Origin of a novel regulatory module by duplication and degeneration of an ancient plant transcription factor

Molecular Phylogenetics and Evolution

Volumn 81, Issue , 2014, Pages 159-173

  Floyd, Sandra K ^a   Ryan, Joseph G ^a   Conway, Stephanie J ^b   Brenner, Eric ^c   Burris, Kellie P ^d   Burris, Jason N ^d   Chen, Tao ^e   Edger, Patrick P ^f   Graham, Sean W ^g   Leebens Mack, James H ^h   Pires, J Chris ^f   Rothfels, Carl J ^g   Sigel, Erin M ⁱ   Stevenson, Dennis W ^j   Neal Stewart, C ^d   Wong, Gane Ka Shu ^k,l   Bowman, John L ^a,m  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c NEW YORK UNIVERSITY   (United States)

^d UNIVERSITY OF TENNESSEE   (United States)

^e Fairylake Botanical Garden   (China)

^f UNIVERSITY OF MISSOURI   (United States)

^g UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^h UNIVERSITY OF GEORGIA   (United States)

ⁱ DUKE UNIVERSITY   (United States)

^j NEW YORK BOTANICAL GARDEN   (United States)

^k UNIVERSITY OF ALBERTA   (Canada)

^l BGI SHENZHEN   (China)

^m UNIVERSITY OF CALIFORNIA   (United States)

more..

Author keywords

Evolution of development; Gene duplication; Gene family evolution; Homeodomain Leucine Zipper; LITTLE ZIPPER

Indexed keywords

DNA BINDING PROTEIN; LEUCINE ZIPPER PROTEIN; PLANT DNA; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; DNA SEQUENCE; EVOLUTION; FERN; GENE DUPLICATION; GENETICS; GYMNOSPERM; HUPERZIA; MOLECULAR GENETICS; MOSS; PHYLOGENY; PLANT;

AMINO ACID SEQUENCE; ARABIDOPSIS; BIOLOGICAL EVOLUTION; BRYOPHYTA; DNA, PLANT; DNA-BINDING PROTEINS; FERNS; GENE DUPLICATION; GYMNOSPERMS; HUPERZIA; LEUCINE ZIPPERS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT PROTEINS; PLANTS; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS;

EID: 84908005568     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2014.06.017     Document Type: Article

References (56)

