MYB52 negatively regulates ADF9-meditated actin filament bundling in Arabidopsis pavement cell morphogenesis

Tianqi Qiu , Yuanyuan Su , Nannan Guo , Xinyuan Zhang , Pengfei Jia , Tonglin Mao , Xianling Wang

Journal of Integrative Plant Biology ›› 2024, Vol. 66 ›› Issue (11) : 2379 -2394.

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Journal of Integrative Plant Biology ›› 2024, Vol. 66 ›› Issue (11) : 2379 -2394. DOI: 10.1111/jipb.13762
Research Article

MYB52 negatively regulates ADF9-meditated actin filament bundling in Arabidopsis pavement cell morphogenesis

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Abstract

It has been proposed that cortical fine actin filaments are needed for the morphogenesis of pavement cells (PCs). However, the precise role and regulation mechanisms of actin filaments in PC morphogenesis are not well understood. Here, we found that Arabidopsis thaliana ACTIN DEPOLYMERIZING FACTOR9 (ADF9) is required for the morphogenesis of PC, which is negatively regulated by the R2R3 MYELOBLASTOSIS (MYB) transcription factor MYB52. In adf9 mutants, the lobe number of cotyledon PCs was significantly reduced, while the average lobe length did not differ significantly compared to that of wild type (Col-0), except for the variations in cell area and circularity, whereas the PC shapes in ADF9 overexpression seedlings showed different results. ADF9 decorated actin filaments, and colocalized with plasma membrane. The extent of filament bundling and actin filament bundling activity in adf9 mutant decreased. In addition, MYB52 directly targeted the promoter of ADF9 and negatively regulated its expression. The myb52-2 mutant showed increased lobe number and cell area, reduced cell circularity of PCs, and the PC phenotypes were suppressed when ADF9 was knocked out. Taken together, our data demonstrate that actin filaments play an important role in the morphogenesis of PC and reveal a transcriptional mechanism underlying MYB52 regulation of ADF9-mediated actin filament bundling in PC morphogenesis.

Keywords

actin filament bundling / ADF9 / MYB52 / pavement cell

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Tianqi Qiu, Yuanyuan Su, Nannan Guo, Xinyuan Zhang, Pengfei Jia, Tonglin Mao, Xianling Wang. MYB52 negatively regulates ADF9-meditated actin filament bundling in Arabidopsis pavement cell morphogenesis. Journal of Integrative Plant Biology, 2024, 66(11): 2379-2394 DOI:10.1111/jipb.13762

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References

[1]

Altartouri, B.,Bidhendi, A.J.,Tani, T.,Suzuki, J.,Conrad, C.,Chebli, Y.,Liu, N.,Karunakaran, C.,Scarcelli, G., and Geitmann, A. (2019). Pectin chemistry and cellulose crystallinity govern pavement cell morphogenesis in a multi-step mechanism. Plant Physiol. 181:127–141.

[2]

Andrianantoandro, E., and Pollard, T.D. (2006). Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol. Cell 24:13–23.

[3]

Armour, W.J.,Barton, D.A.,Law, A.M.K., and Overall, R.L. (2015). Differential growth in periclinal and anticlinal walls during lobe formation in Arabidopsis cotyledon pavement cells. Plant Cell 27:2484–2500.

[4]

Belteton, S.A.,Li, W.,Yanagisawa, M.,Hatam, F.A.,Quinn, M.I.,Szymanski, M.K.,Marley, M.W.,Turner, J.A., and Szymanski, D.B. (2021). Real-time conversion of tissue-scale mechanical forces into an interdigitated growth pattern. Nat Plants 7:826–841.

[5]

Bi, S.,Li, M.,Liu, C.,Liu, X.,Cheng, J.,Wang, L.,Wang, J.,Lv, Y.,He, M.,Cheng, X., et al. (2022). Actin depolymerizing factor ADF7 inhibits actin bundling protein VILLIN1 to regulate root hair formation in response to osmotic stress in Arabidopsis. PLoS Genet. 18: e1010338.

[6]

Bou Daher, F.,Van Oostende, C., and Geitmann, A. (2011). Spatial and temporal expression of actin depolymerizing factors ADF7 and ADF10 during male gametophyte development in Arabidopsis thaliana. Plant Cell Physiol. 52:1177–1192.

[7]

Burgos-Rivera, B.,Ruzicka, D.R.,Deal, R.B.,McKinney, E.C.,King-Reid, L., and Meagher, R.B. (2008). ACTIN DEPOLYMERIZING FACTOR9 controls development and gene expression in Arabidopsis. Plant Mol. Biol. 68:619–632.

