The MAPK substrate MASS proteins regulate stomatal development in Arabidopsis

English version

Autoři: Xueyi Xue ^aff001; Chao Bian ^aff001; Xiaoyu Guo ^aff001; Rong Di ^aff002; Juan Dong ^aff001
Působiště autorů: The Waksman Institute of Microbiology, Rutgers, the State University of New Jersey; Piscataway, New Jersey, United States of America ^aff001; Department of Plant Biology, Rutgers, the State University of New Jersey, New Brunswick, New Jersey, United States of America ^aff002
Vyšlo v časopise: The MAPK substrate MASS proteins regulate stomatal development in Arabidopsis. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1008706
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008706

Souhrn

Stomata are specialized pores in the epidermis of the aerial parts of a plant, where stomatal guard cells close and open to regulate gas exchange with the atmosphere and restrict excessive water vapor from the plant. The production and patterning of the stomatal lineage cells in higher plants are influenced by the activities of the widely-used mitogen-activated protein kinase (MAPK) signaling components. The phenotype caused by the loss-of-function mutations suggested pivotal roles of the canonical MAPK pathway in the suppression of stomatal formation and regulation of stomatal patterning in Arabidopsis, whilst the cell type-specific manipulation of individual MAPK components revealed the existence of a positive impact on stomatal production. Among a large number of putative MAPK substrates in plants, the nuclear transcription factors SPEECHLESS (SPCH) and SCREAM (SCRM) are targets of MAPK 3 and 6 (MPK3/6) in the inhibition of stomatal formation. The polarity protein BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (BASL) is phosphorylated by MPK3/6 for localization and function in driving divisional asymmetries. Here, by functionally characterizing three MAPK SUBSTRATES IN THE STOMATAL LINEAGE (MASS) proteins, we establish that they are plasma membrane-associated, positive regulators of stomatal production. MPK6 can phosphorylate the MASS proteins in vitro and mutating the putative substrate sites interferes the subcellular partition and function of MASS in planta. Our fine-scale domain analyses identify critical subdomains of MASS2 required for specific subcellular localization and biological function, respectively. Furthermore, our data indicate that the MASS proteins may directly interact with the MAPKK Kinase YODA (YDA) at the plasma membrane. Thus, the deeply conserved MASS proteins are tightly connected with MAPK signaling in Arabidopsis to fine-tune stomatal production and patterning, providing a functional divergence of the YDA-MPK3/6 cascade in the regulation of plant developmental processes.

Klíčová slova:

Arabidopsis thaliana – Cell membranes – Epidermis – MAPK signaling cascades – Membrane proteins – Phosphorylation – Stomata – Plant cotyledon

Zdroje

1. Xu J, Zhang S. Mitogen-activated protein kinase cascades in signaling plant growth and development. Trends in plant science. 2015;20(1):56–64. Epub 2014/12/03. doi: 10.1016/j.tplants.2014.10.001 25457109.

2. de Zelicourt A, Colcombet J, Hirt H. The Role of MAPK Modules and ABA during Abiotic Stress Signaling. Trends in plant science. 2016;21(8):677–85. Epub 2016/05/05. doi: 10.1016/j.tplants.2016.04.004 27143288.

3. Meng X, Zhang S. MAPK cascades in plant disease resistance signaling. Annual review of phytopathology. 2013;51:245–66. Epub 2013/05/15. doi: 10.1146/annurev-phyto-082712-102314 23663002.

4. Cargnello M, Roux PP. Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiology and molecular biology reviews: MMBR. 2011;75(1):50–83. Epub 2011/03/05. doi: 10.1128/MMBR.00031-10 21372320; PubMed Central PMCID: PMC3063353.

5. Bergmann DC, Lukowitz W, Somerville CR. Stomatal development and pattern controlled by a MAPKK kinase. Science. 2004;304(5676):1494–7. doi: 10.1126/science.1096014 15178800

6. Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S. Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell. 2007;19(1):63–73. doi: 10.1105/tpc.106.048298 17259259; PubMed Central PMCID: PMC1820971.

7. Lampard GR, Lukowitz W, Ellis BE, Bergmann DC. Novel and expanded roles for MAPK signaling in Arabidopsis stomatal cell fate revealed by cell type-specific manipulations. Plant Cell. 2009;21(11):3506–17. doi: 10.1105/tpc.109.070110 19897669; PubMed Central PMCID: PMC2798322.

