Skip to main content
Log in

Knots in the family tree: evolutionary relationships and functions of knox homeobox genes

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Knotted-like homeobox (knox) genes constitute a gene family in plants. Class I knox genes are expressed in shoot apical meristems, and (with notable exceptions) not in lateral organ primordia. Class II genes have more diverse expression patterns. Loss and gain of function mutations indicate that knox genes are important regulators of meristem function. Gene duplication has contributed to the evolution of families of homeodomain proteins in metazoans. We believe that similar mechanisms have contributed to the diversity of knox gene function in plants. Knox genes may have contributed to the evolution of compound leaves in tomato and could be involved in the evolution of morphological traits in other species. Alterations in cis-regulatory regions in some knox genes correlate with novel patterns of gene expression and distinctive morphologies. Preliminary data from the analysis of class I knox gene expression illustrates the evolution of complex patterns of knox expression is likely to have occurred through loss and gain of domains of gene expression.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Abouheif E: Developmental genetics and homology: a heirarchical approach. Trends Evol Ecol 12: 405–408 (1997).

    Google Scholar 

  2. Abouheif E, Akam M, Dickinson W, Holland PWH, Meyer A, Patel N, Raff R, Roth VL, Wray GA: Homology and developmental genes. Trends Genet 13: 432–433 (1997).

    Google Scholar 

  3. Ahn S, Tanksley SD: Comparative linkage maps of the rice and maize genomes. Proc Natl Acad Sci USA 90: 7980–7984 (1993).

    Google Scholar 

  4. Averof M, Akam M: Hox genes and the diversification of insect and crustacean body plans. Nature 376: 420–423 (1995).

    Google Scholar 

  5. Averof M, Dawes R, Ferrier D: Diversification of arthropod HOX genes as a paradigm for the evolution of gene functions. Cell Dev Biol 7: 539–551 (1996).

    Google Scholar 

  6. Barton MK, Poethig RS: Formation of the shoot apical meristem in Arabidopsis thaliana: an analysis of development in the wild type and in the shoot meristemless mutant. Development 119: 823–831 (1993).

    Google Scholar 

  7. Baum DA: The evolution of development. Curr Opin Plant Biol 1: 79–86 (1998).

    Google Scholar 

  8. Becraft PW, Freeling M: Genetic analysis of Rough sheath1 developmental mutants of maize. Genetics 136: 295–311 (1994).

    Google Scholar 

  9. Bharathan G, Janssen B-J, Kellogg EA, Sinha N: Did homeodomain proteins duplicate before the origin of angiosperms, fungi and metazoa? Proc Natl Acad Sci USA 94: 13749–13753 (1997).

    Google Scholar 

  10. Bharathan G, Janssen B-J, Kellogg EA, Sinha N: Phylogenetic relationships and evolution of the KNOTTED class of plant homeodomain proteins. Mol Biol Evol, in press (1999).

  11. Boivin R, Hamel F, Beauseigle D, Bellemare G: Stage-specific transcription of the homeobox gene Bnhd1 in young tissues and flowers of Brassica napus. Biochim Biophys Acta 1219: 201–204 (1994).

    Google Scholar 

  12. Brooks D, McLennan: Phylogeny, Ecology and Behavior. University of Chicago Press, Chicago (1991).

    Google Scholar 

  13. Bürglin TR: Analysis of TALE superclass homeobox genes (MEIS, PBC, Iriquois, TGIF) reveals a novel domain conserved between plants and animals. Nucl Acids Res 25: 4173–4180 (1997).

    Google Scholar 

  14. Burglin TR: The PBC domain contains a MEINOX domain: coevolution of Hox and TALE homeobox genes. Dev Genes Evol 208: 113–116 (1998).

    Google Scholar 

  15. 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 9: 1289–1304 (1997).

    Google Scholar 

  16. Chuck G, Lincoln C, Hake S: KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell 8: 1277–1289 (1996).

    Google Scholar 

  17. Dockx J, Quaedvlieg N, Keultjes G, Kock P, Weisbeek P, Smeekens S: The homeobox gene ATK1 of Arabidopsis thaliana is expressed in the shoot apex of the seedling and in flowers and inflorescence stems of mature plants. Plant Mol Biol 28: 723–737 (1995).

