. VARICOSE, a WD-domain protein, is required for leaf blade. Development 130, 6577–6588 (2003). PubMed

Jin H., Song Z. & Nikolau B. J. Reverse genetic characterization of two paralogous acetoacetyl CoA thiolase genes in Arabidopsis reveals their importance in plant growth and development. Plant J. 70, 1015–1032 (2012). PubMed

Suarez M. F. et al. Metacaspase-dependent programmed cell death is essential for plant embryogenesis. Curr. Biol. CB 14, R339–340 (2004). PubMed

Guo D. et al. Cis-cinnamic acid-enhanced 1 gene plays a role in regulation of Arabidopsis bolting. Plant Mol. Biol. 75, 481–495 (2011). PubMed

Suzuki K. et al. Plastid chaperonin proteins Cpn60α and Cpn60β are required for plastid division in Arabidopsis thaliana. BMC Plant Biol. 9, 38 (2009). PubMed PMC

Chen M. & Thelen J. J. The plastid isoform of triose phosphate isomerase is required for the postgerminative transition from heterotrophic to autotrophic growth in Arabidopsis. Plant Cell 22, 77–90 (2010). PubMed PMC

Ma X., Song L., Yang Y. & Liu D. A gain-of-function mutation in the ROC1 gene alters plant architecture in Arabidopsis. New Phytol. 197, 751–762 (2013). PubMed

Strompen G. et al. Arabidopsis vacuolar H-ATPase subunit E isoform 1 is required for Golgi organization and vacuole function in embryogenesis. Plant J. Cell Mol. Biol. 41, 125–132 (2005). PubMed

Uváčková Ľ., Takáč T., Boehm N., Obert B. & Šamaj J. Proteomic and biochemical analysis of maize anthers after cold pretreatment and induction of androgenesis reveals an important role of anti-oxidative enzymes. J. Proteomics 75, 1886–1894 (2012). PubMed

Kim S. Y. & Nam K. H. Physiological roles of ERD10 in abiotic stresses and seed germination of Arabidopsis. Plant Cell Rep. 29, 203–209 (2010). PubMed

Pereira L. A. R. et al. Methyl recycling activities are co-ordinately regulated during plant development. J. Exp. Bot. 58, 1083–1098 (2007). PubMed

Yang M., Hu Y., Lodhi M., McCombie W. R. & Ma H. The Arabidopsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation. Proc. Natl. Acad. Sci. USA 96, 11416–11421 (1999). PubMed PMC

Yang X., Timofejeva L., Ma H. & Makaroff C. A. The Arabidopsis SKP1 homolog ASK1 controls meiotic chromosome remodeling and release of chromatin from the nuclear membrane and nucleolus. J. Cell Sci. 119, 3754–3763 (2006). PubMed

Porat R., Lu P. & O’Neill S. D. Arabidopsis SKP1, a homologue of a cell cycle regulator gene, is predominantly expressed in meristematic cells. Planta 204, 345–351 (1998). PubMed

Liu F. et al. The ASK1 and ASK2 genes are essential for Arabidopsis early development. Plant Cell 16, 5–20 (2004). PubMed PMC

Kim J. Y. et al. Functional characterization of a glycine-rich RNA-binding protein 2 in Arabidopsis thaliana under abiotic stress conditions. Plant J. 50, 439–451 (2007). PubMed

Fusaro A. F. et al. AtGRP2, a cold-induced nucleo-cytoplasmic RNA-binding protein, has a role in flower and seed development. Planta 225, 1339–1351 (2007). PubMed

Linkies A. et al. Ethylene Interacts with Abscisic Acid to Regulate Endosperm Rupture during Germination: A Comparative Approach Using Lepidium sativum and Arabidopsis thaliana. Plant Cell 21, 3803–3822 (2009). PubMed PMC

Qin Y.-M. et al. Saturated very-long-chain fatty acids promote cotton fiber and Arabidopsis cell elongation by activating ethylene biosynthesis. Plant Cell 19, 3692–3704 (2007). PubMed PMC

Péret B. et al. Auxin regulates aquaporin function to facilitate lateral root emergence. Nat. Cell Biol. 14, 991–998 (2012). PubMed

Shen L., Kang Y. G. G., Liu L. & Yu H. The J-domain protein J3 mediates the integration of flowering signals in Arabidopsis. Plant Cell 23, 499–514 (2011). PubMed PMC

Renault H. et al. γ-Aminobutyric acid transaminase deficiency impairs central carbon metabolism and leads to cell wall defects during salt stress in Arabidopsis roots. Plant Cell Environ. 36, 1009–1018 (2013). PubMed

Kandasamy M. K., McKinney E. C. & Meagher R. B. A single vegetative actin isovariant overexpressed under the control of multiple regulatory sequences is sufficient for normal Arabidopsis development. Plant Cell 21, 701–718 (2009). PubMed PMC

Thitamadee S., Tuchihara K. & Hashimoto T. Microtubule basis for left-handed helical growth in Arabidopsis. Nature 417, 193–196 (2002). PubMed

Matsumoto S. et al. Gravity-induced modifications to development in hypocotyls of Arabidopsis tubulin mutants. Plant Physiol. 152, 918–926 (2010). PubMed PMC

Kandasamy M. K., Gilliland L. U., McKinney E. C. & Meagher R. B. One plant actin isovariant, ACT7, is induced by auxin and required for normal callus formation. Plant Cell 13, 1541–1554 (2001). PubMed PMC

Gilliland L. U., Pawloski L. C., Kandasamy M. K. & Meagher R. B. Arabidopsis actin gene ACT7 plays an essential role in germination and root growth. Plant J. Cell Mol. Biol. 33, 319–328 (2003). PubMed

Uraji M. et al. Cooperative function of PLDδ and PLDα1 in abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol. 159, 450–460 (2012). PubMed PMC

Guo J. & Chen J.-G. RACK1 genes regulate plant development with unequal genetic redundancy in Arabidopsis. BMC Plant Biol. 8, 108 (2008). PubMed PMC

Vellosillo T. et al. Oxylipins produced by the 9-lipoxygenase pathway in Arabidopsis regulate lateral root development and defense responses through a specific signaling cascade. Plant Cell 19, 831–846 (2007). PubMed PMC

Gallois J.-L. et al. The Arabidopsis proteasome RPT5 subunits are essential for gametophyte development and show accession-dependent redundancy. Plant Cell 21, 442–459 (2009). PubMed PMC

Ueda M. et al. Arabidopsis RPT2a Encoding the 26S Proteasome Subunit is Required for Various Aspects of Root Meristem Maintenance, and Regulates Gametogenesis Redundantly with its Homolog, RPT2b. Plant Cell Physiol. 52, 1628–1640 (2011). PubMed

Hossain Z. et al. The translation elongation factor eEF-1Bβ1 is involved in cell wall biosynthesis and plant development in Arabidopsis thaliana. PloS One 7, e30425 (2012). PubMed PMC

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