Antagonistic Roles for KNOX1 and KNOX2 Genes in Patterning the Land Plant Body Plan Following an Ancient Gene Duplication

PLoS Genetics

Volumn 11, Issue 2, 2015, Pages 1-24

  Furumizu, Chihiro ^a   Alvarez, John Paul ^a   Sakakibara, Keiko ^a,b   Bowman, John L ^a,c  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS THALIANA; ARTICLE; CARDAMINE; CARDAMINE HIRSUTA; CONTROLLED STUDY; EPISTASIS; GAMETOPHYTE; GENE DUPLICATION; GENE FUNCTION; GENETIC VARIABILITY; HETEROLOGOUS EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; KNOX1 GENE; KNOX2 GENE; LOSS OF FUNCTION MUTATION; MORPHOGENESIS; NONHUMAN; SPOROPHYTE; ARABIDOPSIS; DIPLOIDY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HAPLOIDY; LIFE CYCLE STAGE; MOLECULAR EVOLUTION; PHENOTYPE; PLANT LEAF;

ARABIDOPSIS; BRYOPHYTA; CARDAMINE HIRSUTA; EMBRYOPHYTA; MAGNOLIOPHYTA;

HOMEODOMAIN PROTEIN; KNOX1 PROTEIN, PLANT; VEGETABLE PROTEIN;

ARABIDOPSIS; CARDAMINE; DIPLOIDY; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE EXPRESSION REGULATION, PLANT; HAPLOIDY; HOMEODOMAIN PROTEINS; LIFE CYCLE STAGES; PHENOTYPE; PLANT LEAVES; PLANT PROTEINS;

EID: 84924419149     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004980     Document Type: Article

References (81)

