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Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
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Overexpression of three related root-cap outermost-cell-specific C2H2-type zinc-finger protein genes suppresses the growth of Arabidopsis in an EAR-motif-dependent manner

  • Received : 2019.11.15
  • Accepted : 2020.01.01
  • Published : 2020.03.31
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Abstract

The root meristem of Arabidopsis thaliana is protected by the root cap, the size of which is tightly regulated by the balance between the formative cell divisions and the dispersal of the outermost cells. We isolated an enhancer-tagged dominant mutant displaying the short and twisted root by the overexpression of ZINC-FINGER OF ARABIDOPSIS THALIANA1 (ZAT1) encoding an EAR motif-containing zinc-finger protein. The growth inhibition by ZAT1 was shared by ZAT4 and ZAT9, the ZAT1 homologues. The ZAT1 promoter was specifically active in the outermost cells of the root cap, in which ZAT1-GFP was localized when expressed by the ZAT1 promoter. The outermost cell-specific expression pattern of ZAT1 was not altered in the sombrero (smb) or smb bearskin1 (brn1) brn2 accumulating additional root-cap layers. In contrast, ZAT4-GFP and ZAT9-GFP fusion proteins were distributed to the inner root-cap cells in addition to the outermost cells where ZAT4 and ZAT9 promoters were active. Overexpression of ZAT1 induced the ectopic expression of PUTATIVE ASPARTIC PROTEASE3 involved in the programmed cell death. The EAR motif was essential for the growth inhibition by ZAT1. These results suggest that the three related ZATs might regulate the maturation of the outermost cells of the root cap.

