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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)
  • 투고 : 2021.07.30
  • 심사 : 2021.09.22
  • 발행 : 2021.11.30

초록

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.

키워드

과제정보

We thank the members of the Lee lab for assisting in the experiments at various stages. This work was supported by the grants NRF-2018R1A5A1023599 to J.Y.L. and C.S. and NRF-2021R1A2C3006061 to J.Y.L. from National Research Foundation of Korea. S.D. was supported by the Brain Korea 21 Plus Program. H.K. was supported by WooDuk Foundation.

참고문헌

  1. 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. https://doi.org/10.3390/ijms21030963
  2. Aichinger, E., Kornet, N., Friedrich, T., and Laux, T. (2012). Plant stem cell niches. Annu. Rev. Plant Biol. 63, 615-636. https://doi.org/10.1146/annurev-arplant-042811-105555
  3. 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. https://doi.org/10.1016/j.cell.2004.09.018
  4. 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. https://doi.org/10.1093/jxb/erv180
  5. 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. https://doi.org/10.1093/jxb/ert330
  6. 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. https://doi.org/10.1093/jxb/eru366
  7. 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. https://doi.org/10.1016/j.cub.2011.04.017
  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. https://doi.org/10.1038/s41477-021-00874-5
  9. 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. https://doi.org/10.1016/j.cell.2016.01.044
  10. 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. https://doi.org/10.1016/j.tplants.2014.09.007
  11. 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. https://doi.org/10.1038/nrm.2015.6
  12. 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. https://doi.org/10.1242/dev.119.1.71
  13. 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. https://doi.org/10.1016/j.cub.2020.12.048
  14. 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. https://doi.org/10.4161/psb.4.6.8697
  15. 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. https://doi.org/10.1146/annurev-phyto-080516-035623
  16. 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. https://doi.org/10.1371/journal.ppat.1004331
  17. 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. https://doi.org/10.1073/pnas.0603727103
  18. 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. https://doi.org/10.2307/3870862
  19. 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. https://doi.org/10.1038/s41598-017-10634-1
  20. 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. https://doi.org/10.1080/15592324.2018.1451707
  21. 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. https://doi.org/10.1105/tpc.18.00757
  22. 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. https://doi.org/10.1105/tpc.19.00455
  23. 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. https://doi.org/10.1242/dev.127613
  24. 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. https://doi.org/10.1073/pnas.0510607103
  25. 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. https://doi.org/10.1111/jipb.12171
  26. 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. https://doi.org/10.1126/science.1118875
  27. 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. https://doi.org/10.1105/tpc.109.069658
  28. 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
  29. 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. https://doi.org/10.1111/nph.17064
  30. 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. https://doi.org/10.3389/fpls.2019.01741
  31. Perini, S., Mambro, R., and Sabatini, S. (2012). Growth and development of the root apical meristem. Curr. Opin. Plant Biol. 15, 17-23. https://doi.org/10.1016/j.pbi.2011.10.006
  32. 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. https://doi.org/10.1371/journal.pone.0185808
  33. 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. https://doi.org/10.1016/j.cub.2021.04.057
  34. 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. https://doi.org/10.3389/fpls.2020.00570
  35. 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. https://doi.org/10.1105/tpc.20.00154
  36. 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. https://doi.org/10.1101/gad.252503
  37. 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. https://doi.org/10.1038/nature05703
  38. Scheres, B. (2007). Stem-cell niches: nursery rhymes across kingdoms. Nat. Rev. Mol. Cell Biol. 8, 345-354. https://doi.org/10.1038/nrm2164
  39. 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. https://doi.org/10.1371/journal.pgen.1004973
  40. 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. https://doi.org/10.1016/j.pbi.2020.08.002
  41. 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. https://doi.org/10.3389/fpls.2021.632078
  42. Sevilem, I., Miyashima, S., and Helariutta, Y. (2013). Cell-to-cell communication via plasmodesmata in vascular plants. Cell Adh. Migr. 7, 27-32. https://doi.org/10.4161/cam.22126
  43. 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. https://doi.org/10.1016/j.cub.2018.12.041
  44. 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. https://doi.org/10.1038/s41586-018-0837-0
  45. Stadler, R. and Sauer, N. (1996). The Arabidopsis thaliana AtSUC2 gene is specifically expressed in companion cells. Bot. Acta 109, 299-306. https://doi.org/10.1111/j.1438-8677.1996.tb00577.x
  46. 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. https://doi.org/10.1073/pnas.1707400114
  47. Yamaguchi, Y. and Huffaker, A. (2011). Endogenous peptide elicitors in higher plants. Curr. Opin. Plant Biol. 14, 351-357. https://doi.org/10.1016/j.pbi.2011.05.001
  48. 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. https://doi.org/10.1105/tpc.109.068874
  49. 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. https://doi.org/10.1016/j.cub.2021.05.036
  50. 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. https://doi.org/10.1038/s41477-019-0522-9
  51. 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. https://doi.org/10.1016/j.cell.2020.01.013
  52. 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. https://doi.org/10.1105/tpc.112.102210
  53. 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. https://doi.org/10.1038/nature02485