Suppression of class I compensated cell enlargement by xs2 mutation is mediated by salicylic acid signaling
Autoři:
Fujikura Ushio aff001; Kazune Ezaki aff002; Gorou Horiguchi aff003; Mitsunori Seo aff004; Yuri Kanno aff004; Yuji Kamiya aff004; Michael Lenhard aff005; Hirokazu Tsukaya aff002; Ushio Fujikura aff001
Působiště autorů:
Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Japan
aff001; Graduate School of Science, The University of Tokyo, Japan
aff002; Department of Life Science, College of Science, Rikkyo University, Japan
aff003; RIKEN Center for Sustainable Resource Science, Japan
aff004; Institute for Biochemistry and Biology, University of Potsdam, Germany
aff005; Institut für Biochemie und Biologie, Universität Potsdam, Potsdam-Golm, Germany
aff005; Okazaki Institute for Integrative Bioscience, Japan
aff006
Vyšlo v časopise:
Suppression of class I compensated cell enlargement by xs2 mutation is mediated by salicylic acid signaling. PLoS Genet 16(6): e32767. doi:10.1371/journal.pgen.1008873
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008873
Souhrn
The regulation of leaf size has been studied for decades. Enhancement of post-mitotic cell expansion triggered by impaired cell proliferation in Arabidopsis is an important process for leaf size regulation, and is known as compensation. This suggests a key interaction between cell proliferation and cell expansion during leaf development. Several studies have highlighted the impact of this integration mechanism on leaf size determination; however, the molecular basis of compensation remains largely unknown. Previously, we identified extra-small sisters (xs) mutants which can suppress compensated cell enlargement (CCE) via a specific defect in cell expansion within the compensation-exhibiting mutant, angustifolia3 (an3). Here we revealed that one of the xs mutants, namely xs2, can suppress CCE not only in an3 but also in other compensation-exhibiting mutants erecta (er) and fugu2. Molecular cloning of XS2 identified a deleterious mutation in CATION CALCIUM EXCHANGER 4 (CCX4). Phytohormone measurement and expression analysis revealed that xs2 shows hyper activation of the salicylic acid (SA) response pathway, where activation of SA response can suppress CCE in compensation mutants. All together, these results highlight the regulatory connection which coordinates compensation and SA response.
Klíčová slova:
Arabidopsis thaliana – Cell proliferation – Gene expression – Leaf development – Leaves – Phenotypes – Plant hormones – Salicylic acid
Zdroje
1. Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG. Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol. 1999; 215: 407–419. doi: 10.1006/dbio.1999.9443 10545247
2. Ichihashi Y, Kawade K, Usami T, Horiguchi G, Takahashi T, Tsukaya H. Key proliferative activity in the junction between the leaf blade and leaf petiole of Arabidopsis. Plant Physiol. 2011; 157: 1151–1162. doi: 10.1104/pp.111.185066 21880932
3. White DW. PEAPOD regulates lamina size and curvature in Arabidopsis. Proc Natl Acad Sci U S A. 2006; 103: 13238–13243. doi: 10.1073/pnas.0604349103 16916932
4. Ichihashi Y, Horiguchi G, Gleissberg S, Tsukaya H. The bHLH transcription factor SPATULA controls final leaf size in Arabidopsis thaliana. Plant Cell Physiol. 2010; 51: 252–261. doi: 10.1093/pcp/pcp184 20040585
5. Nath U, Crawford BC, Carpenter R, Coen E. Genetic control of surface curvature. Science 2003; 299: 1404–1407. doi: 10.1126/science.1079354 12610308
6. Kazama T, Ichihashi Y, Murata S, Tsukaya H. The mechanism of cell cycle arrest front progression explained by a KLUH/CYP78A5-dependent mobile growth factor in developing leaves of Arabidopsis thaliana. Plant Cell Physiol. 2010; 51: 1046–1054. doi: 10.1093/pcp/pcq051 20395288
7. Beemster GT, Fiorani F, Inzé D. Cell cycle: the key to plant growth control? Trends Plant Sci. 2003; 8: 154–158. doi: 10.1016/S1360-1385(03)00046-3 12711226
