AMP1 and CYP78A5/7 act through a common pathway to govern cell fate maintenance in Arabidopsis thaliana

English version

Autoři: Olena Poretska ^aff001; Saiqi Yang ^aff001; Delphine Pitorre ^aff002; Brigitte Poppenberger ^aff003; Tobias Sieberer ^aff001
Působiště autorů: Research Unit Plant Growth Regulation, TUM School of Life Sciences Weihenstephan, Technical University of Munich, Freising, Germany ^aff001; Department for Microbiology, Immunobiology and Genetics, Max F. Perutz Laboratories, University of Vienna, Vienna, Austria ^aff002; Biotechnology of Horticultural Crops, TUM School of Life Sciences Weihenstephan, Technical University of Munich, Freising, Germany ^aff003
Vyšlo v časopise: AMP1 and CYP78A5/7 act through a common pathway to govern cell fate maintenance in Arabidopsis thaliana. PLoS Genet 16(9): e32767. doi:10.1371/journal.pgen.1009043
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009043

Souhrn

Higher plants can continuously form new organs by the sustained activity of pluripotent stem cells. These stem cells are embedded in meristems, where they produce descendants, which undergo cell proliferation and differentiation programs in a spatiotemporally-controlled manner. Under certain conditions, pluripotency can be reestablished in descending cells and this reversion in cell fate appears to be actively suppressed by the existing stem cell pool. Mutation of the putative carboxypeptidase ALTERED MERISTEM PROGRAM1 (AMP1) in Arabidopsis causes defects in the suppression of pluripotency in cells normally programmed for differentiation, giving rise to unique hypertrophic phenotypes during embryogenesis as well as in the shoot apical meristem. A role of AMP1 in the miRNA-dependent control of translation has recently been established, however, how this activity is connected to its developmental functions is not resolved. Here we identify members of the cytochrome P450 clade CYP78A to act in parallel with AMP1 to control cell fate in Arabidopsis. Mutation of CYP78A5 and its close homolog CYP78A7 in a cyp78a5,7 double mutant caused suspensor-to-embryo conversion and ectopic stem cell pool formation in the shoot meristem, phenotypes characteristic for amp1. The tissues affected in the mutants showed pronounced expression levels of AMP1 and CYP78A5 in wild type. A comparison of mutant transcriptomic responses revealed an intriguing degree of overlap and highlighted alterations in protein lipidation processes. Moreover, we also found elevated protein levels of selected miRNA targets in cyp78a5,7. Based on comprehensive genetic interaction studies we propose a model in which both enzyme classes act on a common downstream process to sustain cell fate decisions in the early embryo and the shoot apical meristem.

Klíčová slova:

Arabidopsis thaliana – Leaves – Meristems – MicroRNAs – Phenotypes – Pluripotency – Seedlings – Stem cells

Zdroje

1. Uchida N, Torii KU. Stem cells within the shoot apical meristem: identity, arrangement and communication. Cell Mol Life Sci. 2019;76(6):1067–80. doi: 10.1007/s00018-018-2980-z 30523363

2. Pilkington M. The Regeneration of the Stem Apex. New Phytologist. 1929;28(1):37–53.

3. Sussex IM. Regeneration of the Potato Shoot Apex. Nature. 1952;170(4331):755–7. doi: 10.1038/170755a0 13002436

4. Loiseau JE. Observations et experimentation sur la phyllotaxie et le fonctionnement du sommet vegetatif chez quelques Balsaminacees. Ann Sci Nat Bot Ser. 1959;11:201–14.

