Journal of Molecular Evolution

, Volume 85, Issue 3–4, pp 107–119 | Cite as

Evolution of the Aux/IAA Gene Family in Hexaploid Wheat

  • Linyi Qiao
  • Li Zhang
  • Xiaojun Zhang
  • Lei Zhang
  • Xin Li
  • Jianzhong Chang
  • Haixian Zhan
  • Huijuan Guo
  • Jun Zheng
  • Zhijian Chang
Original Article


The Aux/IAA (IAA) gene family, involved in the auxin signalling pathway, acts as an important regulator in plant growth and development. In this study, we explored the evolutionary trajectory of the IAA family in common wheat. The results showed ten pairs of paralogs among 34 TaIAA family members. Seven of the pairs might have undergone segmental duplication, and the other three pairs appear to have experienced tandem duplication. Except for TaIAA15-16, these duplication events occurred in the ancestral genomes before the divergence of Triticeae. After that point, two polyploidization events shaped the current TaIAA family consisting of three subgenomic copies. The structure or expression pattern of the TaIAA family begins to differentiate in the hexaploid genome, where TaIAAs in the D genome lost more genes (eight) and protein secondary structures (α1, α3 and β5) than did the other two genomes. Expression analysis showed that six members of the TaIAA family were not expressed, and members such as TaIAA8, 15, 16, 28 and 33 exhibited tissue-specific expression patterns. In addition, three of the ten pairs of paralogs (TaIAA512, TaIAA1516 and TaIAA2930) showed similar expression patterns, and another five paralog pairs displayed differential expression patterns. Phylogenetic analysis showed that paralog pairs with high rates of evolution (ω > ω 0), particularly TaIAA1516 and TaIAA2930, experienced greater motif loss, with only zero to two interacting IAA proteins. In contrast, most paralogous genes with low ω, such as TaIAA5–12, had more complete motifs and higher degrees of interaction with other family members.


Molecular evolution Aux/IAA gene family Wheat Expression analysis 



This study was funded by the National Key Research and Development Plan of China (2016YFD0102004-07), the National Natural Science Foundation of China (31601307), Shanxi Province Science Foundation for Youths (2015021145), Shanxi Province Natural Science Foundation (201601D102051) and Shanxi Province International Cooperation Project (201603D421003). We thank Dr. Xiaoyan Li (Beijing Anzhen Hospital Affiliated to the Capital Medical University) and Dr. Wenping Zhang (Fujian Agriculture and Forestry University) for their assistance in the RT-PCR experiment.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

239_2017_9810_MOESM1_ESM.docx (1.7 mb)
Supplementary material 1 (DOCX 1691 KB)


