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Kiwifruit SVP2 controls developmental and drought-stress pathways

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Genome-wide targets of Actinidia chinensis SVP2 confirm roles in ABA- and dehydration-mediated growth repression and reveal a conservation in mechanism of action between SVP genes of taxonomically distant Arabidopsis and a woody perennial kiwifruit.

Abstract

The molecular mechanisms underlying growth and dormancy in woody perennials are largely unknown. In Arabidopsis, the MADS-box transcription factor SHORT VEGETATIVE PHASE (SVP) plays a key role in the progression from vegetative to floral development, and in woody perennials SVP-like genes are also proposed to be involved in controlling dormancy. During kiwifruit development SVP2 has a role in growth inhibition, with high-chill kiwifruit Actinidia deliciosa transgenic lines overexpressing SVP2 showing suppressed bud outgrowth. Transcriptomic analyses of these plants suggests that SVP2 mimics the well-documented abscisic acid (ABA) effect on the plant dehydration response. To corroborate the growth inhibition role of SVP2 in kiwifruit development at the molecular level, we analysed the genome-wide direct targets of SVP2 using chromatin immunoprecipitation followed by high-throughput sequencing in kiwifruit A. chinensis. SVP2 was found to bind to at least 297 target sites in the kiwifruit genome, and potentially modulates 252 genes that function in a range of biological processes, especially those involved in repressing meristem activity and ABA-mediated dehydration pathways. In addition, our ChIP-seq analysis reveals remarkable conservation in mechanism of action between SVP genes of taxonomically distant plant species.

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References

  • Andrés F, Porri A, Torti S, Mateos J, Romera-Branchat M, García-Martínez JL, Fornara F, Gregis V, Kater MM, Coupland G (2014) SHORT VEGETATIVE PHASE reduces gibberellin biosynthesis at the Arabidopsis shoot apex to regulate the floral transition. Proc Natl Acad Sci 111:E2760–E2769

    Article  PubMed  PubMed Central  Google Scholar 

  • Bailey T, Krajewski P, Ladunga I, Lefebvre C, Li Q, Liu T, Madrigal P, Taslim C, Zhang J (2013) Practical guidelines for the comprehensive analysis of ChIP-seq data. PLoS Comput Biol 9:e1003326

    Article  PubMed  PubMed Central  Google Scholar 

  • Bechtold U, Penfold CA, Jenkins DJ, Legaie R, Moore JD (2016) Time-series transcriptomics reveals that AGAMOUS-LIKE22 affects primary metabolism and developmental processes in drought-stressed Arabidopsis. Plant Cell 28:345–366. https://doi.org/10.1105/tpc.15.00910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bielenberg DG, Wang Y, Li ZG, Zhebentyayeva T, Fan SH, Reighard GL, Scorza R, Abbott AG (2008) Sequencing and annotation of the evergrowing locus in peach [Prunus persica (L.) Batsch] reveals a cluster of six MADS-box transcription factors as candidate genes for regulation of terminal bud formation. Tree Genet Genomes 4:495–507

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Deng W, Ying H, Helliwell CA, Taylor JM, Peacock WJ, Dennis ES (2011) FLOWERING LOCUS C (FLC) regulates development pathways throughout the life cycle of Arabidopsis. Proc Natl Acad Sci 108:6680–6685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Devic M (2008) The importance of being essential: EMBRYO-DEFECTIVE genes in Arabidopsis. C R Biol 331:726–736

    Article  CAS  PubMed  Google Scholar 

  • Doelling JH, Yan N, Kurepa J, Walker J, Vierstra RD (2001) The ubiquitin-specific protease UBP14 is essential for early embryo development in Arabidopsis thaliana. Plant J 27:393–405

