Advertisement

Journal of Plant Research

, Volume 123, Issue 3, pp 281–290 | Cite as

Perspectives on leaf dorsoventral polarity

  • Dóra Szakonyi
  • Alexis Moschopoulos
  • Mary E. ByrneEmail author
JPR Symposium International Conference on Arabidopsis Research 2010

Abstract

Leaves occur in a vast array of shapes and sizes, with complex diversity contributing to optimization of the principal function of photosynthesis. The program of development from a self-renewing stem cell population to a mature leaf has been of interest to biologists for years. Many genes involved in this process have been identified, particularly in the model eudicot Arabidopsis, so that now we have a greater understanding of mechanisms of stem cell maintenance, cell differentiation and organogenesis. One aspect of leaf development that is of particular interest is the establishment of dorsoventral polarity: the distinct adaxial (upper) and abaxial (lower) sides of the leaf. Early studies postulated conceptual models of how establishment of polarity leads to the development of planar leaves. Studies over the past decade have defined genetic details of this model, and uncovered diverse mechanisms of gene regulation that facilitate development of leaf dorsoventral polarity, including transcriptional regulation, chromatin modification, DNA modification, regulation by short RNAs and translational and post-translational regulation. This review will discuss these regulatory mechanisms in the context of leaf dorsoventrality, and will conclude with unresolved questions and areas of future research.

Keywords

Dorsoventral Leaf Polarity 

Notes

Acknowledgments

This work was funded by Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/G007802/1 and Royal Society Wolfson Merit Award to M.E.B. A.M. is a recipient of a BBSRC studentship.

