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Genetic dissection of the auxin response network

Abstract

The expansion of gene families during evolution, which can generate functional overlap or specialization among their members, is a characteristic feature of signalling pathways in complex organisms. For example, families of transcriptional activators and repressors mediate responses to the plant hormone auxin. Although these regulators were identified more than 20 years ago, their overlapping functions and compensating negative feedbacks have hampered their functional analyses. Studies using loss-of-function approaches in basal land plants and gain-of-function approaches in angiosperms have in part overcome these issues but have still left an incomplete understanding. Here, we propose that renewed emphasis on genetic analysis of multiple mutants and species will shed light on the role of gene families in auxin response. Combining loss-of-function mutations in auxin-response activators and repressors can unravel complex outputs enabled by expanded gene families, such as fine-tuned developmental outcomes and robustness. Similar approaches and concepts may help to analyse other regulatory pathways whose components are also encoded by large gene families.

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Fig. 1: Auxin response.
Fig. 2: Schematic illustration demonstrating the presumptive non-specific versus specific effects of gain-of-function and loss-of-function iaa mutants.
Fig. 3: In-depth genetic analysis for understanding complexity.

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References

  1. Long, J. A., Moan, E. I., Medford, J. I. & Barton, M. K. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379, 66–69 (1996).

    CAS  PubMed  Google Scholar 

  2. Nüsslein-Volhard, C. & Wieschaus, E. Mutations affecting segment number and polarity in Drosophila. Nature 287, 795–801 (1980).

    PubMed  Google Scholar 

  3. Soyk, S. et al. Duplication of a domestication locus neutralized a cryptic variant that caused a breeding barrier in tomato. Nat. Plants 5, 471 (2019).

    CAS  PubMed  Google Scholar 

  4. Rodriguez-Leal, D. et al. Evolution of buffering in a genetic circuit controlling plant stem cell proliferation. Nat. Genet. 51, 786–792 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Lempe, J., Lachowiec, J., Sullivan, A. M. & Queitsch, C. Molecular mechanisms of robustness in plants. Curr. Opin. Plant Biol. 16, 62–69 (2013).

    CAS  PubMed  Google Scholar 

  6. Boukhibar, L. M. & Barkoulas, M. The developmental genetics of biological robustness. Ann. Bot. 117, 699–707 (2016).

    Google Scholar 

  7. Thomas, J. H. Thinking about genetic redundancy. Trends Genet. 9, 395–399 (1993).

    CAS  PubMed  Google Scholar 

  8. Panchy, N., Lehti-Shiu, M. D. & Shiu, S.-H. Evolution of gene duplication in plants. Plant Physiol. 171, 2294–2316 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Blázquez, M. A., Nelson, D. C. & Weijers, D. Evolution of Plant Hormone Response Pathways. Annu. Rev. Plant Biol. 71, 1–27 (2020).

    Google Scholar 

  10. Gan, X. et al. The Cardamine hirsuta genome offers insight into the evolution of morphological diversity. Nat. Plants 2, 16167 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Salman-Minkov, A., Sabath, N. & Mayrose, I. Whole-genome duplication as a key factor in crop domestication. Nat. Plants 2, 16115 (2016).

    CAS  PubMed  Google Scholar 

  12. Kafri, R., Springer, M. & Pilpel, Y. Genetic redundancy: new tricks forold genes. Cell 136, 389–392 (2009).

    CAS  PubMed  Google Scholar 

  13. El-Brolosy, M. A. & Stainier, D. Y. R. Genetic compensation: a phenomenon in search of mechanisms. PLoS Genet. 13, e1006780 (2017).

    PubMed  PubMed Central  Google Scholar 

  14. Veitia, R. A., Bottani, S. & Birchler, J. A. Gene dosage effects: nonlinearities, genetic interactions, and dosage compensation. Trends Genet. 29, 385–393 (2013).

    CAS  PubMed  Google Scholar 

  15. Leyser, O. Auxin signaling. Plant Physiol. 176, 465–479 (2018).

    CAS  PubMed  Google Scholar 

  16. Weijers, D. & Wagner, D. Transcriptional responses to the auxin hormone. Annu. Rev. Plant Biol. 67, 539–574 (2016).

    CAS  PubMed  Google Scholar 

  17. Mutte, S. K. et al. Origin and evolution of the nuclear auxin response system. eLife 7, e33399 (2018).

    PubMed  PubMed Central  Google Scholar 

  18. Finet, C., Berne-Dedieu, A., Scutt, C. P. & Marlétaz, F. Evolution of the ARF gene family in land plants: old domains, new tricks. Mol. Biol. Evol. 30, 45–56 (2013).