    Google Scholar 

  18. Doebley J, Lukens L: Transcriptional regulators and the evolution of plants. Plant Cell 10: 1075–1082 (1998).

    Google Scholar 

  19. Doyle J: Evolution of a plant homeotic multigene family: toward connecting molecular systematics and molecular developmental genetics. Syst Biol 43: 307–328 (1994).

    Google Scholar 

  20. Endrizzi K, Moussian B, Haecker A, Levin JZ, Laux T: The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J 10: 101–113 (1996).

    Google Scholar 

  21. Fitch WM: Distinguishing homologous from analogous proteins. Syst Zool 19: 99–113 (1970).

    Google Scholar 

  22. Foster T, Hake S: It's a Gnarley one! (Gn1). Maize Genet Coop Newsl 68: 2 (1994).

    Google Scholar 

  23. Foster T, Veit B, Hake S: Mosaic analysis of the dominant mutant Gnarley1-R reveals distinct lateral and transverse signaling pathways during maize leaf development. Development 126: 305–313 (1999).

    Google Scholar 

  24. Foster T, Yamaguchi J, Wong B, Veit B, Hake S: Gnarley1 is a dominant mutation in the knox4 homeobox gene that affects cell identity and cell shape. Plant Cell, in press (1999).

  25. Fowler JE, Freeling M: Genetic analysis of mutations that alter cell fates in maize leaves: dominant Liguleless mutations. Dev Genet 18: 198–222 (1996).

    Google Scholar 

  26. Fowler JE, Meuhlbauer GJ, Freeling M: Mosaic analysis of the Liguleless3 mutant phenotype in maize by coordinate suppression of mutator insertion alleles. Genetics 143: 489–503 (1996).

    Google Scholar 

  27. Freeling M, Hake S: Developmental genetics of mutants that specify Knotted leaves in maize. Genetics 111: 617–634 (1985).

    Google Scholar 

  28. Gaut BS, F. DJ: DNA sequence evidence for the segmental allotetraploid origin of maize. Proc Natl Acad Sci USA 94: 6809–6814 (1997).

    Google Scholar 

  29. Greene B, Walko R, Hake S: Mutator insertions in an intron of the maize knotted1 gene result in dominant suppressible mutations. Genetics 138: 1275–1285 (1994).

    Google Scholar 

  30. Hake S, Char BR, Chuck G, Foster T, Long J, Jackson D: Homeobox genes in the functioning of plant meristems. Phil Trans R Soc Lond 350: 45–51 (1995).

    Google Scholar 

  31. Hall BK: Homology: The Hierarchical Basis of Comparative Morphology. Academic Press, San Diego (1994).

    Google Scholar 

  32. Hareven D, Gutfinger T, Parnis A, Eshed Y, Lifschitz E: The making of a compound leaf: genetic manipulation of leaf architecture in tomato. Cell 84: 735–744 (1996).

    Google Scholar 

  33. Helentjaris T, Weber D, Wright S: Identification of the genomic locations of duplicate nucleotide sequences in maize by analysis of restriction fragment length polymorphisms. Genetics 118: 353–363 (1988).

    Google Scholar 

  34. Hillis DM: Homology in molecular biology. In: Hall BK (ed), Homology, the Hierarchical Basis of Comparative Morphology, pp. 339–368. Academic Press, San Diego (1994).

    Google Scholar 

  35. Hofer J, Turner L, Hellens R, Ambrose M, Matthews P, Michael A, Ellis N: UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr Biol 7: 581–587 (1997).

    Google Scholar 

  36. Holland P: Homeobox genes and vertebrate evolution. BioEssays 14: 267–273 (1992).

    Google Scholar 

  37. Holland PW, Garcia-Fernandez J: Hox genes and chordate evolution. Dev Biol 173: 382–395 (1996).

    Google Scholar 

  38. Holland PW, Garcia-Fernandez J, Williams NA, Sidow A: Gene duplications and the origins of vertebrate development. Development (Suppl): 125–133 (1994).

