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http://dx.doi.org/10.14348/molcells.2021.0203

The Danger-Associated Peptide PEP1 Directs Cellular Reprogramming in the Arabidopsis Root Vascular System  

Dhar, Souvik (School of Biological Sciences, College of Natural Science, Seoul National University)
Kim, Hyoujin (School of Biological Sciences, College of Natural Science, Seoul National University)
Segonzac, Cecile (Department of Agriculture, Forestry and Bioresources, Seoul National University)
Lee, Ji-Young (School of Biological Sciences, College of Natural Science, Seoul National University)
Abstract
When perceiving microbe-associated molecular patterns (MAMPs) or plant-derived damage-associated molecular patterns (DAMPs), plants alter their root growth and development by displaying a reduction in the root length and the formation of root hairs and lateral roots. The exogenous application of a MAMP peptide, flg22, was shown to affect root growth by suppressing meristem activity. In addition to MAMPs, the DAMP peptide PEP1 suppresses root growth while also promoting root hair formation. However, the question of whether and how these elicitor peptides affect the development of the vascular system in the root has not been explored. The cellular receptors of PEP1, PEPR1 and PEPR2 are highly expressed in the root vascular system, while the receptors of flg22 (FLS2) and elf18 (EFR) are not. Consistent with the expression patterns of PEP1 receptors, we found that exogenously applied PEP1 has a strong impact on the division of stele cells, leading to a reduction of these cells. We also observed the alteration in the number and organization of cells that differentiate into xylem vessels. These PEP1-mediated developmental changes appear to be linked to the blockage of symplastic connections triggered by PEP1. PEP1 dramatically disrupts the symplastic movement of free green fluorescence protein (GFP) from phloem sieve elements to neighboring cells in the root meristem, leading to the deposition of a high level of callose between cells. Taken together, our first survey of PEP1-mediated vascular tissue development provides new insights into the PEP1 function as a regulator of cellular reprogramming in the Arabidopsis root vascular system.
Keywords
DAMP; MAMP; PEP1; root development; vascular system;
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1 Chaiwanon, J., Wang, W., Zhu, J.Y., Oh, E., and Wang, Z.Y. (2016). Information integration and communication in plant growth regulation. Cell 164, 1257-1268.   DOI
2 Kurihara, D., Mizuta, Y., Sato, Y., and Higashiyama, T. (2015). ClearSee: a rapid optical clearing reagent for whole-plant fluorescence imaging. Development 142, 4168-4179.   DOI
3 Millet, Y.A., Danna, C.H., Clay, N.K., Songnuan, W., Simon, M.D., Werck-Reichhart, D., and Ausubel, F.M. (2010). Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 22, 973-990.   DOI
4 Abdul Malik, N.A., Kumar, I.S., and Nadarajah, K. (2020). Elicitor and receptor molecules: orchestrators of plant defense and immunity. Int. J. Mol. Sci. 21, 963.   DOI
5 Aida, M., Beis, D., Heidstra, R., Willemsen, V., Blilou, I., Galinha, C., Nussaume, L., Noh, Y.S., Amasino, R., and Scheres, B. (2004). The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119, 109-120.   DOI
