The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Arabidopsis MORC1 and MED9 Interact to Regulate Defense Gene Expression and Plant Fitness

  • Received : 2024.07.22
  • Accepted : 2024.08.11
  • Published : 2024.10.01
Download PDF
⟨ Previous Next ⟩

Abstract

Arabidopsis MORC1 (Microrchidia) is required for multiple levels of immunity. We identified 14 MORC1-interacting proteins (MIPs) via yeast two-hybrid screening, eight of which have confirmed or putative nuclear-associated functions. While a few MIP mutants displayed altered bacterial resistance, MIP13 was unusual. The MIP13 mutant was susceptible to Pseudomonas syringae, but when combined with morc1/2, it regained wild-type resistance; notably, morc1/2 is susceptible to the same pathogen. MIP13 encodes MED9, a mediator complex component that interfaces with RNA polymerase II and transcription factors. Expression analysis of defense genes PR1, PR2, and PR5 in response to avirulent P. syringae revealed that morc1/2 med9 expressed these genes in a slow but sustained manner, unlike its lower-order mutants. This expression pattern may explain the restored resistance and suggests that the interplay of MORC1/2 and MED9 might be important in curbing defense responses to maintain fitness. Indeed, repeated challenges with avirulent P. syringae triggered significant growth inhibition in morc1/2 med9, indicating that MED9 and MORC1 may play an important role in balancing defense and growth. Furthermore, the in planta interaction of MED9 and MORC1 occurred 24 h, not 6 h, post-infection, suggesting that the interaction functions late in the defense signaling. Our study reveals a complex interplay between MORC1 and MED9 in maintaining an optimal balance between defense and growth in Arabidopsis.

Keywords

Acknowledgement

We thank Nicole Beisel for her assistance in constructing the clone, and to Angela Kang for reviewing the manuscript. This work was supported by the National Science Foundation (IOS-1553613, H.K).

References

  1. Allen, B. L. and Taatjes, D. J. 2015. The Mediator complex: a central integrator of transcription. Nat. Rev. Mol. Cell Biol. 16:155-166. 
  2. An, C. and Mou, Z. 2013. The function of the Mediator complex in plant immunity. Plant Signal. Behav. 8:e23182.
  3. Bassil, E., Tajima, H., Liang, Y.-C., Ohto, M.-A., Ushijima, K., Nakano, R., Esumi, T., Coku, A., Belmonte, M. and Blumwald, E. 2011. The Arabidopsis Na+ /H+  antiporters NHX1 and NHX2 control vacuolar pH and K+  homeostasis to regulate growth, flower development, and reproduction. Plant Cell 23:3482-3497. 
  4. Bonawitz, N. D., Kim, J. I., Tobimatsu, Y., Ciesielski, P. N., Anderson, N. A., Ximenes, E., Maeda, J., Ralph, J., Donohoe, B. S., Ladisch, M. and Chapple, C. 2014. Disruption of Mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant. Nature 509:376-380. 
  5. Bonfig, K. B., Schreiber, U., Gabler, A., Roitsch, T. and Berger, S. 2006. Infection with virulent and avirulent P. syringae strains differentially affects photosynthesis and sink metabolism in Arabidopsis leaves. Planta 225:1-12. 
  6. Bordiya, Y., Zheng, Y., Nam, J.-C., Bonnard, A. C., Choi, H. W., Lee, B.-K., Kim, J., Klessig, D. F., Fei, Z. and Kang, H.-G. 2016. Pathogen infection and MORC proteins affect chromatin accessibility of transposable elements and expression of their proximal genes in Arabidopsis. Mol. Plant-Microbe Interact. 29:674-687. 
  7. Boyer, L. A., Latek, R. R. and Peterson, C. L. 2004. The SANT domain: a unique histone-tail-binding module? Nat. Rev. Mol. Cell Biol. 5:158-163. 
  8. Brabbs, T. R., He, Z., Hogg, K., Kamenski, A., Li, Y., Paszkiewicz, K. H., Moore, K. A., O'Toole, P., Graham, I. A. and Jones, L. 2013. The stochastic silencing phenotype of Arabidopsis morc6 mutants reveals a role in efficient RNA-directed DNA methylation. Plant J. 75:836-846. 