    Google Scholar 

  39. Jackson D, Veit B, Hake S: Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120: 405–413 (1994).

    Google Scholar 

  40. Janssen B-J, Lund L, Sinha N: Overexpression of a homeobox gene, Let6, reveals indeterminate features of the tomato compound leaf. Plant Physiol 117: 771–786 (1998).

    Google Scholar 

  41. Janssen B-J, Williams A, Chen J-J, Mathern J, Hake S, Sinha N: Isolation and characterization of two knotted-like homeobox genes from tomato. Plant Mol Biol 36: 417–425 (1998).

    Google Scholar 

  42. Kenyon C: If birds can fly, why can't we? Homeotic genes and evolution. Cell 78: 175–180 (1994).

    Google Scholar 

  43. Kerstetter R, Vollbrecht E, Lowe B, Veit B, Yamaguchi J, Hake S: Sequence analysis and expression patterns divide the maize knotted1-like homeobox genes into two classes. Plant Cell 6: 1877–1887 (1994).

    Google Scholar 

  44. Kerstetter RA, Laudencia-Chingcuanco D, Smith LG, Hake S: Loss of function mutations in the maize homeobox gene, knotted1, are defective in shoot meristem maintenance. Development 124: 3045–3054 (1997).

    Google Scholar 

  45. Krumlauf R: Hox genes in vertebrate development. Cell 78: 191–201 (1994).

    Google Scholar 

  46. Lane B, Freeling M: The maize leaf. In: Freeling M, Walbot V (eds), The Maize Handbook, Springer-Verlag, New York (1994).

    Google Scholar 

  47. Laufs P, Dockx J, Kronenberger J, Traas J: MGOUN1 and MGOUN2: two genes required for primordium initiation at the shoot apical and floral meristems in Arabidopsis thaliana. Development 125: 1253–1260 (1998).

    Google Scholar 

  48. Lincoln C, Long J, Yamaguchi J, Serikawa K, Hake S: A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell 6: 1859–1876 (1994).

    Google Scholar 

  49. Long J, Barton MK: The development of apical embryonic pattern in Arabidopsis. Development 125: 3027–3035 (1998).

    Google Scholar 

  50. Long JA, Moan EI, Medford JI, Barton MK: A member of the KNOTTED class of homeodomain proteins encoded by the SHOOTMERISTEMLESS gene of Arabidopsis. Nature 379: 66–69 (1996).

    Google Scholar 

  51. Ma H, McMullen MD, Finer JJ: Identification of a homeoboxcontaining gene with enhanced expression during soybean (Glycine max L.) somatic embryo development. Plant Mol Biol 24: 465–473 (1994).

    Google Scholar 

  52. Mann R, Chan S-K: Extra specificty from extradenticle: the partnership between HOX and PBX/EXD homeodomain proteins. Trends Genet 12: 258–262 (1996).

    Google Scholar 

  53. Mann RS, Affolter M: Hox proteins meet more partners. Curr Opin Genet Dev 8: 423–429 (1998).

    Google Scholar 

  54. Mathern J, Hake S: Mu element-generated gene conversions in maize attenuate the dominant Knotted1 phenotype. Genetics 147: 305–314 (1997).

    Google Scholar 

  55. Matsuoka M, Ichikawa H, Saito A, Tamda Y, Fujimura T, Kano-Murakami Y: Expression of a rice homeobox gene causes altered morphology of transgenic plants. Plant Cell 5: 1039–1048 (1993).

    Google Scholar 

  56. McGinnis W, Krumlauf R: Homeobox genes and axial patterning. Cell 68: 283–302 (1992).

    Google Scholar 

  57. Meyer A: The evolution of body plans: HOM/hox cluster evolution, model systems, and the importance of phylogeny. In: Harvey PH (ed), New Uses for New Phylogenies, pp. 99–113. Oxford University Press, London (1996).

