SHATTERPROOF 2 regulates TAA1 expression for the establishment of the gynoecium valve margins. Gynoecium development and patterning play a crucial role in determining the ultimate structure of the fruit and, thus, seed production. The MADS-box transcription factor SHATTERPROOF 2 (SHP2) contributes to valve margin differentiation and plays a major role in fruit dehiscence and seed dispersal. Despite the acknowledged contribution of auxin to gynoecium development, its precise role in valve margin establishment remains somewhat enigmatic. Our study addresses this gap by uncovering the role of SHP2 as a positive regulator of key auxin biosynthetic genes, TAA1 and YUCCA 4. Genetic and molecular analyses revealed that SHP2 directly regulates the expression of TAA1 in the valve margins of a stage 12 gynoecium with known regulators of flower and ovule development, such as AGAMOUS, SEEDSTICK, and SEPATALA 3. Collectively, our findings define a previously unrecognized function of SHP2 in the regulation of auxin biosynthetic genes during gynoecium development and raise the possibility that the auxin produced under SHP2 regulation may contribute significantly to the valve margin establishment.

Hormonal Crosstalk in Plant Development Mendel Center for Plant Genomics and Proteomics CEITEC MU Central European Institute of Technology Masaryk University 625 00 Brno Czech Republic

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Attuluri VPS, Sánchez López JF, Maier L, Paruch K, Robert HS (2022) Comparing the efficiency of six clearing methods in developing seeds of Arabidopsis thaliana. Plant Reprod 35(4):279-293 10.1007/s00497-022-00453-4 PubMed PMC

Barro-Trastoy D, Dolores Gomez M, Tornero P, Perez-Amador MA (2020) On the way to ovules: The hormonal regulation of ovule development. Crit Rev Plant Sci 39(5):431–456. 10.1080/07352689.2020.1820203

Chakraborty A, Singh B, Pandey V et al (2024) MicroRNA164e suppresses NAC100 transcription factor-mediated synthesis of seed storage proteins in chickpea. N Phytol 242:2652–2668. 10.1111/nph.19770 PubMed

Chávez Montes RA, Herrera-Ubaldo H, Serwatowska J, de Folter S (2015) Towards a comprehensive and dynamic gynoecium gene regulatory network. Curr Plant Biol. 10.1016/j.cpb.2015.08.002

Cheng Y, Dai X, Zhao Y (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 20(13):1790–1799. 10.1101/gad.1415106 PubMed PMC

Colombo M, Brambilla V, Marcheselli R et al (2010) A new role for the SHATTERPROOF genes during Arabidopsis gynoecium development. Dev Biol 337:294–302. 10.1016/j.ydbio.2009.10.043 PubMed

de Folter S (2016) Auxin is required for valve margin patterning in Arabidopsis after all. Mol Plant 9(6):768–770. 10.1016/j.molp.2016.05.005 PubMed

Favaro R, Pinyopich A, Battaglia R, Kooiker M, Borghi L, Ditta G, Yanofsky MF, Kater MM, Colombo L (2003) MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell 15(11):2603–2611. 10.1105/tpc.015123 PubMed PMC

Ferrándiz C, Liljegren SJ, Yanofsky MF (2000) Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science 289(5478):436–438. 10.1126/science.289.5478.436 PubMed

Gendrel A-V, Lippman Z, Martienssen R, Colot V (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods 2(3):213–218. 10.1038/nmeth0305-213 PubMed

Li H, Luan S (2010) AtFKBP53 is a histone chaperone required for repression of ribosomal RNA gene expression in Arabidopsis. Cell Res 20(3):357–366. 10.1038/cr.2010.22 PubMed

Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL, Yanofsky MF (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404(6779):766–770. 10.1038/35008089 PubMed

Liljegren SJ, Roeder AHK, Kempin SA, Gremski K, Østergaard L, Guimil S, Reyes DK, Yanofsky MF (2004) Control of fruit patterning in <em>Arabidopsis</em> by INDEHISCENT. Cell 116(6):843–853. 10.1016/S0092-8674(04)00217-X PubMed

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402–408. 10.1006/meth.2001.1262 PubMed

Luna-García V, Bernal Gallardo JJ, Rethoret-Pasty M, Pasha A, Provart NJ, de Folter S (2024) A high-resolution gene expression map of the medial and lateral domains of the gynoecium of Arabidopsis. Plant Physiol 195(1):410–429. 10.1093/plphys/kiad658 PubMed

Marsch-Martínez N, Zúñiga-Mayo VM, Herrera-Ubaldo H, Ouwerkerk PB, Pablo-Villa J, Lozano-Sotomayor P, Greco R, Ballester P, Balanzá V, Kuijt SJ, Meijer AH, Pereira A, Ferrándiz C, de Folter S (2014) The NTT transcription factor promotes replum development in Arabidopsis fruits. Plant J 80(1):69–81. 10.1111/tpj.12617 PubMed

Martínez-Fernández I, Sanchís S, Marini N, Balanzá V, Ballester P, Navarrete-Gómez M, Oliveira AC, Colombo L, Ferrándiz C (2014) The effect of NGATHA altered activity on auxin signaling pathways within the Arabidopsis gynoecium. Front Plant Sci. 10.3389/fpls.2014.00210 PubMed PMC

Mashiguchi K, Tanaka K, Sakai T, Sugawara S, Kawaide H, Natsume M, Hanada A, Yaeno T, Shirasu K, Yao H, McSteen P, Zhao Y, Hayashi K-I, Kamiya Y, Kasahara H (2011) The main auxin biosynthesis pathway in Arabidopsis. Proc Nat Acad Sci 108(45):18512–18517. 10.1073/pnas.1108434108 PubMed PMC

