Skip to main content
Log in

SlCAND1, encoding cullin-associated Nedd8-dissociated protein 1, regulates plant height, flowering time, seed germination, and root architecture in tomato

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Key message

Silencing of SlCAND1 expression resulted in dwarfish, loss of apical dominance, early flowering, suppression of seed germination, and abnormal root architecture in tomato

Abstract

Cullin-RING E3 ligases (CRLs)-dependent ubiquitin proteasome system mediates degradation of numerous proteins that controls a wide range of developmental and physiological processes in eukaryotes. Cullin-associated Nedd8-dissociated protein 1 (CAND1) acts as an exchange factor allowing substrate recognition part exchange and plays a vital role in reactivating CRLs. The present study reports on the identification of SlCAND1, the only one CAND gene in tomato. SlCAND1 expression is ubiquitous and positively regulated by multiple plant hormones. Silencing of SlCAND1 expression using RNAi strategy resulted in a pleiotropic and gibberellin/auxin-associated phenotypes, including dwarf plant with reduced internode length, loss of apical dominance, early flowering, low seed germination percentage, delayed seed germination speed, short primary root, and increased lateral root proliferation and elongation. Moreover, application of exogenous GA3 or IAA could partly rescue some SlCAND1-silenced phenotypes, and the expression levels of gibberellin/auxin-related genes were altered in SlCAND1-RNAi lines. These facts revealed that SlCAND1 is required for gibberellin/auxin-associated regulatory network in tomato. Although SlCAND1 is crucial for multiple developmental processes during vegetative growth stage, SlCAND1-RNAi lines didn’t exhibit visible effect on fruit development and ripening. Meanwhile, we discussed that multiple physiological functions of SlCAND1 in tomato are different to previous report of its ortholog in Arabidopsis. Our study adds a new perspective on the functional roles of CAND1 in plants, and strongly supports the hypothesis that CAND1 and its regulated ubiquitin proteasome system are pivotal for plant vegetative growth but possibly have different roles in diverse plant species.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aoki T, Okada N, Ishida M, Yogosawa S, Makino Y, Tamura TA (1999) TIP120B: a novel TIP120-family protein that is expressed specifically in muscle tissues. Biochem Biophys Res Commun 261:911–916

    CAS  PubMed  Google Scholar 

  • Appleford NE, Wilkinson MD, Ma Q, Evans DJ, Stone MC, Pearce SP, Powers SJ, Thomas SG, Jones HD, Phillips AL, Hedden P, Lenton JR (2007) Decreased shoot stature and grain α-amylase activity following ectopic expression of a gibberellin 2-oxidase gene in transgenic wheat. J Exp Bot 58:3213–3226

    CAS  PubMed  Google Scholar 

  • Ariizumi T, Steber CM (2007) Seed germination of GA-insensitive sleepy1 mutants does not require RGL2 protein disappearance in Arabidopsis. Plant Cell 19:791–804

    CAS  PubMed  PubMed Central  Google Scholar 

  • Blazquez MA, Green R, Nilsson O, Sussman MR, Weigel D (1998) Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell 10:791–800

    CAS  PubMed  PubMed Central  Google Scholar 

  • Boss PK, Thomas MR (2002) Association of dwarfism and floral induction with a grape 'green revolution' mutation. Nature 416:847–850

    CAS  PubMed  Google Scholar 

  • Bosu DR, Feng H, Min K, Kim Y, Wallenfang MR, Kipreos ET (2010) C. elegans CAND-1 regulates cullin neddylation, cell proliferation and morphogenesis in specific tissues. Dev Biol 346:113–126

    CAS  PubMed  PubMed Central  Google Scholar 

  • Busov V, Meilan R, Pearce DW, Rood SB, Ma C, Tschaplinski TJ, Strauss SH (2006) Transgenic modification of gai or rgl1 causes dwarfing and alters gibberellins, root growth, and metabolite profiles in Populus. Planta 224:288–299

    CAS  PubMed  Google Scholar 

  • Cavidini S, Fischer ES, Bunker RD, Potenza A, Lingaraju GM, Goldie KN, Mohamed WI, Faty M, Petzold G, Beckwith RE, Tichkule RB, Hassiepen U, Abdulrahman W, Pantelic RS, Matsumoto S, Sugasawa K, Stahlberg H, Thomä NH (2016) Cullin-RING ubiquitin E3 ligase regulation by the COP9 signalosome. Nature 531:598–603

    Google Scholar 

  • Cheng Y, Dai X, Zhao Y (2004) AtCAND1, a HEAT-repeat protein that participates in auxin signaling in Arabidopsis. Plant Physiol 135:1020–1026

