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Temporal and Spatial Distribution of Auxin Response Factor Genes During Tomato Flower Abscission

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Abstract

Abscission facilitates growth and reproduction and improves plant defenses against pathogens. This tightly regulated process is triggered by environmental cues and hormones such as ethylene and auxin. Because auxin is crucial for abscission, auxin response factors (ARFs) may play important roles in this process. Here, we examined changes in gene expression during abscission in tomato, focusing on regulation of genes encoding ARFs. Specifically, we analyzed the pattern of ARF gene expression in tomato flower pedicel explants treated with ethylene, the ethylene blocker 1-methylcyclopropene (1-MCP), or auxin to determine how auxin and ethylene affect ARF gene expression. In addition, we examined the spatial and temporal distribution of IAA during abscission by examining transgenic tomato plants expressing an IAA-inducible promoter fused to the GUS reporter gene (the P5::GUS ‘Chico III’ line). Flower removal from the explants quickly induced abscission by ethylene, which was inhibited by exogenous auxin or 1-MCP. During early abscission, auxin (or 1-MCP) regulated the expression of various ARFs, including ARF1, 2, 3, 4, 5, 7, 8-1, 9, 11, 12, 13, 13-1, 14, and 17, whereas ethylene had the opposite effect on most of these genes. Further analysis shows that during this stage, auxin may mediate the expression of ARF8-1, 9, 11, 12, 13, 13-1, and 14, whereas ethylene may mediate ARF13-1. During the later stage of abscission, ARF2, 8, 10, 11, and 19 were upregulated, and 8-1, 12, 13, and 13-1 were downregulated, compared with nonabscising parts of plants. Fluorometric GUS analysis indicated that GUS activity in the abscission zone remained stable at 4 h and sharply decreased after 8 h until abscission was complete (32 h).

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References

  • Agusti J, Merelo P, Cercós M, Tadeo FR, Talón M (2008) Ethylene-induced differential gene expression during abscission of citrus leaves. J Exp Bot 59:2717–2733

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Agusti J, Merelo P, Cercós M, Tadeo FR, Talón M (2009) Comparative transcriptional survey between laser-microdissected cells from laminar abscission zone and petiolar tissue during ethylene-promoted abscission in citrus leaves. BMC Plant Biol 9:127

    Article  PubMed Central  PubMed  Google Scholar 

  • Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JD, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500

    Article  CAS  PubMed  Google Scholar 

  • Cho SK, Larue CT, Chevalier D, Wang H, Jinn TL, Zhang S, Walker JC (2008) Regulation of floral organ abscission in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:15629–15634

    Article  PubMed Central  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 1:160–170

    Article  Google Scholar 

  • Ellis CM, Nagpal P, Young JC, Hagen G, Guilfoyle TJ, Reed JW (2005) Auxin response factor1 and auxin response factor2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132:4563–4574

    Article  CAS  PubMed  Google Scholar 

  • Fukaki H, Nakao Y, Okushima Y, Theologis A, Tasaka M (2005) Tissue-specific expression of stabilized SOLITARY-ROOT/IAA14 alters lateral root development in Arabidopsis. Plant J 44:382–395

    Article  CAS  PubMed  Google Scholar 

  • Gray W, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414:271–276

    Article  CAS  PubMed  Google Scholar 

  • Hardtke CS, Ckurshumova W, Vidaurre DP, Singh SA, Stamatiou G, Tiwari SB, Hagen G, Guilfoyle TJ, Berleth T (2004) Overlapping and non-redundant functions of the Arabidopsis auxin response factors monopteros and nonphototropic hypocotyl 4. Development 131:1089–1100

    Article  CAS  PubMed  Google Scholar 

  • Jain M, Nijhawan A, Tyagi AK, Khurana JP (2006) Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun 345:646–651

