Skip to main content
SpringerLink
Log in

Genomic Survey, Gene Expression, and Interaction Analysis Suggest Diverse Roles of ARF and Aux/IAA Proteins in Solanaceae

  • Original Paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

Auxin response factor (ARF) and Auxin/INDOLE-3-ACETIC ACID (Aux/IAA) proteins are the foremost regulators of auxin action and play an essential role in the coordination of many aspects of plant growth and development. Though many members of both ARF and Aux/IAA gene families have been identified and characterized in tomato, they are less studied in other Solanaceae species. In the present study, we focused on gaining insights into their functional conservation as well as diversification during auxin-mediated responses in Solanaceae. First, we identified their full complement in tomato, potato, pepper, Nicotiana benthamiana, eggplant, and petunia and found that both the gene families have expanded in N. benthamiana. We also looked into the structural variations associated with all the members of these two classes of genes in tomato and showed that huge natural variation exists in their sequence in wild relatives. The comprehensive gene expression analysis provided evidence of high conservation in the expression of orthologous ARFs and Aux/IAAs during fruit development and ripening in tomato and pepper. Furthermore, the molecular changes caused by exogenous plant hormones and abiotic stress conditions on their transcript levels were investigated which showed that many members of both the gene families may participate in various hormone- and stress-mediated responses in tomato and potato. Some of these genes may play a role in linking the hormone-controlled plant growth and stress-related signaling pathways. Finally, we demonstrate that single tomato ARF can interact with multiple Aux/IAA proteins and vice versa. Overall, our study will be very helpful in establishing both conserved as well as non-conserved functions of these genes in Solanaceae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abel S, Theologis A (1996) Early genes and auxin action. Plant Physiol 111:9–17

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Abel S, Oeller PW, Theologis A (1994) Early auxin-induced genes encode short-lived nuclear proteins. Proc Natl Acad Sci U S A 91:326–330

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Abel S, Nguyen MD, Chow W, Theologis A (1995) ACS4, a primary indoleacetic acid-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis thaliana. Structural characterization, expression in Escherichia coli, and expression characteristics in response to auxin. J Biol Chem 270:19093–19099

    Article  CAS  PubMed  Google Scholar 

  • Audran-Delalande C, Bassa C, Mila I, Regad F, Zouine M, Bouzayen M (2012) Genome-wide identification, functional analysis and expression profiling of the Aux/IAA gene family in tomato. Plant Cell Physiol 53:659–672

    Article  CAS  PubMed  Google Scholar 

  • Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488. doi:10.1007/s11103-008-9435-0

    Article  CAS  PubMed  Google Scholar 

  • Bassa C, Mila I, Bouzayen M, Audran-Delalande C (2012) Phenotypes associated with down-regulation of Sl-IAA27 support functional diversity among Aux/IAA family members in tomato. Plant Cell Physiol 53:1583–1595. doi:10.1093/pcp/pcs101

    Article  CAS  PubMed  Google Scholar 

  • Bhalerao RP, Eklof J, Ljung K, Marchant A, Bennett M, Sandberg G (2002) Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. Plant J 29:325–332

    Article  CAS  PubMed  Google Scholar 

  • Bombarely A, Rosli HG, Vrebalov J, Moffett P, Mueller LA, Martin GB (2012) A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol Plant Microbe Interact 25:1523–1530. doi:10.1094/MPMI-06-12-0148-TA

    Article  CAS  PubMed  Google Scholar 

  • Chaabouni S, Jones B, Delalande C, Wang H, Li Z, Mila I, Frasse P, Latche A, Pech JC, Bouzayen M (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. doi:10.1093/jxb/erp009

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chapman EJ, Estelle M (2009) Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet 43:265–285. doi:10.1146/annurev-genet-102108-134148

    Article  CAS  PubMed  Google Scholar 

  • Chaw SM, Chang CC, Chen HL, Li WH (2004) Dating the monocot-dicot divergence and the origin of core eudicots using whole chloroplast genomes. J Mol Evol 58:424–441. doi:10.1007/s00239-003-2564-9

    Article  CAS  PubMed  Google Scholar 

  • Chitwood DH, Maloof JN, Sinha NR (2013) Dynamic transcriptomic profiles between tomato and a wild relative reflect distinct developmental architectures. Plant Physiol 162:537–552. doi:10.1104/pp. 112.213546

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Clarkson JJ, Lim KY, Kovarik A, Chase MW, Knapp S, Leitch AR (2005) Long-term genome diploidization in allopolyploid Nicotiana section Repandae (Solanaceae). New Phytol 168:241–252. doi:10.1111/j.1469-8137.2005.01480.x