    Article  CAS  PubMed  Google Scholar 

  • Fernandez DE, Wang C-T, Zheng Y, Adamczyk B, Singhal R, Hall PK, Perry SE (2014) The MADS-domain factors AGL15 and AGL18, along with SVP and AGL24, are necessary to block floral gene expression during the vegetative phase. Plant Physiol 165:1591–1603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fornara F, Gregis V, Pelucchi N, Colombo L, Kater M (2008) The rice StMADS11-like genes OsMADS22 and OsMADS47 cause floral reversions in Arabidopsis without complementing the svp and agl24 mutants. J Exp Bot 59:2181–2190. https://doi.org/10.1093/jxb/ern083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujiwara S, Oda A, Yoshida R, Niinuma K, Miyata K, Tomozoe Y, Tajima T, Nakagawa M, Hayashi K, Coupland G, Mizoguchi T (2008) Circadian clock proteins LHY and CCA1 regulate SVP protein accumulation to control flowering in Arabidopsis. Plant Cell 20:2960–2971

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia-Maroto F, Ortega N, Lozano R, Carmona MJ (2000) Characterization of the potato MADS-box gene STMADS16 and expression analysis in tobacco transgenic plants. Plant Mol Biol 42:499–513

    Article  CAS  PubMed  Google Scholar 

  • Grant CE, Bailey TL, Noble WS (2011) FIMO: scanning for occurrences of a given motif. Bioinformatics 27:1017–1018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gregis V, Sessa A, Dorca-Fornell C, Kater MM (2009) The Arabidopsis floral meristem identity genes AP1, AGL24 and SVP directly repress class B and C floral homeotic genes. Plant J 60:626–637. https://doi.org/10.1111/j.1365-313X.2009.03985.x

    Article  CAS  PubMed  Google Scholar 

  • Gregis V, Andrés F, Sessa A, Guerra RF, Simonini S, Mateos JL, Torti S, Zambelli F, Prazzoli GM, Bjerkan KN (2013) Identification of pathways directly regulated by SHORT VEGETATIVE PHASE during vegetative and reproductive development in Arabidopsis. Genom Biol 14:R56. https://doi.org/10.1186/gb-2013-14-6-r56

    Article  Google Scholar 

  • Hartmann U, Hohmann S, Nettesheim K, Wisman E, Saedler H, Huijser P (2000) Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J 21:351–360. https://doi.org/10.1046/j.1365-313x.2000.00682.x

    Article  CAS  PubMed  Google Scholar 

  • Hellens RP, Allan AC, Friel EN, Bolitho K, Grafton K, Templeton MD, Karunairetnam S, Gleave AP, Laing WA (2005) Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1:13

    Article  PubMed  PubMed Central  Google Scholar 

  • Horvath DP, Chao WS, Suttle JC, Thimmapuram J, Anderson JV (2008) Transcriptome analysis identifies novel responses and potential regulatory genes involved in seasonal dormancy transitions of leafy spurge (Euphorbia esula L.). BMC Genomics 9:536

    Article  PubMed  PubMed Central  Google Scholar 

  • Horvath DP, Sung S, Kim D, Chao W, Anderson J (2010) Characterization, expression and function of DORMANCY ASSOCIATED MADS-BOX genes from leafy spurge. Plant Mol Biol 73:169–179. https://doi.org/10.1007/s11103-009-9596-5

    Article  CAS  PubMed  Google Scholar 

  • Howe GT, Horvath DP, Dharmawardhana P, Priest HD, Mockler TC, Strauss SH (2015) Extensive transcriptome changes during natural onset and release of vegetative bud dormancy in Populus. Front Plant Sci 6:989. https://doi.org/10.3389/fpls.2015.00989

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang S, Ding J, Deng D, Tang W, Sun H, Liu D, Zhang L, Niu X, Zhang X, Meng M, Yu J, Liu J, Han Y, Shi W, Zhang D, Cao S, Wei Z, Cui Y, Xia Y, Zeng H, Bao K, Lin L, Min Y, Zhang H, Miao M, Tang X, Zhu Y, Sui Y, Li G, Sun H, Yue J, Sun J, Liu F, Zhou L, Lei L, Zheng X, Liu M, Huang L, Song J, Xu C, Li J, Ye K, Zhong S, Lu B-R, He G, Xiao F, Wang H-L, Zheng H, Fei Z, Liu Y (2013) Draft genome of the kiwifruit Actinidia chinensis. Nat Commun. https://doi.org/10.1038/ncomms3640

