The function of the plant hormone jasmonic acid (JA) in the development of tomato (Solanum lycopersicum) flowers was analyzed with a mutant defective in JA perception (jasmonate-insensitive1-1, jai1-1). In contrast with Arabidopsis (Arabidopsis thaliana) JA-insensitive plants, which are male sterile, the tomato jai1-1 mutant is female sterile, with major defects in female development. To identify putative JA-dependent regulatory components, we performed transcriptomics on ovules from flowers at three developmental stages from wild type and jai1-1 mutants. One of the strongly downregulated genes in jai1-1 encodes the MYB transcription factor SlMYB21. Its Arabidopsis ortholog plays a crucial role in JA-regulated stamen development. SlMYB21 was shown here to exhibit transcription factor activity in yeast, to interact with SlJAZ9 in yeast and in planta, and to complement Arabidopsis myb21-5 To analyze SlMYB21 function, we generated clustered regularly interspaced short palindromic repeats(CRISPR)/CRISPR associated protein 9 (Cas9) mutants and identified a mutant by Targeting Induced Local Lesions in Genomes (TILLING). These mutants showed female sterility, corroborating a function of MYB21 in tomato ovule development. Transcriptomics analysis of wild type, jai1-1, and myb21-2 carpels revealed processes that might be controlled by SlMYB21. The data suggest positive regulation of JA biosynthesis by SlMYB21, but negative regulation of auxin and gibberellins. The results demonstrate that SlMYB21 mediates at least partially the action of JA and might control the flower-to-fruit transition. .

Department of Cell and Metabolic Biology Institute of Plant Biochemistry 06120 Halle Germany

Laboratory of Growth Regulators Palacky University and Institute of Experimental Botany Czech Academy of Sciences v v i CZ 78371 Olomouc Czech Republic

Martin Luther University Halle Wittenberg Biocenter Electron Microscopy 06120 Halle Germany

Max Planck Institute for Plant Breeding Research 50829 Köln Germany

Tsukuba Plant Innovation Research Center University of Tsukuba Tsukuba Japan

Zobrazit více v PubMed

Balcke G.U., Handrick V., Bergau N., Fichtner M., Henning A., Stellmach H., Tissier A., Hause B., Frolov A. (2012). An UPLC-MS/MS method for highly sensitive high-throughput analysis of phytohormones in plant tissues. Plant Methods 8: 47. PubMed PMC

Bradford K.J., Trewavas A.J. (1994). Sensitivity thresholds and variable time scales in plant hormone action. Plant Physiol. 105: 1029–1036. PubMed PMC

Brooks C., Nekrasov V., Lippman Z.B., Van Eck J. (2014). Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol. 166: 1292–1297. PubMed PMC

Browse J. (2009a). The power of mutants for investigating jasmonate biosynthesis and signaling. Phytochemistry 70: 1539–1546. PubMed

Browse J. (2009b). Jasmonate passes muster: A receptor and targets for the defense hormone. Annu. Rev. Plant Biol. 60: 183–205. PubMed

Brukhin V., Hernould M., Gonzalez N., Chevalier C., Mouras A. (2003). Flower development schedule in tomato Lycopersicon esculentum cv. sweet cherry. Sex. Plant Reprod. 15: 311–320.

Carrera E., Ruiz-Rivero O., Peres L.E.P., Atares A., Garcia-Martinez J.L. (2012). Characterization of the procera tomato mutant shows novel functions of the SlDELLA protein in the control of flower morphology, cell division and expansion, and the auxin-signaling pathway during fruit-set and development. Plant Physiol. 160: 1581–1596. PubMed PMC

Čermák T., Baltes N.J., Čegan R., Zhang Y., Voytas D.F. (2015). High-frequency, precise modification of the tomato genome. Genome Biol. 16: 232. PubMed PMC

Chini A., Fonseca S., Fernández G., Adie B., Chico J.M., Lorenzo O., García-Casado G., López-Vidriero I., Lozano F.M., Ponce M.R., Micol J.L., Solano R. (2007). The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448: 666–671. PubMed

Clough S.J., Bent A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735–743. PubMed

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

de Jong M., Wolters-Arts M., Schimmel B.C.J., Stultiens C.L.M., de Groot P.F.M., Powers S.J., Tikunov Y.M., Bovy A.G., Mariani C., Vriezen W.H., Rieu I. (2015). Solanum lycopersicum AUXIN RESPONSE FACTOR 9 regulates cell division activity during early tomato fruit development. J. Exp. Bot. 66: 3405–3416. PubMed PMC