8. Powell AE, Lenhard M. Control of organ size in plants. Curr Biol. 2012; 22: R360–R367. doi: 10.1016/j.cub.2012.02.010 22575478
9. Kierzkowski D, Runions A, Vuolo F, Strauss S, Lymbouridou R, Routier-Kierzkowska AL, et al. A growth-based framework for leaf shape development and diversity. Cell. 2019; 177: 1405–1418. doi: 10.1016/j.cell.2019.05.011 31130379
10. Tsukaya H. Interpretation of mutants in leaf morphology: genetic evidence for a compensatory system in leaf morphogenesis that provides a new link between cell and organismal theories. Int Rev Cytol. 2002; 217: 1–39. doi: 10.1016/s0074-7696(02)17011-2 12019561
11. Horiguchi G, Ferjani A, Fujikura U, Tsukaya H. Coordination of cell proliferation and cell expansion in the control of leaf size in Arabidopsis thaliana. J Plant Res. 2006; 119: 37–42. doi: 10.1007/s10265-005-0232-4 16284709
12. Tsukaya H. Mechanism of leaf-shape determination. Annu Rev Plant Biol. 2006; 57: 477–496. doi: 10.1146/annurev.arplant.57.032905.105320 16669771
13. Ferjani A, Horiguchi G, Yano S, Tsukaya H. Analysis of leaf development in fugu mutants of Arabidopsis reveals three compensation modes that modulate cell expansion in determinate organs. Plant Physiol. 2007; 144: 988–999. doi: 10.1104/pp.107.099325 17468216
14. Tsukaya H. Controlling size in multicellular organs: Focus on the leaf. PLoS Biol. 2008; 6: e174. doi: 10.1371/journal.pbio.0060174 18630989
15. Micol JL. Leaf development: Time to turn over a new leaf? Curr Opin Plant Biol. 2009; 12: 9–16. doi: 10.1016/j.pbi.2008.11.001 19109050
16. Ferjani A, Horiguchi G, Tsukaya H. Organ size control in Arabidopsis: insights from compensation studies. Plant Morphol. 2010; 22: 65–71. doi: 10.5685/plmorphol.22.65
17. Horiguchi G, Tsukaya H. Organ size regulation in plants: insights from compensation. Front Plant Sci. 2011; 2: 1–6. doi: 10.3389/fpls.2011.00001 22639570
18. Ferjani A, Ishikawa K, Asaoka M, Ishida M, Horiguchi G, Maeshima M, et al. Enhanced cell expansion in a KRP2 overexpressor is mediated by increased V-ATPase activity. Plant Cell Physiol. 2013a; 54: 1989–1998. doi: 10.1093/pcp/pct138 24068796
19. Ferjani A, Ishikawa K, Asaoka M, Ishida M, Horiguchi G, Maeshima M, Tsukaya H. Class III compensation, represented by KRP2 overexpression, depends on V-ATPase activity in proliferative cells. Plant Signal Behav. 2013b; 8:11. doi: 10.4161/psb.27204 24305734
20. Hisanaga T, Kawade K, Tsukaya H. Compensation: a key to clarifying the organ-level regulation of lateral organ size in plants. J Exp Bot. 2015; 66: 1055–1063. doi: 10.1093/jxb/erv028 25635111
21. Kawade K, Horiguchi G, Tsukaya H. Non-cell-autonomously coordinated organ size regulation in leaf development. Development. 2010; 137: 4221–4227. doi: 10.1242/dev.057117 21068059
22. Hisanaga T, Ferjani A, Horiguchi G, Ishikawa N, Fujikura U, Kubo M, et al. The ATM-dependent DNA damage response acts as an upstream trigger for compensation in the fas1 mutation during Arabidopsis leaf development. Plant Physiol. 2013; 162: 831–841. doi: 10.1104/pp.113.216796 23616603
23. Ferjani A, Horiguchi G, Tsukaya H. Keep an Eye on PPi: The Vacuolar-type H+-Pyrophosphatase regulates postgerminative development in Arabidopsis. Plant Cell. 2011; 23: 2895–2908. doi: 10.1105/tpc.111.085415 21862707
24. Ferjani A, Kawade K, Asaoka M, Oikawa A, Okada T, Mochizuki A, et al. Pyrophosphate inhibits gluconeogenesis by restricting UDP-glucose formation in vivo. Sci Rep. 2018; 8: 14696. doi: 10.1038/s41598-018-32894-1 30279540
25. Fujikura U, Horiguchi G, Ponce MR, Micol JL, Tsukaya H. Coordination of cell proliferation and cell expansion mediated by ribosome-related processes in the leaves of Arabidopsis thaliana. Plant J. 2009; 59: 499–508. doi: 10.1111/j.1365-313X.2009.03886.x 19392710
26. Fujikura U, Horiguchi G, Tsukaya H. Dissection of enhanced cell expansion processes in leaves triggered by a defect in cell proliferation, with reference to roles of endoreduplication. Plant Cell Physiol. 2007; 48: 278–286. doi: 10.1093/pcp/pcm002 17205970