References

  1. Adenot X, Elmayan T, Lauressergues D, Boutet S, Bouché N, Gasciolli V, Vaucheret H (2006) DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr Biol 16:927–932CrossRefPubMedGoogle Scholar
  2. Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221CrossRefPubMedGoogle Scholar
  3. Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741CrossRefPubMedGoogle Scholar
  4. Axtell MJ, Jan C, Rajagopalan R, Bartel DP (2006) A two-hit trigger for siRNA biogenesis in plants. Cell 127:565–577CrossRefPubMedGoogle Scholar
  5. Baima S, Nobili F, Sessa G, Lucchetti S, Ruberti I, Morelli G (1995) The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Development 121:4171–4182PubMedGoogle Scholar
  6. Barakat A, Szick-Miranda K, Chang IF, Guyot R, Blanc G, Cooke R, Delseny M, Bailey-Serres J (2001) The organization of cytoplasmic ribosomal protein genes in the Arabidopsis genome. Plant Physiol 127:398–415CrossRefPubMedGoogle Scholar
  7. Bharathan G, Goliber TE, Moore C, Kessler S, Pham T, Sinha NR (2002) Homologies in leaf form inferred from KNOXI gene expression during development. Science 296:1858–1860CrossRefPubMedGoogle Scholar
  8. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190CrossRefPubMedGoogle Scholar
  9. Byrne ME (2009) A role for the ribosome in development. Trends Plant Sci 14:512–519CrossRefPubMedGoogle Scholar
  10. Byrne ME, Barley R, Curtis M, Arroyo JM, Dunham M, Hudson A, Martienssen RA (2000) Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408:967–971CrossRefPubMedGoogle Scholar
  11. Byrne ME, Simorowski J, Martienssen RA (2002) ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129:1957–1965PubMedGoogle Scholar
  12. Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025CrossRefPubMedGoogle Scholar
  13. Chen X (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25:21–44CrossRefPubMedGoogle Scholar
  14. Chitwood DH, Nogueira FT, Howell MD, Montgomery TA, Carrington JC, Timmermans MC (2009) Pattern formation via small RNA mobility. Genes Dev 23:549–554CrossRefPubMedGoogle Scholar
  15. Chua YL, Channeliere S, Mott E, Gray JC (2005) The bromodomain protein GTE6 controls leaf development in Arabidopsis by histone acetylation at ASYMMETRIC LEAVES1. Genes Dev 19:2245–2254CrossRefPubMedGoogle Scholar
  16. Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A, Baum SF, Bowman JL (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13:1768–1774CrossRefPubMedGoogle Scholar
  17. Eshed Y, Baum SF, Perea JV, Bowman JL (2001) Establishment of polarity in lateral organs of plants. Curr Biol 11:1251–1260CrossRefPubMedGoogle Scholar
  18. Eshed Y, Izhaki A, Baum SF, Floyd SK, Bowman JL (2004) Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities. Development 131:2997–3006CrossRefPubMedGoogle Scholar
  19. Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC (2006) Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16:939–944CrossRefPubMedGoogle Scholar
  20. Fujikura U, Horiguchi G, Ponce MR, Micol JL, Tsukaya H (2009) Coordination of cell proliferation and cell expansion mediated by ribosome-related processes in the leaves of Arabidopsis thaliana. Plant J 59:499–508CrossRefPubMedGoogle Scholar
  21. Gandikota M, Birkenbihl RP, Hohmann S, Cardon GH, Saedler H, Huijser P (2007) The miRNA156/157 recognition element in the 3’ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J 49:683–693CrossRefPubMedGoogle Scholar
  22. Garcia D, Collier SA, Byrne ME, Martienssen RA (2006) Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr Biol 16:933–938CrossRefPubMedGoogle Scholar
  23. Gasciolli V, Mallory AC, Bartel DP, Vaucheret H (2005) Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr Biol 15:1494–1500CrossRefPubMedGoogle Scholar
  24. Goldshmidt A, Alvarez JP, Bowman JL, Eshed Y (2008) Signals derived from YABBY gene activities in organ primordia regulate growth and partitioning of Arabidopsis shoot apical meristems. Plant Cell 20:1217–1230CrossRefPubMedGoogle Scholar
  25. Hareven D, Gutfinger T, Parnis A, Eshed Y, Lifschitz E (1996) The making of a compound leaf: genetic manipulation of leaf architecture in tomato. Cell 84:735–744CrossRefPubMedGoogle Scholar
  26. Hay A, Tsiantis M (2006) The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nat Genet 38:942–947CrossRefPubMedGoogle Scholar
  27. Huang W, Pi L, Liang W, Xu B, Wang H, Cai R, Huang H (2006) The proteolytic function of the Arabidopsis 26S proteasome is required for specifying leaf adaxial identity. Plant Cell 18:2479–2492CrossRefPubMedGoogle Scholar