5. Reinhardt D, Frenz M, Mandel T, Kuhlemeier C. Microsurgical and laser ablation analysis of interactions between the zones and layers of the tomato shoot apical meristem. Development. 2003;130(17):4073–83. doi: 10.1242/dev.00596 12874128

6. Yadav RK, Tavakkoli M, Reddy GV. WUSCHEL mediates stem cell homeostasis by regulating stem cell number and patterns of cell division and differentiation of stem cell progenitors. Development. 2010;137(21):3581–9. doi: 10.1242/dev.054973 20876644

7. Hohm T, Zitzler E, Simon R. A dynamic model for stem cell homeostasis and patterning in Arabidopsis meristems. PLoS One. 2010;5(2):e9189. doi: 10.1371/journal.pone.0009189 20169148

8. Chaudhury AM, Letham S, Craig S, Dennis ES. amp1—a mutant with high cytokinin levels and altered embryonic pattern, faster vegetative growth, constitutive photomorphogenesis and precocious flowering. Plant J. 1993;4(6):907–16.

9. Helliwell CA, Chin-Atkins AN, Wilson IW, Chapple R, Dennis ES, Chaudhury A. The Arabidopsis AMP1 gene encodes a putative glutamate carboxypeptidase. Plant Cell. 2001;13(9):2115–25. doi: 10.1105/tpc.010146 11549767

10. Huang W, Pitorre D, Poretska O, Marizzi C, Winter N, Poppenberger B, et al. ALTERED MERISTEM PROGRAM1 suppresses ectopic stem cell niche formation in the shoot apical meristem in a largely cytokinin-independent manner. Plant Physiol. 2015;167(4):1471–86. doi: 10.1104/pp.114.254623 25673776

11. Radoeva T, Weijers D. A roadmap to embryo identity in plants. Trends Plant Sci. 2014;19(11):709–16. doi: 10.1016/j.tplants.2014.06.009 25017700

12. Vidaurre DP, Ploense S, Krogan NT, Berleth T. AMP1 and MP antagonistically regulate embryo and meristem development in Arabidopsis. Development. 2007;134(14):2561–7. doi: 10.1242/dev.006759 17553903

13. Barinka C, Rojas C, Slusher B, Pomper M. Glutamate carboxypeptidase II in diagnosis and treatment of neurologic disorders and prostate cancer. Current medicinal chemistry. 2012;19(6):856–70. doi: 10.2174/092986712799034888 22214450

14. Vorlova B, Knedlik T, Tykvart J, Konvalinka J. GCPII and its close homolog GCPIII: from a neuropeptidase to a cancer marker and beyond. Front Biosci (Landmark Ed). 2019;24:648–87. 30844704

15. Mesters JR, Barinka C, Li W, Tsukamoto T, Majer P, Slusher BS, et al. Structure of glutamate carboxypeptidase II, a drug target in neuronal damage and prostate cancer. EMBO J. 2006;25(6):1375–84. doi: 10.1038/sj.emboj.7600969 16467855

16. Poretska O, Yang S, Pitorre D, Rozhon W, Zwerger K, Uribe MC, et al. The Small Molecule Hyperphyllin Enhances Leaf Formation Rate and Mimics Shoot Meristem Integrity Defects Associated with AMP1 Deficiency. Plant Physiol. 2016;171(2):1277–90. doi: 10.1104/pp.15.01633 27208298

17. Li S, Liu L, Zhuang X, Yu Y, Liu X, Cui X, et al. MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell. 2013;153(3):562–74. doi: 10.1016/j.cell.2013.04.005 23622241

18. Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C. AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J. 1998;17(1):170–80. doi: 10.1093/emboj/17.1.170 9427751

19. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, et al. Widespread translational inhibition by plant miRNAs and siRNAs. Science. 2008;320(5880):1185–90. doi: 10.1126/science.1159151 18483398

20. Yang L, Wu G, Poethig RS. Mutations in the GW-repeat protein SUO reveal a developmental function for microRNA-mediated translational repression in Arabidopsis. Proc Natl Acad Sci U S A. 2012;109(1):315–20. doi: 10.1073/pnas.1114673109 22184231

21. Reis RS, Hart-Smith G, Eamens AL, Wilkins MR, Waterhouse PM. Gene regulation by translational inhibition is determined by Dicer partnering proteins. Nat Plants. 2015;1(3).