27. Malamy J, Carr JP, Klessig DF, Raskin I. Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science. 1990; 250: 1002–1004. doi: 10.1126/science.250.4983.1002 17746925
28. Yalpani N, León J, Lawton MA, Raskin I. Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco. Plant Physiol. 1993; 103: 315–321. doi: 10.1104/pp.103.2.315 12231938
29. Carswell GK, Johnson CM, Shillito RD, Harms CT. O-acetylsalicylic acid promotes colony formation from protoplasts of an elite maize inbred. Plant Cell Rep. 1989; 8: 282–284. doi: 10.1007/BF00274130 24233226
30. Rate DN, Cuenca JV, Bowman GR, Guttman DS, Greenberg JT. The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defenses, and cell growth. Plant Cell. 1999; 11: 1695–1708. doi: 10.1105/tpc.11.9.1695 10488236
31. Rate DN, Greenberg JT. The Arabidopsis aberrant growth and death2 mutant shows resistance to Pseudomonas syringae and reveals a role for NPR1 in suppressing hypersensitive cell death. Plant J. 2001; 27: 203–211. doi: 10.1046/j.0960-7412.2001.1075umedoc.x 11532166
32. Vanacker H, Lu H, Rate DN, Greenberg JT. A role for salicylic acid and NPR1 in regulating cell growth in Arabidopsis. Plant J. 2001; 28: 209–216. doi: 10.1046/j.1365-313x.2001.01158.x 11722764
33. Morris J, Tian H, Park S, Sreevidya CS, Ward JM, Hirschi KD. AtCCX3 is an Arabidopsis endomembrane H+ -dependent K+ transporter. Plant Physiol. 2008; 148: 1474–1486. doi: 10.1104/pp.108.118810 18775974
34. Du L, Ali GS, Simons KA, Hou J, Yang T, Reddy A, Poovaiah B. Ca2+/calmodulin regulates salicylic-acid-mediated plant immunity. Nature. 2009; 457: 1154–1158. doi: 10.1038/nature07612 19122675
35. Xia J, Zhao H, Liu W, Li L, He Y. Role of cytokinin and salicylic acid in plant growth at low temperatures. Plant Growth Regul. 2009; 57: 211–221. doi: 10.1007/s10725-008-9338-8
36. Cui H, Tsuda K, Parker JE. Effector-triggered immunity: from pathogen perception to robust defense. Annu Rev Plant Biol. 2015; 66: 487–511. doi: 10.1146/annurev-arplant-050213-040012 25494461
37. Li J, Brader G, Palva ET. The WRKY70 transcription factor: A node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell. 2004; 16: 319–331. doi: 10.1105/tpc.016980 14742872
38. Li J, Brader G, Kariola T, Palva ET. WRKY70 modulates the selection of signaling pathways in plant defense. Plant J. 2006; 46: 477–491. doi: 10.1111/j.1365-313X.2006.02712.x 16623907
39. Overmyer K, Brosché M, Kangasjärvi J. Reactive oxygen species and hormonal control of cell death. Trends Plant Sci. 2003; 8: 335–342. doi: 10.1016/S1360-1385(03)00135-3 12878018
40. Chen Z, Silva H, Klessig DF. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science. 1993; 262: 1883–1886. doi: 10.1126/science.8266079 8266079
41. Rao MV, Paliyath G, Ormrod DP, Murr DP, Watkins CB. Influence of salicylic acid on H2O2 production, oxidative stress and H2O2-metabolizing enzymes. Plant Physiol. 1997: 115: 137–149. doi: 10.1104/pp.115.1.137 9306697
42. Rao MV, Lee HI, Creelman RA, Mullet JE, Davis KR. Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell. 2000; 12: 1633–1646. doi: 10.1105/tpc.12.9.1633 11006337
43. Urquhart W, Gunawardena AH, Moeder W, Ali R, Berkowitz GA, Yoshioka K. The chimeric cyclic nucleotide- gated ion channel ATCNGC11/12 constitutively induces programmed cell death in a Ca2+ dependent manner. Plant Mol Biol. 2007; 65: 747–761. doi: 10.1007/s11103-007-9239-7 17885810
44. Leng Q, Mercier RW, Yao W, Berkowitz GA. Cloning and first functional characterization of a plant cyclic nucleotide-gated cation channel. Plant Physiol. 1999; 121: 753–761. doi: 10.1104/pp.121.3.753 10557223
45. Yu IC, Parker J, Bent AF. Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc Natl Acad Sci U S A. 1998;95(13):7819–7824. doi: 10.1073/pnas.95.13.7819 9636234
