Leaf morphology is one of the most variable, yet inheritable, traits in the plant kingdom. How plants develop a variety of forms and shapes is a major biological question. Here, we discuss some recent progress in understanding the development of compound or dissected leaves in model species, such as tomato ( Solanum lycopersicum), Cardamine hirsuta and Medicago truncatula, with an emphasis on recent discoveries in legumes. We also discuss progress in gene regulations and hormonal actions in compound leaf development. These studies facilitate our understanding of the underlying regulatory mechanisms and put forward a prospective in compound leaf studies.
References
[1]
Nealson, K.; Conrad, P. Life: Past, present and future. Phil. Trans. R. Soc. B 1999, 354, 1923–1939, doi:10.1098/rstb.1999.0532.
[2]
Field, C.; Behrenfeld, M.; Randerson, J.; Falkowski, P. Primary production of the biosphere: Integrating terrestrial and oceanic components. Science 1998, 281, 237–240, doi:10.1126/science.281.5374.237.
[3]
Zimmermann, W. Main results of the telome theory. Palaeobotanist 1952, 1, 456–470.
[4]
Champagne, C.; Sinha, N. Compound leaves: Equal to the sum of their parts? Development 2004, 131, 4401–4412, doi:10.1242/dev.01338.
[5]
Goliber, T.; Kessler, S.; Chen, J.J.; Bharathan, G.; Sinha, N. Genetic, molecular, and morphological analysis of compound leaf development. Curr. Top. Dev. Biol. 1999, 43, 259–290.
[6]
Allsopp, A. Land and water forms: Physiological aspects. Handb. Pflanzenphysiol. 1965, 15, 1236–1255.
[7]
Hay, A.; Tsiantis, M. The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nat. Genet. 2006, 38, 942–947, doi:10.1038/ng1835.
[8]
Merrill, E. Heteroblastic seedlings of green ash. I. Predictability of leaf form and primordial length. Can. J. Bot. 1986, 64, 2645–2649, doi:10.1139/b86-348.
[9]
Wang, H.; Chen, J.; Wen, J.; Tadege, M.; Li, G.; Liu, Y.; Mysore, K.S.; Ratet, P.; Chen, R. Control of compound leaf development by FLORICAULA/LEAFY ortholog SINGLE LEAFLET1 in Medicago truncatula. Plant Physiol. 2008, 146, 1759–1772, doi:10.1104/pp.108.117044.
[10]
Givnish, T.J. Comparative studies of leaf form: Assessing the relative roles of selective pressures and phylogenetic constraints. New Phytol. 1987, 106, 131–160, doi:10.1111/j.1469-8137.1987.tb04687.x.
[11]
Niinemets, ü. Are compound-leaved woody species inherently shade-intolerant? An analysis of species ecological requirements and foliar support costs. Plant Ecol. 1998, 134, 1–11, doi:10.1023/A:1009773704558.
[12]
Popma, J.; Bongers, F.; Werger, M. Gap-dependence and leaf characteristics of trees in a tropical lowland rain forest in Mexico. Oikos 1992, 63, 207–214, doi:10.2307/3545380.
[13]
Champagne, C.E.; Goliber, T.E.; Wojciechowski, M.F.; Mei, R.W.; Townsley, B.T.; Wang, K.; Paz, M.M.; Geeta, R.; Sinha, N.R. Compound leaf development and evolution in the legumes. Plant Cell 2007, 19, 3369–3378, doi:10.1105/tpc.107.052886.
[14]
Cronk, Q.C. Plant evolution and development in a post-genomic context. Nat. Rev. Genet. 2001, 2, 607–619, doi:10.1038/35084556.
[15]
Bharathan, G.; Sinha, N.R. The regulation of compound leaf development. Plant Physiol. 2001, 127, 1533–1538, doi:10.1104/pp.010867.
[16]
Hake, S.; Smith, H.M.; Holtan, H.; Magnani, E.; Mele, G.; Ramirez, J. The role of knox genes in plant development. Annu. Rev. Cell Dev. Biol. 2004, 20, 125–151, doi:10.1146/annurev.cellbio.20.031803.093824.