  1. Abel S, Theologis A (1995) A polymorphic bipartite motif signals nuclear targeting of early auxin-inducible proteins related to PS-IAA4 from pea (Pisum sativum). Plant J 8:87–96CrossRefPubMedGoogle Scholar
  2. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202-208CrossRefGoogle Scholar
  3. Birchler JA, Veitia RA (2007) The gene balance hypothesis: from classical genetics to modern genomics. Plant Cell 19:395–402CrossRefPubMedPubMedCentralGoogle Scholar
  4. Brassica rapa Genome Sequencing Project Consortium (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039CrossRefGoogle Scholar
  5. Brenchley R, Spannagl M, Pfeifer M, Barker GL, D’Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolser D, Kay S, Waite D, Trick M, Bancroft I, Gu Y, Huo N, Luo MC, Sehgal S, Gill B, Kianian S, Anderson O, Kersey P, Dvorak J, McCombie WR, Hall A, Mayer KF, Edwards KJ, Bevan MW, Hall N (2012) Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491:705–710CrossRefPubMedPubMedCentralGoogle Scholar
  6. Buggs RJ, Zhang L, Miles N, Tate JA, Gao L, Wei W, Schnable PS, Barbazuk WB, Soltis PS, Soltis DE (2011) Transcriptomic shock generates evolutionary novelty in a newly formed, natural allopolyploid plant. Curr Biol 21:551–556CrossRefPubMedGoogle Scholar
  7. Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58:377–406CrossRefPubMedPubMedCentralGoogle Scholar
  8. Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846CrossRefPubMedGoogle Scholar
  9. Cooke TJ, Poli D, Sztein AE, Cohen JD (2002) Evolutionary patterns in auxin action. Plant Mol Biol 49:319–338CrossRefPubMedGoogle Scholar
  10. D’Hont A, Denoeud F, Aury JM (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488:213–217CrossRefPubMedGoogle Scholar
  11. De Smet I, Voss U, Lau S, Wilson M, Shao N, Timme RE, Swarup R, Kerr I, Hodgman C, Bock R, Bennett M, Jürgens G, Beeckman T (2011) Unraveling the evolution of auxin signaling. Plant Physiol 155:209–221CrossRefPubMedGoogle Scholar
  12. Dinesh DC, Kovermann M, Gopalswamy M, Hellmuth A, Calderón Villalobos LI, Lilie H, Balbach J, Abel S (2015) Solution structure of the PsIAA4 oligomerization domain reveals interaction modes for transcription factors in early auxin response. Proc Natl Acad Sci USA 112:6230–6235CrossRefPubMedPubMedCentralGoogle Scholar
  13. Errami M, Geourjon C, Deléage G (2003) Detection of unrelated proteins in sequences multiple alignments by using predicted secondary structures. Bioinformatics 19:506–512CrossRefPubMedGoogle Scholar
  14. Freeling M, Thomas BC (2006) Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res 16:805–814CrossRefPubMedGoogle Scholar
  15. Gaut BS, Morton BR, McCaig BC, Clegg MT (1996) Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc Natl Acad Sci USA 93:10274–10279CrossRefPubMedPubMedCentralGoogle Scholar
  16. Guo Y, Qiu LJ (2013) Genome-wide analysis of the Dof transcription factor gene family reveals soybean-specific duplicable and functional characteristics. PLoS ONE 8:e76809CrossRefPubMedPubMedCentralGoogle Scholar
  17. Halliday KJ, Martínez-García JF, Josse EM (2009) Integration of light and auxin signaling. Cold Spring Harb Perspect Biol 1:a001586CrossRefPubMedPubMedCentralGoogle Scholar
  18. Huang Z, Duan W, Song X, Tang J, Wu P, Zhang B, Hou X (2015) Retention, molecular evolution, and expression divergence of the auxin/indole acetic acid and auxin response factor gene families in Brassica rapa shed light on their evolution patterns in plants. Genome Biol Evol 8:302–316CrossRefPubMedPubMedCentralGoogle Scholar
  19. Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314Google Scholar
  20. International Wheat Genome Sequencing Consortium (IWGSC) (2014) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345:1251788CrossRefGoogle Scholar
  21. Jing H, Yang X, Zhang J, Liu X, Zheng H, Dong G, Nian J, Feng J, Xia B, Qian Q, Li J, Zuo J (2015) Peptidyl-prolyl isomerization targets rice Aux/IAAs for proteasomal degradation during auxin signalling. Nat Commun 6:7395CrossRefPubMedGoogle Scholar
