Pattern Dynamics in Adaxial-Abaxial Specific Gene Expression Are Modulated by a Plastid Retrograde Signal during Leaf Development

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The maintenance and reformation of gene expression domains are the basis for the morphogenic processes of multicellular systems. In a leaf primordium of Arabidopsis thaliana, the expression of FILAMENTOUS FLOWER (FIL) and the activity of the microRNA miR165/166 are specific to the abaxial side. This miR165/166 activity restricts the target gene expression to the adaxial side. The adaxial and abaxial specific gene expressions are crucial for the wide expansion of leaf lamina. The FIL-expression and the miR165/166-free domains are almost mutually exclusive, and they have been considered to be maintained during leaf development. However, we found here that the position of the boundary between the two domains gradually shifts from the adaxial side to the abaxial side. The cell lineage analysis revealed that this boundary shifting was associated with a sequential gene expression switch from the FIL-expressing (miR165/166 active) to the miR165/166-free (non-FIL-expressing) states. Our genetic analyses using the enlarged fil expression domain2 (enf2) mutant and chemical treatment experiments revealed that impairment in the plastid (chloroplast) gene expression machinery retards this boundary shifting and inhibits the lamina expansion. Furthermore, these developmental effects caused by the abnormal plastids were not observed in the genomes uncoupled1 (gun1) mutant background. This study characterizes the dynamic nature of the adaxial-abaxial specification process in leaf primordia and reveals that the dynamic process is affected by the GUN1-dependent retrograde signal in response to the failure of plastid gene expression. These findings advance our understanding on the molecular mechanism linking the plastid function to the leaf morphogenic processes.

Vyšlo v časopise: Pattern Dynamics in Adaxial-Abaxial Specific Gene Expression Are Modulated by a Plastid Retrograde Signal during Leaf Development. PLoS Genet 9(7): e32767. doi:10.1371/journal.pgen.1003655
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003655

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1. BecamI, RafelN, HongX, CohenSM, MilánM (2011) Notch-mediated repression of bantam miRNA contributes to boundary formation in the Drosophila wing. Development 138: 3781–3789.

2. AlieeM, RöperJC, LandsbergKP, PentzoldC, WidmannTJ, et al. (2012) Physical mechanisms shaping the Drosophila dorsoventral compartment boundary. Curr Biol 22: 967–976.

3. BlairSS, BrowerDL, ThomasJB, ZavortinkM (1994) The role of apterous in the control of dorsoventral compartmentalization and PS integrin gene expression in the developing wing of Drosophila. Development 120: 1805–1815.

4. Diaz-BenjumeaFJ, CohenSM (1993) Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila. Cell 75: 741–752.

5. KidnerCA, TimmermansMC (2010) Signaling sides adaxial-abaxial patterning in leaves. Curr Top Dev Biol 91: 141–168.

6. EfroniI, EshedY, LifschitzE (2010) Morphogenesis of simple and compound leaves: a critical review. Plant Cell 22: 1019–1032.

7. SzakonyiD, MoschopoulosA, ByrneME (2010) Perspectives on leaf dorsoventral polarity. J Plant Res 123: 281–290.

8. YamaguchiT, NukazukaA, TsukayaH (2012) Leaf adaxial-abaxial polarity specification and lamina outgrowth: evolution and development. Plant Cell Physiol 53: 1180–1194.

9. McConnellJR, EmeryJ, EshedY, BaoN, BowmanJ, et al. (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411: 709–713.

10. OtsugaD, DeGuzmanB, PriggeMJ, DrewsGN, ClarkSE (2001) REVOLUTA regulates meristem initiation at lateral positions. Plant J 25: 223–236.

11. EshedY, BaumSF, PereaJV, BowmanJL (2001) Establishment of polarity in lateral organs of plants. Curr Biol 11: 1251–1260.