1. Ohno S, (1970) Evolution by Gene Duplication. Heidelberg, Germany: Springer-Verlag.
2. Taylor JS, Raes J, (2004) Duplication and divergence: The evolution of new genes and old ideas. Annu Rev Genet 38: 615–643. 15568988
3. Conant GC, Wolfe KH, (2008) Turning a hobby into a job: How duplicated genes find new functions. Nat Rev Genet 9: 938–950. doi: 10.1038/nrg2482 19015656
4. Davis RL, Turner DL, (2001) Vertebrate hairy and Enhancer of split related proteins: transcriptional repressors regulating cellular differentiation and embryonic patterning. Oncogene 20: 8342–8357. 11840327
5. Bertolino E, Reimund B, WildtPerinic D, Clerc RG, (1995) A novel homeobox protein which recognizes a TGT core and functionally interferes with a retinoid-responsive motif. J Biol Chem 270: 31178–31188. 8537382
6. Burglin TR, (1997) Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals. Nucleic Acids Res 25: 4173–4180. 9336443
7. Derelle R, Lopez P, Le Guyader H, Manuel M, (2007) Homeodomain proteins belong to the ancestral molecular toolkit of eukaryotes. Evol Dev 9: 212–219. 17501745
8. Mukherjee K, Brocchieri L, Burglin TR, (2009) A Comprehensive Classification and Evolutionary Analysis of Plant Homeobox Genes. Mol Biol Evol 26: 2775–2794. doi: 10.1093/molbev/msp201 19734295
9. Kerstetter R, Vollbrecht E, Lowe B, Veit B, Yamaguchi J, et al. (1994) Sequence-Analysis and Expression Patterns Divide the Maize Knotted1-Like Homeobox Genes into 2 Classes. Plant Cell 6: 1877–1887. 7866030
10. Vollbrecht E, Veit B, Sinha N, Hake S, (1991) The Developmental Gene Knotted-1 Is a Member of a Maize Homeobox Gene Family. Nature 350: 241–243. 1672445
11. Efroni I, Eshed Y, Lifschitz E, (2010) Morphogenesis of Simple and Compound Leaves: A Critical Review. Plant Cell 22: 1019–1032. doi: 10.1105/tpc.109.073601 20435903
12. Hake S, Smith HMS, Holtan H, Magnani E, Mele G, et al. (2004) The role of knox genes in plant development. Annu Rev Cell Dev Biol 20: 125–151. 15473837
13. Hay A, Tsiantis M, (2010) KNOX genes: versatile regulators of plant development and diversity. Development 137: 3153–3165. doi: 10.1242/dev.030049 20823061
14. Sakakibara K, Nishiyama T, Deguchi H, Hasebe M, (2008) Class 1 KNOX genes are not involved in shoot development in the moss Physcomitrella patens but do function in sporophyte development. Evol Dev 10: 555–566. doi: 10.1111/j.1525-142X.2008.00271.x 18803774
15. Serikawa KA, MartinezLaborda A, Kim HS, Zambryski PC, (1997) Localization of expression of KNAT3, a class 2 knotted1-like gene. Plant J 11: 853–861. 9161040
16. Serikawa KA, MartinezLaborda A, Zambryski P, (1996) Three knotted1-like homeobox genes in Arabidopsis. Plant Mol Biol 32: 673–683. 8980519
17. Janssen BJ, Williams A, Chen JJ, Mathern J, Hake S, et al. (1998) Isolation and characterization of two knotted-like homeobox genes from tomato. Plant Mol Biol 36: 417–425. 9484482
18. Li EY, Bhargava A, Qiang WY, Friedmann MC, Forneris N, et al. (2012) The Class II KNOX gene KNAT7 negatively regulates secondary wall formation in Arabidopsis and is functionally conserved in Populus. New Phytol 194: 102–115. doi: 10.1111/j.1469-8137.2011.04016.x 22236040
19. Li EY, Wang SC, Liu YY, Chen JG, Douglas CJ, (2011) Ovate Family Protein4 (Ofp4) Interaction with Knat7 Regulates Secondary Cell Wall Formation in Arabidopsis Thaliana. Plant J 67: 328–341. doi: 10.1111/j.1365-313X.2011.04595.x 21457372
20. Truernit E, Siemering KR, Hodge S, Grbic V, Haseloff J, (2006) A map of KNAT gene expression in the Arabidopsis root. Plant Mol Biol 60: 1–20. 16463096
21. Zhong RQ, Lee CH, Zhou JL, McCarthy RL, Ye ZH, (2008) A Battery of Transcription Factors Involved in the Regulation of Secondary Cell Wall Biosynthesis in Arabidopsis. Plant Cell 20: 2763–2782. doi: 10.1105/tpc.108.061325 18952777
22. Kim D, Cho YH, Ryu H, Kim Y, Kim TH, et al. (2013) BLH1 and KNAT3 modulate ABA responses during germination and early seedling development in Arabidopsis. Plant J 75: 755–766. doi: 10.1111/tpj.12236 23663178
23. Herskowitz I, (1989) A Regulatory Hierarchy for Cell Specialization in Yeast. Nature 342: 749–757. 2513489
24. Kues U, Richardson WVJ, Tymon AM, Mutasa ES, Gottgens B, et al. (1992) The Combination of Dissimilar Alleles of the a-Alpha and a-Beta Gene Complexes, Whose Proteins Contain Homeo Domain Motifs, Determines Sexual Development in the Mushroom Coprinus-Cinereus. Genes Dev 6: 568–577. 1348484
25. Lee J-H, Lin H, Joo S, Goodenough U, (2008) Early Sexual Origins of Homeoprotein Heterodimerization and Evolution of the Plant KNOX/BELL Family. Cell 133: 829–840. doi: 10.1016/j.cell.2008.04.028 18510927
26. Sakakibara K, Ando S, Yip HK, Tamada Y, Hiwatashi Y, et al. (2013) KNOX2 Genes Regulate the Haploid-to-Diploid Morphological Transition in Land Plants. Science 339: 1067–1070. doi: 10.1126/science.1230082 23449590