    Google Scholar 

  58. Moore GK, Devos KM, Z W, Gale MD: Grasses, line up and form a circle. Curr Biol 5: 737–739 (1995).

    Google Scholar 

  59. Muehlbaur GJ, Fowler JE, Freeling M: Sectors expressing the homeobox gene liguless3 implicate a time-dependent mechanism for cell fate acquisition along the proximal-distal axis of the maize leaf. Development 124: 5097–5106 (1997).

    Google Scholar 

  60. Müller K, Romano N, Gerstner O, Garcia-Maroto F, Pozzi C, Salamini F, Rohde W: The barley Hooded mutation caused by a duplication in a homeobox gene intron. Nature 374: 727–730 (1995).

    Google Scholar 

  61. Ohno S: Evolution by Gene Duplication. Springer-Verlag, Heidelberg (1970).

    Google Scholar 

  62. 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 9: 2143–2158 (1997).

    Google Scholar 

  63. Postma-Haarsma AD, Verwoert II GS, Stronk OP, Koster J, Lamer G, EM, Hoge HC, Meijer AH: Characterization of the KNOX class homeobox genes Oskn2 and Oskn3 identified in a collection of cDNA libraries covering the early stages of rice embryogenesis. Plant Mol Biol 39: 257–271 (1999).

    Google Scholar 

  64. Purugganan M, Rounsley S, Schmidt R, Yanofsky M: Molecular evolution of flower development: diversification of a plant MADS-box regulatory gene family. Genetics 140: 345–356 (1995).

    Google Scholar 

  65. Ruddle FH, Bartels JL, Bentley KL, Kappen C, Murtha MT, Pendelton JW: Evolution of Hox genes. Annu Rev Genet 28: 423–442 (1994).

    Google Scholar 

  66. Sato Y, Sentoku N, Matsuoka M: Analysis of the functions of rice homeobox genes. In: Shimamoto K (ed), Molecular Biology of Rice, pp. 119–135. Springer-Verlag, Tokyo (1999).

    Google Scholar 

  67. Sato Y, Sentoku N, Miura Y, Hirochicka H, Kitano H, Matsuoka M: Loss-of-function mutations in the rice homeobox gene, OSH15, cause defects in the development of hypodermal schlerenchyma in internodes resulting in dwarf plants. EMBO J 18: 992–1002 (1999).

    Google Scholar 

  68. Sato Y, Sentoku N, Nagato Y, Matsuoka M: Isolation and characterization of a rice homeobox gene OSH15. Plant Mol Biol 38: 983–998 (1998).

    Google Scholar 

  69. Sato Y, Tamaoki M, Murakami T, Yamamoto N, Kano-Murakami Y, Matsuoka M: Abnormal cell divisions in leaf primordia caused by the expression of the rice homeobox gene OSH1 lead to altered morphology of leaves in transgenic tobacco. Mol Gen Genet 251: 13–22 (1996).

    Google Scholar 

  70. Scanlon MJ, Schneeberger RG, Freeling M: The maize mutant narrow sheath fails to establish leaf margin identity in a meristematic domain. Development 122: 1683–1691 (1996).

    Google Scholar 

  71. Schneeberger R, Tsantis M, Freeling M, Langdale JA: The rough sheath2 gene negatively regulates homeobox gene expression during maize leaf development. Development 125: 2857–2865 (1998).

    Google Scholar 

  72. Schneeberger RG, Becraft PW, Hake S, Freeling M: Ectopic expression of the knox homeobox gene rough sheath1 alters cell fate in the maize leaf. Genes Dev 9: 2292–2304 (1995).

    Google Scholar 

  73. Serikawa KA, Martinez-Laborda A, Kim H-S, Zambryski P: Localization of expression of KNAT3, a class 2 knotted1-like gene. Plant J 11: 853–861 (1997).

    Google Scholar 

  74. Serikawa KA, Martinez-Laborda A, Zambryski P: Three knotted1-like homeobox genes in Arabidopsis. Plant Mol Biol 32: 673–683 (1996).