12. IwakawaH, IwasakiM, KojimaS, UenoY, SomaT, et al. (2007) Expression of the ASYMMETRIC LEAVES2 gene in the adaxial domain of Arabidopsis leaves represses cell proliferation in this domain and is critical for the development of properly expanded leaves. Plant J 51: 173–184.

13. SiegfriedKR, EshedY, BaumSF, OtsugaD, DrewsGN, et al. (1999) Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126: 4117–4128.

14. SawaS, WatanabeK, GotoK, LiuYG, ShibataD, et al. (1999) FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. Genes Dev 13: 1079–1088.

15. WatanabeK, OkadaK (2003) Two discrete cis elements control the Abaxial side-specific expression of the FILAMENTOUS FLOWER gene in Arabidopsis. Plant Cell 15: 2592–2602.

16. SarojamR, SapplPG, GoldshmidtA, EfroniI, FloydSK, et al. (2010) Differentiating Arabidopsis shoots from leaves by combined YABBY activities. Plant Cell 22: 2113–2130.

17. KerstetterRA, BollmanK, TaylorRA, BombliesK, PoethigRS (2001) KANADI regulates organ polarity in Arabidopsis. Nature 411: 706–709.

18. EshedY, IzhakiA, BaumSF, FloydSK, BowmanJL (2004) Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities. Development 131: 2997–3006.

19. PekkerI, AlvarezJP, EshedY (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17: 2899–2910.

20. ChitwoodDH, NogueiraFT, HowellMD, MontgomeryTA, CarringtonJC, et al. (2009) Pattern formation via small RNA mobility. Genes Dev 23: 549–554.

21. KidnerCA, MartienssenRA (2004) Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428: 81–84.

22. GarciaD, CollierSA, ByrneME, MartienssenRA (2006) Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr Biol 16: 933–938.

23. CarlsbeckerA, LeeJY, RobertsCJ, DettmerJ, LehesrantaS, et al. (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465: 316–321.

24. MiyashimaS, KoiS, HashimotoT, NakajimaK (2011) Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 138: 2303–2313.

25. La RotaC, ChopardJ, DasP, PaindavoineS, RozierF, FarcotE, et al. (2011) A data-driven integrative model of sepal primordium polarity in Arabidopsis. Plant Cell 23: 4318–4333.

26. Murray JD (2003) Mathematical Biology II: Spatial Models and Biomedical Applications. 3rd Ed. New York: Springer-Verlag New York. pp. 1–70.

27. JaegerJ, SurkovaS, BlagovM, JanssensH, KosmanD, et al. (2004) Dynamic control of positional information in the early Drosophila embryo. Nature 430: 368–371.

28. JilkineA, MaréeAF, Edelstein-KeshetL (2007) Mathematical model for spatial segregation of the Rho-family GTPases based on inhibitory crosstalk. Bull Math Biol 69: 1943–1978.

29. ToyokuraK, WatanabeK, OiwakaA, KusanoM, TameshigeT, et al. (2011) Succinic semialdehyde dehydrogenase is involved in the robust patterning of Arabidopsis leaves along the adaxial-abaxial axis. Plant Cell Physiol 52: 1340–1353.

30. HeislerMG, OhnoC, DasP, SieberP, ReddyGV, et al. (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol 15: 1899–1911.

31. GillmorCS, ParkMY, SmithMR, PepitoneR, KerstetterRA, et al. (2010) The MED12-MED13 module of Mediator regulates the timing of embryo patterning in Arabidopsis. Development 137: 113–122.

32. GolzJF, RoccaroM, KuzoffR, HudsonA (2004) GRAMINIFOLIA promotes growth and polarity of Antirrhinum leaves. Development 131: 3661–3670.

33. YamadaT, YokotaS, HirayamaY, ImaichiR, KatoM, et al. (2011) Ancestral expression patterns and evolutionary diversification of YABBY genes in angiosperms. Plant J 67: 26–36.