  22. Jung H, Lee DK, Choi YD, Kim JK (2015) OsIAA6, a member of the rice Aux/IAA gene family, is involved in drought tolerance and tiller outgrowth. Plant Sci 236:304–312CrossRefPubMedGoogle Scholar
  23. Kazan K, Manners JM (2009) Linking development to defense: auxin in plant-pathogen interactions. Trends Plant Sci 14:373–382CrossRefPubMedGoogle Scholar
  24. Koonin EV (2005) Orthologs, paralogs, and evolutionary genomics. Annu Rev Genet 39:309–338CrossRefPubMedGoogle Scholar
  25. 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 23:2947–2948CrossRefPubMedGoogle Scholar
  26. Leitch A, Leitch I (2008) Genomic plasticity and the diversity of polyploid plants. Science 320:481–483CrossRefPubMedGoogle Scholar
  27. Letunic I, Doerks T, Bork P (2015) SMART: recent updates, new developments and status in 2015. Nucleic Acids Res 43:257–260CrossRefGoogle Scholar
  28. Li WH (1997) Molecular evolution. Sinauer Associates, SunderlandGoogle Scholar
  29. Liu B, Vega JM, Feldman M (1998) Rapid genomic changes in newly synthesized amphiploids of Triticum and Aegilops II Changes in low-copy coding DNA sequences. Genome 41:535–542CrossRefPubMedGoogle Scholar
  30. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  31. Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate gene. Science 290:1151–1155CrossRefPubMedGoogle Scholar
  32. Masterson J (1994) Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264:421–424CrossRefPubMedGoogle Scholar
  33. Michael TP, VanBuren R (2015) Progress, challenges and the future of crop genomes. Curr Opin Plant Biol 24:71–81CrossRefPubMedGoogle Scholar
  34. Nanao MH, Vinos-Poyo T, Brunoud G, Thévenon E, Mazzoleni M, Mast D, Lainé S, Wang S, Hagen G, Li H, Guilfoyle TJ, Parcy F, Vernoux T, Dumas R (2014) Structural basis for oligomerization of auxin transcriptional regulators. Nat Commun 5:3617CrossRefPubMedGoogle Scholar
  35. Nystedt B, Street NR, Wetterbom A (2013) The Norway spruce genome sequence and conifer genome evolution. Nature 497:579–584CrossRefPubMedGoogle Scholar
  36. Otto SP (2007) The evolutionary consequences of polyploidy. Cell 131:452–462CrossRefPubMedGoogle Scholar
  37. Paponov IA, Teale W, Lang D, Paponov M, Reski R, Rensing SA, Palme K (2009) The evolution of nuclear auxin signalling. BMC Evol Biol 9:126CrossRefPubMedPubMedCentralGoogle Scholar
  38. Petersen G, Seberg O, Yde M, Berthelsen K (2006) Phylogenetic relationships of Triticum and Aegilops and evidence for the origin of the A, B, and D genomes of common wheat (Triticum aestivum). Mol Phylogenet Evol 39:70–82CrossRefPubMedGoogle Scholar
  39. Pfeifer M, Kugler KG, Sandve SR, Zhan B, Rudi H, Hvidsten TR, International Wheat Genome Sequencing Consortium, Mayer KF, Olsen OA (2014) Genome interplay in the grain transcriptome of hexaploid bread wheat. Science 345:1250091CrossRefPubMedGoogle Scholar
  40. Pont C, Murat F, Guizard S, Flores R, Foucrier S, Bidet Y, Quraishi UM, Alaux M, Doležel J, Fahima T, Budak H, Keller B, Salvi S, Maccaferri M, Steinbach D, Feuillet C, Quesneville H, Salse J (2013) Wheat syntenome unveils new evidences of contrasted evolutionary plasticity between paleo- and neoduplicated subgenomes. Plant J 76:1030–1044CrossRefPubMedGoogle Scholar
  41. Priya R, Ive DS (2013) Evolutionary aspects of auxin signalling. In: Zažímalová E (ed) Auxin and its role in plant development, 1st edn. Springer, Vienna, pp 265–290Google Scholar
  42. Qiao L, Zhang X, Han X, Zhang L, Li X, Zhan H, Ma J, Luo P, Zhang W, Cui L, Li X, Chang Z (2015) A genome-wide analysis of the auxin/indole-3-acetic acid gene family in hexaploid bread wheat (Triticum aestivum L). Front Plant Sci 6:770CrossRefPubMedPubMedCentralGoogle Scholar
  43. Raes J, Van de Peer Y (2003) Gene duplications, the evolution of novel gene functions, and detecting functional divergence of duplicates in silico. Appl Bioinformatics 2:92–101Google Scholar
  44. Roulin A, Auer PL, Libault M, Schlueter J, Farmer A, May G, Stacey G, Doerge RW, Jackson SA (2013) The fate of duplicated genes in a polyploid plant genome. Plant J 73:143–153CrossRefPubMedGoogle Scholar