[8]

Chen, B.,Dang, X.,Bai, W.,Liu, M.,Li, Y.,Zhu, L.,Yang, Y.,Yu, P.,Ren, H.,Huang, D., et al. (2022). The IPGA1-ANGUSTIFOLIA module regulates microtubule organisation and pavement cell shape in Arabidopsis. New Phytol. 236:1310–1325.

[9]

Clement, M.,Ketelaar, T.,Rodiuc, N.,Banora, M.Y.,Smertenko, A.,Engler, G.,Abad, P.,Hussey, P.J., and de Almeida Engler, J. (2009). Actin-depolymerizing factor2-mediated actin dynamics are essential for root-knot nematode infection of Arabidopsis. Plant Cell 21:2963–2979.

[10]

Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16:735–743.

[11]

Ding, A.,Tang, X.,Yang, D.,Wang, M.,Ren, A.,Xu, Z.,Hu, R.,Zhou, G.,O’Neill, M., and Kong, Y. (2021). ERF4 and MYB52 transcription factors play antagonistic roles in regulating homogalacturonan de-methylesterification in Arabidopsis seed coat mucilage. Plant Cell 33:381–403.

[12]

Dong, C.-H., and Hong, Y. (2013). Arabidopsis CDPK6 phosphorylates ADF1 at N-terminal serine 6 predominantly. Plant Cell Rep. 32:1715–1728.

[13]

Dubos, C.,Stracke, R.,Grotewold, E.,Weisshaar, B.,Martin, C., and Lepiniec, L. (2010). MYB transcription factors in Arabidopsis. Trends Plant Sci. 15:573–581.

[14]

Franco-Zorrilla, J.M.,López-Vidriero, I.,Carrasco, J.L.,Godoy, M.,Vera, P., and Solano, R. (2014). DNA-binding specificities of plant transcription factors and their potential to define target genes. Proc. Natl. Acad. Sci. U.S.A. 111:2367–2372.

[15]

Fu, Y. (2002). The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis. Plant Cell 14:777–794.

[16]

Fu, Y.,Gu, Y.,Zheng, Z.,Wasteneys, G., and Yang, Z. (2005). Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 120:687–700.

[17]

Gao, X.,Yang, B.,Zhang, J.,Wang, C.,Ren, H.,Fu, Y., and Yang, Z. (2023). PRL1 negatively regulates Rho GTPase-independent and—dependent signaling pathways maintaining actin microfilament dynamic for pavement cell morphogenesis. bioRxiv.

[18]

Haas, K.T.,Wightman, R.,Meyerowitz, E.M., and Peaucelle, A. (2020). Pectin homogalacturonan nanofilament expansion drives morphogenesis in plant epidermal cells. Science 367:1003–1007.

[19]

Henty, J.L.,Bledsoe, S.W.,Khurana, P.,Meagher, R.B.,Day, B.,Blanchoin, L., and Staiger, C.J. (2011). Arabidopsis actin depolymerizing factor4 modulates the stochastic dynamic behavior of actin filaments in the cortical array of epidermal cells. Plant Cell 23:3711–3726.

[20]

Henty-Ridilla, J.L.,Li, J.,Day, B., and Staiger, C.J. (2014). ACTIN DEPOLYMERIZING FACTOR4 regulates actin dynamics during innate immune signaling in Arabidopsis. Plant Cell 26:340–352.

[21]

Inada, N.,Higaki, T., and Hasezawa, S. (2016). Nuclear function of subclass I actin depolymerizing factor contributes to susceptibility in Arabidopsis to an adapted powdery mildew fungus. Plant Physiol. 170:1420–1434.

[22]

Jiang, C.-K., and Rao, G.-Y. (2020). Insights into the diversification and evolution of R2R3-MYB transcription factors in plants. Plant Physiol. 183:637–655.

[23]

Jumper, J.,Evans, R.,Pritzel, A.,Green, T.,Figurnov, M.,Ronneberger, O.,Tunyasuvunakool, K.,Bates, R.,Žídek, A.,Potapenko, A., et al. (2021). Highly accurate protein structure prediction with AlphaFold. Nature 596:583–589.

[24]

Ko, J.,Kim, W., and Han, K. (2009). Ectopic expression of MYB46 identifies transcriptional regulatory genes involved in secondary wall biosynthesis in Arabidopsis. Plant J. 60:649–665.

