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Genome-Wide Identification of the Aux/IAA Family Genes (MdIAA) and Functional Analysis of MdIAA18 for Apple Tree Ideotype

  • Limin Wang
  • Ke Xu
  • Yongzhou Li
  • Wenbo Cai
  • Yanan Zhao
  • Boyang Yu
  • Yuandi ZhuEmail author
Original Article
  • 12 Downloads

Abstract

The Aux/IAA (auxin/indole-3-acetic acid) gene family is one of the early auxin-responsive gene families, which play a central role in auxin response. Few reports are involved in Aux/IAA genes in fruit trees, especially in apple (Malus × domestica Borkh.). A total of 33 MdIAA members were identified, of which 27 members contained four conserved domains, whereas the others lost one or two conserved domains. Several cis-elements in promoters of MdIAAs were predicted responsive to hormones and abiotic stress. Tissue-specific expression patterns of MdIAAs in different apple tree ideotypes were investigated by quantitative real-time PCR. A large number of MdIAAs were highly expressed in leaf buds and reproductive organs, and MdIAAs clustered in same group showed similar expression profiles. Overexpression of MdIAA18 in Arabidopsis resulted in compact phenotype. These results indicated that MdIAA genes may be involved in vegetative and reproductive growth of apple. Taken together, the results provide useful clues to reveal the function of MdIAAs in apple and control apple tree architecture by manipulation of MdIAAs.

Keywords

Malus × domestica Borkh. MdIAA Auxin-responsive genes Plant architecture 

Notes

Acknowledgement

The financial support of this work was from the National Natural Science Foundation of China (Project No. 31672109). The authors thank Emma Tacken, Ph.D., from Liwen Bianji, Edanz Group China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

10528_2019_9919_MOESM1_ESM.tif (576 kb)
Supplementary file1 (TIFF 577 kb). Figure S1 Gene structure of MdIAAs. The orange boxes represent the exons and the black lines represent the introns.
10528_2019_9919_MOESM2_ESM.tif (17 mb)
Supplementary file2 (TIFF 17428 kb). Figure S2 Phenotypes of MdIAA18-ox Arabidopsis at one-month growth after seedling transplanting.
10528_2019_9919_MOESM3_ESM.docx (19 kb)
Supplementary file3 (DOCX 19 kb). Table S1 The primers of MdIAA family genes.
10528_2019_9919_MOESM4_ESM.docx (20 kb)
Supplementary file4 (DOCX 20 kb). Table S2 The sister pairs of MdIAAs.