1. Aburomia R., Khaner O., Sidow A. Functional evolution in the ancestral lineage of vertebrates or when genomic complexity was wagging its morphological tail. J. Struct. Funct. Genomics 2003, 3:45-52.
2. Allen E., Xie Z.X., Gustafson A.M., Sung G.H., Spatafora J.W., Carrington J.C. Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat. Genet. 2004, 36:1282-1290.
3. Amoutzias G.D., Robertson D.L., de Peer Y.V., Oliver S.G. Choose your partners: dimerization in eukaryotic transcription factors. Trends Biochem. Sci. 2008, 33:220-229.
4. Aso K., Kato M., Banks J.A., Hasebe M. Characterization of homeodomain-leucine zipper genes in the fern Ceratopteris richardii and the evolution of the homeodomain-leucine zipper gene family in vascular plants. Mol. Biol. Evol. 1999, 16:544-552.
5. Banks H.P. The role of Psilophyton in the evolution of vascular plants. Rev. Palaeobot. Palynol. 1980, 29:165-176.
6. Banks J.A., Nishiyama T., Hasebe M., Bowman J.L., Gribskov M., dePamphilis C., Albert V.A., Aono N., Aoyama T., Ambrose B.A., Ashton N.W., Axtell M.J., Barker E., Barker M.S., Bennetzen J.L., Bonawitz N.D., Chapple C., Cheng C.Y., Correa L.G.G., Dacre M., DeBarry J., Dreyer I., Elias M., Engstrom E.M., Estelle M., Feng L., Finet C., Floyd S.K., Frommer W.B., Fujita T., Gramzow L., Gutensohn M., Harholt J., Hattori M., Heyl A., Hirai T., Hiwatashi Y., Ishikawa M., Iwata M., Karol K.G., Koehler B., Kolukisaoglu U., Kubo M., Kurata T., Lalonde S., Li K.J., Li Y., Litt A., Lyons E., Manning G., Maruyama T., Michael T.P., Mikami K., Miyazaki S., Morinaga S., Murata T., Mueller-Roeber B., Nelson D.R., Obara M., Oguri Y., Olmstead R.G., Onodera N., Petersen B.L., Pils B., Prigge M., Rensing S.A., Riano-Pachon D.M., Roberts A.W., Sato Y., Scheller H.V., Schulz B., Schulz C., Shakirov E.V., Shibagaki N., Shinohara N., Shippen D.E., Sorensen I., Sotooka R., Sugimoto N., Sugita M., Sumikawa N., Tanurdzic M., Theissen G., Ulvskov P., Wakazuki S., Weng J.K., Willats W.W.G.T., Wipf D., Wolf P.G., Yang L.X., Zimmer A.D., Zhu Q.H., Mitros T., Hellsten U., Loque D., Otillar R., Salamov A., Schmutz J., Shapiro H., Lindquist E., Lucas S., Rokhsar D., Grigoriev I.V. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 2011, 332:960-963.
7. Blanc G., Wolfe K.H. Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 2004, 16:1679-1691.
8. Brandt R., Xie Y.K., Musielak T., Graeff M., Stierhof Y.D., Huang H., Liu C.M., Wenkel S. Control of stem cell homeostasis via interlocking microRNA and microProtein feedback loops. Mech. Dev. 2013, 130:25-33.
9. Bridgham J.T., Brown J.E., Rodriguez-Mari A., Catchen J.M., Thornton J.W. Evolution of a new function by degenerative mutation in cephalochordate steroid receptors. PLoS Genet. 2008, 4.
10. Chi Y.J., Yang Y., Zhou Y., Zhou J., Fan B.F., Yu J.Q., Chen Z.X. Protein-protein interactions in the regulation of WRKY transcription factors. Mol. Plant 2013, 6:287-300.
11. Corvez A., Barriel V., Dubuisson J.Y. Diversity and evolution of the megaphyll in Euphyllophytes: phylogenetic hypotheses and the problem of foliar organ definition. C.R. Palevol 2012, 11:403-418.
12. Delaux P.M., Xie X.N., Timme R.E., Puech-Pages V., Dunand C., Lecompte E., Delwiche C.F., Yoneyama K., Becard G., Sejalon-Delmas N. Origin of strigolactones in the green lineage. New Phytol. 2012, 195:857-871.
13. Doran J.B. A new species of Psilophyton from the Lower Devonian of Northern New-Brunswick, Canada. Can. J. Bot. - Rev. Can. Bot. 1980, 58:2241-2262.
14. Edger P.P., Pires J.C. Gene and genome duplications: the impact of dosage-sensitivity on the fate of nuclear genes. Chromosome Res. 2009, 17:699-717.
15. Emery J.F., Floyd S.K., Alvarez J., Eshed Y., Hawker N.P., Izhaki A., Baum S.F., Bowman J.L. Radial patterning of Arabidopsis shoots by class III HD-Zip and KANADI genes. Curr. Biol. 2003, 13:1768-1774.