    CAS  PubMed  Google Scholar 

  19. Kato, H. et al. The roles of the sole activator-type auxin response factor in pattern formation of Marchantia polymorpha. Plant Cell Physiol. 58, 1642–1651 (2017).

    CAS  PubMed  Google Scholar 

  20. Kato, H., Nishihama, R., Weijers, D. & Kohchi, T. Evolution of nuclear auxin signaling: lessons from genetic studies with basal land plants. J. Exp. Bot. 69, 291–301 (2018).

    CAS  PubMed  Google Scholar 

  21. Wang, C., Liu, Y., Li, S.-S. & Han, G.-Z. Insights into the origin and evolution of the plant hormone signaling machinery. Plant Physiol. 167, 872–886 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. McSteen, P. Auxin and monocot development. Cold Spring Harb. Perspect. Biol. 2, a001479 (2010).

    PubMed  PubMed Central  Google Scholar 

  23. Galli, M. et al. Auxin signaling modules regulate maize inflorescence architecture. Proc. Natl Acad. Sci. USA 112, 13372–13377 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Ludwig, Y., Zhang, Y. & Hochholdinger, F. Gene family: phylogeny, synteny, and unique root-type and tissue-specific expression patterns during development. PLoS ONE 8, e78859 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Remington, D. L. Contrasting modes of diversification in the Aux/IAA and ARF gene families. Plant Physiol. 135, 1738–1752 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Audran-Delalande, C. et al. Genome-wide identification, functional analysis and expression profiling of the Aux/IAA gene family in tomato. Plant Cell Physiol. 53, 659–672 (2012).

    CAS  PubMed  Google Scholar 

  27. Prigge, M. J. et al. Genetic analysis of the Arabidopsis TIR1/AFB auxin receptors reveals both overlapping and specialized functions. eLife 9, e54740 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Liscum, E. & Reed, J. W. Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol. Biol. 49, 387–400 (2002).

    CAS  PubMed  Google Scholar 

  29. Roosjen, M., Paque, S. & Weijers, D. Auxin response factors: output control in auxin biology. J. Exp. Bot. 69, 179–188 (2018).

    CAS  PubMed  Google Scholar 

  30. Diss, G. & Gagnon-Arsenault, I. Gene duplication can impart fragility, not robustness, in the yeast protein interaction network. Science 355, 630–634 (2017).

    CAS  PubMed  Google Scholar 

  31. Eberlein, C., Evans-Yamamoto, D. & Aube, S. The role of structural pleiotropy and regulatory evolution in the retention of heteromers of paralogs. eLife 8, e46754 (2019).

    PubMed  PubMed Central  Google Scholar 

  32. Tao, S. & Estelle, M. Mutational studies of the Aux/IAA proteins in Physcomitrella reveal novel insights into their function. New Phytol. 218, 1534–1542 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Lavy, M. et al. Constitutive auxin response in Physcomitrella reveals complex interactions between Aux/IAA and ARF proteins. eLife 5, e13325 (2016).

    PubMed  PubMed Central  Google Scholar 

  34. Kato, H. et al. Design principles of a minimal auxin response system. Nat. Plants 6, 473–482 (2020).

    CAS  PubMed  Google Scholar 

  35. Flores-Sandoval, E. et al. Class C ARFs evolved before the origin of land plants and antagonize differentiation and developmental transitions in Marchantia polymorpha. New Phytol. 218, 1612–1630 (2018).

    CAS  PubMed  Google Scholar 

  36. Kato, H. et al. Auxin-mediated transcriptional system with a minimal set of components is critical for morphogenesis through the life cycle in Marchantia polymorpha. PLoS Genet. 11, e1005084 (2015).