34. NakataM, MatsumotoN, TsugekiR, RikirschE, LauxT, et al. (2012) Roles of the middle domain-specific WUSCHEL-RELATED HOMEOBOX genes in early development of leaves in Arabidopsis. Plant Cell 24: 519–535.

35. LifschitzE, EviatarT, RozmanA, ShalitA, GoldshmidtA, et al. (2006) The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc Natl Acad Sci U S A 103: 6398–6403.

36. WoodsonJD, ChoryJ (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9: 383–395.

37. PogsonBJ, WooNS, FörsterB, SmallID (2008) Plastid signalling to the nucleus and beyond. Trends Plant Sci 13: 602–609.

38. LarkinRM, RuckleME (2008) Integration of light and plastid signals. Curr Opin Plant Biol 11: 593–599.

39. PfannschmidtT (2010) Plastidial retrograde signalling–a true “plastid factor” or just metabolite signatures? Trends Plant Sci 15: 427–435.

40. InabaT, YazuF, Ito-InabaY, KakizakiT, NakayamaK (2011) Retrograde signaling pathway from plastid to nucleus. Int Rev Cell Mol Biol 290: 167–204.

41. BrocardJ, FeilR, ChambonP, MetzgerD (1998) A chimeric Cre recombinase inducible by synthetic, but not by natural ligands of the glucocorticoid receptor. Nucleic Acids Res 26: 4086–4090.

42. AnastasiouE, KenzS, GerstungM, MacLeanD, TimmerJ, et al. (2007) Control of plant organ size by KLUH/CYP78A5-dependent intercellular signaling. Dev Cell 13: 843–856.

43. WachsmanG, HeidstraR, ScheresB (2011) Distinct cell-autonomous functions of RETINOBLASTOMA-RELATED in Arabidopsis stem cells revealed by the Brother of Brainbow clonal analysis system. Plant Cell 23: 2581–2591.

44. PriggeMJ, OtsugaD, AlonsoJM, EckerJR, DrewsGN, et al. (2005) Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17: 61–76.

45. ZhangZ, WangH, LuoD, ZengM, HuangH, et al. (2011) Convergence of the 26S proteasome and the REVOLUTA pathways in regulating inflorescence and floral meristem functions in Arabidopsis. J Exp Bot 62: 359–369.

46. FuY, XuL, XuB, YangL, LingQ, et al. (2007) Genetic interactions between leaf polarity-controlling genes and ASYMMETRIC LEAVES1 and 2 in Arabidopsis leaf patterning. Plant Cell Physiol 48: 724–735.

47. ZhouGK, KuboM, ZhongR, DemuraT, YeZH (2007) Overexpression of miR165 affects apical meristem formation, organ polarity establishment and vascular development in Arabidopsis. Plant Cell Physiol 48: 391–404.

48. LiH, XuL, WangH, YuanZ, CaoX, et al. (2005) The Putative RNA-dependent RNA polymerase RDR6 acts synergistically with ASYMMETRIC LEAVES1 and 2 to repress BREVIPEDICELLUS and MicroRNA165/166 in Arabidopsis leaf development. Plant Cell 17: 2157–2171.

49. McConnellJR, BartonMK (1998) Leaf polarity and meristem formation in Arabidopsis. Development 125: 2935–2942.

50. LiuZ, JiaL, WangH, HeY (2011) HYL1 regulates the balance between adaxial and abaxial identity for leaf flattening via miRNA-mediated pathways. J Exp Bot 62: 4367–4381.

51. GraingerRJ, BeggsJD (2005) Prp8 protein: at the heart of the spliceosome. RNA 11: 533–557.

52. FerroM, BrugièreS, SalviD, Seigneurin-BernyD, CourtM, et al. (2010) AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol Cell Proteomics 9: 1063–1084.

53. MajeranW, FrisoG, AsakuraY, QuX, HuangM, et al. (2012) Nucleoid-enriched proteomes in developing plastids and chloroplasts from maize leaves: a new conceptual framework for nucleoid functions. Plant Physiol 158: 156–189.