  9. Buendia-Monreal, M. and Gillmor, C. S. 2016. Mediator: a key regulator of plant development. Dev. Biol. 419:7-18. 
  10. Burdon, J. J. and Thrall, P. H. 2003. The fitness costs to plants of resistance to pathogens. Genome Biol. 4:227. 
  11. Caillaud, M.-C., Asai, S., Rallapalli, G., Piquerez, S., Fabro, G. and Jones, J. D. G. 2013. A downy mildew effector attenuates salicylic acid-triggered immunity in Arabidopsis by interacting with the host mediator complex. PLoS Biol. 11:e1001732. 
  12. Cambiagno, D. A., Torres, J. R. and Alvarez, M. E. 2021. Convergent epigenetic mechanisms avoid constitutive expression of immune receptor gene subsets. Front. Plant Sci. 12:703667. 
  13. Campos, M. L., Yoshida, Y., Major, I. T., de Oliveira Ferreira, D., Weraduwage, S. M., Froehlich, J. E., Johnson, B. F., Kramer, D. M., Jander, G., Sharkey, T. D. and Howe, G. A. 2016. Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs. Nat. Commun. 7:12570. 
  14. Chan, C. and Zimmerli, L. 2019. The histone demethylase IBM1 positively regulates Arabidopsis immunity by control of defense gene expression. Front. Plant Sci. 10:1587. 
  15. Chen, R., Jiang, H., Li, L., Zhai, Q., Qi, L., Zhou, W., Liu, X., Li, H., Zheng, W., Sun, J. and Li, C. 2012. The Arabidopsis mediator subunit MED25 differentially regulates jasmonate and abscisic acid signaling through interacting with the MYC2 and ABI5 transcription factors. Plant Cell 24:2898-2916. 
  16. Chisholm, S. T., Coaker, G., Day, B. and Staskawicz, B. J. 2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803-814. 
  17. Conaway, R. C. and Conaway, J. W. 2011. Origins and activity of the Mediator complex. Semin. Cell Dev. Biol. 22:729-734. 
  18. Daviere, J.-M. and Achard, P. 2013. Gibberellin signaling in plants. Development 140:1147-1151. 
  19. Dempsey, D. A., Pathirana, M. S., Wobbe, K. K. and Klessig, D. F. 1997. Identification of an Arabidopsis locus required for resistance to turnip crinkle virus. Plant J. 11:301-311. 
  20. Dhawan, R., Luo, H., Foerster, A. M., Abuqamar, S., Du, H.-N., Briggs, S. D., Mittelsten Scheid, O. and Mengiste, T. 2009. HISTONE MONOUBIQUITINATION1 interacts with a subunit of the mediator complex and regulates defense against necrotrophic fungal pathogens in Arabidopsis. Plant Cell 21:1000-1019. 
  21. Droge-Laser, W., Snoek, B. L., Snel, B. and Weiste, C. 2018. The Arabidopsis bZIP transcription factor family: an update. Curr. Opin. Plant Biol. 45:36-49. 
  22. Ebbs, M. L. and Bender, J. 2006. Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 18:1166-1176. 
  23. Fallath, T., Kidd, B. N., Stiller, J., Davoine, C., Bjorklund, S., Manners, J. M., Kazan, K. and Schenk, P. M. 2017. MEDIATOR18 and MEDIATOR20 confer susceptibility to Fusarium oxysporum in Arabidopsis thaliana. PLoS ONE 12:e0176022. 
  24. Fan, J., Crooks, C. and Lamb, C. 2008. High-throughput quantitative luminescence assay of the growth in planta of Pseudomonas syringae chromosomally tagged with Photorhabdus luminescens luxCDABE. Plant J. 53:393-399. 
  25. Gangappa, S. N., Berriri, S. and Kumar, S. V. 2017. PIF4 coordinates thermosensory growth and immunity in Arabidopsis. Curr. Biol. 27:243-249. 
  26. Gieni, R. S. and Hendzel, M. J. 2009. Actin dynamics and functions in the interphase nucleus: moving toward an understanding of nuclear polymeric actin. Biochem. Cell Biol. 87:283-306. 
  27. Gonzalez, D., Bowen, A. J., Carroll, T. S. and Conlan, R. S. 2007. The transcription corepressor LEUNIG interacts with the histone deacetylase HDA19 and mediator components MED14 (SWP) and CDK8 (HEN3) to repress transcription. Mol. Cell. Biol. 27:5306-5315. 
