, Volume 236, Issue 6, pp 1927–1941 | Cite as

ARABIDILLO gene homologues in basal land plants: species-specific gene duplication and likely functional redundancy

  • Laura A. Moody
  • Younousse Saidi
  • Emma J. Smiles
  • Susan J. Bradshaw
  • Matthew Meddings
  • Peter J. Winn
  • Juliet C. Coates
Original Article


ARABIDILLO proteins regulate multicellular root development in Arabidopsis thaliana. Conserved ARABIDILLO homologues are present throughout land plants, even in early-evolving plants that do not possess complex root architecture, suggesting that ARABIDILLO genes have additional functions. Here, we have cloned and characterised ARABIDILLO gene homologues from two early-evolving land plants, the bryophyte Physcomitrella patens and the lycophyte Selaginella moellendorffii. We show that two of the PHYSCODILLO genes (PHYSCODILLO1A and -1B) exist as a tail-to-tail tandem array of two almost identical 12 kb sequences, while a third related gene (PHYSCODILLO2) is located elsewhere in the Physcomitrella genome. Physcomitrella possesses a very low percentage of tandemly arrayed genes compared with the later-evolving plants whose genomes have been sequenced to date. Thus, PHYSCODILLO1A and -1B genes represent a relatively unusual gene arrangement. PHYSCODILLO promoters are active largely in the haploid gametophyte, with additional activity at the foot of the sporophyte. The pattern of promoter activity is uniform in filamentous and leafy tissues, suggesting pleiotropic gene functions and likely functional redundancy: the latter possibility is confirmed by the lack of discernible phenotype in a physcodillo2 deletion mutant. Interestingly, the pattern of PHYSCODILLO promoter activity in female reproductive organs is strikingly similar to that of an Arabidopsis homologue, suggesting co-option of some PHYSCODILLO functions or regulation into both the sporophyte and gametophyte. In conclusion, our work identifies and characterises some of the earliest-evolving land plant ARABIDILLO homologues. We confirm that all land plant ARABIDILLO genes arose from a single common ancestor and suggest that PHYSCODILLO proteins have novel and pleiotropic functions, some of which may be conserved in later-evolving plants.


Development Evolution Gene locus Physcomitrella Promoter activity Sequencing 



Chalcone synthase




Heat shock promoter


Million years ago


Tandemly arrayed gene


Untranslated region



We thank Chris Franklin for useful discussions. We thank Drs. Yasuko Kamisugi and Andrew Cuming, University of Leeds, UK, for the kind gift of the pAHG1 vector. This work was funded by a Leverhulme Trust Research Project Grant (F/00094/BA) and a Royal Society Research Grant (RG081075) to JC, a Biotechnology and Biological Sciences Research Council Doctoral Training Grant to LAM and a Nuffield Foundation Undergraduate Research bursary to ES. Sequencing was carried out at the University of Birmingham Functional Genomics and Proteomics Unit.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

425_2012_1742_MOESM1_ESM.pdf (1.2 mb)
Supplementary material (PDF 1226 kb)