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chuang HW, Zhang W, Gray WM (2004) Arabidopsis ETA2, an apparent ortholog of the human cullin-interacting protein CAND1, is required for auxin responses mediated by the SCFTIR1 ubiquitin ligase. Plant Cell 16:1883–1897

    CAS  PubMed  PubMed Central  Google Scholar 

  • Deshaies RJ, Joazeiro CA (2009) RING domain E3 ubiquitin ligases. Ann Rev Biochem 78:399–434

    CAS  PubMed  Google Scholar 

  • Dill A, Thomas SG, Hu J, Steber CM, Sun TP (2004) The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell 16:1392–1405

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duda DM, Borg LA, Scott DC, Hunt HW, Hammel M, Schulman BA (2008) Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation. Cell 134:995–1006

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duda MD, Scott DC, Calabrese MF, Zimmerman ES, Zheng N, Schulman BA (2011) Structural regulation of cullin-RING ubiquitin ligase complexes. Curr Opin Struct Biol 21:257–264

    CAS  PubMed  PubMed Central  Google Scholar 

  • Feng S, Shen Y, Sullivan JA, Rubio V, Xiong Y, Sun TP, Deng XW (2004) Arabidopsis CAND1, an unmodified CUL1-interacting protein, is involved in multiple developmental pathways controlled by ubiquitin/proteasome-mediated protein degradation. Plant Cell 16:1870–1882

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fleet CM, Sun TP (2005) A DELLAcate balance: the role of gibberellin in plant morphogenesis. Curr Opin Plant Biol 8:77–85

    CAS  PubMed  Google Scholar 

  • Frigerio M, Alabadí D, Pérez-Gómez J, García-Cárcel L, Phillips AL, Hedden P, Blázquez MA (2006) Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis. Plant Physiol 142:553–563

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gallego-Giraldo L, García-Martínez JL, Moritz T, López-Díaz I (2007) Flowering in tobacco needs gibberellins but is not promoted by the levels of active GA1 and GA4 in the apical shoot. Plant Cell Physiol 48:615–625

    CAS  PubMed  Google Scholar 

  • García-Hurtado N, Carrera E, Ruiz-Rivero O, López-Gresa MP, Hedden P, Gong F, García-Martínez JL (2012) The characterization of transgenic tomato overexpressing gibberellin 20-oxidase reveals induction of parthenocarpic fruit growth, higher yield, and alteration of the gibberellin biosynthetic pathway. J Exp Bot 63:5803–5813

    PubMed  Google Scholar 

  • Gargul JM, Mibus H, Serek M (2013) Constitutive overexpression of Nicotiana GA 2ox leads to compact phenotypes and delayed flowering in Kalancho blossfeldiana and Petunia hybrida. Plant Cell Tissue Organ Cult 115:407–418

    CAS  Google Scholar 

  • Goldberg-Moeller R, Shalom L, Shlizerman L, Samuels S, Zur N, Ophir R, Blumwald E, Sadka A (2013) Effects of gibberellin treatment during flowering induction period on global gene expression and the transcription of flowering-control genes in Citrus buds. Plant Sci 198:46–57

    CAS  PubMed  Google Scholar 

  • Goldenberg SJ, Cascio TC, Shumway SD, Garbutt KC, Liu J, Xiong Y, Zheng N (2004) Structure of the Cand1-Cul1-Roc1 complex reveals regulatory mechanisms for the assembly of the multisubunit cullin-dependent ubiquitin ligases. Cell 119:517–528

    CAS  PubMed  Google Scholar 

  • Gou J, Strauss SH, Tsai CJ, Fang K, Chen Y, Jiang X, Busov VB (2010) Gibberellins regulate lateral root formation in Populus through interactions with auxin and other hormones. Plant Cell 22:623–639

    CAS  PubMed  Google Scholar 

  • Griffiths J, Murase K, Rieu I, Zentella R, Zhang ZL, Powers SJ, Gong F, Phillips AL, Hedden P, Sun TP, Thomas SG (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18:3399–3414

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo X, Zhang Y, Tu Y, Wang Y, Cheng W, Yang Y (2018) Overexpression of an EIN3-binding F-box protein2-like gene caused elongated fruit shape and delayed fruit development and ripening in tomato. Plant Sci 272:131–141

    CAS  PubMed  Google Scholar 

  • Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425–479

    CAS  PubMed  Google Scholar 

  • Hua Z, Vierstra RD (2011) The cullin-RING ubiquitin-protein ligases. Annu Rev Plant Biol 62:299–334

    CAS  PubMed  Google Scholar 

  • Kelley DR, Estelle M (2012) Ubiquitin-mediated control of plant hormone signaling. Plant Physiol 160:47–55