References

  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 8:87–96CrossRefGoogle Scholar
  2. Abel S, Theologis A (1996) Early genes and auxin action. Plant Physiol 111:9–17CrossRefGoogle Scholar
  3. Asif M et al (2006) Isolation of high-quality RNA from apple (Malus domestica) fruit. J Agr Food Chem 54:5227–5229.  https://doi.org/10.1021/jf053137n CrossRefGoogle Scholar
  4. Bai T et al (2012) Fine genetic mapping of the Co locus controlling columnar growth habit in apple. Mol Genet Genom 287:437–450.  https://doi.org/10.1007/s00438-012-0689-5 CrossRefGoogle Scholar
  5. Baldi P et al (2013) Genetic and physical characterisation of the locus controlling columnar habit in apple (Malus × domestica Borkh.). Mol Breed 31:429–440.  https://doi.org/10.1007/s11032-012-9800-1 CrossRefGoogle Scholar
  6. Benkova E et al (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602CrossRefGoogle Scholar
  7. Catala C, Rose JK, Bennett AB (2000) Auxin-regulated genes encoding cell wall-modifying proteins are expressed during early tomato fruit growth. Plant Physiol 122:527–534CrossRefGoogle Scholar
  8. Chaabouni S et al (2009) Sl-IAA3, a tomato Aux/IAA at the crossroads of auxin and ethylene signalling involved in differential growth. J Exp Bot 60:1349–1362.  https://doi.org/10.1093/jxb/erp009 CrossRefGoogle Scholar
  9. Chapman EJ, Estelle M (2009) Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet 43:265–285.  https://doi.org/10.1146/annurev-genet-102108-134148 CrossRefGoogle Scholar
  10. Chen H et al (2018) E3 ubiquitin ligase SOR1 regulates ethylene response in rice root by modulating stability of Aux/IAA protein. Proc Natl Acad Sci USA 115:4513–4518.  https://doi.org/10.1073/pnas.1719387115 CrossRefGoogle Scholar
  11. Choi HS, Seo M, Cho HT (2018) Two TPL-binding motifs of ARF2 are involved in repression of auxin responses. Front Plant Sci 9:372.  https://doi.org/10.3389/fpls.2018.00372 CrossRefGoogle Scholar
  12. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefGoogle Scholar
  13. Devoghalaere F et al (2012) A genomics approach to understanding the role of auxin in apple (Malus x domestica) fruit size control. BMC Plant Biol 12:7.  https://doi.org/10.1186/1471-2229-12-7 CrossRefGoogle Scholar
  14. Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445.  https://doi.org/10.1038/nature03543 CrossRefGoogle Scholar
  15. Fukaki H et al (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29:153–168CrossRefGoogle Scholar
  16. Galli M et al (2015) Auxin signaling modules regulate maize inflorescence architecture. Proc Natl Acad Sci USA 112:13372–13377.  https://doi.org/10.1073/pnas.1516473112 CrossRefGoogle Scholar
  17. Gray WM et al (2001) Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 414:271CrossRefGoogle Scholar
  18. Guilfoyle TJ, Hagen G (2012) Getting a grasp on domain III/IV responsible for Auxin Response Factor-IAA protein interactions. Plant Sci 190:82–88.  https://doi.org/10.1016/j.plantsci.2012.04.003 CrossRefGoogle Scholar
  19. Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385CrossRefGoogle Scholar
  20. Hofgen R, Willmitzer L (1988) Storage of competent cells for Agrobacterium transformation. Nucleic Acids Res 16:9877CrossRefGoogle Scholar
  21. Hollender CA, Dardick C (2015) Molecular basis of angiosperm tree architecture. New Phytol 206:541–556.  https://doi.org/10.1111/nph.13204 CrossRefGoogle Scholar
  22. Hu B et al (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297.  https://doi.org/10.1093/bioinformatics/btu817 CrossRefGoogle Scholar
  23. Jain M et al (2006) Structure and expression analysis of early auxin-responsive Aux/IAA gene family in rice (Oryza sativa). Funct Integr Genom 6:47–59.  https://doi.org/10.1007/s10142-005-0005-0 CrossRefGoogle Scholar
  24. Jain M et al (2006) The auxin-responsive GH3 gene family in rice (Oryza sativa). Funct Integr Genom 6:36–46.  https://doi.org/10.1007/s10142-005-0142-5 CrossRefGoogle Scholar