    Google Scholar 

  • Jang S, Torti S, Coupland G (2009) Genetic and spatial interactions between FT, TSF and SVP during the early stages of floral induction in Arabidopsis. Plant J 60:614–625. https://doi.org/10.1111/j.1365-313X.2009.03986.x

    Article  CAS  PubMed  Google Scholar 

  • Jin J, Zhang H, Kong L, Gao G, Luo J (2013) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res 42:1182–1187

    Article  Google Scholar 

  • Lee J, Park S, Lee J, Ahn J (2007a) A conserved role of SHORT VEGETATIVE PHASE (SVP) in controlling flowering time of Brassica plants. Biochim Biophys Acta Gene Struct Express 1769:455–461

    Article  CAS  Google Scholar 

  • Lee JH, Yoo SJ, Park SH, Hwang I, Lee JS, Ahn JH (2007b) Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev 21:397–402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li D, Liu C, Shen L, Wu Y, Chen H, Robertson M, Helliwell CA, Ito T, Meyerowitz E, Yu H (2008) A repressor complex governs the integration of flowering signals in Arabidopsis. Dev Cell 15:110–120

    Article  CAS  PubMed  Google Scholar 

  • Li ZG, Reighard GL, Abbott AG, Bielenberg DG (2009) Dormancy-associated MADS genes from the EVG locus of peach [Prunus persica (L.) Batsch] have distinct seasonal and photoperiodic expression patterns. J Exp Bot 60:3521–3530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li ZM, Zhang JZ, Mei L, Deng XX, Hu CG, Yao JL (2010) PtSVP, an SVP homolog from trifoliate orange (Poncirus trifoliata L. Raf.), shows seasonal periodicity of meristem determination and affects flower development in transgenic Arabidopsis and tobacco plants. Plant Mol Biol 74:129–142. https://doi.org/10.1007/s11103-010-9660-1

    Article  PubMed  Google Scholar 

  • Li Q, Brown JB, Huang H, Bickel PJ (2011) Measuring reproducibility of high-throughput experiments. Ann Appl Stat 5:1752–1779

    Article  Google Scholar 

  • Machanick P, Bailey TL (2011) MEME-ChIP: motif analysis of large DNA datasets. Bioinformatics 27:1696–1697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masiero S, Li M, Will I, Hartmann U, Saedler H, Huijser P, Schwarz-Sommer Z, Sommer H (2004) INCOMPOSITA: a MADS-box gene controlling prophyll development and floral meristem identity in Antirrhinum. Development (Camb) 131:5981–5990. https://doi.org/10.1242/dev.01517

    Article  CAS  Google Scholar 

  • Mateos JL, Madrigal P, Tsuda K, Rawat V, Richter R, Romera-Branchat M, Fornara F, Schneeberger K, Krajewski P, Coupland G (2015) Combinatorial activities of SHORT VEGETATIVE PHASE and FLOWERING LOCUS C define distinct modes of flowering regulation in Arabidopsis. Genom Biol 16:31

    Article  Google Scholar 

  • Mathelier A, Fornes O, Arenillas DJ, Chen C-y, Denay G, Lee J, Shi W, Shyr C, Tan G, Worsley-Hunt R, Zhang AW, Parcy F, Lenhard B, Sandelin A, Wasserman WW (2016) JASPAR 2016: a major expansion and update of the open-access database of transcription factor binding profiles. Nucleic Acids Res 44:D110-D115. https://doi.org/10.1093/nar/gkv1176

    Article  Google Scholar 

  • Mazzitelli L, Hancock RD, Haupt S, Walker PG, Pont SDA, McNicol J, Cardle L, Morris J, Viola R, Brennan R, Hedley PE, Taylor MA (2007) Co-ordinated gene expression during phases of dormancy release in raspberry (Rubus idaeus L.) buds. J Exp Bot 58:1035–1045

