CUP-SHAPED COTYLEDON1 (CUC1) and CUC2 regulate cytokinin homeostasis to determine ovule number in Arabidopsis

. 2018 Oct 12 ; 69 (21) : 5169-5176.

Jazyk angličtina Země Anglie, Velká Británie Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid30312436

Seeds derive from ovules upon fertilization and therefore the total number of ovules determines the final seed yield, a fundamental trait in crop plants. Among the factors that co-ordinate the process of ovule formation, the transcription factors CUP-SHAPED COTYLEDON 1 (CUC1) and CUC2 and the hormone cytokinin (CK) have a particularly prominent role. Indeed, the absence of both CUC1 and CUC2 causes a severe reduction in ovule number, a phenotype that can be rescued by CK treatment. In this study, we combined CK quantification with an integrative genome-wide target identification approach to select Arabidopsis genes regulated by CUCs that are also involved in CK metabolism. We focused our attention on the functional characterization of UDP-GLUCOSYL TRANSFERASE 85A3 (UGT85A3) and UGT73C1, which are up-regulated in the absence of CUC1 and CUC2 and encode enzymes able to catalyse CK inactivation by O-glucosylation. Our results demonstrate a role for these UGTs as a link between CUCs and CK homeostasis, and highlight the importance of CUCs and CKs in the determination of seed yield.

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Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M. 1997. Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. The Plant Cell 9, 841–857. PubMed PMC

Antoniadi I, Plačková L, Simonovik B, Doležal K, Turnbull C, Ljung K, Novák O. 2015. Cell-type-specific cytokinin distribution within the Arabidopsis primary root apex. The Plant Cell 27, 1955–1967. PubMed PMC

Ashburner M, Ball CA, Blake JA, et al. . 2000. Gene Ontology: tool for the unification of biology. Nature Genetics 25, 25–29. PubMed PMC

Bartrina I, Otto E, Strnad M, Werner T, Schmülling T. 2011. Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. The Plant Cell 23, 69–80. PubMed PMC

Bencivenga S, Simonini S, Benková E, Colombo L. 2012. The transcription factors BEL1 and SPL are required for cytokinin and auxin signaling during ovule development in Arabidopsis. The Plant Cell 24, 2886–2897. PubMed PMC

Carbon S, Ireland A, Mungall CJ, Shu S, Marshall B, Lewis S, AmiGO Hub, Web Presence Working Group 2009. AmiGO: online access to ontology and annotation data. Bioinformatics 25, 288–289. PubMed PMC

Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735–743. PubMed

Cucinotta M, Colombo L, Roig-Villanova I. 2014. Ovule development, a new model for lateral organ formation. Frontiers in Plant Science 5, 117. PubMed PMC

Cucinotta M, Manrique S, Guazzotti A, Quadrelli NE, Mendes MA, Benkova E, Colombo L. 2016. Cytokinin response factors integrate auxin and cytokinin pathways for female reproductive organ development. Development 143, 4419–4424. PubMed

Dewitte W, Scofield S, Alcasabas A, et al. . 2007. Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proceedings of the National Academy of Sciences, USA 104, 14537–14542. PubMed PMC

Galbiati F, Sinha Roy D, Simonini S, et al. . 2013. An integrative model of the control of ovule primordia formation. The Plant Journal 76, 446–455. PubMed

The Gene Ontology Consortium 2017. Expansion of the gene ontology knowledgebase and resources. Nucleic Acids Research 45, D331–D338. PubMed PMC

Higuchi M, Pischke MS, Mähönen AP, et al. . 2004. In planta functions of the Arabidopsis cytokinin receptor family. Proceedings of the National Academy of Sciences, USA 101, 8821–8826. PubMed PMC

Hou B, Lim EK, Higgins GS, Bowles DJ. 2004. N-glucosylation of cytokinins by glycosyltransferases of Arabidopsis thaliana. The Journal of Biological Chemistry 279, 47822–47832. PubMed

Husar S, Berthiller F, Fujioka S, et al. . 2011. Overexpression of the UGT73C6 alters brassinosteroid glucoside formation in Arabidopsis thaliana. BMC Plant Biology 11, 51. PubMed PMC