[25]

Labusch, C.,Shishova, M.,Effendi, Y.,Li, M.,Wang, X., and Scherer, G.F. (2013). Patterns and timing in expression of early auxin-induced genes imply involvement of phospholipases A (pPLAs) in the regulation of auxin responses. Mol. Plant 6:1473–1486.

[26]

Li, J.,Henty-Ridilla, J.L.,Huang, S.,Wang, X.,Blanchoin, L., and Staiger, C.J. (2012). Capping protein modulates the dynamic behavior of actin filaments in response to phosphatidic acid in Arabidopsis. Plant Cell 24:3742–3754.

[27]

Li, S.,Blanchoin, L.,Yang, Z., and Lord, E.M. (2003). The putative Arabidopsis arp2/3 complex controls leaf cell morphogenesis. Plant Physiol. 132:2034–2044.

[28]

Liang, H.,Zhang, Y.,Martinez, P.,Rasmussen, C.G.,Xu, T., and Yang, Z. (2018). The microtubule-associated protein IQ67 DOMAIN5 modulates microtubule dynamics and pavement cell shape. Plant Physiol. 177:1555–1568.

[29]

Liu, S.,Jobert, F.,Rahneshan, Z.,Doyle, S.M., and Robert, S. (2021). Solving the puzzle of shape regulation in plant epidermal pavement cells. Annu. Rev. Plant Biol. 72:525–550.

[30]

Liu, X.,Qin, T.,Ma, Q.,Sun, J.,Liu, Z.,Yuan, M., and Mao, T. (2013). Light-regulated hypocotyl elongation involves proteasome-dependent degradation of the microtubule regulatory protein WDL3 in Arabidopsis. Plant Cell 25:1740–1755.

[31]

Mathur, J. (2004). Cell shape development in plants. Trends Plant Sci. 9:583–590.

[32]

Möller, B.,Poeschl, Y.,Plötner, R., and Bürstenbinder, K. (2017). PaCeQuant: A tool for high-throughput quantification of pavement cell shape characteristics. Plant Physiol. 175:998–1017.

[33]

Nagawa, S.,Xu, T., and Yang, Z. (2010). RHO GTPase in plants: Conservation and invention of regulators and effectors. Small GTPases 1:78–88.

[34]

Nan, Q.,Qian, D.,Niu, Y.,He, Y.,Tong, S.,Niu, Z.,Ma, J.,Yang, Y.,An, L.,Wan, D., et al. (2017). Plant actin-depolymerizing factors possess opposing biochemical properties arising from key amino acid changes throughout evolution. Plant Cell 29:395–408.

[35]

Okreglak, V., and Drubin, D.G. (2007). Cofilin recruitment and function during actin-mediated endocytosis dictated by actin nucleotide state. J. Cell Biol. 178:1251–1264.

[36]

Panteris, E., and Galatis, B. (2005). The morphogenesis of lobed plant cells in the mesophyll and epidermis: Organization and distinct roles of cortical microtubules and actin filaments: Research review. New Phytol. 167:721–732.

[37]

Park, M.Y.,Kang, J., and Kim, S.Y. (2011). Overexpression of AtMYB52 confers ABA hypersensitivity and drought tolerance. Mol. Cells 31:447–454.

[38]

Qian, D.,Zhang, Z.,He, J.,Zhang, P.,Ou, X.,Li, T.,Niu, L.,Nan, Q.,Niu, Y.,He, W., et al. (2019). Arabidopsis ADF5 promotes stomatal closure by regulating actin cytoskeleton remodeling in response to ABA and drought stress. J. Exp. Bot. 70:435–446.

[39]

Rosero, A.,Oulehlová D.,Stillerová L.,Schiebertová P.,Grunt, M.,Žárský V., and Cvrčková F. (2016). Arabidopsis FH1 formin affects cotyledon pavement cell shape by modulating cytoskeleton dynamics. Plant Cell Physiol. 57:488–504.

[40]

Ruzicka, D.R.,Kandasamy, M.K.,McKinney, E.C.,Burgos-Rivera, B., and Meagher, R.B. (2007). The ancient subclasses of Arabidopsis ACTIN DEPOLYMERIZING FACTOR genes exhibit novel and differential expression. Plant J. 52:460–472.

[41]

Sapala, A.,Runions, A.,Routier-Kierzkowska, A.-L.,Das Gupta, M.,Hong, L.,Hofhuis, H.,Verger, S.,Mosca, G.,Li, C.-B.,Hay, A., et al. (2018). Why plants make puzzle cells, and how their shape emerges. eLife 7: e32794.