22. Yang S, Poretska O, Sieberer T. ALTERED MERISTEM PROGRAM1 Restricts Shoot Meristem Proliferation and Regeneration by Limiting HD-ZIP III-Mediated Expression of RAP2.6L. Plant Physiol. 2018;177(4):1580–94. doi: 10.1104/pp.18.00252 29884678

23. Kawakatsu T, Taramino G, Itoh J, Allen J, Sato Y, Hong SK, et al. PLASTOCHRON3/GOLIATH encodes a glutamate carboxypeptidase required for proper development in rice. Plant J. 2009;58(6):1028–40. doi: 10.1111/j.1365-313X.2009.03841.x 19228340

24. Miyoshi K, Ahn BO, Kawakatsu T, Ito Y, Itoh J, Nagato Y, et al. PLASTOCHRON1, a timekeeper of leaf initiation in rice, encodes cytochrome P450. Proc Natl Acad Sci U S A. 2004;101(3):875–80. doi: 10.1073/pnas.2636936100 14711998

25. Bak S, Beisson F, Bishop G, Hamberger B, Hofer R, Paquette S, et al. Cytochromes p450. Arabidopsis Book. 2011;9:e0144. doi: 10.1199/tab.0144 22303269

26. Larkin JC. Isolation of a cytochrome P450 homologue preferentially expressed in developing inflorescences of Zea mays. Plant Mol Biol. 1994;25(3):343–53. doi: 10.1007/BF00043864 8049361

27. Nadeau JA, Zhang XS, Li J, O'Neill SD. Ovule development: identification of stage-specific and tissue-specific cDNAs. Plant Cell. 1996;8(2):213–39. doi: 10.1105/tpc.8.2.213 8742709

28. Zondlo SC, Irish VF. CYP78A5 encodes a cytochrome P450 that marks the shoot apical meristem boundary in Arabidopsis. Plant J. 1999;19(3):259–68. doi: 10.1046/j.1365-313x.1999.00523.x 10476073

29. Anastasiou E, Kenz S, Gerstung M, MacLean D, Timmer J, Fleck C, et al. Control of plant organ size by KLUH/CYP78A5-dependent intercellular signaling. Dev Cell. 2007;13(6):843–56. doi: 10.1016/j.devcel.2007.10.001 18061566

30. Adamski NM, Anastasiou E, Eriksson S, O'Neill CM, Lenhard M. Local maternal control of seed size by KLUH/CYP78A5-dependent growth signaling. Proc Natl Acad Sci U S A. 2009;106(47):20115–20. doi: 10.1073/pnas.0907024106 19892740

31. Ito T, Meyerowitz EM. Overexpression of a gene encoding a cytochrome P450, CYP78A9, induces large and seedless fruit in arabidopsis. The Plant cell. 2000;12(9):1541–50. doi: 10.1105/tpc.12.9.1541 11006330

32. Sun X, Cahill J, Van Hautegem T, Feys K, Whipple C, Novak O, et al. Altered expression of maize PLASTOCHRON1 enhances biomass and seed yield by extending cell division duration. Nat Commun. 2017;8:14752. doi: 10.1038/ncomms14752 28300078

33. Eriksson S, Stransfeld L, Adamski NM, Breuninger H, Lenhard M. KLUH/CYP78A5-dependent growth signaling coordinates floral organ growth in Arabidopsis. Curr Biol. 2010;20(6):527–32. doi: 10.1016/j.cub.2010.01.039 20188559

34. Wang JW, Schwab R, Czech B, Mica E, Weigel D. Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell. 2008;20(5):1231–43. doi: 10.1105/tpc.108.058180 18492871

35. Imaishi H, Matsuo S, Swai E, Ohkawa H. CYP78A1 preferentially expressed in developing inflorescences of Zea mays encoded a cytochrome P450-dependent lauric acid 12-monooxygenase. Biosci Biotechnol Biochem. 2000;64(8):1696–701. doi: 10.1271/bbb.64.1696 10993158

36. Kai K, Hashidzume H, Yoshimura K, Suzuki H, Sakurai N, Shibata D, et al. Metabolomics for the characterization of cytochromes P450-dependent fatty acid hydroxylation reactions in Arabidopsis. Plant Biotechnology. 2009;26(1):175–82.