  1. Banks JA (2009) Selaginella and 400 million years of separation. Annu Rev Plant Biol 60:223–238PubMedCrossRefGoogle Scholar
  2. Banks JA, Nishiyama T, Hasebe M, Bowman JL, Gribskov M, dePamphilis C, Albert VA, Aono N, Aoyama T, Ambrose BA, Ashton NW, Axtell MJ, Barker E, Barker MS, Bennetzen JL, Bonawitz ND, Chapple C, Cheng C, Correa LG, Dacre M, DeBarry J, Dreyer I, Elias M, Engstrom EM, Estelle M, Feng L, Finet C, Floyd SK, Frommer WB, Fujita T, Gramzow L, Gutensohn M, Harholt J, Hattori M, Heyl A, Hirai T, Hiwatashi Y, Ishikawa M, Iwata M, Karol KG, Koehler B, Kolukisaoglu U, Kubo M, Kurata T, Lalonde S, Li K, Li Y, Litt A, Lyons E, Manning G, Maruyama T, Michael TP, Mikami K, Miyazaki S, Morinaga S, Murata T, Mueller-Roeber B, Nelson DR, Obara M, Oguri Y, Olmstead RG, Onodera N, Petersen BL, Pils B, Prigge M, Rensing SA, Riano-Pachon DM, Roberts AW, Sato Y, Scheller HV, Schulz B, Schulz C, Shakirov EV, Shibagaki N, Shinohara N, Shippen DE, Sorensen I, Sotooka R, Sugimoto N, Sugita M, Sumikawa N, Tanurdzic M, Theissen G, Ulvskov P, Wakazuki S, Weng JK, Willats WW, Wipf D, Wolf PG, Yang L, Zimmer AD, Zhu Q, Mitros T, Hellsten U, Loque D, Otillar R, Salamov A, Schmutz J, Shapiro H, Lindquist E, Lucas S, Rokhsar D, Grigoriev IV (2011) The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332:960–963PubMedCrossRefGoogle Scholar
  3. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552PubMedCrossRefGoogle Scholar
  4. Chater C, Kamisugi Y, Movahedi M, Fleming A, Cuming AC, Gray JE, Beerling DJ (2011) Regulatory mechanism controlling stomatal behaviour conserved across 400 million years of land plant evolution. Curr Biol 21:1025–1029PubMedCrossRefGoogle Scholar
  5. Coates JC (2003) Armadillo repeat proteins: beyond the animal kingdom. Trends Cell Biol 13:463–471PubMedCrossRefGoogle Scholar
  6. Coates JC, Laplaze L, Haseloff J (2006) Armadillo-related proteins promote lateral root development in Arabidopsis. Proc Natl Acad Sci USA 103:1621–1626PubMedCrossRefGoogle Scholar
  7. Coates JC, Moody LA, Saidi Y (2011) Plants and the Earth system—past events and future challenges. New Phytol 189:370–373PubMedCrossRefGoogle Scholar
  8. Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224PubMedCrossRefGoogle Scholar
  9. Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, Lucas WJ, Wang X, Xie B, Ni P, Ren Y, Zhu H, Li J, Lin K, Jin W, Fei Z, Li G, Staub J, Kilian A, van der Vossen EA, Wu Y, Guo J, He J, Jia Z, Tian G, Lu Y, Ruan J, Qian W, Wang M, Huang Q, Li B, Xuan Z, Cao J, Asan WuZ, Zhang J, Cai Q, Bai Y, Zhao B, Han Y, Li Y, Li X, Wang S, Shi Q, Liu S, Cho WK, Kim JY, Xu Y, Heller-Uszynska K, Miao H, Cheng Z, Zhang S, Wu J, Yang Y, Kang H, Li M, Liang H, Ren X, Shi Z, Wen M, Jian M, Yang H, Zhang G, Yang Z, Chen R, Ma L, Liu H, Zhou Y, Zhao J, Fang X, Fang L, Liu D, Zheng H, Zhang Y, Qin N, Li Z, Yang G, Yang S, Bolund L, Kristiansen K, Li S, Zhang X, Wang J, Sun R, Zhang B, Jiang S, Du Y (2009) The genome of the cucumber, Cucumis sativus L. Nat Genet 41:1275–1281PubMedCrossRefGoogle Scholar
  10. Kamisugi Y, von Stackelberg M, Lang D, Care M, Reski R, Rensing SA, Cuming AC (2008) A sequence-anchored genetic linkage map for the moss, Physcomitrella patens. Plant J 56:855–866PubMedCrossRefGoogle Scholar
  11. Kenrick P, Wellman CH, Schneider H, Edgecombe GD (2012) A timeline for terrestrialization: consequences for the carbon cycle in the Palaeozoic. Philos Trans R Soc Lond B Biol Sci 367:519–536PubMedCrossRefGoogle Scholar
  12. Koduri PK, Gordon GS, Barker EI, Colpitts CC, Ashton NW, Suh DY (2010) Genome-wide analysis of the chalcone synthase superfamily genes of Physcomitrella patens. Plant Mol Biol 72:247–263PubMedCrossRefGoogle Scholar
  13. Lang D, Zimmer AD, Rensing SA, Reski R (2008) Exploring plant biodiversity: the Physcomitrella genome and beyond. Trends Plant Sci 13:542–549PubMedCrossRefGoogle Scholar