46. Katano M, Takahashi K, Hirano T, Kazama Y, Abe T, Tsukaya H, et al. Suppressor screen and phenotype analyses revealed an emerging role of the monofunctional peroxisomal Enoyl-CoA Hydratase 2 in compensated cell enlargement. Front Plant Sci. 2016; 7: 132. doi: 10.3389/fpls.2016.00132 26925070
47. Shigaki T, Rees I, Nakhleh L, Hirschi KD. Identification of three distinct phylogenetic groups of CAX Cation/Proton Antiporters. J Mol Evol. 2006; 63:815–825. doi: 10.1007/s00239-006-0048-4 17086450
48. Mäser P, Thomine S, Schroeder IJ, Ward JM, Hirschi K, et al. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 2001; 126: 1646–1667. doi: 10.1104/pp.126.4.1646 11500563
49. Greenberg JT. Positive and negative regulation of salicylic acid-dependent cell death and pathogen resistance in Arabidopsis lsd6 and ssi1 mutants. Mol Plant Microbe Interact. 2000; 13: 877–881. doi: 10.1094/MPMI.2000.13.8.877 10939259
50. Shah J, Kachroo P, Klessig DF. The Arabidopsis ssi1 mutation restores pathogenesis-related gene expression in npr1 plants and renders DEFENSIN gene expression salicylic acid dependent. Plant Cell. 1999; 11: 191–206. doi: 10.1105/tpc.11.2.191 9927638
51. Weymann K, Hunt M, Uknes S, Neuenschwander U, Lawton K, Steiner HY, et al. Suppression and restoration of lesion formation in Arabidopsis lsd mutants. Plant Cell. 1995; 7: 2013–2022. doi: 10.1105/tpc.7.12.2013 12242366
52. Yoshimoto K, Jikumaru Y, Kamiya Y, Kusano M, Consonni C, Panstruga R, et al. Autophagy negatively regulates cell death by controlling NPR1-Dependent Salicylic Acid Signaling during senescence and the innate immune response in Arabidopsis. Plant Cell. 2009; 21: 2914–2927. doi: 10.1105/tpc.109.068635 19773385
53. Chamnongpol S, Willekens H, Moeder W, Langebartels C, Sandermann H Jr, Van Montagu M, et al. Defense activation and enhanced pathogen tolerance induced by H2O2 in transgenic tobacco. Proc Natl Acad Sci U S A. 1998; 95: 5818–5823. doi: 10.1073/pnas.95.10.5818 9576968
54. Takahashi H, Chen Z, Du H, Liu Y, Klessig DF. Development of necrosis and activation of disease resistance in transgenic tobacco plants with severely reduced catalase levels. Plant J. 1997; 11: 993–1005. doi: 10.1046/j.1365-313x.1997.11050993.x 9193071
55. Neuenschwander U, Vernooij B, Friedrich L, Uknes S, Kessmann H, Ryals J. Is hydrogen peroxide a second messenger of salicylic acid in systemic acquired resistance? Plant J. 1995; 8: 227–233. doi: 10.1046/j.1365-313X.1995.08020227.x
56. Halliwell B, Gutteridge JMC. Free Radicals in Biology and Medicine, Ed 4. Clarendon Press, Oxford 2006
57. Jambunathan N, Siani JM, McNellis TW. A humidity-sensitive Arabidopsis copine mutant exhibits precocious cell death and increased disease resistance. Plant Cell. 2001; 13: 2225–2240. doi: 10.1105/tpc.010226 11595798
58. Horiguchi G, Kim GT, Tsukaya H. The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J. 2005; 43: 68–78. doi: 10.1111/j.1365-313X.2005.02429.x 15960617
59. Fernández-Bautista N, Domínguez-Núñez J, Moreno MM, Berrocal-Lobo M. Plant tissue trypan blue staining during phytopathogen infection. BIO-PROTOCOL, 2016; 6(24). https://doi.org/10.21769/BioProtoc.2078
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 6
- Distribuce a lokalizace speciálně upravených exosomů může zefektivnit léčbu svalových dystrofií
- Prof. Jan Škrha: Metformin je bezpečný, ale je třeba jej bezpečně užívat a léčbu kontrolovat
- FDA varuje před selfmonitoringem cukru pomocí chytrých hodinek. Jak je to v Česku?
- Masturbační chování žen v ČR − dotazníková studie
- Ibuprofen jako alternativa antibiotik při léčbě infekcí močových cest
Nejčtenější v tomto čísle
- Osteocalcin promotes bone mineralization but is not a hormone
- AXR1 affects DNA methylation independently of its role in regulating meiotic crossover localization
- Super-resolution imaging of RAD51 and DMC1 in DNA repair foci reveals dynamic distribution patterns in meiotic prophase
- Steroid hormones regulate genome-wide epigenetic programming and gene transcription in human endometrial cells with marked aberrancies in endometriosis