Mixing and matching pathways in leaf polarity

Current Opinion in Plant Biology

Volumn 10, Issue 1, 2007, Pages 13-20

  Kidner, Catherine A ^a   Timmermans, Marja CP ^b  

^a ROYAL BOTANIC GARDEN EDINBURGH   (United Kingdom)

^b Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT LEAF; REVIEW; RNA INTERFERENCE; SPECIES DIFFERENCE;

ARABIDOPSIS; PLANT LEAVES; RNA INTERFERENCE; SPECIES SPECIFICITY;

EID: 33846225507     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2006.11.013     Document Type: Review

References (64)

1. Bowman J.L., Eshed Y., and Baum S.F. Establishment of polarity in angiosperm lateral organs. Trends Genet 18 (2002) 134-141
2. Timmermans M.C.P., Juarez M.T., and Phelps-Durr T.L. A conserved microRNA signal specifies leaf polarity. Cold Spring Harb Symp Quant Biol 69 (2004) 409-417
3. Sussex I.M. Experiments on the cause of dorsiventrality in leaves. Nature 167 (1951) 651-652
4. Reinhardt D., Frenz M., Mandel T., and Kuhlemeier C. Microsurgical and laser ablation analysis of leaf positioning and dorsoventral patterning in tomato. Development 132 (2005) 15-26. An extension of the surgical experiments of the earlier twentieth century. Here, laser ablation and surgical excision in the tomato meristem are used to define cell-to-cell signaling during leaf development, demonstrating the importance of the epidermal layer in leaf polarity.
5. McConnell J.R., Emery J., Eshed Y., Bao N., Bowman J., and Barton M.K. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411 (2001) 709-713
6. Emery J.F., Floyd S.K., Alvarez J., Eshed Y., Hawker N.P., Izhaki A., Baum S.F., and Bowman J.L. Radial patterning of Arabidopsis shoots by Class III HD-ZIP and KANADI genes. Curr Biol 13 (2003) 1768-1774
7. Prigge M.J., Otsuga D., Alonso J.M., Ecker J.R., Drews G.N., and Clark S.E. Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17 (2005) 61-76
8. Otsuga D., DeGuzman B., Prigge M.J., Drews G.N., and Clark S.E. REVOLUTA regulates meristem initiation at lateral positions. Plant J 25 (2001) 223-236
9. Kerstetter R.A., Bollman K., Taylor R.A., Bomblies K., and Poethig R.S. KANADI regulates organ polarity in Arabidopsis. Nature 411 (2001) 706-709
10. Eshed Y., Baum S.F., Perea J.V., and Bowman J.L. Establishment of polarity in lateral organs of plants. Curr Biol 11 (2001) 1251-1260
11. Eshed Y., Izhaki A., Baum S.F., Floyd S.K., and Bowman J.L. Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities. Development 131 (2004) 2997-3006
12. Pekker I., Alvarez J.P., and Eshed Y. Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17 (2005) 2899-2910. Mutations in ETTIN (ETT/ARF3) were isolated as second site repressors of ectopic KANADI (KAN) activity. Double mutants affecting ETT and its close homolog ARF4 adaxialize plant organs, and both ETT and ARF4 are abaxially expressed. As KAN is not required for either ETT or ARF4 transcription, and overexpression of these genes cannot rescue kan mutants, the authors propose cooperative activity of KAN, ETT and ARF4 in abaxial fate specification. This study further implies a role for auxin in adaxial-abaxial patterning.
13. Hake S., Smith H.M., Holtan H., Magnani E., Mele G., and Ramirez J. The role of knox genes in plant development. Annu Rev Cell Dev Biol 20 (2004) 125-151
14. Li H., Xu L., Wang H., Yuan Z., Cao X., Yang Z., Zhang D., Xu Y., and Huang H. 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 (2005) 2157-2171. An enhancer of the as2 phenotype is identified as rdr6. Leaves of as2 rdr6 double mutants are abaxialized. These leaves also show increased expression levels of the abaxial determinants miR165 and FIL, and a concomitant reduction in HD-ZIPIII expression.
15. Garcia D., Collier S.A., Byrne M.E., and Martienssen R.A. Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr Biol 16 (2006) 933-938. Microarray analysis confirms that FIL is downstream of both the AS1-AS2 and ta-siRNA pathways. Adaxially expressed TAS3 is proposed to restrict ETT and ARF4 expression, and thereby to act redundantly with AS1-AS2 in preventing adaxial FIL expression.