27. Alvarez JP, Pekker I, Goldshmidt A, Blum E, Amsellem Z, et al. (2006) Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell 18: 1134–1151. 16603651
28. Serikawa KA, Zambryski PC, (1997) Domain exchanges between KNAT3 and KNAT1 suggest specificity of the kn1-like homeodomains requires sequences outside of the third helix and N-terminal arm of the homeodomain. Plant J 11: 863–869. 9161041
29. Kumar R, Kushalappa K, Godt D, Pidkowich MS, Pastorelli S, et al. (2007) The Arabidopsis BEL1-LIKE HOMEODOMAIN proteins SAW1 and SAW2 act redundantly to regulate KNOX expression spatially in leaf margins. Plant Cell 19: 2719–2735. 17873098
30. Reiser L, Modrusan Z, Margossian L, Samach A, Ohad N, et al. (1995) The Bell1 Gene Encodes a Homeodomain Protein Involved in Pattern-Formation in the Arabidopsis Ovule Primordium. Cell 83: 735–742. 8521490
31. Robinson-Beers K, Pruitt RE, Gasser CS, (1992) Ovule Development in Wild-Type Arabidopsis and 2 Female-Sterile Mutants. Plant Cell 4: 1237–1249. 12297633
32. Hackbusch J, Richter K, Muller J, Salamini F, Uhrig JF, (2005) A central role of Arabidopsis thaliana ovate family proteins in networking and subcellular localization of 3-aa loop extension homeodomain proteins. Proc Natl Acad Sci U S A 102: 4908–4912. 15781858
33. Moore I, Galweiler L, Grosskopf D, Schell J, Palme K, (1998) A transcription activation system for regulated gene expression in transgenic plants. Proc Natl Acad Sci U S A 95: 376–381. 9419383
34. Barton MK, Poethig RS, (1993) 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.
35. Belles-Boix E, Hamant O, Witiak SM, Morin H, Traas J, et al. (2006) KNAT6: an Arabidopsis homeobox gene involved in meristem activity and organ separation. Plant Cell 18: 1900–1907. 16798887
36. Long JA, Moan EI, Medford JI, Barton MK, (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379: 66–69. 8538741
37. Pagnussat GC, Yu HJ, Sundaresana V, (2007) Cell-fate switch of synergid to egg cell in Arabidopsis eostre mutant embryo sacs arises from misexpression of the BEL1-like homeodomain gene BLH1. Plant Cell 19: 3578–3592. 18055603
38. Endrizzi K, Moussian B, Haecker A, Levin JZ, Laux T, (1996) 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: 967–979. 9011081
39. Shani E, Burko Y, Ben-Yaakov L, Berger Y, Amsellem Z, et al. (2009) Stage-Specific Regulation of Solanum lycopersicum Leaf Maturation by Class 1 KNOTTED1-LIKE HOMEOBOX Proteins. Plant Cell 21: 3078–3092. doi: 10.1105/tpc.109.068148 19820191
40. Hasson A, Plessis A, Blein T, Adroher B, Grigg S, et al. (2011) Evolution and Diverse Roles of the CUP-SHAPED COTYLEDON Genes in Arabidopsis Leaf Development. Plant Cell 23: 54–68. doi: 10.1105/tpc.110.081448 21258003
41. Nikovics K, Blein T, Peaucelle A, Ishida T, Morin H, et al. (2006) The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 18: 2929–2945. 17098808
42. 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: 942–947. 16823378
43. Bharathan G, Goliber TE, Moore C, Kessler S, Pham T, et al. (2002) Homologies in leaf form inferred from KNOXI gene expression during development. Science 296: 1858–1860. 12052958
44. Piazza P, Bailey CD, Cartolano M, Krieger J, Cao J, et al. (2010) Arabidopsis thaliana Leaf Form Evolved via Loss of KNOX Expression in Leaves in Association with a Selective Sweep. Curr Biol 20: 2223–2228. doi: 10.1016/j.cub.2010.11.037 21129970
45. Doyle JA, (1998) Phylogeny of vascular plants. Annu Rev Ecol Syst 29: 567–599.
46. Nicotra AB, Leigh A, Boyce CK, Jones CS, Niklas KJ, et al. (2011) The evolution and functional significance of leaf shape in the angiosperms. Funct Plant Biol 38: 535–552.
47. Hofer J, Turner L, Hellens R, Ambrose M, Matthews P, et al. (1997) UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr Biol 7: 581–587. 9259553
48. Vlad D, Kierzkowski D, Rast MI, Vuolo F, Dello Ioio R, et al. (2014) Leaf Shape Evolution Through Duplication, Regulatory Diversification, and Loss of a Homeobox Gene. Science 343: 780–783. doi: 10.1126/science.1248384 24531971
49. Harrison CJ, Corley SB, Moylan EC, Alexander DL, Scotland RW, et al. (2005) Independent recruitment of a conserved developmental mechanism during leaf evolution. Nature 434: 509–514. 15791256
50. Sano R, Juarez CM, Hass B, Sakakibara K, Ito M, et al. (2005) KNOX homeobox genes potentially have similar function in both diploid unicellular and multicellular meristems, but not in haploid meristems. Evol Dev 7: 69–78. 15642091
51. Vasco A, Moran RC, Ambrose BA, (2013) The evolution, morphology, and development of fern leaves. Front Plant Sci 4. doi: 10.3389/fpls.2013.00544 24575101
52. Kimura S, Koenig D, Kang J, Yoong FY, Sinha N, (2008) Natural variation in leaf morphology results from mutation of a novel KNOX gene. Curr Biol 18: 672–677. doi: 10.1016/j.cub.2008.04.008 18424140