16. Floyd S.K., Bowman J.L. Distinct developmental mechanisms reflect the independent origins of leaves in vascular plants. Curr. Biol. 2006, 16:1911-1917.
17. Floyd S.K., Bowman J.L. The ancestral developmental tool kit of land plants. Int. J. Plant Sci. 2007, 168:1-35.
18. Floyd S.K., Zalewski C.S., Bowman J.L. Evolution of Class III Homeodomain leucine zipper genes in streptophytes. Genetics 2006, 173:373-388.
19. Freeling M., Thomas B.C. Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res. 2006, 16:805-814.
20. Galtier J. The origins and early evolution of the megaphyllous leaf. Int. J. Plant Sci. 2010, 171:641-661.
21. Gelman A., Rubin D.B. Inference from iterative simulation using multiple sequences. Stat. Sci. 1992, 7:457-511.
22. Gleave A.P. A versatile binary vector system with a T-DNA organizational-structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol. Biol. 1992, 20:1203-1207.
23. Hoffman L.A., Tomescu A.M.F. An early origin of secondary growth: Franhueberia Gerriennei Gen. Et Sp Nov from the Lower Devonian of Gaspe (Quebec, Canada). Am. J. Bot. 2013, 100:754-763.
24. Hong S.Y., Kim O.K., Kim S.G., Yang M.S., Park C.M. Nuclear import and DNA binding of the ZHD5 transcription factor is modulated by a competitive peptide inhibitor in Arabidopsis. J. Biol. Chem. 2011, 286:1659-1668.
25. Hu W., dePamphilis C.W., Ma H. Phylogenetic analysis of the plant-specific Zinc Finger-Homeobox and Mini Zinc Finger gene families. J. Integr. Plant Biol. 2008, 50:1031-1045.
26. Huelsenbeck J., Ronquist F. MrBayes: Bayesian inference of phylogeny. Bioinformatics 2001, 17:754-755.
27. Jiao Y.N., Wickett N.J., Ayyampalayam S., Chanderbali A.S., Landherr L., Ralph P.E., Tomsho L.P., Hu Y., Liang H.Y., Soltis P.S., Soltis D.E., Clifton S.W., Schlarbaum S.E., Schuster S.C., Ma H., Leebens-Mack J., dePamphilis C.W. Ancestral polyploidy in seed plants and angiosperms. Nature 2011, 473:U97-U113.
28. Kelch D.G., Mishler B.D. Inferring phylogeny using genomic characters: a case study using land plant plastomes. Molecular Systematics of Bryophytes: Progress, Problems, and Perspectives 2004, Missouri Botanical Garden Press, St. Louis. B. Goffinet, V.C. Hollowell, R.E. Magill (Eds.).
29. Kenrick P., Crane P.R. The Origin and Early Evolution of Land Plants: A Cladistic Study 1997, Smithsonian Institution Press, Washington, DC.
30. Kim Y.S., Kim S.G., Lee M., Lee I., Park H.Y., Seo P.J., Jung J.H., Kwon E.J., Suh S.W., Paek K.H., Park C.M. HD-ZIP III activity is modulated by competitive inhibitors via a feedback loop in Arabidopsis shoot apical meristem development. Plant Cell 2008, 20:920-933.
31. 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.
32. McConnell J., Emery J., Eshed Y., Bao N., Bowman J., Barton M.K. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 2001, 411:709-713.
33. Needleman S.B., Wunsch C.D. A general method applicable to search for similarities in amino acid sequence of 2 proteins. J. Mol. Biol. 1970, 48:443.
34. Ohno S. Evolution by Gene Duplication 1970, Springer-Verlag, New York.
35. Otsuga D., DeGuzman B., Prigge M.J., Drews G.N., Clark S.E. REVOLUTA regulates meristem initiation at lateral positions. Plant J. 2001, 25:223-236.
36. Prigge M.J., Clark S.E. Evolution of the class III HD-Zip gene family in land plants. Evol. Dev. 2006, 8:350-361.
37. Prigge M.J., Otsuga D., Alonso J.M., Ecker J.R., Drews G.N., Clark S.E. Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 2005, 17:61-76.
38. Prince V.E., Pickett F.B. Splitting pairs: the diverging fates of duplicated genes. Nat. Rev. Genet. 2002, 3:827-837.
39. Pryer K.M., Schneider H., Smith A.R., Cranfill R., Wolf P.G., Hunt J.S., Sipes S.D. Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 2001, 409:618-622.
