Evolutionary analysis of the MIXTA gene family highlights potential targets for the study of cellular differentiation

Molecular Biology and Evolution

Volumn 30, Issue 3, 2013, Pages 526-540

  Brockington, Samuel F ^a   Alvarez Fernandez, Ruben ^a   Landis, Jacob B ^b   Alcorn, Katrina ^a   Walker, Rachel H ^a   Thomas, Murphy M ^a   Hileman, Lena C ^c   Glover, Beverley J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF KANSAS   (United States)

Author keywords

conical cells; cotton; MIXTA; MYB; plant epidermis; trichomes

Indexed keywords

ANGIOSPERM; ARTICLE; ASTERACEAE; BRASSICACEAE; CELL DIFFERENTIATION; EVOLUTION; FABACEAE; GENE; GENE DUPLICATION; GENE LOSS; GENE TARGETING; GENETIC ALGORITHM; GENETIC CONSERVATION; GYMNOSPERM; HETEROLOGOUS EXPRESSION; MAJOR GENE; MARCHANTIA; MIXTA GENE; MULTIGENE FAMILY; NONHUMAN; ORTHOLOGY; PARALOGY; PHYLOGENY; PHYSCOMITRELLA; PLANT EPIDERMIS CELL; PLANT GENE; SEED PLANT; SELAGINELLA; SYNAPOMORPHY; TOBACCO; UNCERTAINTY;

AMINO ACID SEQUENCE; ANGIOSPERMS; BAYES THEOREM; CELL DIFFERENTIATION; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; FLOWERS; GENE DUPLICATION; GENES, PLANT; LIKELIHOOD FUNCTIONS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT EPIDERMIS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 84873595033     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mss260     Document Type: Article

References (59)