    Google Scholar 

  75. Sinha N: Simple or compound leaves: reduction or multiplication? Trends Plant Sci 2: 396–402 (1997).

    Google Scholar 

  76. Sinha NR, Williams RE, Hake S: Overexpression of the maize homeo box gene, KNOTTED-1, causes a switch from determinate to indeterminate cell fates. Genes Dev 7: 787–795 (1993).

    Google Scholar 

  77. Smith LG, Greene B, Veit B, Hake S: A dominant mutation in the maize homeobox gene, Knotted-1, causes its ectopic expression in leaf cells with altered fates. Development 116: 21–30 (1992).

    Google Scholar 

  78. Smith LG, Jackson D, Hake S: The expression of Knotted1 marks shoot meristem formation during maize embryogenesis. Dev Genet 16: 344–348 (1995).

    Google Scholar 

  79. Så ndas-Larsson A, Svenson M, Liao H, Engstrom P: A homeobox gene with potential developmental control function in the meristem of the conifer Picea abies. Proc Natl Acad Sci USA 95: 15118–15122 (1998).

    Google Scholar 

  80. Swofford DL: Phylogenetic Analysis Using Parsimony. Illinois Natural History Survey, Champaign, IL (1991).

    Google Scholar 

  81. Tamaoki M, Kusuba S, Kano-Murakami Y, Matsuoka M: Ectopic expression of a tobacco homeobox gene, NTH15, dramatically alters leaf morphology and hormone levels in transgenic tobacco. Plant Cell Physiol 38: 917–927 (1997).

    Google Scholar 

  82. Theiben G, Kim J, Saedler H: Classification and phylogeny of the MADs box multigene family suggest defined roles of MADS box gene subfamilies in the morphological evolution of eukaryotes. J Mol Evol 43: 484–516 (1996).

    Google Scholar 

  83. Timmermans MCP, Schutes NP, Jankovsky JP, Nelson T: Leafbladeless1 is required for dorsiventrality of lateral organs in maize. Development 125: 2813–2823 (1998).

    Google Scholar 

  84. Veit B, Vollbrecht E, Mathern J, Hake S: A tandem duplication causes the Kn1-O allele of Knotted, a dominant morphological mutant of maize. Genetics 125: 623–631 (1990).

    Google Scholar 

  85. Vollbrecht E, Veit B, Sinha N, Hake S: The developmental gene Knotted-1 is amember of amaize homeobox gene family. Nature 350: 241–243 (1991).

    Google Scholar 

  86. Waites R, Hudson A: phantastica, a gene required for dorsiventrality in leaves of Antirrhinum majus. Development 121: 2143–2154 (1995).

    Google Scholar 

  87. Waites R, Selvadurai HRN, Oliver IR, Hudson A: The PHANTASTICA gene encodes a MYB transcription factor involved in growth and dorsiventrality of lateral organs in Antirrhinum. Cell 93: 779–789 (1998).

    Google Scholar 

  88. Watillon B, Kettmann R, Boxus P, Burney A: Knotted1-like homeobox genes are expressed during apple tree (Malus domestica L. Borkh) growth and development. Plant Mol Biol 33: 757–763 (1997).

    Google Scholar 

  89. Weatherwax P: Position of the scutellum and homology of the coleoptile in maize. Bot Gaz 69: 179–182 (1920).

    Google Scholar 

  90. Williams RW: Plant homeobox genes: many functions stem from a common motif. BioEssays 20: 280–282 (1998).

    Google Scholar 

  91. Williams-Carrier RE, Lie YS, Hake S, Lemaux PG: Ectopic expression of the maize kn1 gene phenocopies the Hooded mutant of barley. Development 124: 3737–3745 (1997).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reiser, L., Sánchez-Baracaldo, P. & Hake, S. Knots in the family tree: evolutionary relationships and functions of knox homeobox genes. Plant Mol Biol 42, 151–166 (2000). https://doi.org/10.1023/A:1006384122567

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006384122567

Navigation