  25. Kalluri UC et al (2007) Genome-wide analysis of Aux/IAA and ARF gene families in Populus trichocarpa. BMC Plant Biol 7:59.  https://doi.org/10.1186/1471-2229-7-59 CrossRefGoogle Scholar
  26. Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451.  https://doi.org/10.1038/nature03542 CrossRefGoogle Scholar
  27. Kim J, Harter K, Theologis A (1997) Protein-protein interactions among the Aux/IAA proteins. Proc Natl Acad Sci USA 94:11786–11791CrossRefGoogle Scholar
  28. Knudsen S (1999) Promoter2.0: for the recognition of PolII promoter sequences. Bioinformatics 15:356–361CrossRefGoogle Scholar
  29. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874.  https://doi.org/10.1093/molbev/msw054 CrossRefGoogle Scholar
  30. Lapins KO (1969) Segregation of compact growth types in certain apple seedling progenies. Can J Plant Sci 49:765–768CrossRefGoogle Scholar
  31. Lescot M et al (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327CrossRefGoogle Scholar
  32. Leyser HM et al (1996) Mutations in the AXR3 gene of Arabidopsis result in altered auxin response including ectopic expression from the SAUR-AC1 promoter. Plant J 10:403–413CrossRefGoogle Scholar
  33. Liscum E, Reed JW (2002) Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol 49:387–400CrossRefGoogle Scholar
  34. Liu S et al (2015) Expression of wild-type PtrIAA14.1, a poplar Aux/IAA gene causes morphological changes in Arabidopsis. Front Plant Sci 6:388.  https://doi.org/10.3389/fpls.2015.00388 Google Scholar
  35. Liu K et al (2017) Genome-wide analysis and characterization of Aux/IAA family genes related to fruit ripening in papaya (Carica papaya L.). BMC Genom 18:351.  https://doi.org/10.1186/s12864-017-3722-6 CrossRefGoogle Scholar
  36. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408CrossRefGoogle Scholar
  37. Ljung K (2013) Auxin metabolism and homeostasis during plant development. Development 140:943–950.  https://doi.org/10.1242/dev.086363 CrossRefGoogle Scholar
  38. Looney NE, Lane WD (1984) Spur-type growth mutants of McIntosh apple: a review of their genetics, physiology and field performance. Acta Hortic 146:31–46CrossRefGoogle Scholar
  39. Lu G et al (2015) OsPIN5b modulates rice (Oryza sativa) plant architecture and yield by changing auxin homeostasis, transport and distribution. Plant J 83:913–925.  https://doi.org/10.1111/tpj.12939 CrossRefGoogle Scholar
  40. Ludwig Y et al (2014) Diversity of stability, localization, interaction and control of downstream gene activity in the Maize Aux/IAA protein family. PLoS ONE 9:e107346.  https://doi.org/10.1371/journal.pone.0107346 CrossRefGoogle Scholar
  41. Luo S et al (2015) Constitutive expression of OsIAA9 affects starch granules accumulation and root gravitropic response in Arabidopsis. Front Plant Sci 6:1156.  https://doi.org/10.3389/fpls.2015.01156 CrossRefGoogle Scholar
  42. Mockaitis K, Estelle M (2008) Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol 24:55–80.  https://doi.org/10.1146/annurev.cellbio.23.090506.123214 CrossRefGoogle Scholar
  43. Nemhauser JL (2018) Back to basics: what is the function of an Aux/IAA in auxin response? New Phytol 218:1295–1297.  https://doi.org/10.1111/nph.15172 CrossRefGoogle Scholar
  44. Okushima Y et al (2005) AUXIN RESPONSE FACTOR 2 (ARF2): a pleiotropic developmental regulator. Plant J 43:29–46.  https://doi.org/10.1111/j.1365-313X.2005.02426.x CrossRefGoogle Scholar
  45. Panchy N, Lehti-Shiu MD, Shiu SH (2016) Evolution of gene duplication in plants. Plant Physiol 171:2294–2316.  https://doi.org/10.1104/pp.16.00523 Google Scholar
  46. Paul KK, Bari MA (1979) Protocol establishment for micro propagation and callus regeneration of Maulavi Kachu (L Schott.) From Cormel Axillary Bud MeristemGoogle Scholar
  47. Peer WA (2013) From perception to attenuation: auxin signalling and responses. Curr Opin Plant Biol 16:561–568.  https://doi.org/10.1016/j.pbi.2013.08.003 CrossRefGoogle Scholar