    Article  CAS  PubMed  Google Scholar 

  • Mimida N, Saito T, Moriguchi T, Suzuki A, Komori S, Wada M (2015) Expression of DORMANCY-ASSOCIATED MADS-BOX (DAM)-like genes in apple. Biol Plant 59:237–244

    Article  CAS  Google Scholar 

  • Moussian B, Schoof H, Haecker A, Jürgens G, Laux T (1998) Role of the ZWILLE gene in the regulation of central shoot meristem cell fate during Arabidopsis embryogenesis. EMBO J 17:1799–1809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muralla R, Lloyd J, Meinke D (2011) Molecular foundations of reproductive lethality in Arabidopsis thaliana. PLoS ONE 6:e28398. https://doi.org/10.1371/journal.pone.0028398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP (2011) Integrative genomics viewer. Nat Biotechnol 29:24–26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saito T, Bai S, Ito A, Sakamoto D, Saito T, Ubi BE, Imai T, Moriguchi T (2013) Expression and genomic structure of the dormancy-associated MADS box genes MADS13 in Japanese pears (Pyrus pyrifolia Nakai) that differ in their chilling requirement for endodormancy release. Tree Physiol 33:654–667

    Article  CAS  PubMed  Google Scholar 

  • Sasaki R, Yamane H, Ooka T, Jotatsu H, Kitamura Y, Akagi T, Tao R (2011) Functional and expressional analyses of PmDAM genes associated with endodormancy in Japanese apricot (Prunus mume). Plant Physiol 157:485–497. https://doi.org/10.1104/pp.111.181982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schaffer RJ, Pilkington SM (2016) Gene family prediction and annotation. In: Testolin R, Huang H-W, Ferguson AR (eds) The kiwifruit genome. Springer International Publishing, Cham, pp 125–134

    Chapter  Google Scholar 

  • Stacklies W, Redestig H, Scholz M, Walther D, Selbig J (2007) pcaMethods: a bioconductor package providing PCA methods for incomplete data. Bioinformatics 23:1164–1167

    Article  CAS  PubMed  Google Scholar 

  • Szymkowiak EJ, Irish EE (2006) JOINTLESS suppresses sympodial identity in inflorescence meristems of tomato. Planta 223:646–658

    Article  CAS  PubMed  Google Scholar 

  • Tao Z, Shen L, Liu C, Liu L, Yan Y, Yu H (2012) Genome-wide identification of SOC1 and SVP targets during the floral transition in Arabidopsis. Plant J 70:549–561. https://doi.org/10.1111/j.1365-313X.2012.04919.x

    Article  CAS  PubMed  Google Scholar 

  • Trevaskis B, Tadege M, Hemming MN, Peacock WJ, Dennis ES, Sheldon C (2007) Short vegetative phase-like MADS-box genes inhibit floral meristem identity in barley. Plant Physiol 143:225–235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuan PA, Bai S, Saito T, Ito A, Moriguchi T (2017) Dormancy-associated MADS-Box (DAM) and the abscisic acid pathway regulate pear endodormancy through a feedback mechanism. Plant Cell Physiol 58:1378–1390. https://doi.org/10.1093/pcp/pcx074

    Article  PubMed  Google Scholar 

  • Vernon DM, Meinke DW (1995) Late embryo-defective mutants of Arabidopsis. Dev Genet 16:311–320. https://doi.org/10.1002/dvg.1020160404

    Article  Google Scholar 

  • Walton EF, Wu RM, Richardson AC, Davy M, Hellens RP, Thodey K, Janssen BJ, Gleave AP, Rae GM, Wood M, Schaffer RJ (2009) A rapid transcriptional activation is induced by the dormancy-breaking chemical hydrogen cyanamide in kiwifruit (Actinidia deliciosa) buds. J Exp Bot 60:3835–3848. https://doi.org/10.1093/Jxb/Erp231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Georgi L, Reighard G, Scorza R, Abbott A (2002) Genetic mapping of the evergrowing gene in peach [Prunus persica (L.) Batsch]. J Hered 93:352–358