[17]
Hay, A.; Tsiantis, M. KNOX genes: Versatile regulators of plant development and diversity. Development 2010, 137, 3153–3165, doi:10.1242/dev.030049.
[18]
Long, J.A.; Moan, E.I.; Medford, J.I.; Barton, M.K. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 1996, 379, 66–69, doi:10.1038/379066a0.
[19]
Burko, Y.; Shleizer-Burko, S.; Yanai, O.; Shwartz, I.; Zelnik, I.D.; Jacob-Hirsch, J.; Kela, I.; Eshed-Williams, L.; Ori, N. A role for APETALA1/FRUITFULL transcription factors in tomato leaf development. Plant Cell 2013, doi:10.1105/tpc.1113.113035.
[20]
Shani, E.; Burko, Y.; Ben-Yaakov, L.; Berger, Y.; Amsellem, Z.; Goldshmidt, A.; Sharon, E.; Ori, N. Stage-specific regulation of Solanum lycopersicum leaf maturation by class 1 KNOTTED1-LIKE HOMEOBOX proteins. Plant Cell 2009, 21, 3078–3092, doi:10.1105/tpc.109.068148.
[21]
Chen, J.J.; Janssen, B.J.; Williams, A.; Sinha, N. A gene fusion at a homeobox locus: Alterations in leaf shape and implications for morphological evolution. Plant Cell 1997, 9, 1289–1304.
[22]
Parnis, A.; Cohen, O.; Gutfinger, T.; Hareven, D.; Zamir, D.; Lifschitz, E. The dominant developmental mutants of tomato, Mouse-ear and Curl, are associated with distinct modes of abnormal transcriptional regulation of a Knotted gene. Plant Cell 1997, 9, 2143–2158.
[23]
Hareven, D.; Gutfinger, T.; Parnis, A.; Eshed, Y.; Lifschitz, E. The making of a compound leaf: genetic manipulation of leaf architecture in tomato. Cell 1996, 84, 735–744, doi:10.1016/S0092-8674(00)81051-X.
[24]
Janssen, B.J.; Lund, L.; Sinha, N. Overexpression of a homeobox gene, LeT6, reveals indeterminate features in the tomato compound leaf. Plant Physiol. 1998, 117, 771–786, doi:10.1104/pp.117.3.771.
[25]
Efroni, I.; Blum, E.; Goldshmidt, A.; Eshed, Y. A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. Plant Cell 2008, 20, 2293–2306, doi:10.1105/tpc.107.057521.
Hagemann, W.; Gleissberg, S. Organogenetic capacity of leaves: The significance of marginal blastozones in angiosperms. Plant Syst. Evol. 1996, 199, 121–152, doi:10.1007/BF00984901.
[28]
Ben-Gera, H.; Ori, N. Auxin and LANCEOLATE affect leaf shape in tomato via different developmental processes. Plant Signal Behav. 2012, 7, 1255–1257, doi:10.4161/psb.21550.
[29]
Yanai, O.; Shani, E.; Russ, D.; Ori, N. Gibberellin partly mediates LANCEOLATE activity in tomato. Plant J. 2011, 68, 571–582, doi:10.1111/j.1365-313X.2011.04716.x.
[30]
Ori, N.; Cohen, A.R.; Etzioni, A.; Brand, A.; Yanai, O.; Shleizer, S.; Menda, N.; Amsellem, Z.; Efroni, I.; Pekker, I.; et al. Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat. Genet. 2007, 39, 787–791, doi:10.1038/ng2036.
[31]
Barkoulas, M.; Hay, A.; Kougioumoutzi, E.; Tsiantis, M. A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta. Nat. Genet. 2008, 40, 1136–1141, doi:10.1038/ng.189.
[32]
Zoulias, N.; Koenig, D.; Hamidi, A.; McCormick, S.; Kim, M. A role for PHANTASTICA in medio-lateral regulation of adaxial domain development in tomato and tobacco leaves. Ann. Bot. 2012, 109, 407–418, doi:10.1093/aob/mcr295.
[33]
Kim, M.; McCormick, S.; Timmermans, M.; Sinha, N. The expression domain of PHANTASTICA determines leaflet placement in compound leaves. Nature 2003, 424, 438–443, doi:10.1038/nature01820.