  48. Petersen R, Krost C (2013) Tracing a key player in the regulation of plant architecture: the columnar growth habit of apple trees (Malus x domestica). Planta 238:1–22.  https://doi.org/10.1007/s00425-013-1898-9 CrossRefGoogle Scholar
  49. Robert X, Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42:W320–W324.  https://doi.org/10.1093/nar/gku316 CrossRefGoogle Scholar
  50. Rogg LE, Lasswell J, Bartel B (2001) A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell 13:465–480CrossRefGoogle Scholar
  51. Roy S et al (2017) MtLAX2, a functional homologue of the auxin importer AtAUX1, is required for nodule organogenesis. Plant Physiol 174:326–338CrossRefGoogle Scholar
  52. Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459:1071–1078.  https://doi.org/10.1038/nature08122 CrossRefGoogle Scholar
  53. Sato A, Yamamoto KT (2008) Overexpression of the non-canonical Aux/IAA genes causes auxin-related aberrant phenotypes in Arabidopsis. Physiol Plant 133:397–405.  https://doi.org/10.1111/j.1399-3054.2008.01055.x CrossRefGoogle Scholar
  54. Shapiro BE et al (2015) Analysis of cell division patterns in the Arabidopsis shoot apical meristem. Proc Natl Acad Sci U S A 112:4815–4820CrossRefGoogle Scholar
  55. Singh VK, Jain M (2015) Genome-wide survey and comprehensive expression profiling of Aux/IAA gene family in chickpea and soybean. Front Plant Sci 6:918.  https://doi.org/10.3389/fpls.2015.00918 Google Scholar
  56. Song Y, Wang L, Xiong L (2009) Comprehensive expression profiling analysis of OsIAA gene family in developmental processes and in response to phytohormone and stress treatments. Planta 229:577–591.  https://doi.org/10.1007/s00425-008-0853-7 CrossRefGoogle Scholar
  57. Swarup R et al (2007) Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19:2186–2196.  https://doi.org/10.1105/tpc.107.052100 CrossRefGoogle Scholar
  58. Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319:1384–1386.  https://doi.org/10.1126/science.1151461 CrossRefGoogle Scholar
  59. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 101:11030–11035.  https://doi.org/10.1073/pnas.0404206101 CrossRefGoogle Scholar
  60. Tan X et al (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446:640–645.  https://doi.org/10.1038/nature05731 CrossRefGoogle Scholar
  61. Tan M et al (2018) Identification and expression analysis of the IPT and CKX gene families during axillary bud outgrowth in apple (Malus domestica Borkh.). Gene 651:106–117.  https://doi.org/10.1016/j.gene.2018.01.101 CrossRefGoogle Scholar
  62. Tao S, Estelle M (2018) Mutational studies of the Aux/IAA proteins in Physcomitrella reveal novel insights into their function. New Phytol 218:1534–1542.  https://doi.org/10.1111/nph.15039 CrossRefGoogle Scholar
  63. Tian Q, Reed JW (1999) Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development 126:711–721Google Scholar
  64. Tiwari SB et al (2001) AUX/IAA proteins are active repressors, and their stability and activity are modulated by auxin. Plant Cell 13:2809–2822CrossRefGoogle Scholar
  65. Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543CrossRefGoogle Scholar
  66. Tiwari SB, Hagen G, Guilfoyle TJ (2004) Aux/IAA proteins contain a potent transcriptional repression domain. Plant Cell 16:533–543.  https://doi.org/10.1105/tpc.017384 CrossRefGoogle Scholar
  67. Uehara T et al (2008) Domain II mutations in CRANE/IAA18 suppress lateral root formation and affect shoot development in Arabidopsis thaliana. Plant Cell Physiol 49:1025–1038.  https://doi.org/10.1093/pcp/pcn079 CrossRefGoogle Scholar
  68. Ulmasov T et al (1995) Composite structure of auxin response elements. Plant Cell 7:1611–1623.  https://doi.org/10.1105/tpc.7.10.1611 CrossRefGoogle Scholar
  69. Ulmasov T, Hagen G, Guilfoyle TJ (1997) ARF1, a transcription factor that binds to auxin response elements. Science 276:1865–1868CrossRefGoogle Scholar
  70. Ulmasov T, Hagen G, Guilfoyle TJ (1999) Activation and repression of transcription by auxin-response factors. Proc Natl Acad Sci USA 96:5844–5849CrossRefGoogle Scholar