  28. Hunter C, Sun H, Poethig RS (2003) The Arabidopsis heterochronic gene ZIPPY is an ARGONAUTE family member. Curr Biol 13:1734–1739CrossRefPubMedGoogle Scholar
  29. Hunter C, Willmann MR, Wu G, Yoshikawa M, de la Luz Gutierrez-Nava M, Poethig SR (2006) Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis. Development 133:2973–2981CrossRefPubMedGoogle Scholar
  30. Husbands A, Bell EM, Shuai B, Smith HM, Springer PS (2007) LATERAL ORGAN BOUNDARIES defines a new family of DNA-binding transcription factors and can interact with specific bHLH proteins. Nucleic Acids Res 35:6663–6671CrossRefPubMedGoogle Scholar
  31. Ilegems M, Douet V, Meylan-Bettex M, Uyttewaal M, Brand L, Bowman JL, Stieger PA (2010) Interplay of auxin, KANADI and Class III HD-ZIP transcription factors in vascular tissue formation. Development 137:975–984CrossRefPubMedGoogle Scholar
  32. Ito T, Kim GT, Shinozaki K (2000) Disruption of an Arabidopsis cytoplasmic ribosomal protein S13-homologous gene by transposon-mediated mutagenesis causes aberrant growth and development. Plant J 22:257–264CrossRefPubMedGoogle Scholar
  33. Iwakawa H, Ueno Y, Semiarti E, Onouchi H, Kojima S, Tsukaya H, Hasebe M, Soma T, Ikezaki M, Machida C, Machida Y (2002) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol 43:467–478CrossRefPubMedGoogle Scholar
  34. Iwakawa H, Iwasaki M, Kojima S, Ueno Y, Soma T, Tanaka H, Semiarti E, Machida Y, Machida C (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 51:173–184CrossRefPubMedGoogle Scholar
  35. Izhaki A, Bowman JL (2007) KANADI and class III HD-Zip gene families regulate embryo patterning and modulate auxin flow during embryogenesis in Arabidopsis. Plant Cell 19:495–508CrossRefPubMedGoogle Scholar
  36. Kerstetter RA, Bollman K, Taylor RA, Bomblies K, Poethig RS (2001) KANADI regulates organ polarity in Arabidopsis. Nature 411:706–709CrossRefPubMedGoogle Scholar
  37. Kidner CA, Martienssen RA (2004) Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428:81–84CrossRefPubMedGoogle Scholar
  38. Kim YS, Kim SG, Lee M, Lee I, Park HY, Seo PJ, Jung JH, Kwon EJ, Suh SW, Paek KH, Park CM (2008) HD-ZIP III activity is modulated by competitive inhibitors via a feedback loop in Arabidopsis shoot apical meristem development. Plant Cell 20:920–933CrossRefPubMedGoogle Scholar
  39. Lanet E, Delannoy E, Sormani R, Floris M, Brodersen P, Crete P, Voinnet O, Robaglia C (2009) Biochemical evidence for translational repression by Arabidopsis microRNAs. Plant Cell 21:1762–1768CrossRefPubMedGoogle Scholar
  40. Li H, Xu L, Wang H, Yuan Z, Cao X, Yang Z, Zhang D, Xu Y, Huang H (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 17:2157–2171CrossRefPubMedGoogle Scholar
  41. Lin WC, Shuai B, Springer PS (2003) The Arabidopsis LATERAL ORGAN BOUNDARIES-domain gene ASYMMETRIC LEAVES2 functions in the repression of KNOX gene expression and in adaxial–abaxial patterning. Plant Cell 15:2241–2252CrossRefPubMedGoogle Scholar
  42. Lynn K, Fernandez A, Aida M, Sedbrook J, Tasaka M, Masson P, Barton MK (1999) The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 126:469–481PubMedGoogle Scholar
  43. Mallory AC, Reinhart BJ, Jones-Rhoades MW, Tang G, Zamore PD, Barton MK, Bartel DP (2004) MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region. EMBO J 23:3356–3364CrossRefPubMedGoogle Scholar
  44. Mallory AC, Hinze A, Tucker MR, Bouche N, Gasciolli V, Elmayan T, Lauressergues D, Jauvion V, Vaucheret H, Laux T (2009) Redundant and specific roles of the ARGONAUTE proteins AGO1 and ZLL in development and small RNA-directed gene silencing. PLoS Genet 5:e1000646CrossRefPubMedGoogle Scholar
  45. McConnell JR, Barton MK (1998) Leaf polarity and meristem formation in Arabidopsis. Development 125:2935–2942PubMedGoogle Scholar
  46. McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:709–713CrossRefPubMedGoogle Scholar
  47. Montgomery TA, Howell MD, Cuperus JT, Li D, Hansen JE, Alexander AL, Chapman EJ, Fahlgren N, Allen E, Carrington JC (2008) Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133:128–141CrossRefPubMedGoogle Scholar
  48. Moussian B, Schoof H, Haecker A, Jurgens G, Laux T (1998) Role of the ZWILLE gene in the regulation of central shoot meristem cell fate during Arabidopsis embryogenesis. EMBO J 17:1799–1809CrossRefPubMedGoogle Scholar
  49. Mukherjee K, Bürglin TR (2006) MEKHLA, a novel domain with similarity to PAS domains, is fused to plant homeodomain-leucine zipper III proteins. Plant Physiol 140:1142–1150CrossRefPubMedGoogle Scholar