  28. Hammond-Kosack, K. E. and Jones, J. D. 1996. Resistance gene-dependent plant defense responses. Plant Cell 8:1773-1791. 
  29. He, Z., Webster, S. and He, S. Y. 2022. Growth-defense trade-offs in plants. Curr. Biol. 32:R634-R639. 
  30. Hoppmann, V., Thorstensen, T., Kristiansen, P. E., Veiseth, S. V., Rahman, M. A., Finne, K., Aalen, R. B. and Aasland, R. 2011. The CW domain, a new histone recognition module in chromatin proteins. EMBO J. 30:1939-1952. 
  31. Huot, B., Yao, J., Montgomery, B. L. and He, S. Y. 2014. Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol. Plant 7:1267-1287. 
  32. Iyer, L. M., Abhiman, S. and Aravind, L. 2008. MutL homologs in restriction-modification systems and the origin of eukaryotic MORC ATPases. Biol. Direct 3:8. 
  33. Jackson, J. P., Lindroth, A. M., Cao, X. and Jacobsen, S. E. 2002. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416:556-560. 
  34. Jones, J. D. G. and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329. 
  35. Kang, H.-G., Choi, H. W., von Einem, S., Manosalva, P., Ehlers, K., Liu, P.-P., Buxa, S. V., Moreau, M., Mang, H.-G., Kachroo, P., Kogel, K.-H. and Klessig, D. F. 2012. CRT1 is a nuclear-translocated MORC endonuclease that participates in multiple levels of plant immunity. Nat. Commun. 3:1297. 
  36. Kang, H.-G. and Klessig, D. F. 2005. Salicylic acid-inducible Arabidopsis CK2-like activity phosphorylates TGA2. Plant Mol. Biol. 57:541-557. 
  37. Kang, H.-G., Kuhl, J. C., Kachroo, P. and Klessig, D. F. 2008. CRT1, an Arabidopsis ATPase that interacts with diverse resistance proteins and modulates disease resistance to turnip crinkle virus. Cell Host Microbe 3:48-57. 
  38. Kang, H.-G., Oh, C.-S., Sato, M., Katagiri, F., Glazebrook, J., Takahashi, H., Kachroo, P., Martin, G. B. and Klessig, D. F. 2010. Endosome-associated CRT1 functions early in resistance gene-mediated defense signaling in Arabidopsis and tobacco. Plant Cell 22:918-936. 
  39. Karasov, T. L., Chae, E., Herman, J. J. and Bergelson, J. 2017. Mechanisms to mitigate the trade-off between growth and defense. Plant Cell 29:666-680. 
  40. Kelleher, R. J. 3rd, Flanagan, P. M. and Kornberg, R. D. 1990. A novel mediator between activator proteins and the RNA polymerase II transcription apparatus. Cell 61:1209-1215. 
  41. Kidd, B. N., Cahill, D. M., Manners, J. M., Schenk, P. M. and Kazan, K. 2011. Diverse roles of the Mediator complex in plants. Semin. Cell Dev. Biol. 22:741-748. 
  42. Kidd, B. N., Edgar, C. I., Kumar, K. K., Aitken, E. A., Schenk, P. M., Manners, J. M. and Kazan, K. 2009. The mediator complex subunit PFT1 is a key regulator of jasmonate-dependent defense in Arabidopsis. Plant Cell 21:2237-2252. 
  43. Kim, H., Yen, L., Wongpalee, S. P., Kirshner, J. A., Mehta, N., Xue, Y., Johnston, J. B., Burlingame, A. L., Kim, J. K., Loparo, J. J. and Jacobsen, S. E. 2019. The gene-silencing protein MORC-1 topologically entraps DNA and forms multimeric assemblies to cause DNA compaction. Mol. Cell 75:700-710. 
  44. Koch, A., Kang, H.-G., Steinbrenner, J., Dempsey, D. A., Klessig, D. F. and Kogel, K.-H. 2017. MORC proteins: novel players in plant and animal health. Front. Plant Sci. 8:1720. 