    PubMed  PubMed Central  Google Scholar 

  37. Eklund, D. M. et al. Auxin produced by the indole-3-pyruvic acid pathway regulates development and gemmae dormancy in the liverwort Marchantia polymorpha. Plant Cell 27, 1650–1669 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Ross, J. J. & Reid, J. B. Evolution of growth-promoting plant hormones. Funct. Plant Biol. 37, 795–805 (2010).

    CAS  Google Scholar 

  39. Chandler, J. W. Auxin response factors. Plant Cell Environ. 39, 1014–1028 (2016).

    CAS  PubMed  Google Scholar 

  40. Israeli, A. et al. Multiple auxin-response regulators enable stability and variability in leaf development. Curr. Biol. 29, 1746–1759 (2019).

    CAS  PubMed  Google Scholar 

  41. Berleth, T. & Jürgens, G. The role of the monopteros gene in organising the basal body region of the Arabidopsis embryos. Development 118, 575–587 (1993).

    Google Scholar 

  42. Hardtke, C. S. & Berleth, T. The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J. 17, 1405–1411 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Yamaguchi, N. et al. A molecular framework for auxin-mediated initiation of flower primordia. Dev. Cell 24, 271–282 (2013).

    CAS  PubMed  Google Scholar 

  44. Guan, C. et al. Spatial auxin signaling controls leaf flattening in Arabidopsis. Curr. Biol. 27, 2940–2950 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Hardtke, C. S. et al. Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4. Development 131, 1089–1100 (2004).

    CAS  PubMed  Google Scholar 

  46. Nagpal, P. et al. Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132, 4107–4118 (2005).

    CAS  PubMed  Google Scholar 

  47. Okushima, Y. et al. Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana. Plant Cell 17, 444–463 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Wilmoth, J. C. et al. NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J. 43, 118–130 (2005).

    CAS  PubMed  Google Scholar 

  49. Reed, J. W. et al. Three auxin response factors promote hypocotyl elongation. Plant Physiol. 178, 864–875 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Damodharan, S., Corem, S., Gupta, S. K. & Arazi, T. Tuning of SlARF10A dosage by sly-miR160a is critical for auxin-mediated compound leaf and flower development. Plant J. 96, 855–868 (2018).

    CAS  PubMed  Google Scholar 

  51. Pekker, I., Alvarez, J. P. & Esheda, Y. Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17, 2899–2910 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Wang, J. et al. Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. 17, 2204–2216 (2005).

  53. Rademacher, E. H. et al. A cellular expression map of the Arabidopsis AUXIN RESPONSE FACTOR gene family. Plant J. 68, 597–606 (2011).

    CAS  PubMed  Google Scholar 

  54. Flores-Sandoval, E., Eklund, D. M. & Bowman, J. L. A simple auxin transcriptional response system regulates multiple morphogenetic processes in the liverwort Marchantia polymorpha. PLoS Genet. 11, e1005207 (2015).

    PubMed  PubMed Central  Google Scholar 

  55. Audran-Delalande, C. et al. Genome-wide identification, functional analysis and expression profiling of the Aux/IAA gene family in tomato. Plant Cell Physiol. 53, 659–672 (2012).

    CAS  PubMed  Google Scholar 

  56. Matthes, M. S. et al. Auxin evodevo: conservation and diversification of genes regulating auxin biosynthesis, transport, and signaling. Mol. Plant 12, 298–320 (2019).

    CAS  PubMed  Google Scholar 

  57. Overvoorde, P. et al. Functional genomic analysis of the AUXIN/INDOLE-3-ACETIC ACID gene family members in Arabidopsis thaliana. Plant Cell 17, 3282–3300 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Reed, J. W. Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci. 6, 420–425 (2001).

    CAS  PubMed  Google Scholar 

  59. Tian, Q., Nagpal, P. & Reed, J. W. Regulation of Arabidopsis SHY2/IAA3 protein turnover. Plant J. 36, 643–651 (2003).

    CAS  PubMed  Google Scholar 

  60. Nagpal, P. et al. AXR2 encodes a member of the Aux/IAA protein family. Plant Physiol. 123, 563–574 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Wang, J.-J. & Guo, H.-S. Cleavage of INDOLE-3-ACETIC ACID INDUCIBLE28 mRNA by microRNA847 upregulates auxin signaling to modulate cell proliferation and lateral organ growth in Arabidopsis. Plant Cell 27, 574–590 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Luo, J., Zhou, J.-J. & Zhang, J.-Z. Aux/IAA gene family in plants: molecular structure, regulation, and function. Int. J. Mol. Sci. 19, 259 (2018).