40. Qiu Y.L., Li L.B., Wang B., Chen Z.D., Knoop V., Groth-Malonek M., Dombrovska O., Lee J., Kent L., Rest J., Estabrook G.F., Hendry T.A., Taylor D.W., Testa C.M., Ambros M., Crandall-Stotler B., Duff R.J., Stech M., Frey W., Quandt D., Davis C.C. The deepest divergences in land plants inferred from phylogenomic evidence. Proc. Natl. Acad. Sci. USA 2006, 103:15511-15516.
41. Qiu Y.L., Li L.B., Wang B., Chen Z.D., Dombrovska O., Lee J., Kent L., Li R.Q., Jobson R.W., Hendry T.A., Taylor D.W., Testa C.M., Ambros M. A nonflowering land plant phylogeny inferred from nucleotide sequences of seven chloroplast, mitochondrial, and nuclear genes. Int. J. Plant Sci. 2007, 168:691-708.
42. Rambaut, A., 1996. Se-Al: Sequence Alignment Editor. http://evolve.zoo.ox.ac.uk/.
43. Rensing S.A., Lang D., Zimmer A.D., Terry A., Salamov A., Shapiro H., Nishiyama T., Perroud P.F., Lindquist E.A., Kamisugi Y., Tanahashi T., Sakakibara K., Fujita T., Oishi K., Shin-I T., Kuroki Y., Toyoda A., Suzuki Y., Hashimoto S., Yamaguchi K., Sugano S., Kohara Y., Fujiyama A., Anterola A., Aoki S., Ashton N., Barbazuk W.B., Barker E., Bennetzen J.L., Blankenship R., Cho S.H., Dutcher S.K., Estelle M., Fawcett J.A., Gundlach H., Hanada K., Heyl A., Hicks K.A., Hughes J., Lohr M., Mayer K., Melkozernov A., Murata T., Nelson D.R., Pils B., Prigge M., Reiss B., Renner T., Rombauts S., Rushton P.J., Sanderfoot A., Schween G., Shiu S.H., Stueber K., Theodoulou F.L., Tu H., Van de Peer Y., Verrier P.J., Waters E., Wood A., Yang L.X., Cove D., Cuming A.C., Hasebe M., Lucas S., Mishler B.D., Reski R., Grigoriev I.V., Quatrano R.S., Boore J.L. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 2008, 319:64-69.
44. Riechmann J.L., Heard J., Martin G., Reuber L., Jiang C.Z., Keddie J., Adam L., Pineda O., Ratcliffe O.J., Samaha R.R., Creelman R., Pilgrim M., Broun P., Zhang J.Z., Ghandehari D., Sherman B.K., Yu C.L. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 2000, 290:2105-2110.
45. Seo P.J., Hong S.Y., Kim S.G., Park C.M. Competitive inhibition of transcription factors by small interfering peptides. Trends Plant Sci. 2011, 16:541-549.
46. Seoighe C., Gehring C. Genome duplication led to highly selective expansion of the Arabidopsis thaliana proteome. Trends Genet. 2004, 20:461-464.
47. Sessa G., Steindler C., Morelli G., Ruberti I. The Arabidopsis Athb-8, -9 and -14 genes are members of a small gene family coding for highly related HD-ZIP proteins. Plant Mol. Biol. 1998, 38:609-622.
48. Siriwardana N.S., Lamb R.S. A conserved domain in the N-terminus is important for LEAFY dimerization and function in Arabidopsis thaliana. Plant J. 2012, 71:736-749.
49. Staudt A.C., Wenkel S. Regulation of protein function by 'microProteins'. EMBO Rep. 2011, 12:35-42.
50. Swofford, D.L., 2003. PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.
51. Talbert P.B., Adler H.T., Parks D.W., Comai L. The REVOLUTA gene is necessary for apical meristem development and for limiting cell divisions in the leaves and stems of Arabidopsis thaliana. Development 1995, 121:2723-2735.
52. Tanabe Y., Hasebe M., Sekimoto H., Nishiyama T., Kitani M., Henschel K., Munster T., Theissen G., Nozaki H., Ito M. Characterization of MADS-box genes in charophycean green algae and its implication for the evolution of MADS-box genes. Proc. Natl. Acad. Sci. USA 2005, 102:2436-2441.
53. Trant C.A., Gensel P.G. Branching in Psilophyton - a new species from the Lower Devonian of New-Brunswick, Canada. Am. J. Bot. 1985, 72:1256-1273.
54. Wenkel S., Emery J., Hou B.H., Evans M.M.S., Barton M.K. A feedback regulatory module formed by LITTLE ZIPPER and HD-ZIPIII genes. Plant Cell 2007, 19:3379-3390.
55. Zalewski C.S., Floyd S.K., Furumizu C., Sakakibara K., Stevenson D.W., Bowman J.L. Phylogeny of Class IV HD-Zip genes and the evolution of epidermal complexity in land plants. Mol. Biol. Evol. 2013, 30:2347-2365.
56. Zhang J.Z. Evolution by gene duplication: an update. Trends Ecol. Evol. 2003, 18:292-298.