6 Bartels, S., Lori, M., Mbengue, M., van Verk, M., Klauser, D., Hander, T., Boni, R., Robatzek, S., and Boller, T. (2013). The family of Peps and their precursors in Arabidopsis: differential expression and localization but similar induction of pattern-triggered immune responses. J. Exp. Bot. 64, 5309-5321.   DOI
7 Beck, M., Wyrsch, I., Strutt, J., Wimalasekera, R., Webb, A., Boller, T., and Robatzek, S. (2014). Expression patterns of FLAGELLIN SENSING 2 map to bacterial entry sites in plant shoots and roots. J. Exp. Bot. 65, 6487-6498.   DOI
8 Bjornson, M., Pimprikar, P., Nurnberger, T., and Zipfel, C. (2021). The transcriptional landscape of Arabidopsis thaliana pattern-triggered immunity. Nat. Plants 7, 579-586.   DOI
9 De Rybel, B., Mahonen, A.P., Helariutta, Y., and Weijers, D. (2016). Plant vascular development: from early specification to differentiation. Nat. Rev. Mol. Cell Biol. 17, 30-40.   DOI
10 Dolan, L., Janmaat, K., Willemsen, V., Linstead, P., Poethig, S., Roberts, K., and Scheres, B. (1993). Cellular organisation of the Arabidopsis thaliana root. Development 119, 71-84.   DOI
11 Imlau, A., Truernit, E., and Sauer, N. (1999). Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11, 309-322.   DOI
12 Gimenez-Ibanez, S., Ntoukakis, V., and Rathjen, J.P. (2009). The LysM receptor kinase CERK1 mediates bacterial perception in Arabidopsis. Plant Signal. Behav. 4, 539-541.   DOI
13 Hacquard, S., Spaepen, S., Garrido-Oter, R., and Schulze-Lefert, P. (2017). Interplay between innate immunity and the plant microbiota. Annu. Rev. Phytopathol. 55, 565-589.   DOI
14 Huffaker, A., Pearce, G., and Ryan, C.A. (2006). An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc. Natl. Acad. Sci. U. S. A. 103, 10098-10103.   DOI
15 Jang, G., Chang, S.H., Um, T.Y., Lee, S., Kim, J.K., and Choi, Y.D. (2017). Antagonistic interaction between jasmonic acid and cytokinin in xylem development. Sci. Rep. 7, 10212.   DOI
16 Jing, Y., Zheng, X., Zhang, D., Shen, N., Wang, Y., Yang, L., Fu, A., Shi, J., Zhao, F., Lan, W., et al. (2019). Danger-associated peptides interact with PIN-dependent local auxin distribution to inhibit root growth in Arabidopsis. Plant Cell 31, 1767-1787.   DOI
17 Okada, K., Kubota, Y., Hirase, T., Otani, K., Goh, T., Hiruma, K., and Saijo, Y. (2021). Uncoupling root hair formation and defence activation from growth inhibition in response to damage-associated Pep peptides in Arabidopsis thaliana. New Phytol. 229, 2844-2858.   DOI
18 Kim, H., Zhou, J., Kumar, D., Jang, G., Ryu, K.H., Sebastian, J., Miyashima, S., Helariutta, Y., and Lee, J.Y. (2020). SHORTROOT-mediated intercellular signals coordinate phloem development in Arabidopsis roots. Plant Cell 32, 1519-1535.   DOI
19 Lee, J.Y., Colinas, J., Wang, J.Y., Mace, D., Ohler, U., and Benfey, P.N. (2006). Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots. Proc. Natl. Acad. Sci. U. S. A. 103, 6055-6060.   DOI
20 Mahonen, A.P., Bishopp, A., Higuchi, M., Nieminen, K.M., Kinoshita, K., Tormakangas, K., Ikeda, Y., Oka, A., Kakimoto, T., and Helariutta, Y. (2006). Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311, 94-98.   DOI
21 Pascale, A., Proietti, S., Pantelides, I.S., and Stringlis, I.A. (2020). Modulation of the root microbiome by plant molecules: the basis for targeted disease suppression and plant growth promotion. Front. Plant Sci. 10, 1741.   DOI