    PubMed Central  Google Scholar 

  63. Jung, H., Lee, D.-K., Choi, Y., Do & Kim, J.-K. OsIAA6, a member of the rice Aux/IAA gene family, is involved in drought tolerance and tiller outgrowth. Plant Sci. 236, 304–312 (2015).

    CAS  PubMed  Google Scholar 

  64. Dello Ioio, R. et al. A genetic framework for the control of cell division and differentiation in the root meristem. Science 322, 1380–1384 (2008).

    CAS  PubMed  Google Scholar 

  65. Orosa-Puente, B. et al. Root branching toward water involves posttranslational modification of transcription factor ARF7. Science 362, 1407–1410 (2018).

    CAS  PubMed  Google Scholar 

  66. Shani, E. et al. Plant stress tolerance requires auxin-sensitive report plant stress tolerance requires auxin-sensitive. Curr. Biol. 27, 437–444 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Ben-Gera, H. et al. ENTIRE and GOBLET promote leaflet development in tomato by modulating auxin response. Plant J. 70, 903–915 (2012).

    CAS  PubMed  Google Scholar 

  68. Koenig, D., Bayer, E., Kang, J., Kuhlemeier, C. & Sinha, N. Auxin patterns Solanum lycopersicum leaf morphogenesis. Development 136, 2997–3006 (2009).

    CAS  PubMed  Google Scholar 

  69. Wang, H. et al. The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell 17, 2676–2692 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Berger, Y. et al. The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development 136, 823–832 (2009).

    CAS  PubMed  Google Scholar 

  71. Zhang, J. et al. A single-base deletion mutation in SlIAA9 gene causes tomato (Solanum lycopersicum) entire mutant. J. Plant Res. 120, 671–678 (2007).

    CAS  PubMed  Google Scholar 

  72. Bassa, C., Mila, I., Bouzayen, M. & Audran-Delalande, C. Phenotypes associated with down-regulation of Sl-IAA27 support functional diversity among Aux/IAA family members in tomato. Plant Cell Physiol. 53, 1583–1595 (2012).

    CAS  PubMed  Google Scholar 

  73. Chaabouni, S. et al. Sl-IAA3, a tomato Aux/IAA at the crossroads of auxin and ethylene signalling involved in differential growth. J. Exp. Bot. 60, 1349–1362 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Deng, W. et al. The tomato SlIAA15 is involved in trichome formation and axillary shoot development. New Phytol. 194, 379–390 (2012).

    CAS  PubMed  Google Scholar 

  75. Guillotin, B., Etemadi, M., Audran, C., Bouzayen, M. & Guillaume, B. Sl-IAA27 regulates strigolactone biosynthesis and mycorrhization in tomato (var. MicroTom). New Phytol. 213, 1124–1132 (2016).

    PubMed  Google Scholar 

  76. Su, L. et al. The auxin Sl-IAA17 transcriptional repressor controls fruit size via the regulation of endoreduplication-eelated cell expansion. Plant Cell Physiol. 55, 1969–1976 (2014).

    CAS  PubMed  Google Scholar 

  77. Wang, H. et al. Regulatory features underlying pollination-dependent and -independent tomato fruit set revealed by transcript and primary metabolite profiling. Plant Cell 21, 1428–1452 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Liu, S. et al. Tomato AUXIN RESPONSE FACTOR 5 regulates fruit set and development via the mediation of auxin and gibberellin signaling. Sci. Rep. 8, 2971 (2018).

    PubMed  PubMed Central  Google Scholar 

  79. Alvarez, J. P. et al. Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell 18, 1134–1151 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Liu, Z. et al. ARF2 – ARF4 and ARF5 are essential for female and male gametophyte development in Arabidopsis. Plant Cell Physiol. 59, 179–189 (2018).

    CAS  PubMed  Google Scholar 

  81. Flores-Sandoval, E. et al. Class C ARFs evolved before the origin of land plants and antagonize differentiation and developmental transitions in Marchantia polymorpha. New Phytol. 218, 1612–1630 (2018).