1. Andersson KB, Berge T, Matre V, Gabrielsen OS. 1999. Sequence selectivity of c-MYB in vivo. Resolution of a DNA target specificity paradox. J Biol Chem. 274:21986-21994.
2. Baumann K, Perez-Rodriguez M, BradleyD, Venail J, Bailey P, Jin H, Koes R, Roberts K, Martin C. 2007. Control of cell and petal morphogenesis by R2R3 MYB transcription factors. Development 134:1691-1701.
3. Brewer CA, Smith WK. 1997. Patterns of leaf surface wetness for mountain and subalpine plants. Plant Cell Environ. 20:1-11.
4. Carr MD, Mott RF. 1991. The transcriptional control proteins c-Myb and v-Myb contain a basic region DNA bindingmotif. FEBS Lett. 282: 293-294.
5. Di Stilio VS, Martin C, Schulfer AF, Connelly CF. 2009. An ortholog of MIXTA-like 2 controls epidermal cell shape in flowers of Thalictrum. New Phytol. 183:718-728.
6. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L. 2010. MYB transcription factors in Arabidopsis. Trends Plant Sci. 15: 573-581.
7. Ehleringer J. 1984. Ecology and ecophysiology of leaf pubescence in North American desert plants. In: Rodriguez E, Healey PL, Mehta I, editors. Biology and chemistry of plant trichomes. New York: Plenum Press. p. 113-132.
8. Gilding EK, Marks MD. 2010. Analysis of purified glabra3-shapeshifter trichomes reveals a role for NOECK in regulating early trichome morphogenic events. Plant J. 64:304-317.
9. Glover BJ, Martin C. 1998. The role of petal cell shape and pigmentation in pollination success in Antirrhinum majus. Heredity 80:778-784.
10. Glover BJ, Perez-Rodriguez M, Martin C. 1998. Development of several epidermal cell types can be specified by the same MYB-related plant transcription factor. Development 125:3497-3508.
11. Green PB, Linstead P. 1990. A procedure for SEM of complex shoot structures applied to the inflorescence of snapdragon (Antirrhinum). Protoplasma 158:33-38.
12. Hayat MQ, Ashraf M, Khan MA, Yasmin G, Shaheen N, Jabeen S. 2009. Diversity of foliar trichomes and their systematic implications in the genus Artemisia (Asteraceae). Int J Agric Biol. 11:542-546.
13. Hellens RP, Edwards EA, Leyland NR, Bean S, Mullineaux PM. 2000. pGreen: a versatile and flexible binary Ti vector for Agrobacteriummediated plant transformation. Plant Mol Biol. 42:819-832.
14. Horsch RB, Fry JE, Hoffmann NL, Eichholtz D, Rogers SG, Fraley RT. 1985. A simple and general method for transferring genes into plants. Science 227:1229-1231.
15. Hovav R, Udall JA, Hovav E, Rapp R, Flagel L, Wendel JF. 2008. A majority of cotton genes are expressed in single-celled fiber. Planta 227: 319-329.
16. Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755.
17. Hulskamp M, Schnittger A, Folkers U. 1999. Pattern formation and cell differentiation: trichomes in Arabidopsis as a genetic model system. Int Rev Cytol. 186:147-178.
18. Jaffe FW, Tattersall A, Glover BJ. 2007. A truncated MYB transcription factor from Antirrhinum majus regulates epidermal cell outgrowth. J Exp Bot. 58:1515-1524.
19. Jia L, Clegg MT, Jiang T. 2004. Evolutionary dynamics of the DNA-binding domains in putative R2R3-MYB genes identified from rice subspecies indica and japonica genomes. Plant Physiol. 134:575-585.
20. Jiang C, Gu J, Chopra S, Gu X, Peterson T. 2004. Ordered origin of the typical two-and three-repeat Myb genes. Gene 326:13-22.
21. Jin H, Martin C. 1999. Multifunctionality and diversity within the plant MYB gene family. Plant Mol Biol. 41:557-585.
22. Johnson HB. 1975. Plant pubescence: an ecological perspective. Bot Rev. 41:233-253.
23. Kim HJ, Triplett BA. 2001. Cotton fiber growth in planta and in vitro. Models for plant cell elongation and cell wall biogenesis. Plant Physiol. 127:1361-1366.
24. Kranz HD, Denekamp M, Greco R, et al. (14 co-authors). 1998. Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana. Plant J. 16:263-276.
25. Kupper H, Lombi E, Zhao FJ, McGrath SP. 2000. Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212:75-84.
26. Landis JB, Barnett LL, Hileman LC. 2012. Evolution of petaloid sepals independent of shifts in B-class MADS box gene expression. Development, Genes, and Evolution 222:19-28.
27. Leech M, Kammerer W, Cove D, Martin C, Wang T. 1993. Expression of MYB-related genes in the moss Physcomitrella patens. Plant J. 3: 51-61.
28. Lipsick JS. 1996. One billion years of MYB. Oncogene 13:223-235.
29. Machado A, Wu Y, Yang Y, Llewellyn DJ, Dennis ES. 2009. The MYB transcription factor GhMYB25 regulates early fibre and trichome development. Plant J. 59:52-62.
30. Martin C, Bhatt K, Baumann K, Jin H, Zachgo S, Roberts K, Schwarz-Sommer Z, Glover BJ, Perez-Rodrigues M. 2002. The mechanics of cell fate determination in petals. Philos Trans R Soc Lond B Biol Sci. 357:809-813.
31. Martin C, Paz-Ares J. 1997. MYB transcription factors in plants. Trends Genet. 13:67-73.