22 Ramachandran, P., Augstein, F., Mazumdar, S., Van Nguyen, T., Minina, E.A., Melnyk, C.W., and Carlsbecker, A. (2021). Abscisic acid signaling activates distinct VND transcription factors to promote xylem differentiation in Arabidopsis. Curr. Biol. 31, 3153-3161.e5.   DOI
23 Emonet, A., Zhou, F., Vacheron, J., Heiman, C.M., Tendon, V.D., Ma, K.W., Schulze-Lefert, P., Keel, C., and Geldner, N. (2021). Spatially restricted immune responses are required for maintaining root meristematic activity upon detection of bacteria. Curr. Biol. 31, 1012-1028.e7.   DOI
24 Jang, G. and Choi, Y.D. (2018). Drought stress promotes xylem differentiation by modulating the interaction between cytokinin and jasmonic acid. Plant Signal. Behav. 13, e1451707.   DOI
25 Poncini, L., Wyrsch, I., Denervaud Tendon, V., Vorley, T., Boller, T., Geldner, N., Metraux, J.P., and Lehmann, S. (2017). In roots of Arabidopsis thaliana, the damage-associated molecular pattern AtPep1 is a stronger elicitor of immune signalling than flg22 or the chitin heptamer. PLoS One 12, e0185808.   DOI
26 Rich-Griffin, C., Eichmann, R., Reitz, M.U., Hermann, S., Woolley-Allen, K., Brown, P.E., Wiwatdirekkul, K., Esteban, E., Pasha, A., Kogel, K.H., et al. (2020). Regulation of cell type-specific immunity networks in Arabidopsis roots. Plant Cell 32, 2742-2762.   DOI
27 Scheres, B. (2007). Stem-cell niches: nursery rhymes across kingdoms. Nat. Rev. Mol. Cell Biol. 8, 345-354.   DOI
28 Sebastian, J., Ryu, K.H., Zhou, J., Tarkowska, D., Tarkowski, P., Cho, Y.H., Yoo, S.D., Kim, E.S., and Lee, J.Y. (2015). PHABULOSA controls the quiescent center-independent root meristem activities in Arabidopsis thaliana. PLoS Genet. 11, e1004973.   DOI
29 Seo, M. and Lee, J.Y. (2021). Dissection of functional modules of AT-HOOK MOTIF NUCLEAR LOCALIZED PROTEIN 4 in the development of the root xylem. Front. Plant Sci. 12, 632078.   DOI
30 Smet, W., Sevilem, I., de Luis Balaguer, M.A., Wybouw, B., Mor, E., Miyashima, S., Blob, B., Roszak, P., Jacobs, T.B., Boekschoten, M., et al. (2019). DOF2. 1 controls cytokinin-dependent vascular cell proliferation downstream of TMO5/LHW. Curr. Biol. 29, 520-529.e6.   DOI
31 Wendrich, J.R., Moller, B.K., Li, S., Saiga, S., Sozzani, R., Benfey, P.N., De Rybel, B., and Weijers, D. (2017). Framework for gradual progression of cell ontogeny in the Arabidopsis root meristem. Proc. Natl. Acad. Sci. U. S. A. 114, E8922-E8929.   DOI
32 Ye, L., Wang, X., Lyu, M., Siligato, R., Eswaran, G., Vainio, L., Blomster, T., Zhang, J., and Mahonen, A.P. (2021). Cytokinins initiate secondary growth in the Arabidopsis root through a set of LBD genes. Curr. Biol. 31, 3365-3373.e7.   DOI
33 Nurnberger, T. and Kemmerling, B. (2018). Pathogen-associated molecular patterns (PAMP) and PAMP-triggered immunity. In Annual Plant Reviews Online, J.A. Roberts, ed. (Hoboken, NJ: John Wiley & Sons), https://doi.org/10.1002/9781119312994.apr0362
34 Zhou, J., Wang, X., Lee, J.Y., and Lee, J.Y. (2013). Cell-to-cell movement of two interacting AT-hook factors in Arabidopsis root vascular tissue patterning. Plant Cell 25, 187-201.   DOI
35 Ramachandran, P., Augstein, F., Nguyen, V., and Carlsbecker, A. (2020). Coping with water limitation: hormones that modify plant root xylem development. Front. Plant Sci. 11, 570.   DOI