  50. Ochando I, Jover-Gil S, Ripoll JJ, Candela H, Vera A, Ponce MR, Martinez-Laborda A, Micol JL (2006) Mutations in the microRNA complementarity site of the INCURVATA4 gene perturb meristem function and adaxialize lateral organs in arabidopsis. Plant Physiol 141:607–619CrossRefPubMedGoogle Scholar
  51. Ori N, Eshed Y, Chuck G, Bowman JL, Hake S (2000) Mechanisms that control knox gene expression in the Arabidopsis shoot. Development 127:5523–5532PubMedGoogle Scholar
  52. Otsuga D, DeGuzman B, Prigge MJ, Drews GN, Clark SE (2001) REVOLUTA regulates meristem initiation at lateral positions. Plant J 25:223–236CrossRefPubMedGoogle Scholar
  53. Pekker I, Alvarez JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899–2910CrossRefPubMedGoogle Scholar
  54. Peragine A, Yoshikawa M, Wu G, Albrecht HL, Poethig RS (2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev 18:2368–2379CrossRefPubMedGoogle Scholar
  55. Phelps-Durr TL, Thomas J, Vahab P, Timmermans MC (2005) Maize rough sheath2 and its Arabidopsis orthologue ASYMMETRIC LEAVES1 interact with HIRA, a predicted histone chaperone, to maintain knox gene silencing and determinacy during organogenesis. Plant Cell 17:2886–2898CrossRefPubMedGoogle Scholar
  56. Pinon V, Etchells JP, Rossignol P, Collier SA, Arroyo JM, Martienssen RA, Byrne ME (2008) Three PIGGYBACK genes that specifically influence leaf patterning encode ribosomal proteins. Development 135:1315–1324CrossRefPubMedGoogle Scholar
  57. Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, Clark SE (2005) Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17:61–76CrossRefPubMedGoogle Scholar
  58. Reinhardt D, Frenz M, Mandel T, Kuhlemeier C (2005) Microsurgical and laser ablation analysis of leaf positioning and dorsoventral patterning in tomato. Development 132:15–26CrossRefPubMedGoogle Scholar
  59. Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626CrossRefPubMedGoogle Scholar
  60. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520CrossRefPubMedGoogle Scholar
  61. Rosado A, Sohn EJ, Drakakaki G, Pan S, Swidergal A, Xiong Y, Kang BH, Bressan RA, Raikhel NV (2010) Auxin-mediated ribosomal biogenesis regulates vacuolar trafficking in Arabidopsis. Plant Cell 22:143–158CrossRefPubMedGoogle Scholar
  62. Roudier F, Teixeira FK, Colot V (2009) Chromatin indexing in Arabidopsis: an epigenomic tale of tails and more. Trends Genet 25:511–517CrossRefPubMedGoogle Scholar
  63. Sawa S, Ito T, Shimura Y, Okada K (1999a) FILAMENTOUS FLOWER controls the formation and development of arabidopsis inflorescences and floral meristems. Plant Cell 11:69–86CrossRefPubMedGoogle Scholar
  64. Sawa S, Watanabe K, Goto K, Liu YG, Shibata D, Kanaya E, Morita EH, Okada K (1999b) FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. Genes Dev 13:1079–1088CrossRefPubMedGoogle Scholar
  65. Schrick K, Nguyen D, Karlowski WM, Mayer KF (2004) START lipid/sterol-binding domains are amplified in plants and are predominantly associated with homeodomain transcription factors. Genome Biol 5:R41CrossRefPubMedGoogle Scholar
  66. Schwab R, Maizel A, Ruiz-Ferrer V, Garcia D, Bayer M, Crespi M, Voinnet O, Martienssen RA (2009) Endogenous tasiRNAs mediate non-cell autonomous effects on gene regulation in Arabidopsis thaliana. PLoS One 4:e5980CrossRefPubMedGoogle Scholar
  67. Semiarti E, Ueno Y, Tsukaya H, Iwakawa H, Machida C, Machida Y (2001) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves. Development 128:1771–1783PubMedGoogle Scholar
  68. Sessa G, Steindler C, Morelli G, Ruberti I (1998) The Arabidopsis Athb-8, -9 and -14 genes are members of a small gene family coding for highly related HD-ZIP proteins. Plant Mol Biol 38:609–622CrossRefPubMedGoogle Scholar
  69. Sessions A, Nemhauser JL, McColl A, Roe JL, Feldmann KA, Zambryski PC (1997) ETTIN patterns the Arabidopsis floral meristem and reproductive organs. Development 124:4481–4491PubMedGoogle Scholar
  70. Shuai B, Reynaga-Pena CG, Springer PS (2002) The LATERAL ORGAN BOUNDARIES gene defines a novel, plant-specific gene family. Plant Physiol 129:747–761CrossRefPubMedGoogle Scholar
  71. Siegfried KR, Eshed Y, Baum SF, Otsuga D, Drews GN, Bowman JL (1999) Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126:4117–4128PubMedGoogle Scholar