    Article  CAS  PubMed  Google Scholar 

  • de Jong M, Wolters-Arts M, Feron R, Mariani C, Vriezen WH (2009) The Solanum lycopersicum auxin response factor 7 (SlARF7) regulates auxin signaling during tomato fruit set and development. Plant J 57:160–170. doi:10.1111/j.1365-313X.2008.03671.x

    Article  PubMed  Google Scholar 

  • Deng W, Yang Y, Ren Z, Audran-Delalande C, Mila I, Wang X, Song H, Hu Y, Bouzayen M, Li Z (2012) The tomato SlIAA15 is involved in trichome formation and axillary shoot development. New Phytol 194:379–390. doi:10.1111/j.1469-8137.2012.04053.x

    Article  CAS  PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005a) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445. doi:10.1038/nature03543

    Article  CAS  PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jurgens G, Estelle M (2005b) Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9:109–119. doi:10.1016/j.devcel.2005.05.014

    Article  CAS  PubMed  Google Scholar 

  • Ghanashyam C, Jain M (2009) Role of auxin-responsive genes in biotic stress responses. Plant Signal Behav 4:846–848

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 414:271–276. doi:10.1038/3510450035104500

    Article  CAS  PubMed  Google Scholar 

  • Guillon F, Philippe S, Bouchet B, Devaux M-F, Frasse P, Jones B, Bouzayen M, Lahaye M (2008) Down-regulation of an Auxin Response Factor in the tomato induces modification of fine pectin structure and tissue architecture. J Exp Bot 59:273–288

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Halliday KJ, Martinez-Garcia JF, Josse EM (2009) Integration of light and auxin signaling. Cold Spring Harbor Perspect Biol 1:a001586. doi:10.1101/cshperspect.a001586

    Article  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jain M, Kaur N, Garg R, Thakur JK, Tyagi AK, Khurana JP (2006) Structure and expression analysis of early auxin-responsive Aux/IAA gene family in rice (Oryza sativa). Funct Integr Genomics 6:47–59. doi:10.1007/s10142-005-0005-0

    Article  CAS  PubMed  Google Scholar 

  • Jones B, Frasse P, Olmos E, Zegzouti H, Li ZG, Latche A, Pech JC, Bouzayen M (2002) Down-regulation of DR12, an auxin-response-factor homolog, in the tomato results in a pleiotropic phenotype including dark green and blotchy ripening fruit. Plant J 32:603–613

    Article  CAS  PubMed  Google Scholar 

  • Kalluri UC, Difazio SP, Brunner AM, Tuskan GA (2007) Genome-wide analysis of Aux/IAA and ARF gene families in Populus trichocarpa. BMC Plant Biol 7:59

    Article  PubMed Central  PubMed  Google Scholar 

  • Kenworthy AK (2001) Imaging protein-protein interactions using fluorescence resonance energy transfer microscopy. Methods 24:289–296. doi:10.1006/meth.2001.1189

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kim S, Park M, Yeom SI et al (2014) Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat Genet 46:270–278. doi:10.1038/ng.2877

    Article  CAS  PubMed  Google Scholar 

  • Kloosterman B, Visser RG, Bachem CW (2006) Isolation and characterization of a novel potato Auxin/Indole-3-Acetic Acid family member (StIAA2) that is involved in petiole hyponasty and shoot morphogenesis. Plant Physiol Biochem 44:766–775. doi:10.1016/j.plaphy.2006.10.026

    Article  CAS  PubMed  Google Scholar 

  • Koenig D, Jimenez-Gomez JM, Kimura S, Fulop D, Chitwood DH, Headland LR, Kumar R, Covington MF, Devisetty UK, Tat AV, Tohge T, Bolger A, Schneeberger K, Ossowski S, Lanz C, Xiong G, Taylor-Teeples M, Brady SM, Pauly M, Weigel D, Usadel B, Fernie AR, Peng J, Sinha NR, Maloof JN (2013) Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato. Proc Natl Acad Sci U S A 110:2655–2662. doi:10.1073/pnas.1309606110

    Article  Google Scholar 

  • Kumar R, Tyagi AK, Sharma AK (2011) Genome-wide analysis of auxin response factor (ARF) gene family from tomato and analysis of their role in flower and fruit development. Mol Genet Genomics 285:245–260. doi:10.1007/s00438-011-0602-7

    Article  CAS  PubMed  Google Scholar 

  • Kumar R, Agarwal P, Tyagi AK, Sharma AK (2012a) Genome-wide investigation and expression analysis suggest diverse roles of auxin-responsive GH3 genes during development and response to different stimuli in tomato (Solanum lycopersicum). Mol Genet Genomics 287:221–235

    Article  CAS  PubMed  Google Scholar 

  • Kumar R, Sharma MK, Kapoor S, Tyagi AK, Sharma AK (2012b) Transcriptome analysis of rin mutant fruit and in silico analysis of promoters of differentially regulated genes provides insight into LeMADS-RIN-regulated ethylene-dependent as well as ethylene-independent aspects of ripening in tomato. Mol Genet Genomics 287:189–203. doi:10.1007/s00438-011-0671-7