16. Xu L., Yang L., Pi L., Liu Q., Ling Q., Wang H., Poethig R.S., and Huang H. Genetic interaction between the AS1-AS2 and RDR6-SGS3-AGO7 pathways for leaf morphogenesis. Plant Cell Physiol 47 (2006) 853-863
17. Waites R., and Hudson A. phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121 (1995) 2143-2154
18. Waites R., Selvadurai H.R., Oliver I.R., and Hudson A. The PHANTASTICA gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. Cell 93 (1998) 779-789
19. Lin W.C., Shuai B., and Springer P.S. 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 (2003) 2241-2252
20. Siegfried K.R., Eshed Y., Baum S.F., Otsuga D., Drews G.N., and Bowman J.L. Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126 (1999) 4117-4128
21. Kidner C.A., and Martienssen R.A. The developmental role of microRNA in plants. Curr Opin Plant Biol 8 (2005) 38-44
22. Jones-Rhoades M.W., Bartel D.P., and Bartel B. MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57 (2006) 19-53
23. Reinhart B.J., Weinstein E.G., Rhoades M.W., Bartel B., and Bartel D.P. MicroRNAs in plants. Genes Dev 16 (2002) 1616-1626
24. Juarez M.T., Kui J.S., Thomas J., Heller B.A., and Timmermans M.C.P. microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428 (2004) 84-88
25. Kidner C.A., and Martienssen R.A. Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428 (2004) 81-84
26. Mallory A.C., Reinhart B.J., Jones-Rhoades M.W., Tang G., Zamore P.D., Barton M.K., and Bartel D.P. MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region. EMBO J 23 (2004) 3356-3364
27. Alvarez J.P., Pekker I., Goldshmidt A., Blum E., Amsellem Z., and Eshed Y. Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell 18 (2006) 1134-1151. By driving the miRNA165 precursor miR165b under tissue-specific promoters, the authors show that ectopic expression of miR165 can induce abaxial cell fate. Using synthetic miRNAs, they confirm that ARF2, ETT and ARF4 are required for abaxial identity. This study also suggests that miRNAs act largely cell autonomously.
28. Bao N., Lye K.W., and Barton M.K. MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome. Dev Cell 7 (2004) 653-662
29. Allen E., Xie Z., Gustafson A.M., and Carrington J.C. microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121 (2005) 207-221. Computational and expression analyses identify five ta-siRNA generating loci, one of which (TAS3) produces a ta-siRNA that directs the cleavage of ARF3 and ARF4 transcripts. This study further shows that miRNA-guided cleavage sets up the 21-nt phase for ta-siRNA precursor processing.
30. Williams L., Carles C.C., Osmont K.S., and Fletcher J.C. A database analysis method identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. Proc Natl Acad Sci USA 102 (2005) 9703-9708. The authors identify a conserved ta-siRNA that targets members of the ARF family.
31. Brodersen P., and Voinnet O. The diversity of RNA silencing pathways in plants. Trends Genet 22 (2006) 268-280
32. Peragine A., Yoshikawa M., Wu G., Albrecht H.L., and Poethig R.S. SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev 18 (2004) 2368-2379
33. Adenot X., Elmayan T., Lauressergues D., Boutet S., Bouche N., Gasciolli V., and Vaucheret H. DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr Biol 16 (2006) 927-932. The authors use mutations in each of the TAS loci and hypomorphic alleles of rdr6 and sgs3 to demonstrate the importance of the TAS3 ta-siRNA pathway to leaf development.
34. Fahlgren N., Montgomery T.A., Howell M.D., Allen E., Dvorak S.K., Alexander A.L., and Carrington J.C. Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16 (2006) 939-944. TAS3 ta-siRNA regulation of ETT requires AGO7. Loss of this regulation accelerates the vegetative phase change. Further overexpression of ARF3 using ta-siRNA resistant alleles revealed additional roles for ARF3 in leaf development, including a role in adaxial-abaxial patterning.