Dobritzsch S., Weyhe M., Schubert R., Dindas J., Hause G., Kopka J., Hause B. (2015). Dissection of jasmonate functions in tomato stamen development by transcriptome and metabolome analyses. BMC Biol. 13: 28. PubMed PMC

Drews G.N., Yadegari R. (2002). Development and function of the angiosperm female gametophyte. Annu. Rev. Genet. 36: 99–124. PubMed

Eck J.V., Kirk D.D., Walmsley A.M. (2006). Tomato (Lycopersicum esculentum). In Agrobacterium Protocols, Wang K., ed (Totowa, NJ: Humana Press; ), pp. 459–474. PubMed

Endress P.K. (2010). Flower structure and trends of evolution in eudicots and their major subclades. Ann. Mo. Bot. Gard. 97: 541–583.

Endress P.K. (2011). Angiosperm ovules: Diversity, development, evolution. Ann. Bot. 107: 1465–1489. PubMed PMC

Engler C., Youles M., Gruetzner R., Ehnert T.-M., Werner S., Jones J.D.G., Patron N.J., Marillonnet S. (2014). A golden gate modular cloning toolbox for plants. ACS Synth. Biol. 3: 839–843. PubMed

Expósito-Rodríguez M., Borges A.A., Borges-Pérez A., Pérez J.A. (2008). Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biol. 8: 131. PubMed PMC

Fernandez A.I., et al. (2009). Flexible tools for gene expression and silencing in tomato. Plant Physiol. 151: 1729–1740. PubMed PMC

Fonseca S., Chini A., Hamberg M., Adie B., Porzel A., Kramell R., Miersch O., Wasternack C., Solano R. (2009). (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat. Chem. Biol. 5: 344–350. PubMed

García-Hurtado N., Carrera E., Ruiz-Rivero O., López-Gresa M.P., Hedden P., Gong F., García-Martínez J.L. (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

Gietz R.D., Schiestl R.H. (2007). Large-scale high-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat. Protoc. 2: 38–41. PubMed

Gillaspy G., Ben-David H., Gruissem W. (1993). Fruits: A developmental perspective. Plant Cell 5: 1439–1451. PubMed PMC

Goetz S., Hellwege A., Stenzel I., Kutter C., Hauptmann V., Forner S., McCaig B., Hause G., Miersch O., Wasternack C., Hause B. (2012). Role of cis-12-oxo-phytodienoic acid in tomato embryo development. Plant Physiol. 158: 1715–1727. PubMed PMC

Goldental-Cohen S., Israeli A., Ori N., Yasuor H. (2017). Auxin response dynamics during wild-type and entire flower development in tomato. Plant Cell Physiol. 58: 1661–1672. PubMed

Gorguet B., van Heusden A.W., Lindhout P. (2005). Parthenocarpic fruit development in tomato. Plant Biol (Stuttg) 7: 131–139. PubMed

Grefen C., Blatt M.R. (2012). A 2in1 cloning system enables ratiometric bimolecular fluorescence complementation (rBiFC). Biotechniques 53: 311–314. PubMed

Haughn G., Chaudhury A. (2005). Genetic analysis of seed coat development in Arabidopsis. Trends Plant Sci. 10: 472–477. PubMed

Hause B., Stenzel I., Miersch O., Maucher H., Kramell R., Ziegler J., Wasternack C. (2000). Tissue-specific oxylipin signature of tomato flowers: Allene oxide cyclase is highly expressed in distinct flower organs and vascular bundles. Plant J. 24: 113–126. PubMed

Hedden P., Phillips A.L. (2000). Manipulation of hormone biosynthetic genes in transgenic plants. Curr. Opin. Biotechnol. 11: 130–137. PubMed

Hedden P., Thomas S.G. (2012). Gibberellin biosynthesis and its regulation. Biochem. J. 444: 11–25. PubMed

Hu J., Israeli A., Ori N., Sun T.P. (2018). 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. PubMed PMC

Huang H., Gao H., Liu B., Qi T., Tong J., Xiao L., Xie D., Song S. (2017). Arabidopsis MYB24 regulates jasmonate-mediated stamen development. Front. Plant Sci. 8: 1525. PubMed PMC

Johri B., Ambegaokar K., Srivastava P. (1992). Comparative embryology of angiosperms. (Berlin: Springer; ).

Kapil R., Tiwari S. (1978). The integumentary tapetum. Bot. Rev. 44: 457–490.