  45. Li, F., Cheng, C., Cui, F., de Oliveira, M. V., Yu, X., Meng, X., Intorne, A. C., Babilonia, K., Li, M., Li, B., Chen, S., Ma, X., Xiao, S., Zheng, Y., Fei, Z., Metz, R. P., Johnson, C. D., Koiwa, H., Sun, W., Li, Z., de Souza Filho, G. A., Shan, L. and He, P. 2014. Modulation of RNA polymerase II phosphorylation downstream of pathogen perception orchestrates plant immunity. Cell Host Microbe 16:748-758. 
  46. Liu, Z.-W., Shao, C.-R., Zhang, C.-J., Zhou, J.-X., Zhang, S.-W., Li, L., Chen, S., Huang, H.-W., Cai, T. and He, X.-J. 2014. The SET domain proteins SUVH2 and SUVH9 are required for Pol V occupancy at RNA-directed DNA methylation loci. PLoS Genet. 10:e1003948. 
  47. Lorkovic, Z. J., Naumann, U., Matzke, A. J. M. and Matzke, M. 2012. Involvement of a GHKL ATPase in RNA-directed DNA methylation in Arabidopsis thaliana. Curr. Biol. 22:933-938. 
  48. Malik, N., Agarwal, P. and Tyagi, A. 2017. Emerging functions of multi-protein complex Mediator with special emphasis on plants. Crit. Rev. Biochem. Mol. Biol. 52:475-502. 
  49. Malinova, I., Mahlow, S., Alseekh, S., Orawetz, T., Fernie, A. R., Baumann, O., Steup, M. and Fettke, J. 2014. Double knockout mutants of Arabidopsis grown under normal conditions reveal that the plastidial phosphorylase isozyme participates in transitory starch metabolism. Plant Physiol. 164:907-921. 
  50. Menke, F. L. H., Kang, H.-G., Chen, Z., Park, J. M., Kumar, D. and Klessig, D. F. 2005. Tobacco transcription factor WRKY1 is phosphorylated by the MAP kinase SIPK and mediates HR-like cell death in tobacco. Mol. Plant-Microbe Interact. 18:1027-1034. 
  51. Mine, A., Seyfferth, C., Kracher, B., Berens, M. L., Becker, D. and Tsuda, K. 2018. The defense phytohormone signaling network enables rapid, high-amplitude transcriptional reprogramming during effector-triggered immunity. Plant Cell 30:1199-1219. 
  52. Moissiard, G., Bischof, S., Husmann, D., Pastor, W. A., Hale, C. J., Yen, L., Stroud, H., Papikian, A., Vashisht, A. A., Wohlschlegel, J. A. and Jacobsen, S. E. 2014. Transcriptional gene silencing by Arabidopsis microrchidia homologues involves the formation of heteromers. Proc. Natl. Acad. Sci. U. S. A. 111:7474-7479. 
  53. Moissiard, G., Cokus, S. J., Cary, J., Feng, S., Billi, A. C., Stroud, H., Husmann, D., Zhan, Y., Lajoie, B. R., McCord, R. P., Hale, C. J., Feng, W., Michaels, S. D., Frand, A. R., Pellegrini, M., Dekker, J., Kim, J. K. and Jacobsen, S. E. 2012. MORC family ATPases required for heterochromatin condensation and gene silencing. Science 336:1448-1451. 
  54. Navarro, L., Bari, R., Achard, P., Lison, P., Nemri, A., Harberd, N. P. and Jones, J. D. G. 2008. DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr. Biol. 18:650-655. 
  55. Ngou, B. P. M., Ahn, H.-K., Ding, P. and Jones, J. D. G. 2021. Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature 592:110-115. 
  56. Nicolau, M., Picault, N., Descombin, J., Jami-Alahmadi, Y., Feng, S., Bucher, E., Jacobsen, S. E., Deragon, J.-M., Wohlschlegel, J. and Moissiard, G. 2020. The plant mobile domain proteins MAIN and MAIL1 interact with the phosphatase PP7L to regulate gene expression and silence transposable elements in Arabidopsis thaliana. PLoS Genet. 16:e1008324. 
  57. Phan, N. Q., Kim, S.-J. and Bassham, D. C. 2008. Overexpression of Arabidopsis sorting nexin AtSNX2b inhibits endocytic trafficking to the vacuole. Mol. Plant 1:961-976. 
  58. Pujara, D. S., Kim, S.-I., Nam, J. C., Mayorga, J., Elmore, I., Kumar, M., Koiwa, H. and Kang, H.-G. 2021. Imaging-based resistance assay using enhanced luminescence-tagged Pseudomonas syringae reveals a complex epigenetic network in plant defense signaling pathways. Mol. Plant-Microbe Interact. 34:990-1000. 