[34]
Reinhardt, D.; Pesce, E.-R.; Stieger, P.; Mandel, T.; Baltensperger, K.; Bennett, M.; Traas, J.; Friml, J.; Kuhlemeier, C. Regulation of phyllotaxis by polar auxin transport. Nature 2003, 426, 255–260, doi:10.1038/nature02081.
[35]
Pinon, V.; Prasad, K.; Grigg, S.P.; Sanchez-Perez, G.F.; Scheres, B. Local auxin biosynthesis regulation by PLETHORA transcription factors controls phyllotaxis in Arabidopsis. Proc. Natl. Acad. Sci. USA 2012, 110, 1–6.
Zhou, C.; Han, L.; Hou, C.; Metelli, A.; Qi, L.; Tadege, M.; Mysore, K.S.; Wang, Z.Y. Developmental analysis of a Medicago truncatula smooth leaf margin1 mutant reveals context-dependent effects on compound leaf development. Plant Cell 2011, 23, 2106–2124, doi:10.1105/tpc.111.085464.
[38]
DeMason, D.A.; Chawla, R. Roles for auxin during morphogenesis of the compound leaves of pea (Pisum sativum). Planta 2004, 218, 435–448, doi:10.1007/s00425-003-1100-x.
[39]
Avasarala, S.; Yang, J.; Caruso, J.L. Production of phenocopies of the lanceolate mutant in tomato using polar auxin transport inhibitors. J. Exp. Bot. 1996, 47, 709–712, doi:10.1093/jxb/47.5.709.
[40]
Peng, J.; Chen, R. Auxin efflux transporter MtPIN10 regulates compound leaf and flower development in Medicago truncatula. Plant Signal Behav. 2011, 6, 1537–1544, doi:10.4161/psb.6.10.17326.
[41]
Kawamura, E.; Horiguchi, G.; Tsukaya, H. Mechanisms of leaf tooth formation in Arabidopsis. Plant J. 2010, 62, 429–441, doi:10.1111/j.1365-313X.2010.04156.x.
Wang, H.; Jones, B.; Li, Z.; Frasse, P.; Delalande, C.; Regad, F.; Chaabouni, S.; Latche, A.; Pech, J.C.; Bouzayen, M. The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell 2005, 17, 2676–2692, doi:10.1105/tpc.105.033415.
[44]
Zhang, J.; Chen, R.; Xiao, J.; Qian, C.; Wang, T.; Li, H.; Ouyang, B.; Ye, Z. A single-base deletion mutation in SlIAA9 gene causes tomato (Solanum lycopersicum) entire mutant. J. Plant Res. 2007, 120, 671–678, doi:10.1007/s10265-007-0109-9.
[45]
Ben-Gera, H.; Shwartz, I.; Shao, M.R.; Shani, E.; Estelle, M.; Ori, N. ENTIRE and GOBLET promote leaflet development in tomato by modulating auxin response. Plant J. 2012, 70, 903–915, doi:10.1111/j.1365-313X.2012.04939.x.
[46]
Hendelman, A.; Buxdorf, K.; Stav, R.; Kravchik, M.; Arazi, T. Inhibition of lamina outgrowth following Solanum lycopersicum AUXIN RESPONSE FACTOR 10 (SlARF10) derepression. Plant Mol. Biol. 2012, 78, 561–576, doi:10.1007/s11103-012-9883-4.
[47]
Dharmasiri, N.; Dharmasiri, S.; Estelle, M. The F-box protein TIR1 is an auxin receptor. Nature 2005, 435, 441–445, doi:10.1038/nature03543.
[48]
Kepinski, S.; Leyser, O. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 2005, 435, 446–451, doi:10.1038/nature03542.
[49]
Berger, Y.; Harpaz-Saad, S.; Brand, A.; Melnik, H.; Sirding, N.; Alvarez, J.P.; Zinder, M.; Samach, A.; Eshed, Y.; Ori, N. The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development 2009, 136, 823–832, doi:10.1242/dev.031625.