Matias-Hernandez L, Battaglia R, Galbiati F, Rubes M, Eichenberger C, Grossniklaus U, Kater MM, Colombo L (2010) VERDANDI is a direct target of the MADS domain ovule identity complex and affects embryo sac differentiation in Arabidopsis. Plant Cell 22(6):1702–1715. 10.1105/tpc.109.068627 PubMed PMC

Mizzotti C, Ezquer I, Paolo D et al (2014) SEEDSTICK is a master regulator of development and metabolism in the Arabidopsis seed coat. PLoS Genet 10:e1004856. 10.1371/journal.pgen.1004856 PubMed PMC

Moubayidin L, Ostergaard L (2014) Dynamic control of auxin distribution imposes a bilateral-to-radial symmetry switch during gynoecium development. Curr Biol 24(22):2743–2748 PubMed PMC

Pinyopich A, Ditta GS, Savidge B, Liljegren SJ, Baumann E, Wisman E, Yanofsky MF (2003) Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424(6944):85–88. 10.1038/nature01741 PubMed

Ramos-Pulido J, de Folter S (2023) Organogenic events during gynoecium and fruit development in Arabidopsis. Curr Opin Plant Biol 75:102440. 10.1016/j.pbi.2023.102440 PubMed

Reyes-Olalde JI, Zúñiga-Mayo VM, Serwatowska J, Chavez Montes RA, Lozano-Sotomayor P, Herrera-Ubaldo H, Gonzalez-Aguilera KL, Ballester P, Ripoll JJ, Ezquer I, Paolo D, Heyl A, Colombo L, Yanofsky MF, Ferrandiz C, Marsch-Martínez N, de Folter S (2017) The bHLH transcription factor SPATULA enables cytokinin signaling, and both activate auxin biosynthesis and transport genes at the medial domain of the gynoecium. PLoS Genet 13(4):e1006726. 10.1371/journal.pgen.1006726 PubMed PMC

Robert HS, Crhak Khaitova L, Mroue S, Benková E (2015) The importance of localized auxin production for morphogenesis of reproductive organs and embryos in Arabidopsis. J Exp Bot 66(16):5029–5042. 10.1093/jxb/erv256 PubMed

Robert HS, Park C, Gutièrrez CL, Wójcikowska B, Pěnčík A, Novák O, Chen J, Grunewald W, Dresselhaus T, Friml J, Laux T (2018) Maternal auxin supply contributes to early embryo patterning in Arabidopsis. Nat Plants 4(8):548–553. 10.1038/s41477-018-0204-z PubMed PMC

Roeder AH, Yanofsky MF (2006) Fruit development in Arabidopsis. Arabidopsis Book 4:e0075. 10.1199/tab.0075 PubMed PMC

Schneitz K, Hülskamp M, Pruitt RE (1995) Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. Plant J 7(5):731–749. 10.1046/j.1365-313X.1995.07050731.x

Sehra B, Franks RG (2017) Redundant CArG box cis-motif activity mediates SHATTERPROOF2 transcriptional regulation during Arabidopsis thaliana gynoecium development. Front Plant Sci 8:1712. 10.3389/fpls.2017.01712 PubMed PMC

Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2(8):755–767. 10.1105/tpc.2.8.755 PubMed PMC

Sohlberg JJ, Myrenås M, Kuusk S et al (2006) STY1 regulates auxin homeostasis and affects apical-basal patterning of the Arabidopsis gynoecium. Plant J 47:112–123. 10.1111/j.1365-313x.2006.02775.x PubMed

Sorefan K, Girin T, Liljegren SJ, Ljung K, Robles P, Galván-Ampudia CS, Offringa R, Friml J, Yanofsky MF, Østergaard L (2009) A regulated auxin minimum is required for seed dispersal in Arabidopsis. Nature 459(7246):583–586. 10.1038/nature07875 PubMed

Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie D-Y, Doležal K, Schlereth A, Jürgens G, Alonso JM (2008) <em>TAA1</em>-Mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133(1):177–191. 10.1016/j.cell.2008.01.047 PubMed

van Gelderen K, van Rongen M, Otten A, Offringa R (2016) An INDEHISCENT-controlled auxin response specifies the separation layer in early Arabidopsis fruit. Molecular Plant. 9(6):857–69. 10.1016/j.molp.2016.03.005 PubMed

Villarino GH, Hu Q, Manrique S, Flores-Vergara M, Sehra B, Robles L, Brumos J, Stepanova AN, Colombo L, Sundberg E, Heber S (2016) Transcriptomic signature of the SHATTERPROOF2 expression domain reveals the meristematic nature of Arabidopsis gynoecial medial domain. Plant Physiol 171(1):42–61. 10.1104/pp.15.01845 PubMed PMC

Weber E, Engler C, Gruetzner R, Werner S, Marillonnet S (2011) A modular cloning system for standardized assembly of multigene constructs. PLoS ONE 6(2):e16765. 10.1371/journal.pone.0016765 PubMed PMC

Yamaguchi N, Huang J, Tatsumi Y, Abe M, Sugano SS, Kojima M, Takebayashi Y, Kiba T, Yokoyama R, Nishitani K, Sakakibara H, Ito T (2018) Chromatin-mediated feed-forward auxin biosynthesis in floral meristem determinacy. Nat Commun 9(1):5290. 10.1038/s41467-018-07763-0 PubMed PMC

Zhang X, Henriques R, Lin S-S, Niu Q-W, Chua N-H (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc 1(2):641–646. 10.1038/nprot.2006.97 PubMed