  71. Velasco R et al (2010) The genome of the domesticated apple (Malus x domestica Borkh.). Nat Genet 42:833–839.  https://doi.org/10.1038/ng.654 CrossRefGoogle Scholar
  72. Wan S et al (2014) Genome-wide identification, characterization and expression analysis of the auxin response factor gene family in Vitis vinifera. Plant Cell Rep 33:1365–1375.  https://doi.org/10.1007/s00299-014-1622-7 CrossRefGoogle Scholar
  73. Wang H et al (2005) The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell 17:2676–2692.  https://doi.org/10.1105/tpc.105.033415 CrossRefGoogle Scholar
  74. Wang Y et al (2010) Genome-wide analysis of primary auxin-responsive Aux/IAA gene family in maize (Zea mays. L.). Mol Biol Rep 37:3991–4001.  https://doi.org/10.1007/s11033-010-0058-6 CrossRefGoogle Scholar
  75. Wang Y et al (2014) Effect of root pruning and irrigation regimes on pear tree: growth, yield and yield components. Hortic Sci 41:34–43CrossRefGoogle Scholar
  76. Wang LM et al (2018) The isolation of the IGT family genes in Malus × domestica and their expressions in four idiotype apple cultivars. Tree Genet Genomes 14:46CrossRefGoogle Scholar
  77. Watanabe M et al (2008) Seasonal changes of IAA and cytokinin in shoots of columnar type apple trees. Acta Hortic 774:75–80CrossRefGoogle Scholar
  78. Wilson BF (2000) Apical control of branch growth and angle in woody plants. Am J Bot 87:601–607CrossRefGoogle Scholar
  79. Wilson AK et al (1990) A dominant mutation in Arabidopsis confers resistance to auxin, ethylene and abscisic acid. Mol Gen Genet 222:377–383CrossRefGoogle Scholar
  80. Winkler M et al (2017) Variation in auxin sensing guides AUX/IAA transcriptional repressor ubiquitylation and destruction. Nat Commun 8:15706.  https://doi.org/10.1038/ncomms15706 CrossRefGoogle Scholar
  81. Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Annals of Botany 95:707CrossRefGoogle Scholar
  82. Wu J et al (2012) Genome-wide analysis of Aux/IAA gene family in Solanaceae species using tomato as a model. Mol Genet Genom 287:295–311.  https://doi.org/10.1007/s00438-012-0675-y CrossRefGoogle Scholar
  83. Wu J et al (2014) Genome-wide identification and transcriptional profiling analysis of auxin response-related gene families in cucumber. BMC Res Notes 7:218.  https://doi.org/10.1186/1756-0500-7-218 CrossRefGoogle Scholar
  84. Wu W et al (2017) Evolution analysis of the Aux/IAA gene family in plants shows dual origins and variable nuclear localization signals. Int J Mol Sci.  https://doi.org/10.3390/ijms18102107 Google Scholar
  85. Xu K et al (2017) Characterization of a SUPERMAN-like Gene, MdSUP11, in apple (Malus × domestica Borkh.). Plant Physiol Biochem 125:136–142CrossRefGoogle Scholar
  86. Yang X et al (2004) The IAA1 protein is encoded by AXR5 and is a substrate of SCF(TIR1). Plant J 40:772–782.  https://doi.org/10.1111/j.1365-313X.2004.02254.x CrossRefGoogle Scholar
  87. Yu H et al (2015) Comprehensive genome-wide analysis of the Aux/IAA gene family in eucalyptus: evidence for the role of EgrIAA4 in wood formation. Plant Cell Physiol 56:700–714CrossRefGoogle Scholar
  88. Yuan H et al (2018) Identification and expression profiling of the Aux/IAA gene family in Chinese hickory (Carya cathayensis Sarg.) during the grafting process. Plant Physiol Biochem 127:55–63.  https://doi.org/10.1016/j.plaphy.2018.03.010 CrossRefGoogle Scholar
  89. Zenser N et al (2001) Auxin modulates the degradation rate of Aux/IAA proteins. Proc Natl Acad Sci U S A 98:11795–11800.  https://doi.org/10.1073/pnas.211312798 CrossRefGoogle Scholar
  90. Zhang S et al (2018) Genome-wide identification of the HKT genes in five Rosaceae species and expression analysis of HKT genes in response to salt-stress in Fragaria vesca. Genes Genom.  https://doi.org/10.1007/s13258-018-0767-0 Google Scholar

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Authors and Affiliations

  1. 1.Department of Pomology, College of HorticultureChina Agricultural UniversityBeijingPeople’s Republic of China

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