  14. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948Google Scholar
  15. Menand B, Yi K, Jouannic S, Hoffmann L, Ryan E, Linstead P, Schaefer DG, Dolan L (2007) An ancient mechanism controls the development of cells with a rooting function in land plants. Science 316:1477–1480PubMedCrossRefGoogle Scholar
  16. Nibau C, Gibbs DJ, Bunting KA, Moody LA, Smiles EJ, Tubby JA, Bradshaw SJ, Coates JC (2011) ARABIDILLO proteins have a novel and conserved domain structure important for the regulation of their stability. Plant Mol Biol 75:77–92PubMedCrossRefGoogle Scholar
  17. Page RD (2002) Visualizing phylogenetic trees using TreeView. Curr Protoc Bioinformatics Chapter 6: Unit 62Google Scholar
  18. Pires ND, Dolan L (2012) Morphological evolution in land plants: new designs with old genes. Philos Trans R Soc Lond B Biol Sci 367:508–518PubMedCrossRefGoogle Scholar
  19. Prigge MJ, Bezanilla M (2010) Evolutionary crossroads in developmental biology: Physcomitrella patens. Development 137:3535–3543PubMedCrossRefGoogle Scholar
  20. Proust H, Hoffmann B, Xie X, Yoneyama K, Schaefer DG, Nogue F, Rameau C (2011) Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138:1531–1539PubMedCrossRefGoogle Scholar
  21. Rensing SA, Ick J, Fawcett JA, Lang D, Zimmer A, Van de Peer Y, Reski R (2007) An ancient genome duplication contributed to the abundance of metabolic genes in the moss Physcomitrella patens. BMC Evol Biol 7:130PubMedCrossRefGoogle Scholar
  22. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y, Tanahashi T, Sakakibara K, Fujita T, Oishi K, Shin IT, Kuroki Y, Toyoda A, Suzuki Y, Hashimoto S, Yamaguchi K, Sugano S, Kohara Y, Fujiyama A, Anterola A, Aoki S, Ashton N, Barbazuk WB, Barker E, Bennetzen JL, Blankenship R, Cho SH, Dutcher SK, Estelle M, Fawcett JA, Gundlach H, Hanada K, Heyl A, Hicks KA, Hughes J, Lohr M, Mayer K, Melkozernov A, Murata T, Nelson DR, Pils B, Prigge M, Reiss B, Renner T, Rombauts S, Rushton PJ, Sanderfoot A, Schween G, Shiu SH, Stueber K, Theodoulou FL, Tu H, Van de Peer Y, Verrier PJ, Waters E, Wood A, Yang L, Cove D, Cuming AC, Hasebe M, Lucas S, Mishler BD, Reski R, Grigoriev IV, Quatrano RS, Boore JL (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69PubMedCrossRefGoogle Scholar
  23. Saidi Y, Finka A, Chakhporanian M, Zryd JP, Schaefer DG, Goloubinoff P (2005) Controlled expression of recombinant proteins in Physcomitrella patens by a conditional heat-shock promoter: a tool for plant research and biotechnology. Plant Mol Biol 59:697–711PubMedCrossRefGoogle Scholar
  24. Saidi Y, Finka A, Muriset M, Bromberg Z, Weiss YG, Maathuis FJ, Goloubinoff P (2009) The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell 21:2829–2843PubMedCrossRefGoogle Scholar
  25. Schaefer DG (2002) A new moss genetics: targeted mutagenesis in Physcomitrella patens. Annu Rev Plant Biol 53:477–501PubMedCrossRefGoogle Scholar
  26. Schaefer DG, Zryd JP (1997) Efficient gene targeting in the moss Physcomitrella patens. Plant J 11:1195–1206PubMedCrossRefGoogle Scholar
  27. Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577PubMedCrossRefGoogle Scholar
  28. Tewari R, Bailes E, Bunting KA, Coates JC (2010) Armadillo-repeat protein functions: questions for little creatures. Trends Cell Biol 20:470–481PubMedCrossRefGoogle Scholar
  29. Wellman CH, Osterloff PL, Mohiuddin U (2003) Fragments of the earliest land plants. Nature 425:282–285PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Laura A. Moody
    • 1
    • 2
  • Younousse Saidi
    • 1
  • Emma J. Smiles
    • 1
  • Susan J. Bradshaw
    • 1
  • Matthew Meddings
    • 1
  • Peter J. Winn
    • 3
  • Juliet C. Coates
    • 1
  1. 1.School of BiosciencesUniversity of BirminghamBirminghamUK
  2. 2.Department of Plant SciencesUniversity of OxfordOxfordUK
  3. 3.Centre for Systems Biology, School of BiosciencesUniversity of BirminghamEdgbastonUK

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