8. Lampard GR, Wengier DL, Bergmann DC. Manipulation of mitogen-activated protein kinase kinase signaling in the Arabidopsis stomatal lineage reveals motifs that contribute to protein localization and signaling specificity. The plant cell. 2014;26(8):3358–71. doi: 10.1105/tpc.114.127415 25172143

9. MacAlister CA, Ohashi-Ito K, Bergmann DC. Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. Nature. 2007;445(7127):537–40. doi: 10.1038/nature05491 17183265.

10. Pillitteri LJ, Sloan DB, Bogenschutz NL, Torii KU. Termination of asymmetric cell division and differentiation of stomata. Nature. 2007;445(7127):501–5. doi: 10.1038/nature05467 17183267.

11. Kanaoka MM, Pillitteri LJ, Fujii H, Yoshida Y, Bogenschutz NL, Takabayashi J, et al. SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to arabidopsis stomatal differentiation. Plant Cell. 2008;20(7):1775–85. doi: 10.1105/tpc.108.060848 18641265; PubMed Central PMCID: PMC2518248.

12. Lampard GR, MacAlister CA, Bergmann DC. Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science. 2008;322(5904):1113–6. doi: 10.1126/science.1162263 19008449

13. Li H, Ding Y, Shi Y, Zhang X, Zhang S, Gong Z, et al. MPK3- and MPK6-Mediated ICE1 Phosphorylation Negatively Regulates ICE1 Stability and Freezing Tolerance in Arabidopsis. Dev Cell. 2017;43(5):630–42 e4. doi: 10.1016/j.devcel.2017.09.025 29056553.

14. Putarjunan A, Ruble J, Srivastava A, Zhao C, Rychel AL, Hofstetter AK, et al. Bipartite anchoring of SCREAM enforces stomatal initiation by coupling MAP kinases to SPEECHLESS. Nature plants. 2019;5(7):742–54. Epub 2019/06/27. doi: 10.1038/s41477-019-0440-x 31235876; PubMed Central PMCID: PMC6668613.

15. Sörensson C, Lenman M, Veide-Vilg J, Schopper S, Ljungdahl T, Grøtli M, et al. Determination of primary sequence specificity of Arabidopsis MAPKs MPK3 and MPK6 leads to identification of new substrates. Biochemical Journal. 2012;446(2):271–8. doi: 10.1042/BJ20111809 22631074

16. Andreasson E, Jenkins T, Brodersen P, Thorgrimsen S, Petersen NH, Zhu S, et al. The MAP kinase substrate MKS1 is a regulator of plant defense responses. The EMBO journal. 2005;24(14):2579–89. Epub 2005/07/02. doi: 10.1038/sj.emboj.7600737 15990873; PubMed Central PMCID: PMC1176463.

17. Singh R, Lee MO, Lee JE, Choi J, Park JH, Kim EH, et al. Rice mitogen-activated protein kinase interactome analysis using the yeast two-hybrid system. Plant physiology. 2012;160(1):477–87. Epub 2012/07/13. doi: 10.1104/pp.112.200071 22786887; PubMed Central PMCID: PMC3440221.

18. Hoehenwarter W, Thomas M, Nukarinen E, Egelhofer V, Rohrig H, Weckwerth W, et al. Identification of novel in vivo MAP kinase substrates in Arabidopsis thaliana through use of tandem metal oxide affinity chromatography. Molecular & cellular proteomics: MCP. 2013;12(2):369–80. Epub 2012/11/23. doi: 10.1074/mcp.M112.020560 23172892; PubMed Central PMCID: PMC3567860.

19. Shpak ED, McAbee JM, Pillitteri LJ, Torii KU. Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science. 2005;309(5732):290–3. doi: 10.1126/science.1109710 16002616

20. Nadeau JA, Sack FD. Control of stomatal distribution on the Arabidopsis leaf surface. Science. 2002;296(5573):1697–700. Epub 2002/06/01. doi: 10.1126/science.1069596 12040198.