[50]
Weiss, D.; Ori, N. Mechanisms of cross talk between gibberellin and other hormones. Plant Physiol. 2007, 144, 1240–1246, doi:10.1104/pp.107.100370.
[51]
Greenboim-Wainberg, Y.; Maymon, I.; Borochov, R.; Alvarez, J.; Olszewski, N.; Ori, N.; Eshed, Y.; Weiss, D. Cross talk between gibberellin and cytokinin: The Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling. Plant Cell 2005, 17, 92–102, doi:10.1105/tpc.104.028472.
[52]
Bolduc, N.; Hake, S. The Maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. Plant Cell 2009, 21, 1647–1658, doi:10.1105/tpc.109.068221.
[53]
Maekawa, T.; Maekawa-Yoshikawa, M.; Takeda, N.; Imaizumi-Anraku, H.; Murooka, Y.; Hayashi, M. Gibberellin controls the nodulation signaling pathway in Lotus japonicus. Plant J. 2009, 58, 183–194, doi:10.1111/j.1365-313X.2008.03774.x.
[54]
Jasinski, S.; Piazza, P.; Craft, J.; Hay, A.; Woolley, L.; Rieu, I.; Phillips, A.; Hedden, P.; Tsiantis, M. KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr. Biol. 2005, 15, 1560–1565, doi:10.1016/j.cub.2005.07.023.
[55]
Perilli, S.; Moubayidin, L.; Sabatini, S. The molecular basis of cytokinin function. Curr. Opin. Plant Biol. 2010, 13, 21–26, doi:10.1016/j.pbi.2009.09.018.
[56]
Hay, A.; Kaur, H.; Phillips, A.; Hedden, P.; Hake, S.; Tsiantis, M. The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr. Biol. 2002, 12, 1557–1565, doi:10.1016/S0960-9822(02)01125-9.
Gray, R.A. Alteration of leaf size and shape and other changes caused by gibberellins in plants. Am. J. Bot. 1957, 674–682, doi:10.2307/2438632.
[59]
Jones, M.G. Gibberellins and the procera mutants of tomato. Planta 1987, 172, 280–284, doi:10.1007/BF00394598.
[60]
Fleishon, S.; Shani, E.; Ori, N.; Weiss, D. Negative reciprocal interactions between gibberellin and cytokinin in tomato. New Phytol. 2011, 190, 609–617, doi:10.1111/j.1469-8137.2010.03616.x.
[61]
Phillips, A.L.; Ward, D.A.; Uknes, S.; Appleford, N.E.J.; Lange, T.; Huttly, A.K.; Gaskin, P.; Graebe, J.E.; Hedden, P. Isolation and expression of three gibberellin 20-oxidase cDNA clones from Arabidopsis. Plant Physiol. 1995, 108, 1049–1057.
[62]
Coles, J.P.; Phillips, A.L.; Croker, S.J.; Garcia-Lepe, R.; Lewis, M.J.; Hedden, P. Modification of gibberellin production and plant development in Arabidopsis by sense and antisense expression of gibberellin 20-oxidase genes. Plant J. 1999, 17, 547–556, doi:10.1046/j.1365-313X.1999.00410.x.
[63]
Thomas, S.G.; Phillips, A.L.; Hedden, P. Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellin deactivation. Proc. Natl. Acad. Sci. USA 1999, 96, 4698–4703, doi:10.1073/pnas.96.8.4698.
[64]
Yamaguchi, S. Gibberellin metabolism and its regulation. Annu. Rev. Plant Biol. 2008, 59, 225–251, doi:10.1146/annurev.arplant.59.032607.092804.
[65]
Silverstone, A.L.; Jung, H.-S.; Dill, A.; Kawaide, H.; Kamiya, Y.; Sun, T.-P. Repressing a repressor: Gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. Plant Cell 2001, 13, 1555–1565.
[66]
Sun, T.P.; Gubler, F. Molecular mechanism of gibberellin signaling in plants. Annu. Rev. Plant Biol. 2004, 55, 197–223, doi:10.1146/annurev.arplant.55.031903.141753.
[67]
Jupe, S.C.; Causton, D.R.; Scott, I.M. Cellular basis of the effects of gibberelin and the PRO gene on stem growth in tomato. Planta 1988, 174, 106–111, doi:10.1007/BF00394881.