Kay S., Hahn S., Marois E., Hause G., Bonas U. (2007). A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318: 648–651. PubMed

Larsson E., Roberts C.J., Claes A.R., Franks R.G., Sundberg E. (2014). Polar auxin transport is essential for medial versus lateral tissue specification and vascular-mediated valve outgrowth in Arabidopsis gynoecia. Plant Physiol. 166: 1998–2012. PubMed PMC

Li L., Zhao Y., McCaig B.C., Wingerd B.A., Wang J., Whalon M.E., Pichersky E., Howe G.A. (2004). The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16: 126–143. PubMed PMC

Liu Z., Miao L., Huo R., Song X., Johnson C., Kong L., Sundaresan V., Yu X. (2018). ARF2–ARF4 and ARF5 are essential for female and male gametophyte development in Arabidopsis. Plant Cell Physiol. 59: 179–189. PubMed

Lu J., Magnani E. (2018). Seed tissue and nutrient partitioning, a case for the nucellus. Plant Reprod. 31: 309–317 PubMed PMC

Machemer K., Shaiman O., Salts Y., Shabtai S., Sobolev I., Belausov E., Grotewold E., Barg R. (2011). Interplay of MYB factors in differential cell expansion, and consequences for tomato fruit development. Plant J. 68: 337–350. PubMed

Mandaokar A., Browse J. (2009). MYB108 acts together with MYB24 to regulate jasmonate-mediated stamen maturation in Arabidopsis. Plant Physiol. 149: 851–862. PubMed PMC

Mandaokar A., Thines B., Shin B., Lange B.M., Choi G., Koo Y.J., Yoo Y.J., Choi Y.D., Choi G., Browse J. (2006). Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling. Plant J. 46: 984–1008. PubMed

Marsch-Martínez N., de Folter S. (2016). Hormonal control of the development of the gynoecium. Curr. Opin. Plant Biol. 29: 104–114. PubMed

Merico D., Isserlin R., Stueker O., Emili A., Bader G.D. (2010). Enrichment map: A network-based method for gene-set enrichment visualization and interpretation. PLoS One 5: e13984. PubMed PMC

Meyer Y., Grosset J., Chartier Y., Cleyet-Marel J.-C. (1988). Preparation by two-dimensional electrophoresis of proteins for antibody production: antibodies against proteins whose synthesis is reduced by auxin in tobacco mesophyll protoplasts. Electrophoresis 9: 704–712. PubMed

Mielke K., Forner S., Kramell R., Conrad U., Hause B. (2011). Cell-specific visualization of jasmonates in wounded tomato and Arabidopsis leaves using jasmonate-specific antibodies. New Phytol. 190: 1069–1080. PubMed

Modrusan Z., Reiser L., Feldmann K.A., Fischer R.L., Haughn G.W. (1994). Homeotic transformation of ovules into carpel-like structures in Arabidopsis. Plant Cell 6: 333–349. PubMed PMC

Moubayidin L., Østergaard L. (2017). Gynoecium formation: An intimate and complicated relationship. Curr. Opin. Genet. Dev. 45: 15–21. PubMed

Nekrasov V., Staskawicz B., Weigel D., Jones J.D.G., Kamoun S. (2013). Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31: 691–693. PubMed

Niwa T., Suzuki T., Takebayashi Y., Ishiguro R., Higashiyama T., Sakakibara H., Ishiguro S. (2018). Jasmonic acid facilitates flower opening and floral organ development through the upregulated expression of SlMYB21 transcription factor in tomato. Biosci. Biotechnol. Biochem. 82: 292–303. PubMed

Okabe Y., Asamizu E., Saito T., Matsukura C., Ariizumi T., Brès C., Rothan C., Mizoguchi T., Ezura H. (2011). Tomato TILLING technology: Development of a reverse genetics tool for the efficient isolation of mutants from Micro-Tom mutant libraries. Plant Cell Physiol. 52: 1994–2005. PubMed PMC

Pattison R.J., Csukasi F., Catalá C. (2014). Mechanisms regulating auxin action during fruit development. Physiol. Plant. 151: 62–72. PubMed

Qi T., Huang H., Song S., Xie D. (2015). Regulation of jasmonate-mediated stamen development and seed production by a bHLH-MYB complex in Arabidopsis. Plant Cell 27: 1620–1633. PubMed PMC

Reeves P.H., et al. (2012). A regulatory network for coordinated flower maturation. PLoS Genet. 8: e1002506. PubMed PMC

Rittenberg D., Foster G.L. (1940). A new procedure for quantitative analysis by isotope dilution with application to the determination of amino acids and fatty acids. J. Biol. Chem. 133: 737–744.