    Article  CAS  PubMed  Google Scholar 

  • Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Report 5:387–405

    Article  CAS  Google Scholar 

  • Jefferson RA, Burgess SM, Hirsch D (1986) β-Glucuronidase from Escherichia coli as a gene-fusion marker. Proc Natl Acad Sci USA 83:8447–8451

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jinn TL, Stone JM, Walker JC (2000) HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission. Genes Dev 14:108–117

    PubMed Central  CAS  PubMed  Google Scholar 

  • Karlova R, Boeren S, Russinova E, Aker J, Vervoort J, de Vries SC (2006) The Arabidopsis somatic embryogenesis receptor-like kinase1 protein complex includes brassinosteroid-insensitive 1. Plant Cell 18:626–638

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kavita P, Burma PK (2008) A comparative analysis of green fluorescent protein and β-glucuronidase protein-encoding genes as a reporter system for studying the temporal expression profiles of promoters. J Biosci 33:337–343

    Article  CAS  PubMed  Google Scholar 

  • Kinoshita T, Caño-Delgado A, Seto H, Hiranuma S, Fujioka S, Yoshida S, Chory J (2005) Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433:167–171

    Article  CAS  PubMed  Google Scholar 

  • Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110:213–222

    Article  CAS  PubMed  Google Scholar 

  • Mallory AC, Bartel DP, Bartel B (2005) MicroRNA-directed regulation of Arabidopsis auxin response factor 17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17:1360–1375

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mazzucato A, Olimpieri I, Rossi M, Caccia R, Soressi GP (2006) A new reporter construct to monitor IAA dynamics during tomato development. TGC Rep 56:26–28. Available at http://tgc.ifas.ufl.edu/vol56/vol56.pdf

    Google Scholar 

  • Meir S, Philosoph-Hadas S, Sundaresan S, Vijay Selvaraj KS, Burd S, Ophir R, Kochanek B, Reid MS, Jiang CZ, Lers A (2010) Microarray analysis of the abscission-related transcriptome in the tomato flower abscission zone in response to auxin depletion. Plant Physiol 4:1929–1956

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D (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 

  • Pasternak TP, Prinsen E, Ayaydin F, Miskolczi P, Potters G, Asard H, Onckelen HAV, Dudits D, Fehér A (2002) The role of auxin, pH, and stress in the activation of embryogenic cell division in leaf protoplast-derived cells of alfalfa. Plant Physiol 129:1807–1819

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Roberts JA, González-Carranza ZH (2007) Abscission. In: Roberts K (ed) Handbook of plant science, vol 1. Wiley, Chicester, pp 512–519

    Google Scholar 

  • Stenvik GE, Tandstad NM, Guo Y, Shi CL, Kristiansen W, Holmgren A, Clark SE, Aalen RB, Butenko MA (2008) The EPIP peptide of inflorescence deficient in abscission is sufficient to induce abscission in Arabidopsis through the receptor-like kinases HAESA and HAESA-LIKE2. Plant Cell 20:1805–1817

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Tatematsu K, Kumagai S, Muto H, Sato A, Watahiki MK, Harper RM, Liscum E, Yamamoto KT (2004) MASSUGU2 encodes Aux/IAA19, an auxin-regulated protein that functions together with the transcriptional activator NPH4/ARF7 to regulate differential growth responses of hypocotyl and formation of lateral roots in Arabidopsis thaliana. Plant Cell 16:379–393

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tian Q, Uhlir NJ, Reed JW (2002) Arabidopsis SHY2/IAA3 inhibits auxin-regulated gene expression. Plant Cell 14:301–319

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Tian CE, Muto H, Higuchi K, Matamura T, Tatematsu K, Koshiba T, Yamamoto KT (2004) Disruption and overexpression of auxin response factor 8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition. Plant J 3:333–343

    Article  Google Scholar 

  • Tucker ML, Yang RH (2012) IDA-like gene expression in soybean and tomato leaf abscission and requirement for a diffusible stelar abscission signal. AoB Plants 2012: pls035. doi:10.1093/aobpla/pls035