    CAS  PubMed  PubMed Central  Google Scholar 

  • King RW, Ben-Tal Y (2001) A florigenic effect of sucrose in Fuchsia hybrida is blocked by gibberellin-induced assimilate competition. Plant Physiol 125:488–496

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Letunic I, Bork P (2018) 20 years of the SMART protein domain annotation resource. Nucleic Acids Res 46:D493–D496

    CAS  PubMed  Google Scholar 

  • Li G, Zhu C, Gan L, Ng D, Xia K (2015) GA3 enhances root responsiveness to exogenous IAA by modulating auxin transport and signalling in Arabidopsis. Plant Cell Rep 34:483–494

    CAS  PubMed  Google Scholar 

  • Liu J, Furukawa M, Matsumoto T, Xiong Y (2002) NEDD8 modification of CUL1 dissociates p120CAND1, an inhibitor of CUL1-SKP1 binding and SCF ligases. Mol Cell 10:1511–1518

    CAS  PubMed  Google Scholar 

  • Liu X, Reitsma JM, Mamrosh JL, Zhang Y, Straube R, Deshaies RJ (2018) Cand1-mediated adaptive exchange mechanism enables variation in f-box protein expression. Mol Cell 69:773–786

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lo SC, Hannink M (2006) CAND1-mediated substrate adaptor recycling is required for efficient repression of Nrf2 by Keap1. Mol Cell Biol 26:1235–1244

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lo SF, Yang SY, Chen KT, Hsing YI, Zeevaart JA, Chen LJ, Yu SM (2008) A novel class of gibberellin 2-oxidases control semidwarfism, tillering, and root development in rice. Plant Cell 20:2603–2618

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lydeard JR, Schulman BA, Harper JW (2013) Building and remodelling Cullin-RING E3 ubiquitin ligases. EMBO Rep 14:1050–1061

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nakajima M, Shimada A, Takashi Y, Kim YC, Park SH, Ueguchi-Tanaka M, Suzuki H, Katoh E, Iuchi S, Kobayashi M, Maeda T, Matsuoka M, Yamaguchi I (2006) Identification and characterization of Arabidopsis gibberellin receptors. Plant J 46:880–889

    CAS  PubMed  Google Scholar 

  • Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604

    CAS  PubMed  PubMed Central  Google Scholar 

  • Overvoorde P, Fukaki H, Beeckman T (2010) Auxin control of root development. Cold Spring Harb Perspect Biol 2:a001537

    PubMed  PubMed Central  Google Scholar 

  • Pierce NW, Lee JE, Liu X, Sweredoski MJ, Graham RLJ, Larimore EA, Rome M, Zheng N, Clurman BE, Hess S, Shan SO, Deshaies RJ (2013) Cand1 promotes assembly of new SCF complexes through dynamic exchange of F box proteins. Cell 153:206–215

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reitsma JM, Liu X, Reichermeier KM, Moradian A, Sweredoski MJ, Hess S, Deshaies RJ (2017) Composition and regulation of the cellular repertoire of SCF ubiquitin ligases. Cell 171:1326–1339

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ren Z, Li Z, Miao Q, Yang Y, Deng W, Hao Y (2011) The auxin receptor homologue in Solanum lycopersicum stimulates tomato fruit set and leaf morphogenesis. J Exp Bot 62:2815–2826

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Santner A, Estelle M (2010) The ubiquitin-proteasome system regulates plant hormone signaling. Plant J 61:1029–1040

    CAS  PubMed  PubMed Central  Google Scholar 

  • Serrani JC, Ruiz-Rivero O, Fos M, Garcia-Martinez JL (2008) Auxin-induced fruit-set in tomato is mediated in part by gibberellins. Plant J 56:922–934

    CAS  PubMed  Google Scholar 

  • Shiraishi S, Zhou C, Aoki T, Sato N, Chiba T, Tanaka K, Yoshida S, Nabeshima Y, Nabeshima Y, Tamura TA (2007) TBP-interacting protein 120B (TIP120B)/cullin-associated and neddylation-dissociated 2 (CAND2) inhibits SCF-dependent ubiquitination of myogenin and accelerates myogenic differentiation. J Biol Chem 282:9017–9028

    CAS  PubMed  Google Scholar 

  • Silva GFF, Silva EM, Correa JPO, Vicente MH, Jiang N, Notini MM, Junior AC, De Jesus FA, Castilho P, Carrera E, López-Díaz I, Grotewold E, Peres LEP, Nogueira FTS (2019) Tomato floral induction and flower development are orchestrated by the interplay between gibberellin and two unrelated microRNA-controlled modules. New Phytol 221:1328–1344

    CAS  PubMed  Google Scholar 

  • Smalle J, Vierstra RD (2004) The ubiquitin in 26S proteasome proteolytic pathway. Annu Rev Plant Biol 55:555–590