    CAS  PubMed  Google Scholar 

  82. Wang, Y. et al. MicroRNA167-directed regulation of the auxin response factors GmARF8a and GmARF8b is required for soybean nodulation and lateral root development. Plant Physiol. 168, 984–999 (2015).

    PubMed  PubMed Central  Google Scholar 

  83. Turner, M. et al. Ectopic expression of miR160 results in auxin hypersensitivity, cytokinin hyposensitivity, and inhibition of symbiotic nodule development in soybean. Plant Physiol. 162, 2042–2055 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Ben-Gera, H. et al. Auxin-mediated lamina growth in tomato leaves is restricted by two parallel mechanisms. Plant J. 86, 443–457 (2016).

    CAS  PubMed  Google Scholar 

  85. Wu, M.-F., Tian, Q. & Reed, J. W. Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133, 4211–4218 (2006).

    CAS  PubMed  Google Scholar 

  86. Liu, N. et al. Down-regulation of AUXIN RESPONSE FACTORS 6 and 8 by microRNA 167 leads to floral development defects and female sterility in tomato. J. Exp. Bot. 65, 2507–2520 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Todesco, M., Rubio-Somoza, I., Paz-Ares, J. & Weigel, D. A collection of target mimics for comprehensive analysis of microRNA function in Arabidopsis thaliana. PLoS Genet. 6, 1–10 (2010).

    Google Scholar 

  88. Hauser, F. et al. Genomic-scale artificial microRNA library as a tool to investigate the functionally redundant gene space in Arabidopsis. Plant Cell 25, 2848–2863 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Alvarez, J. P., Furumizu, C., Efroni, I., Eshed, Y. & Bowman, J. L. Active suppression of a leaf meristem orchestrates determinate leaf growth. eLife 5, e15023 (2016).

    PubMed  PubMed Central  Google Scholar 

  90. Nizampatnam, N. R., Schreier, S. J., Damodaran, S., Adhikari, S. & Subramanian, S. MicroRNA160 dictates stage-specific auxin and cytokinin sensitivities and directs soybean nodule development. Plant J. 84, 140–153 (2015).

    CAS  PubMed  Google Scholar 

  91. Huang, J., Li, Z. & Zhao, D. Deregulation of the OsmiR160 target gene OsARF18 causes growth and developmental defects with an alteration of auxin signaling in rice. Sci. Rep. 6, 29938 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Liu, P. P. et al. Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J. 52, 133–146 (2007).

    CAS  PubMed  Google Scholar 

  93. Mallory, A. C., Bartel, D. P. & Bartel, B. MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17, 1360–1375 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  94. de Jong, M., Wolters-Arts, M., Feron, R., Mariani, C. & Vriezen, W. H. The Solanum lycopersicum auxin response factor 7 (SlARF7) regulates auxin signaling during tomato fruit set and development. Plant J. 57, 160–170 (2009).

    PubMed  Google Scholar 

  95. Liu, H. et al. Four AUXIN RESPONSE FACTOR genes downregulated by microRNA167 are associated with growth and development in Oryza sativa. Funct. Plant Biol. 39, 738–744 (2012).

    Google Scholar 

  96. Hu, J., Israeli, A., Ori, N. & Sun, T. The interaction between DELLA and ARF/IAA mediates crosstalk between gibberellin and auxin signaling to control fruit initiation in tomato. Plant Cell 30, 1710–1728 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Yifhar, T. et al. Failure of the tomato trans-acting short interfering RNA program to regulate AUXIN RESPONSE FACTOR3 and ARF4 underlies the wiry leaf syndrome. Plant Cell 24, 3575–3589 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Plavskin, Y. et al. Ancient trans-acting siRNAs confer robustness and sensitivity onto the auxin response. Dev. Cell 36, 276–289 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Zhang, Y. et al. A transportome-scale amiRNA-based screen identifies redundant roles of Arabidopsis ABCB6 and ABCB20 in auxin transport. Nat. Commun. 9, 4204 (2018).

    PubMed  PubMed Central  Google Scholar 

  100. Calderon-villalobos, L. I., Tan, X., Zheng, N. & Estelle, M. Auxin perception − structural insights. Cold Spring Harb. Perspect. Biol. 2, a005546 (2010).

    PubMed  PubMed Central  Google Scholar 

  101. Mockaitis, K. & Estelle, M. Auxin receptors and plant development: a new signaling paradigm. Annu. Rev. Cell Dev. Biol. 24, 55–80 (2008).