[42]

Sapala, A.,Runions, A., and Smith, R.S. (2019). Mechanics, geometry and genetics of epidermal cell shape regulation: Different pieces of the same puzzle. Curr. Opin. Plant Biol. 47:1–8.

[43]

Shi, D.,Ren, A.,Tang, X.,Qi, G.,Xu, Z.,Chai, G.,Hu, R.,Zhou, G., and Kong, Y. (2018). MYB52 negatively regulates pectin demethylesterification in seed coat mucilage. Plant Physiol. 176:2737–2749.

[44]

Staiger, C.J.,Sheahan, M.B.,Khurana, P.,Wang, X.,McCurdy, D.W., and Blanchoin, L. (2009). Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. J. Cell Biol. 184:269–280.

[45]

Szymanski, D., and Staiger, C.J. (2018). The actin cytoskeleton: Functional arrays for cytoplasmic organization and cell shape control. Plant Physiol. 176:106–118.

[46]

Tholl, S.,Moreau, F.,Hoffmann, C.,Arumugam, K.,Dieterle, M.,Moes, D.,Neumann, K.,Steinmetz, A., and Thomas, C. (2011). Arabidopsis actin-depolymerizing factors (ADFs) 1 and 9 display antagonist activities. FEBS Lett. 585:1821–1827.

[47]

Tian, M.,Chaudhry, F.,Ruzicka, D.R.,Meagher, R.B.,Staiger, C.J., and Day, B. (2009). Arabidopsis actin-depolymerizing factor AtADF4 mediates defense signal transduction triggered by the pseudomonas syringae effector AvrPphB. Plant Physiol. 150:815–824.

[48]

Wang, X.,Bi, S.,Wang, L.,Li, H.,Gao, B.,Huang, S.,Qu, X.,Cheng, J.,Wang, S.,Liu, C., et al. (2020). GLABRA2 regulates actin bundling protein VILLIN1 in root hair growth in response to osmotic stress. Plant Physiol. 184:176–193.

[49]

Wang, Z.,Xing, H.,Dong, L.,Zhang, H.,Han, C.,Wang, X., and Chen, Q. (2015). Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol. 16:144.

[50]

Wu, S.,Xie, Y.,Zhang, J.,Ren, Y.,Zhang, X.,Wang, J.,Guo, X.,Wu, F.,Sheng, P.,Wang, J., et al. (2015). VLN2 regulates plant architecture by affecting microfilament dynamics and polar auxin transport in Rice. Plant Cell 27:2829–2845.

[51]

Xu, T.,Dai, N.,Chen, J.,Nagawa, S.,Cao, M.,Li, H.,Zhou, Z.,Chen, X.,De Rycke, R.,Rakusová H., et al. (2014). Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling. Science 343:1025–1028.

[52]

Xu, T.,Wen, M.,Nagawa, S.,Fu, Y.,Chen, J.-G.,Wu, M.-J.,Perrot-Rechenmann, C.,Friml, J.,Jones, A.M., and Yang, Z. (2010). Cell surface-and Rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143:99–110.

[53]

Zhang, C.,Halsey, L.E., and Szymanski, D.B. (2011). The development and geometry of shape change in Arabidopsis thaliana cotyledon pavement cells. BMC Plant Biol. 11:27.

[54]

Zhao, S.,Jiang, Y.,Zhao, Y.,Huang, S.,Yuan, M.,Zhao, Y., and Guo, Y. (2016). CASEIN KINASE1-LIKE PROTEIN2 regulates actin filament stability and stomatal closure via phosphorylation of actin depolymerizing factor. Plant Cell 28:1422–1439.

[55]

Zheng, Y.,Xie, Y.,Jiang, Y.,Qu, X., and Huang, S. (2013). Arabidopsis ACTIN-DEPOLYMERIZING FACTOR7 severs actin filaments and regulates actin cable turnover to promote normal pollen tube growth. Plant Cell 25:3405–3423.

[56]

Zhu, J.,Nan, Q.,Qin, T.,Qian, D.,Mao, T.,Yuan, S.,Wu, X.,Niu, Y.,Bai, Q.,An, L., et al. (2017). Higher-ordered actin structures remodeled by Arabidopsis ACTIN-DEPOLYMERIZING FACTOR5 are important for pollen germination and pollen tube growth. Mol. Plant 10:1065–1081.

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2024 The Author(s). Journal of Integrative Plant Biology published by John Wiley & Sons Australia, Ltd on behalf of Institute of Botany, Chinese Academy of Sciences.

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