35. Hunter C., Willmann M.R., Wu G., Yoshikawa M., de la Luz Gutierrez-Nava M., and Poethig S.R. Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis. Development 133 (2006) 2973-2981. Mutations affecting ta-siRNA biogenesis accelerate the juvenile-to-adult transition. A screen for second site suppressors of this phenotype identified ETT and ARF4, suggesting that these transcription factors regulate heteroblasty and that their overexpression is responsible for the leaf phenotypes observed in rdr6, sgs3, dcl4 and ago7.
36. Grigg S.P., Canales C., Hay A., and Tsiantis M. SERRATE coordinates shoot meristem function and leaf axial patterning in Arabidopsis. Nature 437 (2005) 1022-1026. The authors show that SERRATE is required for axial polarity and control of meristem size, acting through regulation of HD-ZIPIII genes and subsequent effects on KNOX activity. SERRATE affects HD-ZIPIII expression by regulating the biogenesis of miR166.
37. Yang L., Liu Z., Lu F., Dong A., and Huang H. SERRATE is a novel nuclear regulator in primary microRNA processing in Arabidopsis. Plant J 47 (2006) 841-850. The zinc-finger protein SERRATE is shown to act together with HYL1, a nuclear double-stranded RNA-binding protein, in the processing of multiple miRNAs and ta-siRNAs.
38. Reinhardt D., Pesce E.R., Stieger P., Mandel T., Baltensperger K., Bennett M., Traas J., Friml J., and Kuhlemeier C. Regulation of phyllotaxis by polar auxin transport. Nature 426 (2003) 255-260
39. Tiwari S.B., Hagen G., and Guilfoyle T. The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15 (2003) 533-543
40. Heisler M.G., Ohno C., Das P., Sieber P., Reddy G.V., Long J.A., and Meyerowitz E.M. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol 15 (2005) 1899-1911. Live imaging of fluorescent reporter genes is used to monitor the expression patterns of several proteins during flower development. The expression patterns of the auxin efflux carrier PIN1 and the polarity determinants REV and FIL support a role for auxin transport in phyllotaxis and positioning of the adaxial-abaxial boundary.
41. Floyd S.K., Zalewski C.S., and Bowman J.L. Evolution of class III homeodomain-leucine zipper genes in streptophytes. Genetics 173 (2006) 373-388. Phylogenetic and expression pattern analyses of HD-ZIPIII genes show that this gene family existed in the common ancestor of land plants, and suggest that diversification into paralogs that regulate apical growth, vascular patterning and leaf development has occurred during streptophyte evolution.
42. Floyd S.K., and Bowman J.L. Gene regulation: ancient microRNA target sequences in plants. Nature 428 (2004) 485-486
43. Carlsbecker A., and Helariutta Y. Phloem and xylem specification: pieces of the puzzle emerge. Curr Opin Plant Biol 8 (2005) 512-517
44. Harrison C.J., Corley S.B., Moylan E.C., Alexander D.L., Scotland R.W., and Langdale J.A. Independent recruitment of a conserved developmental mechanism during leaf evolution. Nature 434 (2005) 509-514. Gene expression data from a microphyllous lycophyte, phylogenetic analyses, and a cross-species complementation experiment all show that a common developmental mechanism, KNOX regulation by ARP proteins, can underpin both microphyll and megaphyll formation.
45. McHale N.A., and Koning R.E. PHANTASTICA regulates development of the adaxial mesophyll in Nicotiana leaves. Plant Cell 16 (2004) 1251-1262
46. Kim M., McCormick S., Timmermans M., and Sinha N. The expression domain of PHANTASTICA determines leaflet placement in compound leaves. Nature 424 (2003) 438-443
47. Luo J.H., Yan J., Weng L., Yang J., Zhao Z., Chen J.H., Hu X.H., and Luo D. Different expression patterns of duplicated PHANTASTICA-like genes in Lotus japonicus suggest their divergent functions during compound leaf development. Cell Res 15 (2005) 665-677. Expression analyses of two ARP paralogs in Lotus Japonicus show that both are expressed on the adaxial side of young leaf primordia. In later leaf development, one is expressed in the central region of leaflets, the other adaxially. Two mutants that affect adaxial-abaxial polarity in leaflets and the expression patterns of both ARPs are also described.