    CAS  PubMed  Google Scholar 

  102. Fukaki, H., Tameda, S., Masuda, H. & Tasaka, M. Lateral root formation is blocked by a gain-of-function mutation in the solitary-root/IAA14 gene of Arabidopsis. Plant J. 29, 153–168 (2002).

    CAS  PubMed  Google Scholar 

  103. Szemenyei, H., Hannon, M. & Long, J. A. TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319, 1384–1386 (2008).

    CAS  PubMed  Google Scholar 

  104. Hamann, T., Mayer, U. & Jürgens, G. The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development 126, 1387–1395 (1999).

    CAS  PubMed  Google Scholar 

  105. Timpte, C., Wilson, A. K. & Estelle, M. The axr2-1 mutation of Arabidopsis thaliana is a gain-of-function mutation that disrupts an early step in auxin response. Genetics 138, 1239–1249 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  106. Tian, Q. & Reed, J. W. Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development 126, 711–721 (1999).

    CAS  PubMed  Google Scholar 

  107. Vernoux, T. et al. The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Mol. Syst. Biol. 7, 508 (2011).

    PubMed  PubMed Central  Google Scholar 

  108. Lv, B. et al. Non-canonical AUX/IAA protein IAA 33 competes with canonical AUX/IAA repressor IAA 5 to negatively regulate auxin signaling. EMBO J. 39, e101515 (2019).

    PubMed  PubMed Central  Google Scholar 

  109. Carranco, R., Espinosa, J. M., Prieto-Dapena, P., Almoguera, C. & Jordano, J. Repression by an auxin/indole acetic acid protein connects auxin signaling with heat shock factormediated seed longevity. Proc. Natl Acad. Sci. USA 107, 21908–21913 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Procko, C. et al. The epidermis coordinates auxin-induced stem growth in response to shade. Genes Dev. 30, 1529–1541 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Vermeer, J. E. M. et al. A spatial accommodation by neighboring cells is required for organ initiation in Arabidopsis. Science 343, 178–182 (2014).

    CAS  PubMed  Google Scholar 

  112. Smetana, O. et al. High levels of auxin signalling define the stem-cell organizer of the vascular cambium. Nature 565, 485–489 (2019).

    CAS  PubMed  Google Scholar 

  113. Piya, S., Shrestha, S. K., Binder, B., Stewart, C. N. & Hewezi, T. Protein-protein interaction and gene co-expression maps of ARFs and Aux/IAAs in Arabidopsis. Front. Plant Sci. 5, 744 (2014).

    PubMed  PubMed Central  Google Scholar 

  114. Muto, H., Watahiki, M. K., Nakamoto, D., Kinjo, M. & Yamamoto, K. T. Specificity and similarity of functions of the Aux/IAA genes in auxin signaling of Arabidopsis revealed by promoter-exchange experiments among MSG2/IAA19, AXR2/IAA7, and SLR/IAA14. Plant Physiol. 144, 187–196 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  115. Rademacher, E. H. et al. Different auxin response machineries control distinct cell fates in the early plant embryo. Dev. Cell 22, 211–222 (2012).

    CAS  PubMed  Google Scholar 

  116. Weijers, D. et al. Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO J. 24, 1874–1885 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  117. Ni, J. et al. Intragenic suppressor of Osiaa23 revealed a conserved tryptophan residue crucial for protein–protein interactions. PLoS ONE 9, e85358 (2014).

    PubMed  PubMed Central  Google Scholar 

  118. De Smet, I. et al. Bimodular auxin response controls organogenesis in Arabidopsis. Proc. Natl Acad. Sci. USA 107, 2705–2710 (2010).

    PubMed  PubMed Central  Google Scholar 

  119. Ploense, S. E., Wu, M.-F., Nagpal, P. & Reed, J. W. A gain-of-function mutation in IAA18 alters Arabidopsis embryonic apical patterning. Development 136, 1509–1517 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  120. Zouine, M. et al. Characterization of the tomato ARF gene family uncovers a multi-levels post-transcriptional regulation including alternative splicing. PLoS ONE 9, e84203 (2014).