    CAS  PubMed  Google Scholar 

  • Straube R, Shah M, Flockerzi D, Wolf DA (2017) Trade-off and flexibility in the dynamic regulation of the cullin-RING ubiquitin ligase repertoire. PLoS Comput Biol 13:e1005869

    PubMed  PubMed Central  Google Scholar 

  • Sun TP, Gubler F (2004) Molecular mechanism of gibberellin signaling in plants. Annu Rev Plant Biol 55:197–223

    CAS  PubMed  Google Scholar 

  • Ueguchi-Tanaka M, Nakajima M, Motoyuki A, Matsuoka M (2007) Gibberellin receptor and its role in gibberellin signaling in plants. Annu Rev Plant Biol 58:183–198

    CAS  PubMed  Google Scholar 

  • Vierstra RD (2003) The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant Sci 8:135–142

    CAS  PubMed  Google Scholar 

  • Vierstra RD (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Nat Rev Mol Cell Biol 10:385–397

    CAS  PubMed  Google Scholar 

  • Wang Y, Li J (2008) Molecular basis of plant architecture. Annu Rev Plant Biol 59:253–279

    CAS  PubMed  Google Scholar 

  • Wang H, Jones B, Li Z, Frasse P, Delalande C, Regad F, Chaabouni S, Latché 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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Wu S, Zhu W, Nhan T, Toth JI, Petroski MD, Wolf DA (2013) CAND1 controls in vivo dynamics of the cullin 1-RING ubiquitin ligase repertoire. Nat Commun 4:1642

    PubMed  PubMed Central  Google Scholar 

  • Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251

    CAS  PubMed  Google Scholar 

  • Yang Y, Wu Y, Pirrello J, Regad F, Bouzayen M, Deng W, Li Z (2010) Silencing Sl-EBF1 and Sl-EBF2 expression causes constitutive ethylene response phenotype, accelerated plant senescence, and fruit ripening in tomato. J Exp Bot 61:697–708

    CAS  PubMed  Google Scholar 

  • Yogosawa S, Makino Y, Yoshida T, Kishimoto T, Muramatsu M, Tamura T (1996) Molecular cloning of a novel 120-kDa TBP-interacting protein. Biochem Biophys Res Commun 229:612–617

    CAS  PubMed  Google Scholar 

  • Zemla A, Thomas Y, Kedziora S, Knebel A, Wood NT, Rabut G, Kurz T (2013) CSN- and CAND1-dependent remodelling of the budding yeast SCF complex. Nat Commun 4:1641

    PubMed  Google Scholar 

  • Zhang S, Zhang D, Fan S, Du L, Shen Y, Xing L, Li Y, Ma J, Han M (2016) Effect of exogenous GA3 and its inhibitor paclobutrazol on floral formation, endogenous hormones, and flowering-associated genes in ‘Fuji’ apple (Malus domestica Borkh.). Plant Physiol Biochem 107:178–186

    CAS  PubMed  Google Scholar 

  • Zhang Y, Li Z, Tu Y, Cheng W, Yang Y (2018) Tomato (Solanum lycopersicum) SlIPT4, encoding an isopentenyltransferase, is involved in leaf senescence and lycopene biosynthesis during fruit ripening. BMC Plant Biol 18:107

    PubMed  PubMed Central  Google Scholar 

  • Zheng J, Yang X, Harrell JM, Ryzhikov S, Shim EH, Lykke-Andersen K, Wei N, Sun H, Kobayashi R, Zhang H (2002) CAND1 binds to unneddylated CUL1 and regulates the formation of SCF ubiquitin E3 ligase complex. Mol Cell 10:1519–1526

    CAS  PubMed  Google Scholar 

  • Zheng N, Zhou Q, Wang Z, Wei W (2016) Recent advances in SCF ubiquitin ligase complex: clinical implications. Biochim Biophys Acta 1866:12–22

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31372080) and the Committee of Science and Technology of Chongqing, China (cstc2017jcyjAX0455).

Author information

Authors and Affiliations

Authors

Contributions

YY conceived and designed the research. CW, YS and TY performed the experiments. CW and YY analyzed the data and wrote the manuscript. MH and WY participated in the discussion.

Corresponding author

Correspondence to Yingwu Yang.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1724 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cheng, W., Yin, S., Tu, Y. et al. SlCAND1, encoding cullin-associated Nedd8-dissociated protein 1, regulates plant height, flowering time, seed germination, and root architecture in tomato. Plant Mol Biol 102, 537–551 (2020). https://doi.org/10.1007/s11103-020-00963-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-020-00963-7

Keywords

Navigation