    Article  CAS  PubMed  Google Scholar 

  • Kumar R, Khurana A, Sharma AK (2014) Role of plant hormones and their interplay in development and ripening of fleshy fruits. J Exp Bot 65(16):4561–4575

    Article  PubMed  Google Scholar 

  • Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (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 30:325–327

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liscum E, Reed JW (2002) Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol 49:387–400

    Article  CAS  PubMed  Google Scholar 

  • Liu N, Wu S, Van Houten J, Wang Y, Ding B, Fei Z, Clarke TH, Reed JW, van der Knaap E (2014) 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(9):2507–2520

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lleres D, Swift S, Lamond AI (2007) Detecting protein-protein interactions in vivo with FRET using multiphoton fluorescence lifetime imaging microscopy (FLIM). Current protocols in cytometry / editorial board, J Paul Robinson, managing editor Chapter 12:Unit12 10. doi:10.1002/0471142956.cy1210s42

  • Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE, Ecker JR, Reed JW (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132:4107–4118

    Article  CAS  PubMed  Google Scholar 

  • Nickrent DL, Parkinson CL, Palmer JD, Duff RJ (2000) Multigene phylogeny of land plants with special reference to bryophytes and the earliest land plants. Mol Biol Evol 17:1885–1895

    Article  CAS  PubMed  Google Scholar 

  • Nuez F, Prohens J, Blanca JM (2004) Relationships, origin, and diversity of Galapagos tomatoes: implications for the conservation of natural populations. Am J Bot 91:86–99. doi:10.3732/ajb.91.1.86

    Article  PubMed  Google Scholar 

  • Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17:444–463

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Paponov IA, Teale W, Lang D, Paponov M, Reski R, Rensing SA, Palme K (2009) The evolution of nuclear auxin signalling. BMC Evol Biol 9:126. doi:10.1186/1471-2148-9-126

    Article  PubMed Central  PubMed  Google Scholar 

  • Peralta IE, Knapp S, Spooner DM (2005) New species of wild tomatoes (Solanum Section Lycopersicon: Solanaceae) from Northern Peru. Syst Bot 30:424–434

    Article  Google Scholar 

  • Piya S, Shrestha SK, Binder B, Stewart CN Jr, Hewezi T (2014) Protein-protein interaction and gene co-expression maps of ARFs and Aux/IAAs in Arabidopsis. Front Plant Sci 5:744

    Article  PubMed Central  PubMed  Google Scholar 

  • Rahman A (2013) Auxin: a regulator of cold stress response. Physiol Plant 147:28–35. doi:10.1111/j.1399-3054.2012.01617.x

    Article  CAS  PubMed  Google Scholar 

  • Sagar M, Chervin C, Mila I, Hao Y, Roustan JP, Benichou M, Gibon Y, Biais B, Maury P, Latche A, Pech JC, Bouzayen M, Zouine M (2013) SlARF4, an auxin response factor involved in the control of sugar metabolism during tomato fruit development. Plant Physiol 161:1362–1374. doi:10.1104/pp. 113.213843

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Salinas M, Xing S, Hohmann S, Berndtgen R, Huijser P (2012) Genomic organization, phylogenetic comparison and differential expression of the SBP-box family of transcription factors in tomato. Planta 235:1171–1184. doi:10.1007/s00425-011-1565-y

    Article  CAS  PubMed  Google Scholar 

  • Sharma MK, Kumar R, Solanke AU, Sharma R, Tyagi AK, Sharma AK (2010) Identification, phylogeny, and transcript profiling of ERF family genes during development and abiotic stress treatments in tomato. Mol Genet Genomics 284:455–475. doi:10.1007/s00438-010-0580-1

    Article  CAS  PubMed  Google Scholar 

  • Shen C, Bai Y, Wang S, Zhang S, Wu Y, Chen M, Jiang D, Qi Y (2010) Expression profile of PIN, AUX/LAX and PGP auxin transporter gene families in Sorghum bicolor under phytohormone and abiotic stress. FEBS J 277:2954–2969. doi:10.1111/j.1742-4658.2010.07706.x

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1007/s00425-008-0853-7

    Article  CAS  PubMed  Google Scholar 

  • Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319:1384–1386. doi:10.1126/science.1151461

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • TGC (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641. doi:10.1038/nature11119

    Article  Google Scholar 

  • Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Current protocols in bioinformatics/editoral board, Andreas D Baxevanis Chapter 2:Unit 2 3. doi:10.1002/0471250953.bi0203s00

  • Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1997) ARF1, a transcription factor that binds to auxin response elements. Science 276:1865–1868