[68]
Peng, J.; Carol, P.; Richards, D.E.; King, K.E.; Cowling, R.J.; Murphy, G.P.; Harberd, N.P. The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev. 1997, 11, 3194–3205, doi:10.1101/gad.11.23.3194.
[69]
Van Tuinen, A.; Peters, A.H.L.J.; Kendrick, R.E.; Zeevaart, J.A.D.; Koornneef, M. Characterisation of the procera mutant of tomato and the interaction of gibberellins with end-of-day far-red light treatments. Physiol. Plant 1999, 106, 121–128, doi:10.1034/j.1399-3054.1999.106117.x.
[70]
Marti, C.; Orzaez, D.; Ellul, P.; Moreno, V.; Carbonell, J.; Granell, A. Silencing of DELLA induces facultative parthenocarpy in tomato fruits. Plant J. 2007, 52, 865–876, doi:10.1111/j.1365-313X.2007.03282.x.
[71]
Bassel, G.W.; Mullen, R.T.; Bewley, J.D. procera is a putative DELLA mutant in tomato (Solanum lycopersicum): Effects on the seed and vegetative plant. J. Exp. Bot. 2008, 59, 585–593, doi:10.1093/jxb/erm354.
[72]
Jasinski, S.; Tattersall, A.; Piazza, P.; Hay, A.; Martinez-Garcia, J.F.; Schmitz, G.; Theres, K.; McCormick, S.; Tsiantis, M. PROCERA encodes a DELLA protein that mediates control of dissected leaf form in tomato. Plant J. 2008, 56, 603–612, doi:10.1111/j.1365-313X.2008.03628.x.
[73]
Sakamoto, T.; Kamiya, N.; Ueguchi-Tanaka, M.; Iwahori, S.; Matsuoka, M. KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev. 2001, 15, 581–590, doi:10.1101/gad.867901.
[74]
Werner, T.; Schmuelling, T. Cytokinin action in plant development. Curr. Opin. Plant. Biol. 2009, 12, 527–538, doi:10.1016/j.pbi.2009.07.002.
[75]
Werner, T.; Motyka, V.; Strnad, M.; Schmuelling, T. Regulation of plant growth by cytokinin. Proc. Natl. Acad. Sci. USA 2001, 98, 10487–10492, doi:10.1073/pnas.171304098.
[76]
Giulini, A.; Wang, J.; Jackson, D. Control of phyllotaxy by the cytokinin-inducible response regulator homologue ABPHYL1. Nature 2004, 430, 1031–1034, doi:10.1038/nature02778.
[77]
Leibfried, A.; To, J.P.C.; Busch, W.; Stehling, S.; Kehle, A.; Demar, M.; Kieber, J.J.; Lohmann, J.U. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 2005, 438, 1172–1175, doi:10.1038/nature04270.
[78]
Kurakawa, T.; Ueda, N.; Maekawa, M.; Kobayashi, K.; Kojima, M.; Nagato, Y.; Sakakibara, H.; Kyozuka, J. Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 2007, 445, 652–655, doi:10.1038/nature05504.
[79]
Sablowski, R. The dynamic plant stem cell niches. Curr. Opin. Plant Biol. 2007, 10, 639–644, doi:10.1016/j.pbi.2007.07.001.
[80]
Zhao, Z.; Andersen, S.U.; Ljung, K.; Dolezal, K.; Miotk, A.; Schultheiss, S.J.; Lohmann, J.U. Hormonal control of the shoot stem-cell niche. Nature 2010, 465, U1089–U1154, doi:10.1038/nature09126.
[81]
Werner, T.; Motyka, V.; Laucou, V.; Smets, R.; Van Onckelen, H.; Schmulling, T. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 2003, 15, 2532–2550, doi:10.1105/tpc.014928.
[82]
Lindsay, D.L.; Sawhney, V.K.; Bonham-Smith, P.C. Cytokinin-induced changes in CLAVATA1 and WUSCHEL expression temporally coincide with altered floral development in Arabidopsis. Plant Sci. 2006, 170, 1111–1117, doi:10.1016/j.plantsci.2006.01.015.