48. Byrne M.E., Barley R., Curtis M., Arroyo J.M., Dunham M., Hudson A., and Martienssen R.A. Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408 (2000) 967-971
49. Hay A., and Tsiantis M. The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nat Genet 38 (2006) 942-947. The authors analyze the contribution of ARP and KNOX genes to the variation in leaf form between Arabidopsis thaliana (simple leaves) and its relative Cardamine hirsuta (compound leaves) using mutational, expression, and complementation analyses. The function of ARP in KNOX gene regulation is conserved between the two species. Changes in the KNOX regulation that occur independently of ARP might underlie the differences in leaf form.
50. Tattersall A.D., Turner L., Knox M.R., Ambrose M.J., Ellis T.H., and Hofer J.M. The mutant crispa reveals multiple roles for PHANTASTICA in pea compound leaf development. Plant Cell 17 (2005) 1046-1060. In crispa, a mutant that is affected in the pea ARP ortholog, the main axis of the leaf develops normal polarity but individual leaflets are abaxialized. In addition, ectopic stipules are formed from regions of ectopic KNOX expression on the petiole and rachis. This study provides further evidence for the independent derivation of compound leaves in tomato and pea.
51. Arazi T., Talmor-Neiman M., Stav R., Riese M., Huijser P., and Baulcombe D.C. Cloning and characterization of micro-RNAs from moss. Plant J 43 (2005) 837-848
52. Axtell M.J., and Bartel D.P. Antiquity of microRNAs and their targets in land plants. Plant Cell 17 (2005) 1658-1673
53. Cooke T.J., Poli D., Sztein A.E., and Cohen J.D. Evolutionary patterns in auxin action. Plant Mol Biol 49 (2002) 319-338
54. Timmermans M.C.P., Schultes N.P., Jankovsky J.P., and Nelson T. Leafbladeless1 is required for dorsoventrality of lateral organs in maize. Development 125 (1998) 2813-2823
55. Dunoyer P., Himber C., and Voinnet O. DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nat Genet 37 (2005) 1356-1360
56. Timmermans M.C.P., Hudson A., Becraft P.W., and Nelson T. ROUGH SHEATH2: a Myb protein that represses knox homeobox genes in maize lateral organ primordia. Science 284 (1999) 151-153
57. Tsiantis M., Schneeberger R., Golz J.F., Freeling M., and Langdale J.A. The maize rough sheath2 gene and leaf development programs in monocot and dicot plants. Science 284 (1999) 154-156
58. Golz J.F., Roccaro M., Kuzoff R., and Hudson A. GRAMINIFOLIA promotes growth and polarity of Antirrhinum leaves. Development 131 (2004) 3661-3670
59. Navarro C., Efremova N., Golz J.F., Rubiera R., Kuckenberg M., Castillo R., Tietz O., Saedler H., and Schwarz-Sommer Z. Molecular and genetic interactions between STYLOSA and GRAMINIFOLIA in the control of Antirrhinum vegetative and reproductive development. Development 131 (2004) 3649-3659
60. Kim M., Pham T., Hamidi A., McCormick S., Kuzoff R.K., and Sinha N. Reduced leaf complexity in tomato wiry mutants suggests a role for PHAN and KNOX genes in generating compound leaves. Development 130 (2003) 4405-4415
61. Yamaguchi T., Nagasawa N., Kawasaki S., Matsuoka M., Nagato Y., and Hirano H.Y. The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa. Plant Cell 16 (2004) 500-509
62. Gleissberg S., Groot E.P., Schmalz M., Eichert M., Kolsch A., and Hutter S. Developmental events leading to peltate leaf structure in Tropaeolum majus (Tropaeolaceae) are associated with expression domain changes of a YABBY gene. Dev Genes Evol 215 (2005) 313-319. Expression analysis of a FIL homolog in the basal brassicale Tropaeoleum shows abaxial localization followed by a focus of adaxial expression at a position from which the peltate lamina will grow out.
63. Juarez M.T., Twigg R.W., and Timmermans M.C.P. Specification of adaxial cell fate during maize leaf development. Development 131 (2004) 4533-4544
64. Floyd S.K., and Bowman J.L. Distinct developmental mechanisms reflect the independent origins of leaves in vascular plants. Curr Biol 16 (2006) 1911-1917