Schmittgen T.D., Livak K.J. (2008). Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3: 1101–1108. PubMed

Schneitz K., Hülskamp M., Pruitt R.E. (1995). Wild-type ovule development in Arabidopsis thaliana: A light microscope study of cleared whole-mount tissue. Plant J. 7: 731–749.

Schreiber T., Tissier A. (2016). Libraries of synthetic TALE-activated promoters: Methods and applications. In Meth. Enzymol., O'Connor S.E., ed (London: Academic Press; ), pp. 361–378. PubMed

Schreiber T., Prange A., Hoppe T., Tissier A.F. (2019). Split-TALE: A TALE-based two-component system for synthetic biology applications in planta. Plant Physiol 179:1001–1012. PubMed PMC

Serrani J., Fos M., Atarés A., García-Martínez J. (2007). Effect of gibberellin and auxin on parthenocarpic fruit growth induction in the cv Micro-Tom of tomato. J. Plant Growth Regul. 26: 211–221.

Shimada T.L., Shimada T., Hara-Nishimura I. (2010). A rapid and non-destructive screenable marker, FAST, for identifying transformed seeds of Arabidopsis thaliana. Plant J. 61: 519–528. PubMed

Smyth D.R., Bowman J.L., Meyerowitz E.M. (1990). Early flower development in Arabidopsis. Plant Cell 2: 755–767. PubMed PMC

Song S., Qi T., Huang H., Ren Q., Wu D., Chang C., Peng W., Liu Y., Peng J., Xie D. (2011). The Jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription factors MYB21 and MYB24 to affect Jasmonate-regulated stamen development in Arabidopsis. Plant Cell 23: 1000–1013. PubMed PMC

Sparkes I.A., Runions J., Kearns A., Hawes C. (2006). Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat. Protoc. 1: 2019–2025. PubMed

Spurr A.R. (1969). A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26: 31–43. PubMed

Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. (2005). Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102: 15545–15550. PubMed PMC

Thines B., Katsir L., Melotto M., Niu Y., Mandaokar A., Liu G., Nomura K., He S.Y., Howe G.A., Browse J. (2007). JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448: 661–665. PubMed

Urbanová T., Tarkowská D., Novák O., Hedden P., Strnad M. (2013). Analysis of gibberellins as free acids by ultra performance liquid chromatography-tandem mass spectrometry. Talanta 112: 85–94. PubMed

Varaud E., Brioudes F., Szécsi J., Leroux J., Brown S., Perrot-Rechenmann C., Bendahmane M. (2011). AUXIN RESPONSE FACTOR8 regulates Arabidopsis petal growth by interacting with the bHLH transcription factor BIGPETALp. Plant Cell 23: 973–983. PubMed PMC

Wang H., Schauer N., Usadel B., Frasse P., Zouine M., Hernould M., Latché A., Pech J.-C., Fernie A.R., 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. PubMed PMC

Wasternack C., Hause B. (2013). Jasmonates: Biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann. Bot. 111: 1021–1058. PubMed PMC

Wasternack C., Song S. (2017). Jasmonates: Biosynthesis, metabolism, and signaling by proteins activating and repressing transcription. J. Exp. Bot. 68: 1303–1321. PubMed

Weber E., Engler C., Gruetzner R., Werner S., Marillonnet S. (2011). A modular cloning system for standardized assembly of multigene constructs. PLoS One 6: e16765. PubMed PMC

Werner S., Engler C., Weber E., Gruetzner R., Marillonnet S. (2012). Fast track assembly of multigene constructs using Golden Gate cloning and the MoClo system. Bioeng. Bugs 3: 38–43. PubMed

Xu W., Fiume E., Coen O., Pechoux C., Lepiniec L., Magnani E. (2016). Endosperm and nucellus develop antagonistically in Arabidopsis seeds. Plant Cell 28: 1343–1360. PubMed PMC

Yoo S.-D., Cho Y.-H., Sheen J. (2007). Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nat. Protoc. 2: 1565–1572. PubMed

Zouine M., Maza E., Djari A., Lauvernier M., Frasse P., Smouni A., Pirrello J., Bouzayen M. (2017). TomExpress, a unified tomato RNA-Seq platform for visualization of expression data, clustering and correlation networks. Plant J. 92: 727–735. PubMed