32. Matus JT, Aquea F, Arce-Johnson P. 2008. Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biol. 8:83.
33. Noda K, Glover BJ, Linstead P, Martin C. 1994. Flower colour intensity depends on specialized cell shape controlled by an MYB-related transcription factor. Nature 369:661-664.
34. Nylander J. 2004. MrModeltest v2. Program distributed by the author. Uppsala (Sweden): Evolutionary Biology Centre, Uppsala University.
35. Ogata K, Kanei-Ishii C, Sasaki M, Hatanaka H, Nagadoi A, Enari M, Nakamura H, Nishimura Y, Ishii S, Sarai A. 1996. The cavity in the hydrophobic core ofMyb DNA-binding domain is reserved for DNA recognition and trans-activation. Nat Struct Biol. 3:178-187.
36. Ojeda I, Francisco-Ortega J, Cronk QCB. 2009. Evolution of petal epidermal micromorphology in Leguminosae and its use as a marker of petal identity. Ann Bot. 104:1099-1110.
37. Ojeda I, Santos-Guerra A, Caujapé-Castells J, Jaén-Molina R, Marrero A, Cronk QCB. 2012. Comparative micromorphology of petals in macaronesian lotus (Leguminosae) reveals a loss of papillose conical cells during the evolution of bird pollination. Int J Plant Sci. 173: 365-374.
38. Oppenheimer DG. 1998. Genetics of plant cell shape. Curr Opin Plant Biol. 1:520-524.
39. Pastore JJ, Limpuangthip A, Yamaguchi N, Wu MF, Sang Y, Han SK, Malaspina L, Chavdaroff N, Yamaguchi A, Wagner D. 2011. Late meristem identity 2 acts together with leafy to activate apetala1. Development 138:3189-3198.
40. Perez-Rodriguez M, Jaffe FW, Butelli E, Glover BJ, Martin C. 2005. Development of three different cell types is associated with the activity of a specific MYB transcription factor in the ventral petal of Antirrhinum majus flowers. Development 132: 359-370.
41. Plett JM, Wilkins O, Campbell MM, Ralph SG, Regan S. 2010. Endogenous overexpression of Populus MYB186 increases trichome density, improves insect pest resistance, and impacts plant growth. Plant J. 64:419-432.
42. Rambaut A, Drummond A. 2003. Tracer: MCMC trace analysis tool. Oxford: University of Oxford. tree.bio.ed.ac.uk/software/tracer/(last accessed 2012).
43. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.
44. Romero I, Fuertes A, Benito MJ, Malpica JM, Leyva A, Paz-Ares J. 1998. More than 80R2R3-MYB regulatory genes in the genome of Arabidopsis thaliana. Plant J. 14:273-284.
45. Rozen S, Skaletsky HJ. 2000. Primer3 on theWWWfor general users and for biologist programmers. In: Krawetz S, Misener S, editors. Bioinformatics methods and protocols: methods in molecular biology. Totowa (NJ): Humana Press. p. 365-386.
46. Scoville AG, Barnett LL, Bodbyl-Roels S, Kelly JK, Hileman LC. 2011. Differential regulation of a MYB transcription factor is correlated with transgenerational epigenetic inheritance of trichome density in Mimulus guttatus. New Phytol. 191:251-263.
47. Serna L, Martin C. 2006. Trichomes: different regulatory networks lead to convergent structures. Trends Plant Science. 11: 274-280.
48. Shelton D, Stranne M, Mikkelsen L, et al. (14 co-authors). 2012. Transcription factors of Lotus japonicus: regulation of isoflavonoid biosynthesis requires coordinated changes in transcription factor activity. Plant Physiol. 159:531-547.
49. Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K, Weisshaar B. 2007. Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J. 50: 660-677.
50. Stracke R, Werber M, Weisshaar B. 2001. The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol. 4:447-456.
51. Swofford D. 2000. PAUP: phylogenetic analysis using parsimony and other methods. Version 4. Sunderland (MA): Sinauer Associates.
52. Wagner GJ, Wang E, Shepherd RW. 2004. New approaches for studying and exploiting an old protuberance, the plant trichome. Ann Bot. 93: 3-11.
53. Walford SA, Wu Y, Llewellyn DJ, Dennis ES. 2011. GhMYB25-like: a key factor in early cotton fibre development. Plant J Cell Mol Biol. 65: 785-797.
54. Werker E. 2000. Trichome diversity and development. Adv Bot Res. 31: 1-35.
55. Whitney HM, Bennett KM, Dorling M, Sandbach L, Prince D, Chittka L, Glover BJ. 2011. Why do so many petals have conical epidermal cells? Ann Bot. 108:609-616.
56. Wilkins O, Nahal H, Foong J, Provart NJ, Campbell MM. 2009. Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiol. 149:981-993.
57. Yanhui C, Xiaoyuan Y, Kun H, et al. (18 co-authors). 2006. The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol. 60:107-124.
58. Zhang YF, Cao GY, Qu LJ, Gu HY. 2009. Characterization of Arabidopsis MYB transcription factor gene AtMYB17 and its possible regulation by LEAFY and AGL15. J Genet Genomics. 36:99-107.
59. Zwickl D. 2009. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence data sets under the maximum likelihood criterion [PhD thesis]. [Austin (TX)]: University of Texas at Austin.