    Article  CAS  PubMed  Google Scholar 

  • Wang T, Karunairetnam S, Wu R, Wang Y-Y, Gleave A (2010) High efficiency transformation platforms for kiwifruit (Actinidia spp.) functional genomics. In: XXVIII International Horticultural Congress on Science and Horticulture for People (IHC2010): International Symposium on 929, pp 143–148

  • Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PloS One 2:e718–e718

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu RM, Walton EF, Richardson AC, Wood M, Hellens RP, Varkonyi-Gasic E (2012) Conservation and divergence of four kiwifruit SVP-like MADS-box genes suggest distinct roles in kiwifruit bud dormancy and flowering. J Exp Bot 63:797–807

    Article  CAS  PubMed  Google Scholar 

  • Wu R, Tomes S, Karunairetnam S, Tustin SD, Hellens RP, Allan AC, Macknight RC, Varkonyi-Gasic E (2017a) SVP-like MADS box genes control dormancy and budbreak in apple. Front Plant Sci 8:477

    PubMed  PubMed Central  Google Scholar 

  • Wu R, Wang T, Warren B, Allan AC, Macknight RC, Varkonyi-Gasic E (2017b) Kiwifruit SVP2 gene prevents premature budbreak during dormancy. J Exp Bot 68:1071–1082

    Article  PubMed  Google Scholar 

  • Yu Y, Ji L, Le BH, Zhai J, Chen J, Luscher E, Gao L, Liu C, Cao X, Mo B (2017) ARGONAUTE10 promotes the degradation of miR165/6 through the SDN1 and SDN2 exonucleases in Arabidopsis. PLoS Biol 15:e2001272

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W (2008) Model-based analysis of ChIP-seq (MACS). Genom Biol 9:R137

    Article  Google Scholar 

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Acknowledgements

The authors wish to thank Cecilia Deng and Lindy Guo for assistance in bioinformatics and statistical analysis, Monica Dragulescu and Wade Wadasinghe for maintenance of plants in the glasshouse, Roger Hellens and Jo Putterill for advice on the project design and progress, and Zac Hanley and Ann Gunson for critical reading of the manuscript. This work was funded by the New Zealand Ministry of Business, Innovation and Employment, contract C10 × 0816 MeriNET, and was supported by funding from The New Zealand Institute for Plant and Food Research Limited (Core and KRIP).

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Authors and Affiliations

  1. The New Zealand Institute for Plant and Food Research Limited (PFR) Mt Albert, Auckland Mail Centre, Private Bag 92169, Auckland, 1142, New Zealand

    Rongmei Wu, Tianchi Wang, Ben A. W. Warren, Andrew C. Allan & Erika Varkonyi-Gasic

  2. The New Zealand Institute for Plant and Food Research Limited (PFR) Lincoln, Christchurch Mail Centre, Private Bag 4704, Christchurch, 8140, New Zealand

    Susan J. Thomson

  3. School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand

    Andrew C. Allan

  4. Department of Biochemistry, The New Zealand Institute for Plant and Food Research Limited, University of Otago, PO Box 56, Dunedin, 9054, New Zealand

    Richard C. Macknight

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  1. Rongmei Wu
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  2. Tianchi Wang
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  3. Ben A. W. Warren
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  4. Susan J. Thomson
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  5. Andrew C. Allan
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  7. Erika Varkonyi-Gasic
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Contributions

RW and EV-G designed the study; RW and TW performed the experimental work; RW, BAW and SJT performed bioinformatics analyses; RW interpreted the data and wrote the manuscript; EV-G, RCM and ACA conceived the project and revised the manuscript.

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Correspondence to Erika Varkonyi-Gasic.

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Wu, R., Wang, T., Warren, B.A.W. et al. Kiwifruit SVP2 controls developmental and drought-stress pathways. Plant Mol Biol 96, 233–244 (2018). https://doi.org/10.1007/s11103-017-0688-3

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