  59. Richard, M. M. S., Gratias, A., Meyers, B. C. and Geffroy, V. 2018. Molecular mechanisms that limit the costs of NLR-mediated resistance in plants. Mol. Plant Pathol. 19:2516-2523. 
  60. Samanta, S. and Thakur, J. K. 2015a. Importance of Mediator complex in the regulation and integration of diverse signaling pathways in plants. Front. Plant Sci. 6:757. 
  61. Samanta, S. and Thakur, J. K. 2015b. Role of plant mediator complex in stress response. In: Elucidation of abiotic stress signaling in plants: functional genomics perspectives, ed. by G. K. Pandey, Vol. 2, pp. 3-28. Springer, New York, NY, USA. 
  62. Shah, J., Tsui, F. and Klessig, D. F. 1997. Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Mol. Plant-Microbe Interact. 10:69-78. 
  63. Sun, J., Chen, Q., Qi, L., Jiang, H., Li, S., Xu, Y., Liu, F., Zhou, W., Pan, J., Li, X., Palme, K. and Li, C. 2011. Jasmonate modulates endocytosis and plasma membrane accumulation of the Arabidopsis PIN2 protein. New Phytol. 191:360-375. 
  64. Tao, Y., Xie, Z., Chen, W., Glazebrook, J., Chang, H.-S., Han, B., Zhu, T., Zou, G. and Katagiri, F. 2003. Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317-330. 
  65. Tian, D., Traw, M. B., Chen, J. Q., Kreitman, M. and Bergelson, J. 2003. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74-77. 
  66. Tsuda, K., Sato, M., Stoddard, T., Glazebrook, J. and Katagiri, F. 2009. Network properties of robust immunity in plants. PLoS Genet. 5:e1000772. 
  67. van Hulten, M., Pelser, M., van Loon, L. C., Pieterse, C. M. J. and Ton, J. 2006. Costs and benefits of priming for defense in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 103:5602-5607. 
  68. Wang, C., Yao, J., Du, X., Zhang, Y., Sun, Y., Rollins, J. A. and Mou, Z. 2015. The Arabidopsis mediator complex subunit16 is a key component of basal resistance against the necrotrophic fungal pathogen Sclerotinia sclerotiorum. Plant Physiol. 169:856-872. 
  69. Wood, A. J., Severson, A. F. and Meyer, B. J. 2010. Condensin and cohesin complexity: the expanding repertoire of functions. Nat. Rev. Genet. 11:391-404. 
  70. Yang, Y., Li, L. and Qu, L.-J. 2016. Plant mediator complex and its critical functions in transcription regulation. J. Integr. Plant Biol. 58:106-118. 
  71. Zhang, J., Yuan, J., Lin, J., Chen, L., You, L.-Y., Chen, S., Peng, L., Wang, C.-H., Du, J. and Duan, C.-G. 2023. Molecular basis of locus-specific H3K9 methylation catalyzed by SUVH6 in plants. Proc. Natl. Acad. Sci. U. S. A. 120:e2211155120. 
  72. Zhang, X., Wang, C., Zhang, Y., Sun, Y. and Mou, Z. 2012. The Arabidopsis mediator complex subunit16 positively regulates salicylate-mediated systemic acquired resistance and jasmonate/ethylene-induced defense pathways. Plant Cell 24:4294-4309. 
  73. Zhang, X., Yao, J., Zhang, Y., Sun, Y. and Mou, Z. 2013. The Arabidopsis Mediator complex subunits MED14/SWP and MED16/SFR6/IEN1 differentially regulate defense gene expression in plant immune responses. Plant J. 75:484-497. 
  74. Zhu, X., Zhang, Y., Bjornsdottir, G., Liu, Z., Quan, A., Costanzo, M., Lopez, M. D., Westholm, J. O., Ronne, H., Boone, C., Gustafsson, C. M. and Myers, L. C. 2011. Histone modifications influence mediator interactions with chromatin. Nucleic Acids Res. 39:8342-8354. 
  75. Zipfel, C. and Felix, G. 2005. Plants and animals: a different taste for microbes? Curr. Opin. Plant Biol. 8:353-360.