  45. Salse J, Bolot S, Throude M, Jouffe V, Piegu B, Quraishi UM, Calcagno T, Cooke R, Delseny M, Feuillet C (2008) Identification and characterization of shared duplications between rice and wheat provide new insight into grass genome evolution. Plant Cell 20:11–24CrossRefPubMedPubMedCentralGoogle Scholar
  46. Schaller GE, Bishopp A, Kieber JJ (2015) The Yin-Yang of hormones: cytokinin and auxin interactions in plant development. Plant Cell 27:44–63CrossRefPubMedPubMedCentralGoogle Scholar
  47. Singla B, Chugh A, Khurana JP, Khurana P (2006) An early auxin-responsive Aux/IAA gene from wheat (Triticum aestivum) is induced by epibrassinolide and differentially regulated by light and calcium. J Exp Bot 57:4059–4070CrossRefPubMedGoogle Scholar
  48. Soltis PS, Douglas E. Soltis DE, Savolainen V, Crane PR, Barraclough TG (2002) Rate heterogeneity among lineages of tracheophytes: integration of molecular and fossil data and evidence for molecular living fossils. Proc Natl Acad Sci USA 99:4430–4435CrossRefPubMedPubMedCentralGoogle Scholar
  49. Song Y, You J, Xiong L (2009) Characterization of OsIAA1 gene, a member of rice Aux/IAA family involved in auxin and brassinosteroid hormone responses and plant morphogenesis. Plant Mol Biol 70:297–309CrossRefPubMedGoogle Scholar
  50. Strader LC, Chen GL, Bartel B (2010) Ethylene directs auxin to control root cell expansion. Plant J 64:874–884CrossRefPubMedPubMedCentralGoogle Scholar
  51. Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M, Bork P, Jensen LJ, von Mering C (2015) STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43:D447-452CrossRefGoogle Scholar
  52. Talboys PJ, Healey JR, Withers PJ, Jones DL (2014) Phosphate depletion modulates auxin transport in Triticum aestivum leading to altered root branching. J Exp Bot 65:5023–5032CrossRefPubMedPubMedCentralGoogle Scholar
  53. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  54. Thakur JK, Jain M, Tyagi AK, Khurana JP (2005) Exogenous auxin enhances the degradation of a light down-regulated and nuclear-localized OsiIAA1, an Aux/IAA protein from rice, via proteasome. Biochim Biophys Acta 1730:196–205CrossRefPubMedGoogle Scholar
  55. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview Version 2: a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189–1191CrossRefPubMedPubMedCentralGoogle Scholar
  56. Wheeler TJ, Eddy SR (2013) nhmmer: DNA homology search with profile HMMs. Bioinformatics 29:2487–2489CrossRefPubMedPubMedCentralGoogle Scholar
  57. Winkler M, Niemeyer M, Hellmuth A, Janitza P, Christ G, Samodelov SL, Wilde V, Majovsky P, Trujillo M, Zurbriggen MD, Hoehenwarter W, Quint M, Calderón Villalobos LIA (2017) Variation in auxin sensing guides AUX/IAA transcriptional repressor ubiquitylation and destruction. Nat Commun 8:15706CrossRefPubMedPubMedCentralGoogle Scholar
  58. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555–556PubMedGoogle Scholar
  59. Yasumura Y, Crumptontaylor M, Fuentes S, Harberd NP (2007) Step-by-step acquisition of the gibberellin-DELLA growth-regulatory mechanism during land-plant evolution. Curr Biol 17:1225–1230CrossRefPubMedGoogle Scholar
  60. Zhang H, Zhu B, Qi B, Gou X, Dong Y, Xu C, Zhang B, Huang W, Liu C, Wang X, Yang C, Zhou H, Kashkush K, Feldman M, Wendel JF, Liu B (2014) Evolution of the BBAA component of bread wheat during its history at the allohexaploid level. Plant Cell 26:2761–2776CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Linyi Qiao
    • 1
    • 2
  • Li Zhang
    • 3
  • Xiaojun Zhang
    • 2
  • Lei Zhang
    • 4
  • Xin Li
    • 2
  • Jianzhong Chang
    • 2
  • Haixian Zhan
    • 2
  • Huijuan Guo
    • 2
  • Jun Zheng
    • 2
  • Zhijian Chang
    • 2
  1. 1.Department of Biological Sciences, College of Life ScienceShanxi UniversityTaiyuanChina
  2. 2.Shanxi Key Laboratory of Crop Genetics and Molecular Improvement, Institute of Crop ScienceShanxi Academy of Agricultural SciencesTaiyuanChina
  3. 3.Department of Crop Genetics and Breeding, College of AgricultureNanjing Agricultural UniversityNanjingChina
  4. 4.Department of Plant Protection, College of AgricultureShanxi Agricultural UniversityTaiguChina

Personalised recommendations