  • Uehara T, Okushima Y, Mimura T, Tasaka M, Fukaki H (2008) Domain II mutations in CRANE/IAA18 suppress lateral root formation and affect shoot development in Arabidopsis thaliana. Plant Cell Physiol 49:1025–1038

    Article  CAS  PubMed  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1999a) Activation and repression of transcription by auxin response factors. Proc Natl Acad Sci USA 96:5844–5849

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang SC, Tiwari SB, Hagen G, Guilfoyle TJ (2005a) Auxin response factor7 restores the expression of auxin-responsive genes in mutant Arabidopsis leaf mesophyll protoplasts. Plant Cell 17:1979–1993

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang YC, Li TL, Meng HX, Sun XY (2005b) Optimal and spatial analysis of hormones, degrading enzymes and isozyme profiles in tomato pedicel explants during ethylene-induced abscission. Plant Growth Regul 46:97–107

    Article  CAS  Google Scholar 

  • Weijers D, Benkova E, Jäger KE, Schlereth A, Hamann T, Kientz M, Wilmoth JC, Reed JW, Jürgens G (2005) Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO J 24:1874–1885

    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

    Article  CAS  PubMed  Google Scholar 

  • Zuo XH, Xu T, Qi MF, Lv SS, Li H, Gao S, Li TL (2011) Expression patterns of auxin-responsive genes during tomato flower pedicel abscission and potential effects of calcium. Aust J Bot 60:68–78

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by Grants from the National Natural Science Foundation of China (Nos. 31272153, 31171966, 31071789, and 30900982) and China Agricultural Research System (CARS-25). We also acknowledge Dr. A. Mazzucato for providing transgenic tomato seeds. We thank the native English-speaking scientists of Elixigen Company for editing our manuscript.

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Authors and Affiliations

  1. College of Horticulture, Shenyang Agricultural University, Shenyang, 110161, Liaoning, People’s Republic of China

    Xiaoxi Guan, Tao Xu, Mingfang Qi, Yanling Wang, Xin Liu & Tianlai Li

  2. Liaoning Cash Crop Institute, Liaoyang, 111304, People’s Republic of China

    Song Gao

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  1. Xiaoxi Guan
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  2. Tao Xu
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Correspondence to Tianlai Li.

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Xiaoxi Guan and Tao Xu equally contributed to this work and should be considered co-first authors.

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344_2013_9377_MOESM1_ESM.tif

Supplementary Fig. 1 Relative expression of Cystein-type endopeptidase in AZ of tomato pedicels treated with water for 1 h or with MES for 3 h (TIFF 90 kb)

344_2013_9377_MOESM2_ESM.tif

Supplementary Fig. 2 Localization of GUS activity in flower pedicel explants treated with water for 1 h (a) or MES for 3 h (b) (TIFF 370 kb)

344_2013_9377_MOESM3_ESM.tif

Supplementary Fig. 3 IAA concentration (a) and GUS activity (b) analysis in AZ of tomato pedicels treated with water for 1 h or MES for 3 h (TIFF 110 kb)

344_2013_9377_MOESM4_ESM.tif

Supplementary Fig. 4 After water incubation for 1 h, the different treatments resulted in the differential expression of genes, which comprised two major clusters: cluster A (5 genes) and cluster B (16 genes) (TIFF 114 kb)

344_2013_9377_MOESM5_ESM.tif

Supplementary Fig. 5 After MES incubation for 3 h, the different treatments resulted in differential expression of genes, which comprised two major clusters: cluster A (8 genes) and cluster B (13 genes) (TIFF 121 kb)

Supplementary material 6 (DOCX 13 kb)

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Guan, X., Xu, T., Gao, S. et al. Temporal and Spatial Distribution of Auxin Response Factor Genes During Tomato Flower Abscission. J Plant Growth Regul 33, 317–327 (2014). https://doi.org/10.1007/s00344-013-9377-x

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  • DOI: https://doi.org/10.1007/s00344-013-9377-x

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