    Article  CAS  PubMed  Google Scholar 

  • Vriezen WH, Feron R, Maretto F, Keijman J, Mariani C (2008) Changes in tomato ovary transcriptome demonstrate complex hormonal regulation of fruit set. New Phytol 177:60–76

    CAS  PubMed  Google Scholar 

  • Wang H, Jones B, Li Z, Frasse P, Delalande C, Regad F, Chaabouni S, Latche A, Pech JC, Bouzayen M (2005) The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell 17:2676–2692

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang D, Pajerowska-Mukhtar K, Culler AH, Dong X (2007) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr Biol 17:1784–1790. doi:10.1016/j.cub.2007.09.025

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Diehl A, Wu F, Vrebalov J, Giovannoni J, Siepel A, Tanksley SD (2008) Sequencing and comparative analysis of a conserved syntenic segment in the Solanaceae. Genetics 180:391–408

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang H, Schauer N, Usadel B, Frasse P, Zouine M, Hernould M, Latche A, Pech JC, Fernie AR, Bouzayen M (2009) Regulatory features underlying pollination-dependent and -independent tomato fruit set revealed by transcript and primary metabolite profiling. Plant Cell 21:1428–1452

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wilmoth JC, Wang S, Tiwari SB, Joshi AD, Hagen G, Guilfoyle TJ, Alonso JM, Ecker JR, Reed JW (2005) NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J 43:118–130. doi:10.1111/j.1365-313X.2005.02432.x

    Article  CAS  PubMed  Google Scholar 

  • Wu F, Tanksley SD (2010) Chromosomal evolution in the plant family Solanaceae. BMC Genomics 11:182

    Article  PubMed Central  PubMed  Google Scholar 

  • Wu J, Wang F, Cheng L, Kong F, Peng Z, Liu S, Yu X, Lu G (2011) Identification, isolation and expression analysis of auxin response factor (ARF) genes in Solanum lycopersicum. Plant Cell Rep 30:2059–2073. doi:10.1007/s00299-011-1113-z

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Peng Z, Liu S, He Y, Cheng L, Kong F, Wang J, Lu G (2012) Genome-wide analysis of Aux/IAA gene family in Solanaceae species using tomato as a model. Mol Genet Genomics 287:295–211

    Article  CAS  PubMed  Google Scholar 

  • Xu X, Pan S, Cheng S et al (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195. doi:10.1038/nature10158

    Article  CAS  PubMed  Google Scholar 

  • Yuan H, Zhao K, Lei H, Shen X, Liu Y, Liao X, Li T (2013) Genome-wide analysis of the GH3 family in apple (Malus x domestica). BMC Genomics 14:297. doi:10.1186/1471-2164-14-297

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zouine M, Fu Y, Chateigner-Boutin AL, Mila I, Frasse P, Wang H, Audran C, Roustan JP, Bouzayen M (2014) Characterization of the tomato ARF gene family uncovers a multi-levels post-transcriptional regulation including alternative splicing. PLoS One 9:e84203. doi:10.1371/journal.pone.0084203

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by grants received from the Department of Biotechnology, Government of India. RK, AP, and PA acknowledge DST, CSIR, and UGC, respectively, for the fellowship granted during their tenure as research fellows. RK is grateful to DST for INSPIRE-Faculty Award (grant number IFA-LSPA-15) and to CSIR for Travel Grant (TG/8137/HRD). Authors also acknowledge the Solanaceae Genomics Network for the use of Tomato BAC Sequence Database to retrieve putative promoter sequences. We are grateful to 150 tomato genome consortium for sequence data of wild relatives.

Author information

Authors and Affiliations

  1. Repository of Tomato Genomics Resources, Department of Plant Sciences, University of Hyderabad, Hyderabad, 500046, India

    Rahul Kumar

  2. Department of Plant Molecular Biology, University of Delhi South Campus, New Delhi, 110021, India

    Rahul Kumar, Priyanka Agarwal, Amit Pareek, Akhilesh K. Tyagi & Arun K. Sharma

  3. National Institute of Plant Genome Research, New Delhi, 110067, India

    Akhilesh K. Tyagi

Authors
  1. Rahul Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Priyanka Agarwal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Amit Pareek
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Akhilesh K. Tyagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Arun K. Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Arun K. Sharma.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PPTX 5961 kb)

ESM 2

(DOCX 67 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumar, R., Agarwal, P., Pareek, A. et al. Genomic Survey, Gene Expression, and Interaction Analysis Suggest Diverse Roles of ARF and Aux/IAA Proteins in Solanaceae. Plant Mol Biol Rep 33, 1552–1572 (2015). https://doi.org/10.1007/s11105-015-0856-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-015-0856-z

Keywords

Search

Navigation