LATHYROIDES, encoding a WUSCHEL-related homeobox1 transcription factor, controls organ lateral growth, and regulates tendril and dorsal petal identities in garden pea (Pisum sativum L.)

Molecular Plant

Volumn 5, Issue 6, 2012, Pages 1333-1345

  Zhuang, Li Li ^a   Ambrose, Mike ^b   Rameau, Catherine ^c   Weng, Lin ^d   Yang, Jun ^d   Hu, Xiao He ^e   Luo, Da ^e   Li, Xin ^e  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b JOHN INNES CENTRE   (United Kingdom)

^c INSTITUT JEAN PIERRE BOURGIN   (France)

^d INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^e SUN YAT SEN UNIVERSITY   (China)

Author keywords

lateral growth; LATH; LST; organ identity; pea; TL

Indexed keywords

EID: 84870498218     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/sss067     Document Type: Article

References (64)

1. Aggarwal, P., Das Gupta, M., Joseph, A.P., Chatterjee, N., Srinivasan, N., and Nath, U. (2010). Identification of specific DNA binding residues in the TCP family of transcription factors in Arabidopsis. Plant Cell. 22, 1174-1189.
2. Ambrose, M.J. (2003). Further observations on the expression of lobed standard (lst) and keeled wings (k) and their involvement in petal identity. Pisum Genet. 35, 1-2.
3. Aubert, G., Morin, J., Jacquin, F., Loridon, K., Quillet, M.C., Petit, A., Rameau, C., Lejeune-Hénaut, I., Huguet, T., and Burstin, J. (2006). Functional mapping in pea, as an aid to the candidate gene selection and for investigating synteny with the model legume Medicago truncatula. Theor. Appl. Genet. 112, 1024-1241.
4. Baima, S., Possenti, M., Matteucci, A., Wisman, E., Altamura, M.M., Ruberti, I., and Morelli, G. (2001). The Arabidopsis ATHB-8 HD-ZIP protein acts as a differentiation-promoting transcription factor of the vascular meristems. Plant Physiol. 126, 643-655. (Pubitemid 32566619)
5. Baumann, K., Perez-Rodriguez, M., Bradley, D., Venail, J., Bailey, P., Jin, H.L., Koes, R., Roberts, K., and Martin, C. (2007). Control of cell and petal morphogenesis by R2R3 MYB transcription factors. Development. 134, 1691-1701. (Pubitemid 46796566)
6. Berdnikov, V.A., Gorel, F.L., Kosterin, O.E., and Rozov, S.M. (1997). A lathyroides-phenotype mutation affecting both foliage and flower structures. Pisum Genet. 29, 42.
7. Bonke, M., Thitamadee, S., Mähönen, A.P., Hauser, M.T., and Helariutta, Y. (2003). APL regulates vascular tissue identity in Arabidopsis. Nature. 426, 181-186. (Pubitemid 37442586)
8. Byrne, M., Timmermans, M., Kidner, C., and Martienssen, R. (2001). Development of leaf shape. Curr. Opin. Plant Biol. 4, 38-43. (Pubitemid 32111252)
9. Byrne, M.E. (2005). Networks in leaf development. Curr. Opin. Plant Biol. 8, 59-66. (Pubitemid 40084748)
10. Cannon, S.B., et al. (2006). Legume genome evolution viewed through the Medicago truncatula and Lotus japonicus genomes. Proc. Natl Acad. Sci. U S A. 103, 14959-14964. (Pubitemid 44527836)
11. Chen, C., Wang, S., and Huang, H. (2000). LEUNIG has multiple functions in gynoecium development in Arabidopsis. Genesis. 26, 42-54. (Pubitemid 30123464)
12. Chen, J.H., Pang, J.L., Wang, L.L., Luo, Y.H., Li, X., Cao, X.L., Lin, K., Ma, W., Hu, X.H., and Luo, D. (2006). Wrinkled petals and stamens 1, is required for the morphogenesis of petals and stamens in Lotus japonicus. Cell Res. 16, 499-506. (Pubitemid 43987402)
13. Choi, H.K., et al. (2004). Estimating genome conservation between crop and model legume species. Proc. Natl Acad. Sci. U S A. 101, 15289-15294.
14. Coen, E.S., Romero, J.M., Doyle, S., Elliott, R., Murphy, G., and Carpenter, R. (1990). Floricaula: a homeotic gene required for flower development in Antirrhinum majus. Cell. 63, 1311-1322. (Pubitemid 120035079)
15. Dai, M., Hu, Y., Zhao, Y., Liu, H., and Zhou, D.X. (2007). A WUSCHEL-LIKE HOMEOBOX gene represses a YABBY gene expression required for rice leaf development. Plant Physiol. 144, 380-390. (Pubitemid 46941641)
16. Demason, D.A., and Chetty, V.J. (2011). Interactions between GA, auxin, and UNI expression controlling shoot ontogeny, leaf morphogenesis, and auxin response in Pisum sativum (Fabaceae): or how the uni-tac mutant is rescued. Am. J. Bot. 98, 775-791.