21. Meng X, Chen X, Mang H, Liu C, Yu X, Gao X, et al. Differential function of Arabidopsis SERK family receptor-like kinases in stomatal patterning. Current Biology. 2015;25(18):2361–72. doi: 10.1016/j.cub.2015.07.068 26320950

22. He K, Gou X, Yuan T, Lin H, Asami T, Yoshida S, et al. BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways. Current Biology. 2007;17(13):1109–15. doi: 10.1016/j.cub.2007.05.036 17600708

23. Roux M, Schwessinger B, Albrecht C, Chinchilla D, Jones A, Holton N, et al. The Arabidopsis leucine-rich repeat receptor–like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. The Plant Cell. 2011;23(6):2440–55. doi: 10.1105/tpc.111.084301 21693696

24. Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W. Paternal control of embryonic patterning in Arabidopsis thaliana. Science. 2009;323(5920):1485–8. doi: 10.1126/science.1167784 19286558

25. Yuan G-L, Li H-J, Yang W-C. The integration of Gβ and MAPK signaling cascade in zygote development. Scientific reports. 2017;7(1):8732. doi: 10.1038/s41598-017-08230-4 28821747

26. Kim T-W, Michniewicz M, Bergmann DC, Wang Z-Y. Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature. 2012;482(7385):419. doi: 10.1038/nature10794 22307275

27. Houbaert A, Zhang C, Tiwari M, Wang K, de Marcos Serrano A, Savatin DV, et al. POLAR-guided signalling complex assembly and localization drive asymmetric cell division. Nature. 2018;563(7732):574–8. Epub 2018/11/16. doi: 10.1038/s41586-018-0714-x 30429609.

28. Zhang Y, Wang P, Shao W, Zhu J-K, Dong J. The BASL Polarity Protein Controls a MAPK Signaling Feedback Loop in Asymmetric Cell Division. Developmental Cell. 2015;33(2):136–49. doi: 10.1016/j.devcel.2015.02.022 25843888

29. Mao Y, Zhang H, Xu N, Zhang B, Gou F, Zhu JK. Application of the CRISPR-Cas system for efficient genome engineering in plants. Mol Plant. 2013;6(6):2008–11. doi: 10.1093/mp/sst121 23963532; PubMed Central PMCID: PMC3916745.

30. Magee T, Seabra MC. Fatty acylation and prenylation of proteins: what's hot in fat. Current opinion in cell biology. 2005;17(2):190–6. doi: 10.1016/j.ceb.2005.02.003 15780596

31. Niittyla T, Fuglsang AT, Palmgren MG, Frommer WB, Schulze WX. Temporal analysis of sucrose-induced phosphorylation changes in plasma membrane proteins of Arabidopsis. Molecular & cellular proteomics: MCP. 2007;6(10):1711–26. Epub 2007/06/26. doi: 10.1074/mcp.M700164-MCP200 17586839.

32. Xu J, Xie J, Yan C, Zou X, Ren D, Zhang S. A chemical genetic approach demonstrates that MPK3/MPK6 activation and NADPH oxidase-mediated oxidative burst are two independent signaling events in plant immunity. The Plant journal: for cell and molecular biology. 2014;77(2):222–34. Epub 2013/11/20. doi: 10.1111/tpj.12382 24245741; PubMed Central PMCID: PMC4017028.

33. Hashimoto M, Komatsu K, Maejima K, Okano Y, Shiraishi T, Ishikawa K, et al. Identification of three MAPKKKs forming a linear signaling pathway leading to programmed cell death in Nicotiana benthamiana. BMC plant biology. 2012;12(1):103.

34. Krysan PJ, Colcombet J. Cellular Complexity in MAPK Signaling in Plants: Questions and Emerging Tools to Answer Them. Frontiers in plant science. 2018;9:1674. Epub 2018/12/13. doi: 10.3389/fpls.2018.01674 30538711; PubMed Central PMCID: PMC6277691.

35. Zhang Y, Guo X, Dong J. Phosphorylation of the Polarity Protein BASL Differentiates Asymmetric Cell Fate through MAPKs and SPCH. Current biology: CB. 2016;26(21):2957–65. Epub 2016/10/18. doi: 10.1016/j.cub.2016.08.066 27746029; PubMed Central PMCID: PMC5102774.

36. Freitas N, Cunha C. Mechanisms and signals for the nuclear import of proteins. Current genomics. 2009;10(8):550–7. Epub 2010/06/02. doi: 10.2174/138920209789503941 20514217; PubMed Central PMCID: PMC2817886.