    PubMed  PubMed Central  Google Scholar 

  121. Guilfoyle, T. J. & Hagen, G. Auxin response factors. Curr. Opin. Plant Biol. 10, 453–460 (2007).

    CAS  PubMed  Google Scholar 

  122. Tiwari, S. B., Hagen, G. & Guilfoyle, T. The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15, 533–543 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  123. Galli, M. et al. The DNA binding landscape of the maize AUXIN RESPONSE FACTOR family. Nat. Commun. 9, 4526 (2018).

    PubMed  PubMed Central  Google Scholar 

  124. Martin-Arevalillo, R. et al. Evolution of the auxin response factors from charophyte ancestors. PLoS Genet. 15, e1008400 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  125. Lanctot, A., Taylor-Teeples, M., Oki, E. A. & Nemhauser, J. Specificity in auxin responses is not explained by the promoter preferences of activator ARFs. Plant Physiol. 182, 1533–1536 (2020).

    PubMed  PubMed Central  Google Scholar 

  126. Calderón Villalobos, L. I. A. et al. A combinatorial TIR1/AFB-Aux/IAA co-receptor system for differential sensing of auxin. Nat. Chem. Biol. 8, 477–485 (2012).

    PubMed  Google Scholar 

  127. Parry, G. et al. Complex regulation of the TIR1/AFB family of auxin receptors. Proc. Natl Acad. Sci. USA 106, 22540–22545 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  128. Pierre-Jerome, E., Moss, B. L., Lanctot, A., Hageman, A. & Nemhauser, J. L. Functional analysis of molecular interactions in synthetic auxin response circuits. Proc. Natl Acad. Sci. USA 113, 11354–11359 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  129. Pierre-Jerome, E., Jang, S. S., Havens, K. A., Nemhauser, J. L. & Klavins, E. Recapitulation of the forward nuclear auxin response pathway in yeast. Proc. Natl Acad. Sci. USA 111, 9407–9412 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  130. Havens, K. et al. A synthetic approach reveals extensive tunability of auxin signaling. Plant Physiol. 160, 135–142 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  131. Taylor-Teeples, M., Lanctot, A. & Nemhauser, J. L. As above, so below: auxin’s role in lateral organ development. Dev. Biol. 419, 156–164 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Zhang, Y., Malzahn, A. A., Sretenovic, S. & Qi, Y. The emerging and uncultivated potential of CRISPR technology in plant science. Nat. Plants 5, 778–794 (2019).

    PubMed  Google Scholar 

  133. Brooks, C., Nekrasov, V., Lippman, Z. & Van Eck, J. Efficient gene editing in tomato in the first generation using the CRISPR/Cas9 system. Plant Physiol. 166, 1292–1297 (2014).

    PubMed  PubMed Central  Google Scholar 

  134. Xie, K., Minkenberg, B. & Yang, Y. Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc. Natl Acad. Sci. USA 112, 3570–3575 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  135. Chung, Y. et al. Auxin response factors promote organogenesis by chromatin-mediated repression of the pluripotency gene SHOOTMERISTEMLESS. Nat. Commun. 10, 886 (2019).

    PubMed  PubMed Central  Google Scholar 

  136. Collum, T. D., Padmanabhan, M. S., Hsieh, Y. C. & Culver, J. N. Tobacco mosaic virus-directed reprogramming of auxin/indole acetic acid protein transcriptional responses enhances virus phloem loading. Proc. Natl Acad. Sci. USA 113, E2740–E2749 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  137. Tiwari, S. B., Wang, X.-J., Hagen, G. & Guilfoyle, T. J. AUX/IAA proteins are active repressors, and their stability and activity are modulated by auxin. Plant Cell 13, 2809–2822 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  138. Hagen, G. & Guilfoyle, T. Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol. Biol. 49, 373–385 (2002).

    CAS  PubMed  Google Scholar 

  139. Abel, S., Nguyen, M. D. & Theologis, A. The PS-IAA4/5-like family of early auxin-inducible mRNAs in Arabidopsis thaliana. J. Mol. Biol. 251, 533–549 (1995).

    CAS  PubMed  Google Scholar 

  140. Krogan, N. T., Yin, X., Ckurshumova, W. & Berleth, T. Distinct subclades of Aux/IAA genes are direct targets of ARF5/MP transcriptional regulation. New Phytol. 204, 474–483 (2014).