Kinoshita-Tsujimura K, Kakimoto T. 2011. Cytokinin receptors in sporophytes are essential for male and female functions in Arabidopsis thaliana. Plant Signaling & Behavior 6, 66–71. PubMed PMC

Li Y, Baldauf S, Lim EK, Bowles DJ. 2001. Phylogenetic analysis of the UDP-glycosyltransferase multigene family of Arabidopsis thaliana. The Journal of Biological Chemistry 276, 4338–4343. PubMed

Mi H, Huang X, Muruganujan A, Tang H, Mills C, Kang D, Thomas PD. 2017. PANTHER version 11: expanded annotation data from Gene Ontology and Reactome pathways, and data analysis tool enhancements. Nucleic Acids Research 45, D183–D189. 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 Genetics 10, e1004856. PubMed PMC

Mok DW, Mok MC. 2001. Cytokinin metabolism and action. Annual Review of Plant Physiology and Plant Molecular Biology 52, 89–118. PubMed

Müller B, Sheen J. 2008. Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453, 1094–1097. PubMed PMC

Nahar MA, Ishida T, Smyth DR, Tasaka M, Aida M. 2012. Interactions of CUP-SHAPED COTYLEDON and SPATULA genes control carpel margin development in Arabidopsis thaliana. Plant & Cell Physiology 53, 1134–1143. PubMed PMC

Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C. 2004. Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. The Plant Cell 16, 1365–1377. PubMed PMC

Novák O, Hauserová E, Amakorová P, Dolezal K, Strnad M. 2008. Cytokinin profiling in plant tissues using ultra-performance liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 69, 2214–2224. PubMed

Raman S, Greb T, Peaucelle A, Blein T, Laufs P, Theres K. 2008. Interplay of miR164, CUP-SHAPED COTYLEDON genes and LATERAL SUPPRESSOR controls axillary meristem formation in Arabidopsis thaliana. The Plant Journal 55, 65–76. PubMed

Reyes-Olalde JI, Zuñiga-Mayo VM, Chávez Montes RA, Marsch-Martínez N, de Folter S. 2013. Inside the gynoecium: at the carpel margin. Trends in Plant Science 18, 644–655. PubMed

Riefler M, Novak O, Strnad M, Schmülling T. 2006. Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. The Plant Cell 18, 40–54. PubMed PMC

Riou-Khamlichi C, Huntley R, Jacqmard A, Murray JA. 1999. Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283, 1541–1544. PubMed

Roeder AH, Yanofsky MF. 2006. Fruit development in Arabidopsis. The Arabidopsis Book 4, e0075. PubMed PMC

Sakakibara H. 2006. Cytokinins: activity, biosynthesis, and translocation. Annual Review of Plant Biology 57, 431–449. PubMed

Schneitz K, Hulskamp M, Pruitt RE. 1995. Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. The Plant Journal 7, 731–749.

Šmehilová M, Dobrůšková J, Novák O, Takáč T, Galuszka P. 2016. Cytokinin-specific glycosyltransferases possess different roles in cytokinin homeostasis maintenance. Frontiers in Plant Science 7, 1264. PubMed PMC

Spíchal L, Rakova NY, Riefler M, Mizuno T, Romanov GA, Strnad M, Schmülling T. 2004. Two cytokinin receptors of Arabidopsis thaliana, CRE1/AHK4 and AHK3, differ in their ligand specificity in a bacterial assay. Plant & Cell Physiology 45, 1299–1305. PubMed

Svačinová J, Novák O, Plačková L, Lenobel R, Holík J, Strnad M, Doležal K. 2012. A new approach for cytokinin isolation from Arabidopsis tissues using miniaturized purification: pipette tip solid-phase extraction. Plant Methods 8, 17. PubMed PMC

Woo HH, Jeong BR, Hirsch AM, Hawes MC. 2007. Characterization of Arabidopsis AtUGT85A and AtGUS gene families and their expression in rapidly dividing tissues. Genomics 90, 143–153. PubMed PMC

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