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Research Summary
Research Interests: Genetic and Epigenetic Basis of Fruit Quality Traits
Fleshy fruits are economically highly valuable and provide a substantial part of the daily intake of vitamins and minerals whether they are consumed in a fresh or processed condition. They also contain important bioactives including a range of antioxidants. There is evidence emerging that the genes that regulate ripening have been conserved during the evolution of fruit bearing species. In my laboratory the aim is to understand the molecular circuits that are involved in controlling fruit ripening (Manning et al., 2006. Nature Genetics 38, 948 - 952; Seymour et al., 2008.Current Opinion in Plant Biology, 11: 58-62; The Tomato Genome Consortium 2012 Nature 485: 635-641; Seymour et al., 2013. Annual Review of Plant Biology, 64: 219-241. This mechanistic understanding is essential if step changes are to be made in the pace of crop improvement. Key targets are to enhance shelf-life and therefore reduce post-harvest waste, while enhancing flavour and levels of health promoting compounds. There are several strands to the research programme:
Tomato as a Model for Understanding Ripening - We use tomato as a model to study fruit ripening. This is because of the wealth of genetic and molecular resources available for this species and the extensive research effort that has been focused on understanding tomato fruit ripening over the last 40 years. The resources available include a fully annotated genome sequence which can be found at (http://solgenomics.net/) and also a small number of single gene mutations exist. Tomato ripening is initiated and co-ordinated by ethylene, but there are also regulatory genes that act together with this plant hormone during the ripening process. A number of rare single gene mutations such as ripening-inhibitor (rin), non-ripening (nor) and Colourless non-ripening (Cnr) have pleiotropic effects resulting in the reduction or almost complete abolition of ripening. These mutants represent lesions in master switches controlling the ripening process which appear to act up-stream of ethylene. The molecular basis of the rin mutation was uncovered by positional cloning in 2002 (Vrebalov et al Science 296: 343-346). The RIN gene encodes a MADS-box transcription factor. MADS-box genes have commonly been associated with floral development or other major phase changes. However, their association with ripening is perhaps not that surprising as flowering plants are the only group to possess true fruits.
Ken Manning (then at Warwick University) and I used a genetic map-based approach to isolate the gene at the Cnr locus. This gene encodes a member of the SBP-box class of transcript factors and its gene product is likely to control the expression of specific MADS-box genes. Unexpectedly, Cnr was revealed to be an epigenetic mutation where expression of the CNR gene was silenced by elevated levels of methylation in the gene regulatory region (Manning et al., 2006. Nature Genetics 38, 948 - 952).
Since then several other master switches controlling the ripening process have been identified including the MADS-box genes TDR4 and TAGL1.Interestingly TDR4 and TAGL1 are similar to genes in the model plant Arabidopsis that control the development and dehiscence of its dry fruits, which are known botanically as siliques. We wanted to explore the possibility that many of the master switches found to control ripening in tomato have been conserved during the evolution of fruit bearing species. Together with Ken Manning at Warwick and Jim Giovannoni at Cornell we identified a gene in the same class of transcription factors as RIN that can modulate ripening in strawberry a non-climacteric fruit. Silencing a strawberry SEP1/2-like MADS gene results in slow ripening (Seymour et al 2011, Journal of Experimental Botany 62, 1179-1188.). Other ripening-related genes found in tomato also have homologs in other species. The function of the ripening expressed TDR4 gene in tomato is not known, but Laura Jaakola, then at the University of Oulu in Finland, and now at University of Tromsø, Norway, was able to isolate a TDR4-like gene from ripening bilberry fruits. These berries contain very high levels of anthocyanins that give the fruit their characteristic dark purple colour. We found that silencing the bilberry version of the MADS-box gene TDR4 dramatically altered anthocyanin accumulation in this fruit (Jaakola et al., 2010. Plant Physiology, 153: 1619-1629).
The Tomato Genome - from Genes to Quantitative Trait Loci (QTL) and Networks
I was involved with colleagues from Imperial, Hutton and TGAC in spearheadingthe UK contribution to the international programme to sequence the tomato genome with funding from BBSRC, Defra and SEERAD. The tomato genome sequence has now been published (The Tomato Genome Consortium 2012 Nature 485:635 - 641).It will underpin all future studies of natural variation across the tomato genome and help us better understand the genetic and molecular basis of fruit quality traits. In my lab we have used the sequence to identify genes under a complex QTL for fruit texture (Chapman et al., 2012, Plant Physiology 159, 1644-1657; Uluisik et al, Nature Biotechnology 2016 doi:10.1038/nbt.3602; Wang et al, 2019, Plant Physiology DOI: https://doi.org/10.1104/pp.18.01187) and in collaboration with Dr Philippe Gallusci at INRA we are exploring the role of natural epigenetic variation and its impact on fruit phenotypes (Liu et al, PNAS 112, 10804-10809, 2015).
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