36 Bartels, S. and Boller, T. (2015). Quo vadis, Pep? Plant elicitor peptides at the crossroads of immunity, stress, and development. J. Exp. Bot. 66, 5183-5193.   DOI
37 Bishopp, A., Help, H., El-Showk, S., Weijers, D., Scheres, B., Friml, J., Benkova, E., Mahonen, A.P., and Helariutta, Y. (2011). A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr. Biol. 21, 917-926.   DOI
38 De Coninck, B., Timmermans, P., Vos, C., Cammue, B.P.A., and Kazan, K. (2015). What lies beneath: belowground defense strategies in plants. Trends Plant Sci. 20, 91-101.   DOI
39 Hou, S., Wang, X., Chen, D., Yang, X., Wang, M., Turra, D., Di Pietro, A., and Zhang, W. (2014). The secreted peptide PIP1 amplifies immunity through receptor-like kinase 7. PLoS Pathog. 10, e1004331.   DOI
40 Ma, C., Guo, J., Kang, Y., Doman, K., Bryan, A.C., Tax, F.E., Yamaguchi, Y., and Qi, Z. (2014). AtPEPTIDE RECEPTOR2 mediates the AtPEPTIDE1-induced cytosolic Ca2+ rise, which is required for the suppression of Glutamine Dumper gene expression in Arabidopsis roots. J. Integr. Plant Biol. 56, 684-694.   DOI
41 Perini, S., Mambro, R., and Sabatini, S. (2012). Growth and development of the root apical meristem. Curr. Opin. Plant Biol. 15, 17-23.   DOI
42 Smetana, O., Makila, R., Lyu, M., Amiryousefi, A., Rodriguez, F.S., Wu, M.F., Sole-Gil, A., Gavarron, M.L., Siligato, R., Miyashima, S., et al. (2019). High levels of auxin signalling define the stem-cell organizer of the vascular cambium. Nature 565, 485-489.   DOI
43 Stadler, R. and Sauer, N. (1996). The Arabidopsis thaliana AtSUC2 gene is specifically expressed in companion cells. Bot. Acta 109, 299-306.   DOI
44 Seo, M., Kim, H., and Lee, J.Y. (2020). Information on the move: vascular tissue development in space and time during postembryonic root growth. Curr. Opin. Plant Biol. 57, 110-117.   DOI
45 Yamaguchi, Y. and Huffaker, A. (2011). Endogenous peptide elicitors in higher plants. Curr. Opin. Plant Biol. 14, 351-357.   DOI
46 Zhang, J., Eswaran, G., Alonso-Serra, J., Kucukoglu, M., Xiang, J., Yang, W., Elo, A., Nieminen, K., Damen, T., Joung, J.G., et al. (2019). Transcriptional regulatory framework for vascular cambium development in Arabidopsis roots. Nat. Plants 5, 1033-1042.   DOI
47 Sarkar, A.K., Luijten, M., Miyashima, S., Lenhard, M., Hashimoto, T., Nakajima, K., Scheres, B., Heidstra, R., and Laux, T. (2007). Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446, 811-814.   DOI
48 Zhou, F., Emonet, A., Tendon, V.D., Marhavy, P., Wu, D., Lahaye, T., and Geldner, N. (2020). Co-incidence of damage and microbial patterns controls localized immune responses in roots. Cell 180, 440-453.e18.   DOI
49 Zipfel, C., Robatzek, S., Navarro, L., Oakeley, E.J., Jones, J.D.G., Felix, G., and Boller, T. (2004). Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428, 764-767.   DOI
50 Aichinger, E., Kornet, N., Friedrich, T., and Laux, T. (2012). Plant stem cell niches. Annu. Rev. Plant Biol. 63, 615-636.   DOI
51 Yamaguchi, Y., Huffaker, A., Bryan, A.C., Tax, F.E., and Ryan, C.A. (2010). PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22, 508-522.   DOI
52 Sevilem, I., Miyashima, S., and Helariutta, Y. (2013). Cell-to-cell communication via plasmodesmata in vascular plants. Cell Adh. Migr. 7, 27-32.   DOI
53 Sabatini, S., Heidstra, R., Wildwater, M., and Scheres, B. (2003). SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev. 17, 354-358.   DOI