[83]
Shani, E.; Ben-Gera, H.; Shleizer-Burko, S.; Burko, Y.; Weiss, D.; Ori, N. Cytokinin regulates compound leaf development in tomato. Plant Cell 2010, 22, 3206–3217, doi:10.1105/tpc.110.078253.
[84]
Hofer, J.; Turner, L.; Hellens, R.; Ambrose, M.; Matthews, P.; Michael, A.; Ellis, N. UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr. Biol. 1997, 7, 581–587, doi:10.1016/S0960-9822(06)00257-0.
[85]
Hofer, J.; Gourlay, C.; Michael, A.; Ellis, T.H. Expression of a class 1 knotted1-like homeobox gene is down-regulated in pea compound leaf primordia. Plant Mol. Biol. 2001, 45, 387–398, doi:10.1023/A:1010739812836.
[86]
Peng, J.; Yu, J.; Wang, H.; Guo, Y.; Li, G.; Bai, G.; Chen, R. Regulation of compound leaf development in Medicago truncatula by fused compound leaf1, a class M KNOX gene. Plant Cell 2011, 23, 3929–3943, doi:10.1105/tpc.111.089128.
[87]
Di Giacomo, E.; Sestili, F.; Iannelli, M.A.; Testone, G.; Mariotti, D.; Frugis, G. Characterization of KNOX genes in Medicago truncatula. Plant Mol. Biol. 2008, 67, 135–150, doi:10.1007/s11103-008-9307-7.
[88]
Chen, J.; Yu, J.; Ge, L.; Wang, H.; Berbel, A.; Liu, Y.; Chen, Y.; Li, G.; Tadege, M.; Wen, J.; et al. Control of dissected leaf morphology by a Cys(2)His(2) zinc finger transcription factor in the model legume Medicago truncatula. Proc. Natl. Acad. Sci. USA 2010, 107, 10754–10759, doi:10.1073/pnas.1003954107.
[89]
Ge, L.; Peng, J.; Berbel, A.; Madueno, F.; Chen, R. Regulation of compound leaf development by PHANTASTICA in Medicago truncatula. Plant Physiol. 2013, doi:10.1104/pp.113.229914.
[90]
Young, N.D.; Debellé, F.; Oldroyd, G.E.D.; Geurts, R.; Cannon, S.B.; Udvardi, M.K.; Benedito, V.A.; Mayer, K.F.X.; Gouzy, J.; Schoof, H.; et al. The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 2011, 480, 520–524.
[91]
Benaben, V.; Duc, G.; Lefebvre, V.; Huguet, T. TE7, an inefficient symbiotic mutant of Medicago truncatula Gaertn. cv. Jemalong. Plant. Physiol. 1995, 107, 53–62.
[92]
Rogers, C.; Wen, J.; Chen, R.; Oldroyd, G. Deletion-based reverse genetics in Medicago truncatula. Plant Physiol. 2009, 151, 1077–1086, doi:10.1104/pp.109.142919.
[93]
Wang, H.; Li, G.; Chen, R. Fast neutron bombardment (FNB) induced deletion mutagenesis for forward and reverse genetic studies in plants. In Floriculture, Ornamental and Plant Biotechnology: Advances and Topical Issues, 1st ed.; Da Silva, J.T., Ed.; Global Science Books: Isleworth, UK, 2006; pp. 629–639.
[94]
Scholte, M.; d’Erfurth, I.; Rippa, S.; Mondy, S.; Cosson, V.; Durand, P.; Breda, C.; Trinh, H.; Rodriguez-Llorente, I.; Kondorosi, E.; et al. T-DNA tagging in the model legume Medicago truncatula allows efficient gene discovery. Mol. Breeding 2002, 10, 203–215, doi:10.1023/A:1020564612093.
[95]
d'Erfurth, I.; Cosson, V.; Mondy, S.; Brocard, L.; Kondorosi, A.; Ratet, P. The low level of activity of Arabidopsis thaliana Tag1 transposon correlates with the absence of two minor transcripts in Medicago truncatula. Mol. Breeding 2006, 17, 317–328, doi:10.1007/s11032-006-9003-8.