    CAS  PubMed  Google Scholar 

  141. Goetz, M. et al. Expression of aberrant forms of AUXIN RESPONSE FACTOR8 stimulates parthenocarpy in Arabidopsis and tomato. Plant Physiol. 145, 351–366 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  142. Du, L. et al. SmARF8, a transcription factor involved in parthenocarpy in eggplant. Mol. Genet. Genomics 291, 93–105 (2016).

    CAS  PubMed  Google Scholar 

  143. Goetz, M., Vivian-smith, A., Johnson, S. D. & Koltunow, A. M. AUXIN RESPONSE FACTOR8 is a negative regulator of fruit initiation in Arabidopsis. Plant Cell 18, 1873–1886 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  144. Radoeva, T. et al. A robust auxin response network controls embryo and suspensor development through a basic helix loop helix transcriptional module. Plant Cell 31, 52–67 (2019).

    CAS  PubMed  Google Scholar 

  145. Vanneste, S. et al. Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell 17, 3035–3050 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  146. Wang, Y. & Deng, D. Molecular basis and evolutionary pattern of GA-GID1-DELLA regulatory module. Mol. Genet. Genomics 289, 1–9 (2014).

    CAS  PubMed  Google Scholar 

  147. Bowman, J. L., Briginshaw, L. N., Fisher, T. J. & Flores-Sandoval, E. Something ancient and something neofunctionalized—evolution of land plant hormone signaling pathways. Curr. Opin. Plant Biol. 47, 64–72 (2019).

    CAS  PubMed  Google Scholar 

  148. Monte, I. et al. A single JAZ repressor controls the jasmonate pathway in Marchantia polymorpha. Mol. Plant 12, 185–198 (2019).

    CAS  PubMed  Google Scholar 

  149. Illouz-Eliaz, N. et al. Multiple gibberellin receptors contribute to phenotypic stability under changing environments. Plant Cell 31, 1506–1519 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  150. Ulmasov, T., Hagen, G. & Guilfoyle, T. J. Dimerization and DNA binding of auxin response factors. Plant J. 19, 309–319 (1999).

    CAS  PubMed  Google Scholar 

  151. Lieberman-lazarovich, M., Yahav, C., Israeli, A. & Efroni, I. Deep conservation of cis-element variants regulating plant. Plant Cell 31, 2559–2572 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  152. Guilfoyle, T. J. The PB1 domain in auxin response factor and Aux/IAA proteins: a versatile protein interaction module in the auxin response. Plant Cell 27, 33–43 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  153. Salehin, M., Bagchi, R. & Estelle, M. SCFTIR1/AFB-based auxin perception: mechanism and role in plant growth and development. Plant Cell 27, 9–19 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  154. Dharmasiri, N., Dharmasiri, S. & Estelle, M. The F-box protein TIR1 is an auxin receptor. Nature 435, 441–445 (2005).

    CAS  PubMed  Google Scholar 

  155. Kepinski, S. & Leyser, O. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446–451 (2005).

    CAS  PubMed  Google Scholar 

  156. Harborough, S. R. et al. Direct ETTIN-auxin interaction controls chromatin states in gynoecium development. eLife 9, e51787 (2020).

    Google Scholar 

  157. Simonini, S. et al. A noncanonical auxin-sensing mechanism is required for organ morphogenesis in Arabidopsis. Genes Dev. 30, 2286–2296 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  158. Cao, M. et al. TMK1-mediated auxin signalling regulates differential growth of the apical hook. Nature 568, 240–243 (2019).

    CAS  PubMed  Google Scholar 

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Acknowledgements

Research on auxin response in the Ori and Reed laboratories is supported by grants from the Israel Science Foundation (grant nos. 2407-18 and 248-19) to N.O., and from the U.S.–Israel Binational Agricultural Research and Development Fund (grant no. IS-5103-18 R) to N.O. and J.W.R. A.I. thanks the Azrieli Foundation for the award of an Azrieli fellowship.

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A.I., J.W.R. and N.O. wrote and edited the Perspective.

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Israeli, A., Reed, J.W. & Ori, N. Genetic dissection of the auxin response network. Nat. Plants 6, 1082–1090 (2020). https://doi.org/10.1038/s41477-020-0739-7

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