SPP 1530: Flowering Time Control - from Natural Variation to Crop Improvement

PP-2: Coupland

Mechanistic analysis of the transition from juvenility to maturity in perennial Arabis alpina and comparison with Brassica crop species

Many perennial plants exhibit a clearly defined juvenile phase during which they will not flower even if exposed to inductive environmental cues. We developed Arabis alpina, a member of the Brassicaceae, as a herbaceaous perennial model. In this species juvenile plants do not flower in response to vernalization, and we found that the progressive decline of miRNA156 acts as a timer defining the duration of the juvenile phase. Here we propose to deepen our knowledge of juvenility in perennials. First we will identify targets of miRNA156 that underlie this trait. In A. alpina 10 mRNAs encoding different SQUAMOSA PROMOTER BINDING LIKE PROTEIN (SPL) transcription factors are targets of miRNA156. Five of these are expressed around floral induction and orthologues of A. thaliana genes implicated in flowering. We will generate mutations that prevent miRNA156 binding to each of these 5 mRNAs and test which of the mutations reduce the juvenile phase by enabling younger plants to respond to vernalization. Secondly, we will exploit existing populations made by crossing A. alpina and A. montbretiana, an annual sister of A. alpina with no detectable juvenile phase, to genetically map and isolate loci that confer the difference in juvenility between the two species. Thirdly, we will extend our characterization of the flowering responses of A. alpina accessions collected across its European range to test for intra-species natural-genetic variation for juvenility. Fourthly, we will pursue hybrid crosses carried out between annual and perennial species in the Brassica genus and explore whether allelic variation exists in these species at loci identified in Arabis as controlling the juvenile phase. These experiments build on our earlier work in the priority programme to elucidate a major flowering trait differing between annuals and perennials and to extend the results to crops.


Project-related publications:

Dombrowski N, Schlaeppi K, Agler MT, Hacquard S, Kemen E, Garrido-Oter R, Wunder J, Coupland G, Schulze-Lefert P (2017) Root microbiota dynamics of perennial Arabis alpina are dependent on soil residence time but independent of flowering time. ISME J 11: 43-55 http://www.nature.com/ismej/journal/v11/n1/full/ismej2016109a.html

Jung C, Pillen K, Staiger D, Coupland G, von Korff M (2017) Editorial: Recent Advances in Flowering Time Control. Front. Plant Sci. 7: 2011. https://www.frontiersin.org/research-topics/1728/recent-advances-in-flowering-time-control

Hyun Y, Richter R, Vincent C, Martinez-Gallegos R, Porri A, Coupland G (2016) Multi-layered Regulation of SPL15 and Cooperation with SOC1 Integrate Endogenous Flowering Pathways at the Arabidopsis Shoot Meristem. Dev. Cell 37: 254-266 http://www.sciencedirect.com/science/article/pii/S1534580716301964

Toräng P, Wunder J, Obeso JR, Herzog M, Coupland G, Agren J (2015). Large-scale adaptive differentiation in the alpine perennial herb Arabis alpina. New Phytologist 206: 459-470. DOI

Willing EM, Rawat V, Mandakova T, Maumus F, James GV, Nordstrom KJ, Becker C, Warthmann N, Chica C, Szarzynska B, Zytnicki M, Albani MC, Kiefer C, Bergonzi S, Castaings L, Mateos JL, Berns MC, Bujdoso N, Piofczyk T, de Lorenzo L, Barrero-Sicilia C, Mateos I, Piednoel M, Hagmann J, Chen-Min-Tao R, Iglesias-Fernandez R, Schuster SC, Alonso-Blanco C, Roudier F, Carbonero P, Paz-Ares J, Davis SJ, Pecinka A, Quesneville H, Colot V, Lysak MA, Weigel D, Coupland G, Schneeberger K (2015) Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation. Nature Plants 1: 14023 http://www.nature.com/articles/nplants201423

Castaings L, Bergonzi S, Albani MC, Kemi U, Savolainen O, Coupland G (2014). Evolutionary conservation of cold-induced antisense RNAs of FLOWERING LOCUS C in Arabidopsis thaliana perennial relatives. Nature Communication 5: 4457 http://pubmedcentralcanada.ca/pmcc/articles/PMC4109010/