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References

  1. Scheres B, Benfey P and Dolan L (2002) Root development. The Arabidopsis book/American Society of Plant Biologists 1, 1-18 https://doi.org/10.1199/tab.0021
  2. Nakajima K and Benfey PN (2002) Signaling in and out: control of cell division and differentiation in the shoot and root. Plant Cell 14, S265-S276 https://doi.org/10.1105/tpc.010471
  3. Kumpf RP and Nowack MK (2015) The root cap: a short story of life and death. J Exp Bot 66, 5651-5662 https://doi.org/10.1093/jxb/erv295
  4. Sarkar AK, Luijten M, Miyashima S et al (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446, 811 https://doi.org/10.1038/nature05703
  5. Pi L, Aichinger E, van der Graaff E et al (2015) Organizerderived WOX5 signal maintains root columella stem cells through chromatin-mediated repression of CDF4 expression. Dev Cell 33, 576-588 https://doi.org/10.1016/j.devcel.2015.04.024
  6. Stahl Y, Wink RH, Ingram GC and Simon R (2009) A signaling module controlling the stem cell niche in Arabidopsis root meristems. Current Biol 19, 909-914 https://doi.org/10.1016/j.cub.2009.03.060
  7. Stahl Y, Grabowski S, Bleckmann A et al (2013) Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr Biol 23, 362-371 https://doi.org/10.1016/j.cub.2013.01.045
  8. Willemsen V, Bauch M, Bennett T et al (2008) The NAC domain transcription factors FEZ and SOMBRERO control the orientation of cell division plane in Arabidopsis root stem cells. Dev Cell 15, 913-922 https://doi.org/10.1016/j.devcel.2008.09.019
  9. Del Campillo E, Abdel-Aziz A, Crawford D and Patterson SE (2004) Root cap specific expression of an endo-${\beta}$-1, 4--glucanase (cellulase): a new marker to study root development in Arabidopsis. Plant Mol Biol 56, 309-323 https://doi.org/10.1007/s11103-004-3380-3
  10. Bennett T, van den Toorn A, Sanchez-Perez GF et al (2010) SOMBRERO, BEARSKIN1, and BEARSKIN2 regulate root cap maturation in Arabidopsis. Plant Cell 22, 640-654 https://doi.org/10.1105/tpc.109.072272
  11. Kamiya M, Higashio SY, Isomoto A et al (2016) Control of root cap maturation and cell detachment by BEARSKIN transcription factors in Arabidopsis. Development 143, 4063-4072 https://doi.org/10.1242/dev.142331
  12. Shi CL, von Wangenheim D, Herrmann U et al (2018) The dynamics of root cap sloughing in Arabidopsis is regulated by peptide signalling. Nat Plant 4, 596 https://doi.org/10.1038/s41477-018-0212-z
  13. Fendrych M, Van Hautegem T, Van Durme M et al (2014) Programmed cell death controlled by ANAC033/SOMBRERO determines root cap organ size in Arabidopsis. Curr Biol 24, 931-940 https://doi.org/10.1016/j.cub.2014.03.025
  14. Englbrecht CC, Schoof H and Bohm S (2004) Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 5, 39 https://doi.org/10.1186/1471-2164-5-39
  15. Kagale S and Rozwadowski K (2011) EAR motif-mediated transcriptional repression in plants: an underlying mechanism for epigenetic regulation of gene expression. Epigenetics 6, 141-146 https://doi.org/10.4161/epi.6.2.13627
  16. Kagale S, Links MG and Rozwadowski K (2010) Genomewide analysis of ethylene-responsive element binding factorassociated amphiphilic repression motif-containing transcriptional regulators in Arabidopsis. Plant Physiol 152, 1109-1134 https://doi.org/10.1104/pp.109.151704
  17. Szemenyei H, Hannon M and Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319, 1384-1386 https://doi.org/10.1126/science.1151461
  18. Borg M, Rutley N, Kagale S et al (2014) An EAR-dependent regulatory module promotes male germ cell division and sperm fertility in Arabidopsis. Plant Cell 26, 2098-2113 https://doi.org/10.1105/tpc.114.124743
  19. Ciftci-Yilmaz S and Mittler R (2008) The zinc finger network of plants. Cell Mol Lif Sci 65, 1150-1160 https://doi.org/10.1007/s00018-007-7473-4
  20. Xie M, Sun J, Gong D and Kong Y (2019) The Roles of Arabidopsis C1-2i Subclass of C2H2-type Zinc-Finger Transcription Factors. Genes 10, 653 https://doi.org/10.3390/genes10090653
  21. Waki T, Miyashima S, Nakanishi M, Ikeda Y, Hashimoto T and Nakajima K (2013) A GAL 4-based targeted activation tagging system in A rabidopsis thaliana. Plant J 73, 357-367 https://doi.org/10.1111/tpj.12049
  22. Meissner R and Michael AJ (1997) Isolation and characterisation of a diverse family of Arabidopsis two and threefingered C 2 H 2 zinc finger protein genes and cDNAs. Plant Mol Biol 33, 615-624 https://doi.org/10.1023/A:1005746803089
  23. Hardtke CS and Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17, 1405-1411 https://doi.org/10.1093/emboj/17.5.1405
  24. Hamann T, Benkova E, Baurle I, Kientz M and Jurgens G (2002) The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Gene Dev 16, 1610-1615 https://doi.org/10.1101/gad.229402
  25. Gagne JM, Song SK and Clark SE (2008) POLTERGEIST and PLL1 are required for stem cell function with potential roles in cell asymmetry and auxin signaling. Commun Integr Biol 1, 53-55 https://doi.org/10.4161/cib.1.1.6841
  26. Zhou W, Wei L, Xu J et al (2010) Arabidopsis tyrosylprotein sulfotransferase acts in the auxin/PLETHORA pathway in regulating postembryonic maintenance of the root stem cell niche. Plant Cell 22, 3692-3709 https://doi.org/10.1105/tpc.110.075721
  27. Vidal EA, Moyano TC, Krouk G et al (2013) Integrated RNA-seq and sRNA-seq analysis identifies novel nitrateresponsive genes in Arabidopsis thaliana roots. BMC Genomics 14, 701 https://doi.org/10.1186/1471-2164-14-701
  28. Sun CH, Yu JQ and Hu DG (2017) Nitrate: a crucial signal during lateral roots development. Front Plant Sci 8, 485
  29. Ciftci-Yilmaz S, Morsy MR, Song L et al (2007) The EARmotif of the Cys2/His2-type zinc finger protein Zat7 plays a key role in the defense response of Arabidopsis to salinity stress. J Biol Chem 282, 9260-9268 https://doi.org/10.1074/jbc.M611093200
  30. Olvera-Carrillo Y, Van Bel M, Van Hautegem T et al (2015) A conserved core of programmed cell death indicator genes discriminates developmentally and environmentally induced programmed cell death in plants. Plant Physiol 169, 2684-2699 https://doi.org/10.1104/pp.15.00769
  31. Song SK (2016) Misexpression of AtTX12 encoding a Toll/interleukin-1 receptor domain induces growth defects and expression of defense-related genes partially independently of EDS1 in Arabidopsis. BMB Rep 49, 693 https://doi.org/10.5483/BMBRep.2016.49.12.180
  32. Masucci JD and Schiefelbein JW (1996) Hormones act downstream of TTG and GL2 to promote root hair outgrowth during epidermis development in the Arabidopsis root. Plant Cell 8, 1505-1517 https://doi.org/10.1105/tpc.8.9.1505
  33. Donnelly PM, Bonetta D, Tsukaya H, Dengler RE and Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215, 407-419 https://doi.org/10.1006/dbio.1999.9443
  34. Wada T, Kurata T, Tominaga R et al (2002) Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development 129, 5409-5419 https://doi.org/10.1242/dev.00111
  35. Song SK, Ryu KH, Kang YH et al (2011) Cell fate in the Arabidopsis root epidermis is determined by competition between WEREWOLF and CAPRICE. Plant Physiol 157, 1196-1208 https://doi.org/10.1104/pp.111.185785
  36. Song SK, Hofhuis H, Lee MM and Clark SE (2008) Key divisions in the early Arabidopsis embryo require POL and PLL1 phosphatases to establish the root stem cell organizer and vascular axis. Dev Cell 15, 98-109 https://doi.org/10.1016/j.devcel.2008.05.008
  37. Lee MM and Schiefelbein J (2002) Cell pattern in the Arabidopsis root epidermis determined by lateral inhibition with feedback. Plant Cell 14, 611-618 https://doi.org/10.1105/tpc.010434
  38. Lee MM and Schiefelbein J (1999) WEREWOLF, a MYBrelated protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning. Cell 99, 473-483 https://doi.org/10.1016/S0092-8674(00)81536-6