17. Feng, X., et al. (2006). Control of petal shape and floral zygomorphy in Lotus japonicas. Proc. Natl Acad. Sci. U S A. 103, 4970-4975.
18. Franssen, S.U., Shrestha, R.P., Bräutigam, A., Bornberg-Bauer, E., and Weber, A.P. (2011). Comprehensive transcriptome analysis of the highly complex Pisum sativum genome using next generation sequencing. BMC Genomics. 12, 227.
19. Glover, B.J., Perez-Rodriguez, M., and Martin, C. (1998). Development of several epidermal cell types can be specified by the same MYB-related plant transcription factor. Development. 125, 3497-3508. (Pubitemid 28458348)
20. Golz, J.F., and Hudson, A. (2002). Signalling in plant lateral organ development. Plant Cell. 14 Suppl., S277-S288. (Pubitemid 34609244)
21. Gourlay, C.W., Hofer, J.M., and Ellis, T.H. (2000). Pea compound leaf architecture is regulated by interactions among the genes UNIFOLIATA, cochleata, afila, and tendril-less. Plant Cell. 12, 1279-1294.
22. Green, P.B., and Linstead, P. (1990). A procedure for SEM of complex shoot structures applied to the inflorescence of snapdragon (Antirrhinum). Protoplasma. 158, 33-38.
23. Hofer, J., et al. (2009). Tendril-less regulates tendril formation in pea leaves. Plant Cell. 21, 420-428.
24. Hofer, J., Turner, L., Hellens, R., Ambrose, M., Matthews, P., Michael, A., and Ellis, N. (1997). UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr. Biol. 7, 581-587. (Pubitemid 27335653)
25. Ingram, G.C., and Waites, R. (2006). Keeping it together: co-ordinating plant growth. Curr. Opin. Plant Biol. 9, 12-20. (Pubitemid 43017858)
26. Johnson, K., and Lenhard, M. (2011). Genetic control of plant organ growth. New Phytol. 191, 319-333.
27. Kaló, P., Seres, A., Taylor, S.A., Jakab, J., Kevei, Z., Kereszt, A., Endre, G., Ellis, T.H., and Kiss, G.B. (2004). Comparative mapping between Medicago sativum and Pisum sativum. Mol. Genet. Genomics. 272, 235-246. (Pubitemid 39506558)
28. Kamiya, N., Nagasaki, H., Morikami, A., Sato, Y., and Matsuoka, M. (2003). Isolation and characterization of a rice WUSCHEL-type homeobox gene that is specifically expressed in the central cells of a quiescent center in the root apical meristem. Plant J. 35, 429-441. (Pubitemid 37056826)
29. Kosugi, S., and Ohashi, Y. (2002). DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J. 30, 337-348. (Pubitemid 34553812)
30. Krizek, B.A. (2009). Making bigger plants: key regulators of final organ size. Curr. Opin. Plant Biol. 12, 17-22.
31. Leibfried, A., To, J.P., Busch, W., Stehling, S., Kehle, A., Demar, M., Kieber, J.J., and Lohmann, J.U. (2005). WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature. 438, 1172-1175. (Pubitemid 41831688)
32. Li, C., Potuschak, T., Colón-Carmona, A., Gutiérrez, R.A., and Doerner, P. (2005). Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proc. Natl Acad. Sci. U S A. 102, 12978-12983. (Pubitemid 41279475)
33. Li, X., Rameau, C., Luo D., and Ambrose, M. (2008). Floral mutants: allele designations at the LST and the K loci and the mapping of SYP1. Pisum Genetics. 40, 19-20.
34. Li, X., Zhuang, L.L., Ambrose, M., Rameau, C., Hu, X.H., Yang, J., and Luo, D. (2010). Genetic analysis of ele mutants and comparative mapping of ele1 locus in the control of organ internal asymmetry in garden pea. J. Integr. Plant Biol. 52, 528-535.
35. Lohmann, J.U., Hong, R.L., Hobe, M., Busch, M.A., Parcy, F., Simon, R., and Weigel, D. (2001). A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell. 105, 793-803. (Pubitemid 32635108)
36. Loridon, K., et al. (2005). Microsatellite marker polymorphism and mapping in pea (Pisum sativum L.). Theor. Appl. Genet. 111, 1022-1031. (Pubitemid 41435104)
37. Marx, G.A. (1987). A suite of mutants that modify pattern formation in pea leaves. Plant Mol. Biol. Rep. 5, 311-335.
38. Matsumoto, N., and Okada, K. (2001). A homeobox gene, PRESSED FLOWER, regulates lateral axis-dependent development of Arabidopsis flowers. Genes Dev. 15, 3355-3364. (Pubitemid 34008199)
39. Meicenheimer, R.D., Muehlbauer, F.J., Hindman, J.L., and Gritton, E.T. (1983). Meristem characteristics of genetically modified pea (Pisum sativum) leaf primordia. Can. J. Bot. 61, 3430-3437.