54. YadavRK, GirkeT, PasalaS, XieM, ReddyGV (2009) Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc Natl Acad Sci U S A 106: 4941–4946.

55. IgarashiK, KashiwagiK (1999) Polyamine transport in bacteria and yeast. Biochem J 344: 633–42.

56. ChatterjeeM, SparvoliS, EdmundsC, GarosiP, FindlayK, et al. (1996) DAG, a gene required for chloroplast differentiation and palisade development in Antirrhinum majus. EMBO J 15: 4194–4207.

57. KeddieJS, CarrollB, JonesJD, GruissemW (1996) The DCL gene of tomato is required for chloroplast development and palisade cell morphogenesis in leaves. EMBO J 15: 4208–4217.

58. BabiychukE, FuangthongM, Van MontaguM, InzéD, KushnirS (1997) Efficient gene tagging in Arabidopsis thaliana using a gene trap approach. Proc Natl Acad Sci U S A 94: 12722–12727.

59. HricováA, QuesadaV, MicolJL (2006) The SCABRA3 nuclear gene encodes the plastid RpoTp RNA polymerase, which is required for chloroplast biogenesis and mesophyll cell proliferation in Arabidopsis. Plant Physiol 141: 942–956.

60. BabiychukE, VandepoeleK, WissingJ, Garcia-DiazM, De RyckeR, et al. (2011) Plastid gene expression and plant development require a plastidic protein of the mitochondrial transcription termination factor family. Proc Natl Acad Sci U S A 108: 6674–6679.

61. FleischmannTT, ScharffLB, AlkatibS, HasdorfS, SchöttlerMA, et al. (2011) Nonessential plastid-encoded ribosomal proteins in tobacco: a developmental role for plastid translation and implications for reductive genome evolution. Plant Cell 23: 3137–3155.

62. MoschopoulosA, DerbyshireP, ByrneME (2012) The Arabidopsis organelle-localized glycyl-tRNA synthetase encoded by EMBRYO DEFECTIVE DEVELOPMENT1 is required for organ patterning. J Exp Bot 63: 5233–5243.

63. LeeKH, ParkJ, WilliamsDS, XiongY, HwangI, et al. (2012) Defective chloroplast development inhibits maintenance of normal levels of abscisic acid in a mutant of the Arabidopsis RH3 DEAD-box protein during early post-germination growth. Plant J 73: 720–732.

64. ChoWK, GeimerS, MeurerJ (2009) Cluster analysis and comparison of various chloroplast transcriptomes and genes in Arabidopsis thaliana. DNA Res 16: 31–44.

65. RuckleME, DeMarcoSM, LarkinRM (2007) Plastid signals remodel light signaling networks and are essential for efficient chloroplast biogenesis in Arabidopsis. Plant Cell 19: 3944–3960.

66. Chateigner-BoutinAL, Ramos-VegaM, Guevara-GarcíaA, AndrésC, de la Luz Gutiérrez-NavaM, et al. (2008) CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. Plant J 56: 590–602.

67. BreitenbachJ, ZhuC, SandmannG (2001) Bleaching herbicide norflurazon inhibits phytoene desaturase by competition with the cofactors. J Agric Food Chem 49: 5270–5272.

68. MuloP, PursiheimoS, HouC, TyystjärviT, AroE (2003) Multiple effects of antibiotics on chloroplast and nuclear gene expression. Funct Plant Biol 30: 1097–1103.

69. PetrickaJJ, ClayNK, NelsonTM (2008) Vein patterning screens and the defectively organized tributaries mutants in Arabidopsis thaliana. Plant J 56: 251–263.

70. Serrano-CartagenaJ, RoblesP, PonceMR, MicolJL (1999) Genetic analysis of leaf form mutants from the Arabidopsis Information Service collection. Mol Gen Genet 261: 725–739.

