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


Eukaryotes alternate between haploid (1n) and diploid (2n) stages during their life cycles, and often seen are remarkable differences in morphology and physiology between them. Land plants are multicellular in both generations, in contrast to their presumed ancestral green algae that develop multicellularity only in the haploid stage. TALE class homeodomain transcriptional factors play a key role in the activation of diploid development in diverse lineages of eukaryotes. A gene duplication event within this family in an ancestor of land plants had profound implications for land plant evolution. We show that the two subclasses resulting from the gene duplication event act to pattern, in a complementary manner, most above ground organs of the diploid stage of the flowering plant Arabidopsis. Their opposing activities sculpt the shape of leaves from entire to pinnate and control the architecture of the plant body, and thus providing plasticity for evolutionary tinkering. These results form a foundation for understanding how these genes have been co-opted from an ancestral role of regulating diploid gene expression in a zygote to directing sporophyte land plant body architecture and provide insight into the evolution of various forms of life cycles.


Vyšlo v časopise: Antagonistic Roles for KNOX1 and KNOX2 Genes in Patterning the Land Plant Body Plan Following an Ancient Gene Duplication. PLoS Genet 11(2): e32767. doi:10.1371/journal.pgen.1004980
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004980

Souhrn

Eukaryotes alternate between haploid (1n) and diploid (2n) stages during their life cycles, and often seen are remarkable differences in morphology and physiology between them. Land plants are multicellular in both generations, in contrast to their presumed ancestral green algae that develop multicellularity only in the haploid stage. TALE class homeodomain transcriptional factors play a key role in the activation of diploid development in diverse lineages of eukaryotes. A gene duplication event within this family in an ancestor of land plants had profound implications for land plant evolution. We show that the two subclasses resulting from the gene duplication event act to pattern, in a complementary manner, most above ground organs of the diploid stage of the flowering plant Arabidopsis. Their opposing activities sculpt the shape of leaves from entire to pinnate and control the architecture of the plant body, and thus providing plasticity for evolutionary tinkering. These results form a foundation for understanding how these genes have been co-opted from an ancestral role of regulating diploid gene expression in a zygote to directing sporophyte land plant body architecture and provide insight into the evolution of various forms of life cycles.


Zdroje

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

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