40. Metzker, M.L. (2010). Sequencing technologies: the next generation. Nat. Rev. Gen. 11, 31-46.
41. Mishra, R.K., Chaudhary, S., Kumar, A., and Kumar, S. (2009). Effects of MULTIFOLIATE-PINNA, AFILA, TENDRIL-LESS and UNIFOLIATA genes on leafblade architecture in Pisum sativum. Planta. 230, 177-190.
42. Nardmann, J., Ji, J., Werr, W., and Scanlon, M.J. (2004). The maize duplicate genes narrow sheath1 and narrow sheath2 encode a conserved homeobox gene function in a lateral domain of shoot apical meristems. Development. 131, 2827-2839. (Pubitemid 38997272)
43. Noda, K., Glover, B.J., Linstead, P., and Martin, C. (1994). Flower colour intensity depends on specialized cell shape controlled by a Myb-related transcription factor. Nature. 369, 661-664. (Pubitemid 24199471)
44. Ojeda, I., Francisco-Ortega, J., and Cronk, Q.C. (2009). Evolution of petal epidermal micromorphology in Leguminosae and its use as a marker of petal identity. Ann. Bot. 104, 1099-1110.
45. Pellew, C., and Sverdrup, A. (1923). New observations on the genetics of peas (Pisum sativum). J. Genet. 13, 125-131.
46. Perez-Rodriguez, M., Jaffe, F.W., Butelli, E., Glover, B.J., and Martin, C. (2005). Development of three different cell types is associated with the activity of a specific MYB transcription factor in the ventral petal of Antirrhinum majus flowers. Development. 132, 359-370. (Pubitemid 40268285)
47. Scanlon, M.J., Schneeberger, R.G., and Freeling, M. (1996). The maize mutant narrow sheath fails to establish leaf margin identity in a meristematic domain. Development. 122, 1683-1691. (Pubitemid 26192734)
48. Shimizu, R., Ji, J., Kelsey, E., Ohtsu, K., Schnable, P.S., and Scanlon, M.J. (2009). Tissue specificity and evolution of meristematic WOX3 function. Plant Physiol. 149, 841-850.
49. Tadege, M., et al. (2011). STENOFOLIA regulates blade outgrowth and leaf vascular patterning in Medicago truncatula and Nicotiana sylvestris. Plant Cell. 23, 2125-2142.
50. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599. (Pubitemid 47236692)
51. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680. (Pubitemid 24354800)
52. Tsukaya, H. (2006). Mechanism of leaf-shape determination. Annu. Rev. Plant Biol. 57, 477-496. (Pubitemid 44061034)
53. Tucker, S.C. (1989). Overlapping organ initiation and common primordial in flowers of Pisum sativum (Leguminosae: Papilionoideae). Amer. J. Botany. 76, 714-729.
54. Tucker, S.C. (2003). Floral development in legumes. Plant Physiol. 131, 911-926. (Pubitemid 36400331)
55. Vandenbussche, M., Horstman, A., Zethof, J., Koes, R., Rijpkema, A.S., and Gerats T. (2009). Differential recruitment of WOX transcription factors for lateral development and organ fusion in Petunia and Arabidopsis. Plant Cell. 21, 2269-2283.
56. Varshney, R.K., Close, T.J., Singh, N.K., Hoisington. D.A., and Cook, D.R. (2009). Orphan legume crops enter the genomics era! Curr. Opin. Plant Biol. 12, 202-210.
57. Veit, B. (2006). Stem cell signalling networks in plants. Plant Mol. Biol. 60, 793-810. (Pubitemid 43794832)
58. Villani, P.J., and DeMason, D.A. (1997). Roles of the af and tl genes in pea leaf morphogenesis: characterisation of the double mutant (af/af, tl/tl). Am. J. Bot. 84, 1323-1336. (Pubitemid 27451553)
59. Waites, R., and Hudson, A. (1995). Phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development. 121, 2143-2154.
60. Wang, Z., et al. (2008). Genetic control of floral zygomorphy in pea (Pisum sativum L.). Proc. Natl Acad. Sci. U S A. 105, 10414-10419.
61. Weng, L., Tian, Z., Feng, X., Li, X., Xu, S., Hu, X., Luo, D., and Yang, J. (2011). Petal development in Lotus japonicus. J. Integr. Plant Biol. 53, 770-782.
62. Winfield, P. (1987). A new gene (lst) which influences standard shape in Pisum sativum. Pisum Newslett. 19, 84-85.
63. Young, N.D., and Udvardi, M. (2009). Translating Medicago truncatula genomics to crop legumes. Curr. Opin. Plant Biol. 12, 193-201.
64. Zhao, Y., Hu, Y., Dai, M., Huang, L., and Zhou, D.X. (2009). The WUSCHEL-related homeobox gene WOX11 is required to activate shoot-borne crown root development in rice. Plant Cell. 21, 736-748.