37. Dong J, MacAlister CA, Bergmann DC. BASL controls asymmetric cell division in Arabidopsis. Cell. 2009;137(7):1320–30. Epub 2009/06/16. doi: 10.1016/j.cell.2009.04.018 19523675; PubMed Central PMCID: PMC4105981.

38. Nadeau JA, Sack FD. Stomatal development in Arabidopsis. The arabidopsis book. 2002;1:e0066. Epub 2002/01/01. doi: 10.1199/tab.0066 22303215; PubMed Central PMCID: PMC3243354.

39. Pillitteri LJ, Dong J. Stomatal development in Arabidopsis. The arabidopsis book. 2013;11:e0162. Epub 2013/07/19. doi: 10.1199/tab.0162 23864836; PubMed Central PMCID: PMC3711358.

40. Hara K, Kajita R, Torii KU, Bergmann DC, Kakimoto T. The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. Genes & development. 2007;21(14):1720–5. Epub 2007/07/20. doi: 10.1101/gad.1550707 17639078; PubMed Central PMCID: PMC1920166.

41. Lee JS, Kuroha T, Hnilova M, Khatayevich D, Kanaoka MM, McAbee JM, et al. Direct interaction of ligand-receptor pairs specifying stomatal patterning. Genes & development. 2012;26(2):126–36. Epub 2012/01/14. doi: 10.1101/gad.179895.111 22241782; PubMed Central PMCID: PMC3273837.

42. Richardson LG, Torii KU. Take a deep breath: peptide signalling in stomatal patterning and differentiation. Journal of experimental botany. 2013;64(17):5243–51. Epub 2013/09/03. doi: 10.1093/jxb/ert246 23997204.

43. Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant journal: for cell and molecular biology. 1998;16(6):735–43. Epub 1999/03/09. doi: 10.1046/j.1365-313x.1998.00343.x 10069079.

44. Zhang X, Henriques R, Lin SS, Niu QW, Chua NH. Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nature protocols. 2006;1(2):641–6. Epub 2007/04/05. doi: 10.1038/nprot.2006.97 17406292.

45. Zhang Y, Dong J. Imaging Spatial Reorganization of a MAPK Signaling Pathway Using the Tobacco Transient Expression System. Journal of visualized experiments: JoVE. 2016;(109). Epub 2016/03/31. doi: 10.3791/53790 27022690; PubMed Central PMCID: PMC4829033.

46. Kamat V, Rafique A. Designing binding kinetic assay on the bio-layer interferometry (BLI) biosensor to characterize antibody-antigen interactions. Anal Biochem. 2017;536:16–31. Epub 2017/08/15. doi: 10.1016/j.ab.2017.08.002 28802648.

47. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular biology and evolution. 2013;30(12):2725–9. Epub 2013/10/18. doi: 10.1093/molbev/mst197 24132122; PubMed Central PMCID: PMC3840312.

Článek High expression in maize pollen correlates with genetic contributions to pollen fitness as well as with coordinated transcription from neighboring transposable elements

Článek Dynamic localization of SPO11-1 and conformational changes of meiotic axial elements during recombination initiation of maize meiosis

Článek The plant mobile domain proteins MAIN and MAIL1 interact with the phosphatase PP7L to regulate gene expression and silence transposable elements in Arabidopsis thaliana

Článek Targeting mitochondrial and cytosolic substrates of TRIT1 isopentenyltransferase: Specificity determinants and tRNA-i6A37 profiles

Článek XPF-ERCC1 protects liver, kidney and blood homeostasis outside the canonical excision repair pathways

Článek Technical and social issues influencing the adoption of preprints in the life sciences

Článek The nanophthalmos protein TMEM98 inhibits MYRF self-cleavage and is required for eye size specification

Článek DNA methylation-mediated repression of exosomal miR-652-5p expression promotes oesophageal squamous cell carcinoma aggressiveness by targeting PARG and VEGF pathways

Článek Is imprinting the result of “friendly fire” by the host defense system?

Článek The coordinate actions of calcineurin and Hog1 mediate the stress response through multiple nodes of the cell cycle network

Článek XPF–ERCC1: Linchpin of DNA crosslink repair

Článek A missense variant in Mitochondrial Amidoxime Reducing Component 1 gene and protection against liver disease