71. AnkeleE, KindgrenP, PesquetE, StrandA (2007) In vivo visualization of Mg-protoporphyrin IX, a coordinator of photosynthetic gene expression in the nucleus and the chloroplast. Plant Cell 19: 1964–1979.

72. WoodsonJD, Perez-RuizJM, SchmitzRJ, EckerJR, ChoryJ (2013) Sigma factor-mediated plastid retrograde signals control nuclear gene expression. Plant J 73: 1–13.

73. KoussevitzkyS, NottA, MocklerTC, HongF, Sachetto-MartinsG, et al. (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316: 715–719.

74. Cottage AJ, Mott EK, Wang JH, Sullivan JA, MacLean D, et al.. (2008) GUN1 (GENOMES UNCOUPLED1) encodes a pentatricopeptide repeat (PPR) protein involved in plastid protein synthesis-responsive retrograde signaling to the nucleus. In: Allen JF, Gantt E, Golbeck JH, Osmond B, editors. Photosynthesis. Energy from the Sun; 14th International Congress on Photosynthesis; Springer-Verlag, Berlin. pp. 1205–1211.

75. SusekRE, AusubelFM, ChoryJ (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74: 787–799.

76. MochizukiN, BrusslanJA, LarkinR, NagataniA, ChoryJ (2001) Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci U S A 98: 2053–2058.

77. ZhuH, HuF, WangR, ZhouX, SzeSH, et al. (2011) Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145: 242–256.

78. BrandtR, XieY, MusielakT, GraeffM, StierhofYD, et al. (2013) Control of stem cell homeostasis via interlocking microRNA and microProtein feedback loops. Mech Dev 130: 25–33.

79. Dello IoioR, GalinhaC, FletcherAG, GriggSP, MolnarA, et al. (2012) A PHABULOSA/cytokinin feedback loop controls root growth in Arabidopsis. Curr Biol 22: 1699–1704.

80. MalloryAC, ReinhartBJ, Jones-RhoadesMW, TangG, ZamorePD, et al. (2004) MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region. EMBO J 23: 3356–3364.

81. BaoN, LyeKW, BartonMK (2004) MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome. Dev Cell 7: 653–662.

82. WangW, XuB, WangH, LiJ, HuangH, et al. (2011) YUCCA genes are expressed in response to leaf adaxial-abaxial juxtaposition and are required for leaf margin development. Plant Physiol 157: 1805–1819.

83. KakizakiT, MatsumuraH, NakayamaK, CheFS, TerauchiR, et al. (2009) Coordination of plastid protein import and nuclear gene expression by plastid-to-nucleus retrograde signaling. Plant Physiol 151: 1339–1353.

84. SunX, FengP, XuX, GuoH, MaJ, et al. (2011) A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus. Nat Commun 2: 477.

85. RuckleME, BurgoonLD, LawrenceLA, SinklerCA, LarkinRM (2012) Plastids are major regulators of light signaling in Arabidopsis. Plant Physiol 159: 366–390.

86. PinonV, EtchellsJP, RossignolP, CollierSA, ArroyoJM, et al. (2008) Three PIGGYBACK genes that specifically influence leaf patterning encode ribosomal proteins. Development 135: 1315–1324.

87. YaoY, LingQ, WangH, HuangH (2008) Ribosomal proteins promote leaf adaxial identity. Development 135: 1325–1334.

88. HoriguchiG, Mollá-MoralesA, Pérez-PérezJM, KojimaK, RoblesP, et al. (2011) Differential contributions of ribosomal protein genes to Arabidopsis thaliana leaf development. Plant J 65: 724–736.

89. SzakonyiD, ByrneME (2011) Ribosomal protein L27a is required for growth and patterning in Arabidopsis thaliana. Plant J 65: 269–281.

90. SandersH, RothwellGW, WyattS (2007) Paleontological context for the developmental mechanisms of evolution. Int J Plant Sci 168: 719–728.