37. Tian C, Zhang X, He J, Yu H, Wang Y, Shi B, et al. An organ boundary-enriched gene regulatory network uncovers regulatory hierarchies underlying axillary meristem initiation. Mol Syst Biol. 2014;10:755. doi: 10.15252/msb.20145470 25358340

38. Telfer A, Bollman KM, Poethig RS. Phase change and the regulation of trichome distribution in Arabidopsis thaliana. Development. 1997;124(3):645–54. 9043079

39. He J, Xu M, Willmann MR, McCormick K, Hu T, Yang L, et al. Threshold-dependent repression of SPL gene expression by miR156/miR157 controls vegetative phase change in Arabidopsis thaliana. PLoS Genet. 2018;14(4):e1007337. doi: 10.1371/journal.pgen.1007337 29672610

40. Seefried WF, Willmann MR, Clausen RL, Jenik PD. Global Regulation of Embryonic Patterning in Arabidopsis by MicroRNAs. Plant Physiol. 2014;165(2):670–87. doi: 10.1104/pp.114.240846 24784759

41. Fouracre JP, Chen VJ, Poethig RS. ALTERED MERISTEM PROGRAM1 regulates leaf identity independently of miR156-mediated translational repression. Development. 2020;147(8).

42. Brodersen P, Sakvarelidze-Achard L, Schaller H, Khafif M, Schott G, Bendahmane A, et al. Isoprenoid biosynthesis is required for miRNA function and affects membrane association of ARGONAUTE 1 in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America. 2012;109(5):1778–83. doi: 10.1073/pnas.1112500109 22247288

43. Lopez-Garcia CM, Ruiz-Herrera LF, Lopez-Bucio JS, Huerta-Venegas PI, Pena-Uribe CA, de la Cruz HR, et al. ALTERED MERISTEM PROGRAM 1 promotes growth and biomass accumulation influencing guard cell aperture and photosynthetic efficiency in Arabidopsis. Protoplasma. 2019.

44. Gross-Hardt R, Lenhard M, Laux T. WUSCHEL signaling functions in interregional communication during Arabidopsis ovule development. Genes Dev. 2002;16(9):1129–38. doi: 10.1101/gad.225202 12000795

45. Rozhon W, Mayerhofer J, Petutschnig E, Fujioka S, Jonak C. ASKtheta, a group-III Arabidopsis GSK3, functions in the brassinosteroid signalling pathway. Plant J. 2010;62(2):215–23. doi: 10.1111/j.1365-313X.2010.04145.x 20128883

46. Gleave AP. A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Molecular Biology. 1992;20(6):1203–7. doi: 10.1007/BF00028910 1463857

47. Zuo J, Niu QW, Chua NH. Technical advance: An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J. 2000;24(2):265–73. doi: 10.1046/j.1365-313x.2000.00868.x 11069700

48. Sieber P, Gheyselinck J, Gross-Hardt R, Laux T, Grossniklaus U, Schneitz K. Pattern formation during early ovule development in Arabidopsis thaliana. Dev Biol. 2004;273(2):321–34. doi: 10.1016/j.ydbio.2004.05.037 15328016

49. Hejatko J, Blilou I, Brewer PB, Friml J, Scheres B, Benkova E. In situ hybridization technique for mRNA detection in whole mount Arabidopsis samples. Nat Protoc. 2006;1(4):1939–46. doi: 10.1038/nprot.2006.333 17487180

50. Berleth T, Jürgens G. The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo. Development. 1993;118(2):575–87.

51. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004;3:Article3.

52. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B (Methodological). 1995;57(1):289–300.

53. Tian T, Liu Y, Yan H, You Q, Yi X, Du Z, et al. agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res. 2017;45(W1):W122–W9. doi: 10.1093/nar/gkx382 28472432

54. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, et al. Primer3—new capabilities and interfaces. Nucleic Acids Res. 2012;40(15):e115. doi: 10.1093/nar/gks596 22730293

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