[96]
d’Erfurth, I.; Cosson, V.; Eschstruth, A.; Lucas, H.; Kondorosi, A.; Ratet, P. Efficient transposition of the Tnt1 tobacco retrotransposon in the model legume Medicago truncatula. Plant J. 2003, 34, 95–106, doi:10.1046/j.1365-313X.2003.01701.x.
[97]
d’Erfurth, I.; Cosson, V.; Eschstruth, A.; Rippa, S.; Messinese, E.; Durand, P.; Trinh, H.; Kondorosi, A.; Ratet, P. Rapid inactivation of the maize transposable element En/Spm in Medicago truncatula. Mol. Gen. Genet. 2003, 269, 732–745, doi:10.1007/s00438-003-0889-0.
[98]
Tadege, M.; Wen, J.; He, J.; Tu, H.; Kwak, Y.; Eschstruth, A.; Cayrel, A.; Endre, G.; Zhao, P.X.; Chabaud, M.; et al. Large-scale insertional mutagenesis using the Tnt1 retrotransposon in the model legume Medicago truncatula. Plant J. 2008, 54, 335–347, doi:10.1111/j.1365-313X.2008.03418.x.
[99]
Takatsuji, H. Zinc-finger proteins: The classical zinc finger emerges in contemporary plant science. Plant Mol. Biol. 1999, 39, 1073–1078, doi:10.1023/A:1006184519697.
[100]
Ohta, M.; Matsui, K.; Hiratsu, K.; Shinshi, H.; Ohme-Takagi, M. Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. Plant Cell 2001, 13, 1959–1968.
[101]
Ge, L.; Chen, J.; Chen, R. Palmate-like pentafoliata1 encodes a novel Cys(2)His(2) zinc finger transcription factor essential for compound leaf morphogenesis in Medicago truncatula. Plant Signal Behav. 2010, 5, 1134–1137, doi:10.4161/psb.5.9.12640.
[102]
Uppalapati, S.R.; Ishiga, Y.; Doraiswamy, V.; Bedair, M.; Mittal, S.; Chen, J.; Nakashima, J.; Tang, Y.; Tadege, M.; Ratet, P.; et al. Loss of abaxial leaf epicuticular wax in Medicago truncatula irg1/palm1 mutants results in reduced spore differentiation of anthracnose and nonhost rust pathogens. Plant Cell 2012, 24, 353–370, doi:10.1105/tpc.111.093104.
[103]
Kimura, S.; Koenig, D.; Kang, J.; Yoong, F.Y.; Sinha, N. Natural variation in leaf morphology results from mutation of a novel KNOX gene. Curr. Biol. 2008, 18, 672–677, doi:10.1016/j.cub.2008.04.008.
[104]
Magnani, E.; Hake, S. KNOX lost the OX: The Arabidopsis KNATM gene defines a novel class of KNOX transcriptional regulators missing the homeodomain. Plant Cell 2008, 20, 875–887, doi:10.1105/tpc.108.058495.
[105]
Blein, T.; Pulido, A.; Vialette-Guiraud, A.; Nikovics, K.; Morin, H.; Hay, A.; Johansen, I.E.; Tsiantis, M.; Laufs, P. A conserved molecular framework for compound leaf development. Science 2008, 322, 1835–1839, doi:10.1126/science.1166168.
[106]
Cheng, X.; Peng, J.; Ma, J.; Tang, Y.; Chen, R.; Mysore, K.S.; Wen, J. NO APICAL MERISTEM (MtNAM) regulates floral organ identity and lateral organ separation in Medicago truncatula. New Phytol. 2012, 195, 71–84, doi:10.1111/j.1469-8137.2012.04147.x.
[107]
Chuck, G.; Candela, H.; Hake, S. Big impacts by small RNAs in plant development. Curr. Opin. Plant Biol. 2009, 12, 81–86, doi:10.1016/j.pbi.2008.09.008.
[108]
Pulido, A.; Laufs, P. Co-ordination of developmental processes by small RNAs during leaf development. J. Exp. Bot. 2010, 61, 1277–1291, doi:10.1093/jxb/erp397.