  72. Stahle MI, Kuehlich J, Staron L, von Arnim AG, Golz JF (2009) YABBYs and the transcriptional corepressors LEUNIG and LEUNIG_HOMOLOG maintain leaf polarity and meristem activity in Arabidopsis. Plant Cell 21:3105–3118CrossRefPubMedGoogle Scholar
  73. Sussex IM (1952) Regeneration of the potato shoot apex. Nature 170:755–757CrossRefGoogle Scholar
  74. Sussex IM (1955) Morphogenesis in Solanum tuberosum L.: apical structure and developmental pattern of the juvenile shoot. Phytomorphology 5:253–273Google Scholar
  75. Talbert PB, Adler HT, Parks DW, Comai L (1995) The REVOLUTA gene is necessary for apical meristem development and for limiting cell divisions in the leaves and stems of Arabidopsis thaliana. Development 121:2723–2735PubMedGoogle Scholar
  76. Theodoris G, Inada N, Freeling M (2003) Conservation and molecular dissection of ROUGH SHEATH2 and ASYMMETRIC LEAVES1 function in leaf development. Proc Natl Acad Sci USA 100:6837–6842CrossRefPubMedGoogle Scholar
  77. Tretter EM, Alvarez JP, Eshed Y, Bowman JL (2008) Activity range of Arabidopsis small RNAs derived from different biogenesis pathways. Plant Physiol 147:58–62CrossRefPubMedGoogle Scholar
  78. Tucker MR, Hinze A, Tucker EJ, Takada S, Jurgens G, Laux T (2008) Vascular signalling mediated by ZWILLE potentiates WUSCHEL function during shoot meristem stem cell development in the Arabidopsis embryo. Development 135:2839–2843CrossRefPubMedGoogle Scholar
  79. Ueno Y, Ishikawa T, Watanabe K, Terakura S, Iwakawa H, Okada K, Machida C, Machida Y (2007) Histone deacetylases and ASYMMETRIC LEAVES2 are involved in the establishment of polarity in leaves of Arabidopsis. Plant Cell 19:445–457CrossRefPubMedGoogle Scholar
  80. Van Lijsebettens M, Vanderhaeghen R, De Block M, Bauw G, Villarroel R, Van Montagu M (1994) An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems. EMBO J 13:3378–3388PubMedGoogle Scholar
  81. Vazquez F, Vaucheret H, Rajagopalan R, Lepers C, Gasciolli V, Mallory AC, Hilbert JL, Bartel DP, Crete P (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell 16:69–79CrossRefPubMedGoogle Scholar
  82. Waites R, Hudson A (1995) phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121:2143–2154Google Scholar
  83. Waites R, Selvadurai HR, Oliver IR, Hudson A (1998) The PHANTASTICA gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. Cell 93:779–789CrossRefPubMedGoogle Scholar
  84. Wenkel S, Emery J, Hou BH, Evans MM, Barton MK (2007) A feedback regulatory module formed by LITTLE ZIPPER and HD-ZIPIII genes. Plant Cell 19:3379–3390CrossRefPubMedGoogle Scholar
  85. Williams L, Grigg SP, Xie M, Christensen S, Fletcher JC (2005) Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development 132:3657–3668CrossRefPubMedGoogle Scholar
  86. Wu G, Lin WC, Huang T, Poethig RS, Springer PS, Kerstetter RA (2008) KANADI1 regulates adaxial–abaxial polarity in Arabidopsis by directly repressing the transcription of ASYMMETRIC LEAVES2. Proc Natl Acad Sci USA 105:16393–16398Google Scholar
  87. Xie Z, Allen E, Wilken A, Carrington JC (2005) DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc Natl Acad Sci USA 102:12984–12989CrossRefPubMedGoogle Scholar
  88. Xu L, Xu Y, Dong A, Sun Y, Pi L, Huang H (2003) Novel as1 and as2 defects in leaf adaxial–abaxial polarity reveal the requirement for ASYMMETRIC LEAVES1 and 2 and ERECTA functions in specifying leaf adaxial identity. Development 130:4097–4107CrossRefPubMedGoogle Scholar
  89. Xu L, Yang L, Pi L, Liu Q, Ling Q, Wang H, Poethig RS, Huang H (2006) Genetic interaction between the AS1-AS2 and RDR6-SGS3-AGO7 pathways for leaf morphogenesis. Plant Cell Physiol 47:853–863CrossRefPubMedGoogle Scholar
  90. Yao Y, Ling Q, Wang H, Huang H (2008) Ribosomal proteins promote leaf adaxial identity. Development 135:1325–1334CrossRefPubMedGoogle Scholar
  91. Yoshikawa M, Peragine A, Park MY, Poethig RS (2005) A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev 19:2164–2175CrossRefPubMedGoogle Scholar
  92. Zhong R, Ye ZH (1999) IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein. Plant Cell 11:2139–2152CrossRefPubMedGoogle Scholar
  93. Zhong R, Ye ZH (2004) Amphivasal vascular bundle 1, a gain-of-function mutation of the IFL1/REV gene, is associated with alterations in the polarity of leaves, stems and carpels. Plant Cell Physiol 45:369–385CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer 2010

Authors and Affiliations

  • Dóra Szakonyi
    • 1
  • Alexis Moschopoulos
    • 1
  • Mary E. Byrne
    • 1
    Email author
  1. 1.John Innes CentreNorwichUK

Personalised recommendations