53. Magnani E, Hake S, (2008) KNOX lost the OX: The Arabidopsis KNATM gene defines a novel class of KNOX transcriptional regulators missing the homeodomain. Plant Cell 20: 875–887. doi: 10.1105/tpc.108.058495 18398054
54. Markel H, Chandler J, Werr W, (2002) Translational fusions with the engrailed repressor domain efficiently convert plant transcription factors into dominant-negative functions. Nucleic Acids Res 30: 4709–4719. 12409462
55. Mitsuda N, Ohme-Takagi M, (2009) Functional Analysis of Transcription Factors in Arabidopsis. Plant Cell Physiol 50: 1232–1248. doi: 10.1093/pcp/pcp075 19478073
56. Wang S, Chang Y, Guo J, Chen JG, (2007) Arabidopsis Ovate Family Protein 1 is a transcriptional repressor that suppresses cell elongation. Plant J 50: 858–872. 17461792
57. Hanzawa Y, Money T, Bradley D, (2005) A single amino acid converts a repressor to an activator of flowering. Proc Natl Acad Sci U S A 102: 7748–7753. 15894619
58. Ahn JH, Miller D, Winter VJ, Banfield MJ, Lee JH, et al. (2006) A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. Embo Journal 25: 605–614. 16424903
59. Wenkel S, Emery J, Hou BH, Evans MMS, Barton MK, (2007) A feedback regulatory module formed by LITTLE ZIPPER and HD-ZIPIII genes. Plant Cell 19: 3379–3390. 18055602
60. Liu C, Xi WY, Shen LS, Tan CP, Yu H, (2009) Regulation of Floral Patterning by Flowering Time Genes. Dev Cell 16: 711–722. doi: 10.1016/j.devcel.2009.03.011 19460347
61. Viola IL, Gonzalez DH, (2009) Binding properties of the complex formed by the Arabidopsis TALE homeodomain proteins STM and BLH3 to DNA containing single and double target sites. Biochimie 91: 974–981. doi: 10.1016/j.biochi.2009.04.021 19442701
62. Bower FO, (1908) Origin of a land flora: a theory based on the facts of alternation. London: MacMillan and Co.
63. Haig D, (2008) Homologous versus antithetic alternation of generations and the origin of sporophytes. Bot Rev 74: 395–418.
64. Svedelius N, (1927) Alternation of generations in relation to reduction division. Botanical Gazette 83: 362–384.
65. Cock JM, Godfroy O, Macaisne N, Peters AF, Coelho SM, (2014) Evolution and regulation of complex life cycles: a brown algal perspective. Curr Opin Plant Biol 17: 1–6. doi: 10.1016/j.pbi.2013.09.004 24507487
66. Ragni L, Belles-Boix E, Gunl M, Pautot V, (2008) Interaction of KNAT6 and KNAT2 with BREVIPEDICELLUS and PENNYWISE in Arabidopsis inflorescences. Plant Cell 20: 888–900. doi: 10.1105/tpc.108.058230 18390591
67. Long JA, Barton MK, (1998) The development of apical embryonic pattern in Arabidopsis. Development 125: 3027–3035. 9671577
68. Ori N, Eshed Y, Chuck G, Bowman JL, Hake S, (2000) Mechanisms that control knox gene expression in the Arabidopsis shoot. Development 127: 5523–5532. 11076771
69. Dockx J, Quaedvlieg N, Keultjes G, Kock P, Weisbeek P, et al. (1995) 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. 7647303
70. Yanai O, Shani E, Dolezal K, Tarkowski P, Sablowski R, et al. (2005) Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr Biol 15: 1566–1571. 16139212
71. Alvarez J, Smyth DR, (1999) CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development 126: 2377–2386. 10225997
72. Huelsenbeck JP, Ronquist F, (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755. 11524383
73. Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP, (2001) Evolution—Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294: 2310–2314. 11743192
74. Abascal F, Zardoya R, Posada D, (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104–2105. 15647292
75. Smith HMS, Hake S, (2003) The interaction of two homeobox genes, BREVIPEDICELLUS and PENNYWISE, regulates internode patterning in the Arabidopsis inflorescence. Plant Cell 15: 1717–1727. 12897247
76. Byrne ME, Groover AT, Fontana JR, Martienssen RA, (2003) Phyllotactic pattern and stem cell fate are determined by the Arabidopsis homeobox gene BELLRINGER. Development 130: 3941–3950. 12874117
77. Rutjens B, Bao DP, van Eck-Stouten E, Brand M, Smeekens S, et al. (2009) Shoot apical meristem function in Arabidopsis requires the combined activities of three BEL1-like homeodomain proteins. Plant J 58: 641–654. doi: 10.1111/j.1365-313X.2009.03809.x 19175771
78. Obayashi T, Nishida K, Kasahara K, Kinoshita K, (2011) ATTED-II Updates: Condition-Specific Gene Coexpression to Extend Coexpression Analyses and Applications to a Broad Range of Flowering Plants. Plant Cell Physiol 52: 213–219. doi: 10.1093/pcp/pcq203 21217125
79. Yadav RK, Girke T, Pasala S, Xie MT, Reddy V, (2009) Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc Natl Acad Sci U S A 106: 4941–4946. doi: 10.1073/pnas.0900843106 19258454
80. Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, et al. (2007) An “Electronic Fluorescent Pictograph” Browser for Exploring and Analyzing Large-Scale Biological Data Sets. Plos One 2. doi: 10.1371/journal.pone.0001317 18338032
81. Zuker M, (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406–3415. 12824337