Hu JY, Zhou Y, He F, Dong X, Liu LY, Coupland G, Turck F, de Meaux J (2014). MiR824-regulated AGAMOUS-LIKE-16 contributes to flowering-time repression in Arabidopsis thaliana. Plant Cell 26, 2024-2037 http:/​/​dx.​doi.​org/​10.​1105/​tpc.​114.​124685

Chopra D, Wolff H, Span J, Schellmann, S, Coupland G, Albani MC, Schrader A, Huelskamp M (2014). Analysis of TTG1 function in Arabis alpina. BMC Plant Biol 14, doi:10.1186/1471-2229-14-16

Turck F and Coupland G (2014). Natural variation in epigenetic gene regulation and its effects on plant developmental traits. Evolution; International Journal of organic evolution 68 (3):620-631

Bergonzi S*, Albani MC*,  Ver Loren van Themaat E, Nordstrom KJ , Wang R, Schneeberger K, Moerland PD, and  Coupland G (2013): Mechanisms of age-dependent response to winter temperature in perennial flowering of Arabis alpina. Science 340, 1094-7, doi: 10.1126/science.1234116.*These authors contributed equally to this manuscript

Elrouby N, Bonequi MV, Porri A, Coupland G (2013). Identification of Arabidopsis SUMO-interacting proteins that regulate chromatin activity and developmental transitions. Proc Natl Acad Sci U S A 110 (49): 19956-61, doi:10.1073/pnas.1319985110

Nordström KJV*, Albani MC*, James GV, Gutjahr C, Hartwig B, Turck F, Paszkowski U, Coupland G and Schneeberger K (2013). Mutation identification by direct comparison of whole-genome sequencing data from mutant and wild-type individuals using k-mers", Nature Biotechnology. doi:10.1038/nbt.2515. *These authors contributed equally to this manuscript

Sarnowska EA, Rolicka AT, Bucior E, Cwiek P, Tohge T, Fernie AR, Jikumaru Y, Kamiya Y, Franzen R, Schmelzer E, Porri A, Sacharowski S, Gratkowska DM, Zugaj DL, Taff A, Zalewska A, Archacki R, Davis SJ, Coupland G, Koncz C, Jerzmanowski A, Sarnowski TJ (2013). DELLA-Interacting SWI3C Core Subunit of Switch/Sucrose Nonfermenting Chromatin Remodeling Complex Modulates Gibberellin Responses and Hormonal Cross Talk in Arabidopsis. Plant Physiol.163(1):305-17. doi: 10.1104/pp.113.223933.

Campoli C, Drosse B, Searle I, Coupland G, von Korff M (2012). Functional characterisation of HvCO1, the barley (Hordeum vulgare) flowering time ortholog of CONSTANS. Plant J 69 (5):868-80, doi:10.1111/j.1365-313X.2011.04839.x

Herrero E, Kolmos E, Bujdoso N, Yuan Y, Wang M, Berns MC, Uhlworm H, Coupland G, Saini R, Jaskolski M, Webb A, Goncalves J, Davis SJ (2012). EARLY FLOWERING4 recruitment of EARLY FLOWERING3 in the nucleus sustains the Arabidopsis circadian clock. Plant Cell 24 (2):428-43

Koskela EA, Mouhu K, Albani MC, Kurokura T, Rantanen M, Sargent DJ, Battey NH, Coupland G, Elomaa, P, Hytonen T (2012). Mutation in TERMINAL FLOWER1 reverses the photoperiodic requirement for flowering in the wild strawberry Fragaria vesca. Plant Physiology 159(3):1043-54

Albani MC, Castaings L, Wötzel S, Mateos JL, Wunder J, Wang R, Reymond M, Coupland G (2012). PEP1 of Arabis alpina is encoded by two overlapping genes that contribute to natural genetic variation in perennial flowering. PLOS Genet 8 (12): e1003130. doi:10.1371/journal.pgen.1003130

Andrés F and Coupland G (2012). The genetic basis of flowering responses to seasonal cues. Nature Reviews Genetics 13, 627-639

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